EFFECTS OF HABITAT
FRAGMENTATION ON BIRDS
IN WESTERN LANDSCAPES:
CONTRASTS WITH PARADIGMS
FROM THE EASTERN
UNITED STATES
T. Luke George and David S. Dobkin, editors
Studies in Avian Biology No. 25
A PUBLICATION OF THE COOPER ORNITHOLOGICAL SOCIETY
Cover watercolor painting of a Varied Thrush (lxoreus naevius) in a naturally fragmented western landscape and a
Kentucky Warbler (Oporornis formosus) in an anthropogenically fragmented eastern landscape, by Wendell Minor
STUDIES IN AVIAN BIOLOGY
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Issued: December 18, 2002
Copyright ¸ by the Cooper Ornithological Society 2002
CONTENTS
LIST OF AUTHORS ............................................... 1
PREFACE ......................................................... 3
INTRODUCTION: Habitat fragmentation and western birds .............
.............................. T. Luke George and David S. Dobkin 4
THEORY AND CONTINENTAL COMPARISONS
A multi-scale perspective of the effects of forest fragmentation on birds in
eastern forests ........ Frank R. Thompson, III, Therese M. Donovan,
Richard M. DeGraaf, John Faaborg, and Scott K. Robinson 8
What is habitat fragmentation? .......................................
............... Alan B. Franklin, Barry R. Noon, and T Luke George 20
Habitat edges and avian ecology: geographic patterns and insights for west-
ern landscapes .................... Thomas D. Sisk and James Battin 30
Effects of fire and post-fire salvage logging on avian communities in conifer-
dominated forests of the western United States .....................
Natasha B. Kotliar, Sallie J. Hejl, Richard L. Hutto, Victoria A. Saab,
Cynthia P. Melcher, and Mary E. McFadzen 49
Geographic variation in cowbird distribution, abundance, and parasitism ..
......................... Michael L. Morrison and D. Caldwell Hahn 65
Effects of forest fragmentation on brood parasitism and nest predation in
eastern and western landscapes ....................................
............................... John E Cavitt and Thomas E. Martin 73
Effects of forest fragmentation on tanager and thrush species in eastern and
western North America ...... Ralph S. Hames, Kenneth V. Rosenberg,
James D. Lowe, Sara E. Barker, and Andr6 A. Dhondt 81
EFFECTS OF FRAGMENTATION ON WESTERN ECOSYSTEMS
The effects of habitat fragmentation on birds in coast redwood forests ....
................................. T Luke George and Arriana Brand 92
Effects of habitat fragmentation on birds in the coastal coniferous forests of
the Pacific Northwest ..... David A. Manuwal and Naomi J. Manuwal 103
Birds and changing landscape patterns in conifer forests of the north-central
Rocky Mountains ... Sallie J. Hejl, Diane Evans Mack, Jock S. Young,
James C. Bednarz, and Richard L. Hutto 113
Effects of habitat fragmentation on passerine birds breeding in intermountain
shrubsteppe ................. Steven T Knick and John T. Rotenberry 130
Habitat fragmentation effects on birds in southern California: contrast to the
"top-down" paradigm ........................... Douglas T. Bolger 141
Effects of anthropogenic fragmentation and livestock grazing on western
riparian bird communities ...... Joshua J. Tewksbury, Anne E. Black,
Nadav Nur, Victoria A. Saab, Brian D. Logan, and David S. Dobkin 158
STUDIES ON FOCAL SPECIES
Spotted Owls, forest fragmentation, and forest heterogeneity .............
............................... Alan B. Franklin and R. J. Gutierrez 203
Effects of forest fragmentation on populations of the Marbled Murrelet . ..
........... Martin G. Raphael, Diane Evans Mack, John M. Marzluff,
and John M. Luginbuhl 221
LITERATURE CITED .............................................. 236
LIST OF AUTHORS
SARA E. BARKER
Laboratory of Ornithology
Cornell University
Ithaca, NY 14850
JAMES BATTIN
Department of Biological Sciences
Northern Arizona University
Flagstaff, AZ 86011-5694
JAMES C. BEDNARZ
Department of Biological Sciences
Arkansas State University
State University, AR 72467
ANNE E. BLACK
Colorado National Heritage Program
Fort Collins, CO, and
Point Reyes Bird Observatory
4990 Shoreline Highway
Stinson Beach, CA 94970
DOUGLAS T. BOLGER
Environmental Studies Program
HB6182
Dartmouth College
Hanover, NH 03755
L. ARRIANA BRAND
Department of Fishery and Wildlife Biology
Colorado State University
Fort Collins, CO 80523
JOHN E CAVITI'
U.S. Geological Survey
Montana Cooperative Wildlife Research Unit
University of Montana
Missoula, MT 59812
(Present address: Department of Zoology
Weber State University
2505 University Circle
Ogden, UT 84408-2505)
RICHARD M. DEGRAAF
USDA Forest Service
Northeastern Research Station
Holdsworth Hall
University of Massachusetts
Amherst, MA 01003
ANDRI A. DHONDT
Laboratory of Ornithology
Cornell University
Ithaca, NY 14850
DAVID S. DOBKIN
High Desert Ecological Research Institute
15 SW Colorado Avenue, Ste. 300
Bend, OR 97702
THERESE M. DONOVAN
SUNY College of Environmental Science and
Forestry
1 Forestry Drive
Syracuse, NY 13210
(Present address: Vermont Cooperative Fish and
Wildlife Research Unit
311 Aiken Center
University of Vermont
Burlington, VT 05405)
JOHN FAABORG
Division of Biological Sciences
110 Tucker Hall
University of Missouri
Columbia, MO 65211
ALAN B. FRANKLIN
Colorado Cooperative Fish and Wildlife Research
Unit
Department of Fishery and Wildlife Biology
Colorado State University
Fort Collins, CO 80523
T. LUKE GEORGE
Department of Wildlife
Humboldt State University
Arcata, CA 95521
R. J. GUTIIRREZ
Department of Wildlife
Humboldt State University
Arcata, CA 95521
(Present address: Department of Fisheries and
Wildlife
University of Minnesota
St. Paul, MN 55108)
D. CALDWELL HAHN
U.S. Geological Survey
Patuxent Wildlife Research Center
11410 American Holly Drive
Laurel, MD 20708-4015
RALPH S. HAMES
Laboratory of Ornithology
Cornell University
Ithaca, NY 14850
SALLIE J. HEJL
USDA Forest Service
Rocky Mountain Research Station
P.O. Box 8089
Missoula, MT 59807, and
Sierra Nevada Framework Project
801 I St., Rm. 419
Sacramento, CA 95814
(Present address: Department of Wildlife and
Fisheries Sciences
2258 TAMU
Texas A&M University
College Station, TX 77843-2258)
RICHARD L. HUTTO
Division of Biological Sciences
University of Montana
Missoula, MT 59812
STEVEN T. KNICK
U.S. Geological Survey
Forest and Rangeland Ecosystem Science Center
Snake River Field Station
970 Lusk Street
Boise, ID 83706
NATASHA B. NOTLIAR
U.S. Geological Survey
Fort Collins Science Center
2150 Centre Avenue, Bldg C
Fort Collins CO 80526-8818
2 STUDIES IN AVIAN BIOLOGY NO. 25
BRIAN D. LOGAN
U.S. Geological Survey
Montana Cooperative Wildlife Research Unit
University of Montana
Missoula, MT 59812
JAMES D. LOWE
Laboratory of Ornithology
Cornell University
Ithaca, NY 14850
JOHN g. LUGINBUHL
College of Forest Resources
University of Washington
Seattle, WA 98195-2100
DIANE EVANS MACK
USDA Forest Service
Pacific Northwest Research Station
3625 93rd Ave SW
Olympia, WA 98512-9193
DAVID A. MANUWAL
College of Forest Resources
Box 352100
University of Washington
Seattle, WA 98195
NAOMI J, MANUWAL
19420 194th Ave NE
Woodinville, WA 98072
THOMAS E. MARTIN
U.S. Geological Survey
Montana Cooperative Wildlife Research Unit
University of Montana
Missoula, MT 59812
JOHN M. MARZLUFF
College of Forest Resources
University of Washington
Seattle, WA 98195-2100
MARY E. MCFAZEN
USDA Forest Service
Rocky Mountain Research Station
EO. Box 8089
Missoula, MT 59807
CYNTHIA P, MELCHER
U.S. Geological Survey
Fort Collins Science Center
2150 Centre Avenue, Bldg C
Fort Collins CO 80526-8818
MICHAEL L. MORRISON
University of California
White Mountain Research Station
3000 East Line Street
Bishop, CA 93514
BARRY R. NOON
Department of Fishery and Wildlife Biology
Colorado State University
Fort Collins, CO 80523
NADAV NUR
Point Reyes Bird Observatory
4990 Shoreline Highway
Stinson Beach, CA 94970
MARTIN G. RAPHAEL
USDA Forest Service
Pacific Northwest Research Station
Olympia, WA 98512-9193
SCOTF K. ROBINSON
Department of Animal Biology
172 Natural Resource
University of Illinois
Champaign, IL 61820
KENNETH V. ROSENBERG
Laboratory of Ornithology
Cornell University
Ithaca, NY 14850
JOHN T. ROTENBERRY
Center for Conservation Biology and Department of
Biology
University of California
Riverside, CA 92521
VICTORIA A. SAAB
USDA Forest Service
Rocky Mountain Research Station
316 E. Myrtle St.
Boise, ID 83702
THOMAS D. SISK
Center for Environmental Sciences and Education
Northern Arizona University
Flagstaff, AZ 86011-5694
JOSHUA J. TEWKSBURY
Biological Sciences
University of Montana
Missoula, MT 59812
(Present address: Department of Zoology
Box 118525
University of Florida
Gainesville, FL 32611)
FRANC R. THOMPSON, III
USDA Forest Service
North Central Research Station
202 Natural Resources Bldg.
University of Missouri
Columbia, MO 65211
JOCK S. YOUNG
Division of Biological Sciences
University of Montana
Missoula, MT 59812
Studies in Avian Biology No. 25:3, 2002.
PREFACE
This volume grew from recognition of the
need for a forum to address explicitly the con-
trasts and similarities of fragmentation processes
and fragmentation effects in eastern and western
landscapes. That recognition arose over the
course of several years in informal discussions
between the editors, which crystallized at the
second North American Ornithological Confer-
ence in 1998 in St. Louis, where we conceived
of a symposium and outlined the areas that
should be covered.
A one-day symposium organized by the edi-
tors was held the following year in Portland,
Oregon, at the annual meeting of the Cooper Or-
nithological Society. The central focus of the
symposium was to contrast patterns in the west-
ern versus eastern United States, and to differ-
entiate and contrast natural versus human-
caused fragmentation patterns and associated ef-
fects. From the outset, the symposium was in-
tended to serve as the basis for a monograph in
the STUDIES IN AVI^N BIOLOGY series. Nearly all
of the 16 chapters contained in this volume are
based on symposium presentations, although not
all topics covered in the symposium are repre-
sented here. Each chapter has been peer-re-
viewed and reviewed by the editors, as well.
We are grateful to the Cooper Ornithological
Society for providing logistic support and an ex-
cellent venue for the symposium, and to our col-
leagues who graciously agreed to serve as peer-
reviewers for the chapters in this volume. We
thank the United States Environmental Protec-
tion Agency's Ecosystem Science Branch for
generously providing funds to support publica-
tion of this volume through Assistance Agree-
ment No. 82772001 to the High Desert Ecolog-
ical Research Institute. The research contained
herein has not been subjected to Agency review,
and therefore does not necessarily reflect the
views of the Environmental Protection Agency.
Additional funds in support of the symposium
were provided by the Oregon/Washington office
of the United States Bureau of Land Manage-
ment and the Cooper Ornithological Society.
The editors thank Wendell Minor for providing
the artwork that graces the cover.
David S. Dobkin
T Luke George
Studies in Avian Biology No. 25:4-7, 2002.
INTRODUCTION: HABITAT FRAGMENTATION AND WESTERN
BIRDS
T. LUKE GEORGE AND DAVID S. DOBKIN
Habitat fragmentation and loss due to human
activities has been identified as the most impor-
tant factor contributing to the decline and loss
of species worldwide (Noss and Cooperrider
1994). Although the response of species to hab-
itat loss generally is clear, the effects of habitat
fragmentation are much more complex (Fahrig
1997, Bunnell 1999). Over the last two decades,
our understanding of the effects of habitat frag-
mentation on bird populations has increased tre-
mendously. Early studies viewed habitat frag-
ments as islands and interpreted patterns of spe-
cies richness in the context of island biogeog-
raphy theory (Forman et al. 1976, Galli et al.
1976). It soon became apparent, however, that
in contrast to oceanic islands, the habitat or ma-
tfix surrounding fragments profoundly influ-
enced the ecological conditions within those
fragments. In particular, rates of nest predation
and cowbird parasitism of ground-nesting and
cup-nesting birds were found to be extremely
high close to forest edges (Ambuel and Temple
1983) and in small forest fragments (Wilcove
1985, Robinson 1992). Further study revealed
that patterns of nest predation, and especially
nest parasitism, were influenced by forest cover
in the surrounding landscape (Andr6n and An-
gelstam 1988; Andr6n 1992, 1994, 1995; Rob-
inson et al. 1995, Donovan et al. 1997). Taken
together, these results suggested that declines
and losses of birds from small forest fragments
were related to elevated rates of nest predation
and parasitism. These observations led to the de-
velopment of a top-down hierarchical model that
included regional, landscape-level, and local ef-
fects to explain variation in nesting success
across the landscape and subsequent changes in
abundance and distribution of the affected spe-
cies (Thompson et al. this volume). Because
much of the empirical support for this model
derives from studies conducted in the eastern
United States (i.e., east of the Rocky Moun-
tains), this model embodies what can be viewed
as the "eastern paradigm."
As better understanding of the human-im-
posed dynamics and the natural ecological pro-
cesses that govern western landscapes has ac-
crued in recent years, applicability of the eastern
paradigm to landscapes of the western United
States has become more tenuous. First, the na-
ture of the matrix in most western ecosystems
differs dramatically from the East. Habitat frag-
ments studied in the eastern United States fre-
quently are embedded in agricultural or urban
landscapes, but most studies of habitat fragmen-
tation in the West have focused on forest frag-
ments created by timber harvest. Logging op-
erations result in fragments of mature or old-
growth forest that are embedded in a matrix of
young, regenerating forest. Landscapes com-
posed of young forest, in contrast to agricultural
and exurban landscapes, may not harbor high
densities of predators and brood parasites, and
consequently birds inhabiting fragments may not
suffer the high rates of nest predation and par-
asitism observed in the East. While the extent
of urban and agricultural development is in-
creasing in the West, it is substantially less than
in the East (Fig. 1). As a result, fragments of
natural vegetation generally are embedded in a
matrix of agricultural and urban land in the East,
but urban and agricultural lands generally are
isolated in a matrix of unconverted habitat in the
West (Fig. 2). Clearly there are some regions in
the western United States that exhibit patterns
similar to the East. For instance, 71% of Cali-
fomia's Central Valley and 63% of Oregon's
Willamette Valley have been converted to agri-
cultural or urban uses, which is similar to the
high levels of conversion in many eastern and
Midwestern regions (T. L. George, unpubl. data).
A second suite of fundamental differences be-
tween eastern and western landscapes results in
a higher degree of natural heterogeneity in the
West. Greater aridity, the greater spatial extent
and temporal frequency of fires, and greater to-
pographic diversity made western landscapes in-
herently more patchy than eastern landscapes
long before European settlement (Hejl et al. this
volume, Kotliar et al. this volume). Having con-
tended with the natural heterogeneity of western
landscapes for thousands of generations, avian
populations inhabiting this region may be less
affected by fragmentation processes and conse-
quences than avian populations of the relatively
more homogeneous landscapes of the pre-Eu-
ropean-settlement eastern United States. If noth-
ing else, these differing selective milieus make
it difficult to predict the responses to disturbance
(whether natural or anthropogenic) by species
inhabiting western landscapes.
The primary objective of this volume was to
INTRODUCTIONsGeorge and Dobkin 5
Percent Converted Land by Ecoregion
P½½nt Converted Lnd
/0-10
10-20
20 -30
90 - 100
20t 2t- 400 Iv'files
FIGURE I. Proportion of land converted to agriculture or man-made structures in the conterminous United
States in 66 physiographic regions. Proportions were calculated l¾om the U.S. Geological Survey Land Use and
Land Cover (LULC) database compiled between 1975-1985 (Mitchell et al. 1977). The LULC database included
45 categories (Anderson et al. 1975); we combined all agricultural and developed land into an "altered" category
(see Appendix) and calculated the proportion of altered and unaltered land within each region. The physiographic
regions are those used by Robbins et al. (1986) for analyses of the Breeding Bird Survey data.
examine the effects of habitat fragmentation on
western bird populations, particularly in the con-
text of predictions derived from eastern para-
digms. We defined the western United States as
the area from the Rocky Mountains west to the
Pacific Coast in the conterminous United States.
The lUllowing chapters are grouped into three
sections covering theory and continental-scale
comparisons, effects of fragmentation in specific
western ecosystems, and studies of focal species.
Thompson et al. begin by describing and sum-
marizing evidence for the eastern paradigms and
provide a multi-scale working hypothesis for the
effects of habitat fragmentation on birds. Frank-
lin et al. provide a definition of habitat fragmen-
tation. paying particular attention to the distinc-
tion between habitat fragmentation and habitat
heterogeneity, and Sisk and Battin review the
concept of habitat edge as it applies to western
landscapes. The ubiquitous role of fire in shap-
ing western landscapes and their associated avi-
faunas is addressed by Kotliar et al.
Studies that span the continent offer a unique
opportunity to compare the response of birds
and their nest predators and parasites to frag-
mentation in the East and the West. Morrison
and Hahn summarize studies of the response of
Brown-headed Cowbirds (Molothrus ater) to
fragmentation in the East and the West. Cavitt
and Martin examine differences in rates of nest
predation and parasitism between fragmented
and unfragmented areas in the East and the West
using data on the outcome of tens of thousands
of nests in the BBIRD database (Martin et al.
1997). Employing data from the Cornell Labo-
ratory of Ornithology's "Birds in Forested
Landscapes" project, Hames et al. compare the
responses of tanagers, thrashes, and Brown-
headed Cowbirds to forest fragmentation across
the United States.
Six chapters focus on individual western eco-
systems selected to reflect both the relative im-
portance of specific vegetation communities and
the constraint of where fragmentation-related re-
6 STUDIES IN AVIAN BIOLOGY NO. 25
I NonConverted
,'x, U.S. State Boundaries
Contrasting Landscapes: West rs. Midwest
;' ,. , '.. ,- r "'ø' l, ,"
I ß ,
, -.. ,
/ ',,, ;I
. '.. ' !l
,, '
FIGURE 2. Examples of the distribution of altered and unaltered habitat in the midwestern and the western
United States. Land cover data were obtained from U.S. Geological Survey Land Use and Land Cover (LULC)
database compiled between 1975-1985 (Mitchell et al. 1977).
search has been conducted in the West. Three
chapters focus on coniferous forests. George and
Brand summarize studies in redwood (Sequoia
sempervirens) forests, Manuwal and Manuwal
summarize research in the wet coniferous forests
of the Pacific Northwest, and Hejl et al. examine
forests of the northern Rocky Mountains. Knick
and Rotenberry describe avian responses to frag-
mentation in the Intermo,untain shrubsteppe,
Bolger summarizes a wealth of studies that have
been conducted in the highly urbanized coastal
sage scrub and chaparral regions of southern
California, and Tewksbury ½t al. analyze riparian
bird communities across seven riparian systems
in five western states. Notably lacking are sum-
maries of the effects of fragmentation on birds
in the southern Rocky Mountains and the desert
Southwest. There were too few studies on the
effects of habitat fragmentation on birds in these
regions to warrant reviews. A recent publication
by Knight (2000) provides an overview of the
effects of habitat fragmentation in the southern
Rocky Mountains.
Finally, as a reflection of the relatively great
attention paid to loss and fragmentation of old-
growth forests in the western United States, two
chapters are devoted to multi-scale assessments
of focal species in the context of loss and IYag-
mentation of their old-growth forest habitats.
Franklin and Guti6rrez synthesize information
across subspecies of Spotted Owls (Strix occi-
dentalis), and Raphael et al. examine Marbled
Murrelets (Brachyramphus marmoratus). Both
of these species have had a significant impact on
management of western forests.
Although the picture is far from complete, the
contents of this monograph illustrate the state of
our knowledge regarding fragmentation effects
on western bird populations at the beginning of
the 21st century. We hope this volume will serve
as a landmark contribution to the ecological and
conservation literature by presenting a solid syn-
thesis and foundation to buttress future research,
and by conveying important policy implications
for public land management in the western Unit-
ed States.
INTRODUCTION--George and Dobkin 7
APPENDIX. LAND USE CATEGORIES IN USGS DATABASE DESIGNATED AS ALTERED (1) OR UNALTERED (0) FOR
FIGURES 1 AND 2
Anderson a land use category Altered
Urban or built-up land 1
Residential 1
Commercial and services 1
Industrial 1
Transportation, communication, utilities 1
Industrial and commercial complexes 1
Mixed urban or built-up land 1
Other urban or built-up land 1
Agricultural land 1
Cropland and pasture 1
Orchards, groves, vineyards, nurseries, and ornamental horticultural 1
Confined feeding operations 1
Other agricultural land 1
Rangeland 0
Herbaceous rangeland 0
Shrub and brush rangeland 0
Mixed rangeland 0
Forest land 0
Deciduous forest land 0
Evergreen forest land 0
Mixed forest land 0
Water 0
Streams and canals 0
Lakes 0
Reservoirs 0
Bays and estuaries 0
Wetland 0
Forested wetland 0
Nonforested wetland 0
Barren land 0
Dry salt flats 0
Beaches 0
Sandy areas not beaches 0
Bare exposed rock 0
Strip mines, quarries, gravel pits 0
Transitional areas 0
Tundra 0
Shrub and brush tundra 0
Herbaceous tundra 0
Bare ground 0
Wet tundra 0
Mixed tundra 0
Perennial snow or ice 0
Perennial snowfields 0
Glaciers 0
a From Anderson et al. (1922).
Studies in Avian Biology No. 25:8-19, 2002.
A MULTI-SCALE PERSPECTIVE OF THE EFFECTS OF FOREST
FRAGMENTATION ON BIRDS IN EASTERN FORESTS
FRANK R. THOMPSON, III, THERESE M. DONOVAN, RICHARD M. DEGRAAF, JOHN FAABORG,
AND SCOTT K. ROBINSON
Abstract. We propose a model that considers forest fragmentation within a spatial hierarchy that
includes regional or biogeographic effects, landscape-level fragmentation effects, and local habitat
effects. We hypothesize that effects operate "top down" in that larger scale effects provide constraints
or context for smaller scale effects. Bird species' abundance and productivity vary at a biogeographic
scale, as do the abundances of predators, Brown-headed Cowbirds (Molothrus ater), and land-use
patterns. At the landscape scale the level of forest fragmentation affects avian productivity through its
effect on predator and cowbird numbers. At a local scale, patch size, amount of edge, and the effects
of forest management on vegetation structure affect the abundance of breeding birds as well as the
distribution of predators and Brown-headed Cowbirds in the landscape. These local factors, along with
nest-site characteristics, may affect nest success and be important factors when unconstrained by
processes at larger spatial scales. Landscape and regional source-sink models offer a way to test various
effects at multiple scales on population trends. Our model is largely a hypothesis based on retroduction
from existing studies; nevertheless, we believe it has important conservation and research implications.
Key Words: Brown-headed Cowbirds; eastern forests; edge-effects; fragmentation; landscape; Mol-
othrus ater; multi-scale; nest predation; predators; songbirds.
Much recent research has focused on the effects
of forest fragmentation on breeding neotropical
migrant birds and recent reviews have concluded
that forest fragmentation generally results in in-
creased nest predation and brood parasitism
(Robinson and Wilcove 1994, Faaborg et al.
1995, Walters 1998). For example, numbers of
Brown-headed Cowbirds (Molothrus ater),
brood parasitism, and nest predation are nega-
tively correlated with the amount of forest cover
in landscapes in the midwestern U.S. (Donovan
et al. 1995b, Robinson et al. 1995a, Thompson
et al. 2000). Enough variation or inconsistency
exists among studies, however, that it is difficult
to develop a general model of the effects of for-
est fragmentation on songbirds that addresses
spatial scale, accounts for local and regional var-
iation in observed effects, and describes mech-
anisms for observed effects. Most research has
been conducted in eastern forests. Differences in
ecological patterns and land use between eastern
and western North America, however, has led to
speculation that the effects of fragmentation on
birds may differ among these regions (George
and Dobkin this volume).
We have been developing a conceptual model
that places the effects of landscape-level forest
fragmentation within a spatial hierarchy that
ranges from biogeographic or regional effects to
local effects (Freemark et al. 1995, Donovan et
al. 1997, Robinson et al. 1999, Thompson et al.
2000). Our purpose in developing this model is
to provide a synthesis of the current understand-
ing of forest fragmentation effects in eastern
landscapes, and to stimulate research that will
enhance that understanding in both eastern and
western North America. Our model is a simple
framework within which factors affecting spe-
cies viability can be examined. We present the
model as a series of hypotheses organized by
this framework, and then review key studies that
we used to formulate these hypotheses. We pre-
sent the model as series of hypotheses because
it is formed largely by retroduction. Retroduc-
tion is the construction of a hypothesis about a
process that provides an explanation for ob-
served patterns or facts (Romesburg 1981).
Models of this type are often most useful as hy-
potheses for hypothetico-deductive research
(Romesburg 1981), and we review a few studies
of this type that test our hypotheses. We do not
provide an exhaustive literature review because
recent reviews exist (e.g., Robinson and Wilcove
1994, Faaborg et al. 1995, Walters 1998, Heske
et al. 2001). We primarily review fragmentation
effects at a landscape scale and edge effects at
a habitat scale. However, we also discuss effects
at larger and smaller scales because of important
interactions with edge and landscape effects. For
brevity and because of the focus of this volume
we focus on biogeographic, landscape, and hab-
itat effects on songbird reproductive success.
The context for our review is the eastern decid-
uous forest, although where possible we make
comparisons to western landscapes.
THE MODEL
From a breeding ground perspective, habitat
characteristics associated with reproductive suc-
cess of forest passefines can be evaluated at sev-
eral spatial scales: (1) the nest-site scale--the
FRAGMENTATION IN EASTERN FORESTS--Thompson et al. 9
micro-habitat characteristics directly around the
nest or the immediate vicinity of the nest; (2)
the habitat scale--the features of the habitat
patch in which the nest is located; (3) the land-
scape scale--the collection of different habitat
patches and the position of a particular habitat
within a landscape, the matrix within which the
habitat is embedded, and the juxtaposition and
proximity of other habitats in the landscape
(Freemark et al. 1993); and (4) biogeographic
scales.
For example, vegetation structure at a habitat
scale, or location within a landscape, may be
more important than nest site characteristics
such as concealment in reducing nest depreda-
tion (Bowman and Harris 1980, Leimgruber et
al. 1994, Donovan et al. 1997, Burhans and
Thompson 1999) or parasitism (Best 1978,
Johnson and Temple 1990, Burhans 1997, Morse
and Robinson 1999). Furthermore, nest preda-
tion or brood parasitism may be related to land-
scape composition and structure (Robinson et al.
1995a, Donovan et al. 2000, Thompson et al.
2000). Finally, geographic location and abiotic
and biotic characteristics at multiple scales can
directly impact a population's growth (Hoover
and Brittingham 1993, Leimgruber et al. 1994,
Thompson 1994, Coker and Capen 1995,
Thompson et al. 2000). The essence of our mod-
el is that all spatial scales may contribute to the
ability of a local subpopulation to replace itself
(Sherry and Holmes 1992), but the importance
of each may depend on habitat features at other
scales or the geographic location within the
breeding or non-breeding range. These effects
can be arranged in a hierarchy in which larger
scale effects provide constraints or context for
smaller scale effects (Fig. 1).
What types of evidence directly support this
model? Evidence of top-down constraints comes
from observational, experimental, and meta-
analysis studies across eastern North America.
Although we provide several examples of cor-
relative evidence for such constraints, we em-
phasize that experimental and meta-analysis ap-
proaches that directly test the top-down con-
straint hypothesis have been very instructive be-
cause they attempt to control for factors
operating at other spatial scales. For example,
we tested the hypothesis that landscape effects
are more significant than local edge effects, and
that edge effects are dependent on landscape
context, in a rigorously-designed, large-scale,
randomized field experiment. We found strong
evidence that edge effects in nest predation are
dependent on landscape context, and that land-
scape context is a better predictor of cowbird
abundance than any other local-scale affect mea-
sured (Fig. 2; Donovan et al. 1997). In land-
Large Scale, Biogeographic
Effects
Abundance and demographics
of songbirds, cowbirds, and
predators vary at a geographic
scale.
Landscape-Level Effects
Land cover and use affect the
abundance of breeding birds,
predators and nest predation,
and cowbirds and brood
arasitism.
Habitat and Local Effects
Habitat type, patch size,
proximity to edge, and forest
management affect predator
and cowbird activity, nest
)redation, and brood
)arasitism
Nest-Site Effects
Characteristics such as nest
type, height, and concealment
affect the probability of
predation and parasitism
FIGURE 1. Conceptual model of factors at multiple
spatial scales affecting reproductive success of song-
birds. Larger scale factors are hypothesized to be more
important determinants of species viability because
they provide context or constraints for smaller scale
effects.
scapes with < 15% forest, predation was high in
forest edge and interior; at 45-55% forest cover,
predation was high in forest edge and low in
forest interior; and at >90% forest cover, pre-
dation was low in forest edge and interion Cow-
bird abundance was much greater in landscapes
with high levels of forest fragmentation than
those with low levels of fragmentation (Fig. 2).
While we could not randomly assign landscape
treatments in this study (because the landscape
patterns already existed), study sites were ran-
domly selected from a three-state area. As a re-
sult, we believe these results allow strong infer-
ences for at least Missouri, Illinois, and Indiana.
The results of this research were also confirmed
by a meta-analysis of nest depredation studies in
which researchers compared the landscape con-
text for studies that documented edge effects on
predation patterns with those that failed to find
edge effects (Bayne and Hobson 1997, Hartley
and Hunter 1998).
We believe that these large-scale analyses are
10 STUDIES IN AVIAN BIOLOGY NO. 25
60
so
40
30
20
lO
1.0
0.8
0.6
0.4
0.2
o.o
A AB B
/
A AB B
High Medium Low
Level of fragmentation and
edge (E) or interior (I)
FIGURE 2. Effects of landscape level of fragmen-
tation and local edge effects on nest predation and
cowbird abundance in the midwestern United States.
Fragmentation levels were measured as the amount of
forest cover and were: high, < 15% forest; medium,
45-55% forest; and low, > 90% forest. Edge (E) and
interior (I) treatments were 50 rn and > 250 m from
forest edge, respectively. Levels of forest cover with
different letters, and edge and interior treatments with
an asterisk are significantly different (ANOVA, P <
0.05). Data and figures adapted from Donovan et al.
(1997).
critical for understanding how forest fragmen-
tation impacts songbird populations. Although
artificial nest experiments at large spatial scales
may provide some insights, our hypothesis that
larger scale effects provide constraints or con-
text for smaller scale effects depends on obser-
vations of nesting success at numerous locations
across a species' range. Obviously, collection of
these data is not an easy task, and significant
advances will likely be made through large-scale
collaborations (e.g., Robinson et al. 1995a),
large-scale research programs with standardized
methodology (e.g., BBIRD; Martin et al. 1997),
or through meta-analyses (e.g., Hartley and
Hunter 1998, Chalfoun et al. 2002). We have
focused on direct measures of nesting success,
nest predation, and predator abundance; how-
ever, we recognize that indirect measures will be
necessary and provide insight at large spatial
scales (e.g., Project Tanager; Rosenberg et al.
1999).
LARGE-SCALE, BIOGEOGRAPHIC
EFFECTS
Hypothesis: Breeding birds exhibit geograph-
ic patterns in their demographics. These are in
part the result of geographic patterns in the dis-
tribution of predators and cowbirds, and pro-
vide the context for smaller scale effects and can
affect local reproductive success.
PREDATOR DISTRIBUTION
Predator abundance and species richness vary
across North America. Levels of nest predation
could be higher where the total abundance and
diversity of predators is higher. For example,
Rosenberg et al. (1999) documented biogeo-
graphic patterns in predator communities as part
of Project Tanager. Tanagers (Piranga spp.)
were exposed to different combinations of pred-
ators across their range, and predators responded
differently to forest fragmentation. The highest
incidence of the predators they surveyed oc-
curred in the Midwest. General patterns in the
distribution of avian predators can be generated
from Breeding Bird Survey (BBS) data (Sauer
et al. 1997). Detecting biogeographic patterns in
nest predation related to predator abundance or
diversity will be difficult because of the large
number of potential nest predators and variation
in their distributions across North America. Fur-
ther complicating these patterns is the interac-
tion between diversity and abundance; even in
areas of low predator diversity a single predator
may be very abundant.
BROWN-HEADED COWBIRD DISTRIBUTION
Cowbirds demonstrate strong geographic pat-
terns in abundance; therefore, the potential ef-
fects of fragmentation or habitat effects are con-
strained by this larger-scale effect. More simply
put, in regions of the country where cowbirds
are rare it is unlikely that fragmentation or local
factors will have a strong effect on parasitism
levels.
The strongest evidence of this geographic ef-
fect comes from BBS data. A distribution map
generated from BBS data shows a general pat-
tern of high abundance of cowbirds in the Great
Plains and decreasing abundance with distance
from the Great Plains (Sauer et al. 1997).
Thompson et al. (2000) examined patterns from
the BBS data by regressing mean statewide cow-
bird abundance on distance from the center of
their range in the Great Plains and the percent
of forest cover in that state. Mean statewide
cowbird abundance was negatively related to
forest cover in a state and a state's distance from
FRAGMENTATION IN EASTERN FORESTS--Thompson et al. 11
the center of the cowbird's breeding range (R 2
= 0.67). Regression coefficients for distance to
center of range and forest cover were both sig-
nificant. However, the partial correlation of dis-
tance to center of range with cowbird abundance
was greater than that for forest cover and cow-
bird abundance. While both partial correlations
were significant, the effect of distance to the
center of the range was stronger and provides
some indication of the importance of biogeo-
graphic constraints. Additional evidence of this
effect is seen in parasitism levels. Wood Thrush
(Hylocichla mustelina) parasitism levels de-
crease from Midwest to Mid-Atlantic to New
England (Hoover and Brittingham 1993; see also
Smith and Myers-Smith 1998).
LANDSCAPE-LEVEL EFFECTS
Hypothesis: Nest predation and cowbird par-
asitism increase with forest fragmentation at the
landscape scale. Predation and parasitism is
greater in fragmented landscapes because of a
positive, numerical response by predators and
cowbirds that is the result of increase in the
availability and interspersion of food, hosts, or
other resources.
A landscape is a heterogeneous mosaic of
habitat patches in which individuals live and dis-
perse (Dunning et al. 1992), usually ranging in
size from a few to hundreds of square kilome-
ters. Most research on landscape-level effects
and fragmentation has occurred in the last de-
cade; understanding the logical importance of
these factors required a major shift in our con-
cepts of habitat relationships. Biologists, how-
ever, have been documenting the distribution of
forest passerines in relation to habitat and hab-
itat-patch characteristics for literally decades
(e.g., Robbins et al. 1989b; reviewed by Free-
mark et al. 1995), often using the MacArthur
and Wilson (1967) model of island biogeogra-
phy as a guiding framework (reviewed in Faa-
borg et al. 1995). Patch size, patch shape, and
interpatch distances, as well as forest type, have
important effects on bird community composi-
tion. However, there is ample evidence to sug-
gest that these local patterns are driven in part
by habitat characteristics at the landscape scale,
and also vary regionally. Most investigators of
fragmentation effects recognized that habitat
fragments differed from true islands because the
matrix between the fragments was not ocean, but
was a different habitat that supported its own set
of species. The inclusion of "edge" species in
counts on fragments was certainly one form of
recognition that effects from the surroundings of
the study site could be important. However, to
truly understand all the effects of landscape-lev-
el processes upon forest birds we needed to
study a variety of landscapes, as opposed to a
variety of patches.
PATTERNS OF LAND COVER AND THEIR EFFECTS
ON THE ABUNDANCE OF PREDATORS AND
NEST PREDATION
Land cover can significantly influence the
number and diversity of predators, as well as
constrain the importance of more local-scale
habitat factors such as patch size, vegetation
structure, or distance to edge effects on nest pre-
dation. We begin by reviewing the main effects
of landscape pattern, and then discuss how land-
scape factors potentially constrain more local-
scale effects on nest predation. Detection of this
constraint, however, may be difficult because
predators throughout North America vary great-
ly in habitat use, foraging behavior, and how
they collectively contribute to observed nest pre-
dation patterns in forest passerines (e.g., Gates
and Gysel 1978, Andrdn and Angelstam 1988,
Yosef 1994, Tewksbury et al. 1998, Marzluff
and Restani 1999, Dijak and Thompson 2000).
Robinson et al. (1995a) and Donovan et al.
(1995b) were the first to use empirical data from
real nests to relate nest predation to forest frag-
mentation at a landscape scale. They measured
many landscape variables but used the percent
of forest cover within a 10-km radius as a simple
measure of forest fragmentation and examined
its correlation with daily nest predation. Corre-
lations for all nine species were in the predicted
direction, three correlations were significant (P
< 0.05), and two additional species had P-values
between 0.05 and 0.20. A combined probabili-
ties test on all nine species indicated the overall
effect of percent forest cover was significant (P
< 0.02). Here we present data points and re-
gression lines for two of the species with sig-
nificant effects, and two with marginally signif-
icant effects (Fig. 3). For all these species the
highest nest predation rates occurred in land-
scapes with less than 40% forest cover. Given
the high variability in nest predation rates over
both time and space, we believe these results are
indicative of an important relationship even
though some of the correlations were not statis-
tically significant by the conventional criterion.
Two studies have since corroborated the hy-
pothesis that nest predation increases with forest
fragmentation in eastern forests. In a rigorously
designed observational study, Donovan et al.
(1997) tested hypotheses concerning edge and
landscape effects on nest predation and parasit-
ism. They randomly selected 18 landscapes from
three states with high, moderate, or low levels
of fragmentation and determined predation rates
of artificial nests in interior and edge habitat.
12 STUDIES IN AVIAN BIOLOGY NO. 25
0.12'
0.10.
0.08-
0.06-
0.04-
0.02'
o
0.12
0.0
0.08
0.06
0.04
0.02
Wood Thrush
R 2 = 0.54, P=0.02
Indigo Bunting
Ovenbird
R 2 = 0.24, e=0.21
20 40 60 80 100
Kentucky Warbler
ß R 2 = 0.55, P=0.09
20 40 60 80 100
Percent forest cover
FIGURE 3. Relationship of daily nest predation to the amount of forest cover in landscapes defined by a 10-km
radius in the Midwestern United States. Data are from Robinson et al. (1995a).
Predation rates increased with forest fragmen-
tation, and fragmentation (landscape) effects
overwhelmed local edge effects (Fig. 2). Hartley
and Hunter (1998) conducted a meta-analysis of
a set of artificial nest experiments and showed
that predation rates increased as forest cover de-
creased at 5-, 10-, and 25-km scales of forest
cover. Both Donovan et al. (1997) and Hartley
and Hunter (1998) addressed factors at multiple
scales by investigating the interaction between
local edge effects and landscape fragmentation
effects, and we discuss this later under edge ef-
fects.
Many of the previous studies used percent
forest cover in a defined landscape as the inde-
pendent variable. Most, however, used this mea-
sure because it was a convenient index of frag-
mentation, and hypothesized predation and par-
asitism were high in fragmented landscapes as a
result of increases in the abundance of generalist
predators and cowbirds (Donovan et al. 1995b,
Robinson et al. 1995a, Thompson et al. 2000).
Tewksbury et al. (1998) reported levels of
predation at real nests increased with higher
landscape-levels of forest cover. While their re-
sults are contrary to our hypothesis and findings
for eastern forests, nevertheless they found a
landscape effect on nest predation. They be-
lieved the primary predator in their landscape
was the red squirrel (Tamiasciurus hudsonicus),
and red squirrels were more abundant in heavily
forested landscapes. We believe this difference
can be explained by our overall model as a dif-
ference in predator communities resulting from
biogeographic and habitat differences in preda-
tor communities. Another study (Friesen et al.
1999) found relatively high nesting success in a
highly fragmented landscape in Ontario, but it is
not possible to conclude if this difference was
due to annual variation, biogeographic context,
or a lack of generality of the fragmentation ef-
fect.
The effects of landscape composition on pred-
ator abundance and distribution have received
much less attention than patterns in nest success
(Chalfoun et al. 2002). Raccoons (Procyon lo-
tor) and opossums (Didelphis virginiana) reach
their highest densities in highly fragmented
landscapes (Andrn 1992, Dijak and Thompson
2000), potentially because their distributions are
associated with developed and agricultural hab-
itats that are interspersed with forest habitat. In
eastern North America Blue Jays (Cyanocitta
cristata) are significantly more abundant in
highly fragmented landscapes with < 15% forest
cover than in landscapes with moderate or high
forest cover (T M. Donovan, unpubl. data). Ro-
senberg et al. (1999) surveyed occurrence of
FRAGMENTATION IN EASTERN FORESTS--Thompson et al. 13
some potential nest predators along with tanager
species; they generally found positive relation-
ships between predators and fragmentation, but
responses were often region or species specific.
Abundance of some other predator species, how-
ever, may not be affected by forest patterns at a
landscape scale, but by more local habitat effects
such as edge.
PATTERNS OF L^ND COVER ^ND THEIR EFFECT
ON THE ABUNDANCE OF COWBIRDS AND
BROOD PARASITISM
Landscape considerations seem logical for
cowbirds because cowbirds utilize different hab-
itats for feeding and breeding activities in the
midwestern U.S. (Thompson 1994). Cowbirds
generally feed in open grassy or agricultural ar-
eas, whereas breeding resources (hosts) are often
distributed in forested areas (Rothstein et al.
1984, Thompson 1994, Thompson and Dijak
2000). Telemetry studies in Missouri and New
York show that although feeding and breeding
resources can overlap spatially, cowbirds move
between them to optimize the use of each re-
source (Thompson 1994, Hahn and Hatfield
1995). In Missouri, female cowbirds tend to par-
asitize nests in host-rich forests in the early
morning and move to open grassy or agricultural
areas to feed as the day progresses (Thompson
1994, Morris and Thompson 1998, Thompson
and Dijak 2000). Also, cowbirds are common in
hayfields and mowed roadsides in the White
Mountains of New Hampshire, but do not occur
in adjacent forest even though permanent open-
ings and clearcuts exist in the forest (Yamasaki
et al. 2000). Cowbirds are also more abundant
along corridors such as roads that include
mowed grass, than in forest interior in New Jer-
sey (Rich et al. 1994). While the specific habi-
tats used differ, the same landscape relationships
between feeding and breeding habitat exist in
western landscapes (Rothstein et al. 1984). The
probability that a cowbird occurs in a forest,
therefore, depends at least partly upon the prob-
ability that a feeding area is nearby. As areas
become more forested, cowbird breeding oppor-
tunities may increase but feeding opportunities
may decline. Hence, in heavily forested environ-
ments such as the Missouri Ozarks, cowbird
densities are low and parasitism rates of forest
birds have been recorded in the 2-4% range
(Clawson et al. 1997). In contrast, fragmented
agricultural regions can support massive cow-
bird populations that attack the limited number
of forest breeding birds, resulting in parasitism
rates approaching 100%, with high rates of mul-
tiple-parasitism in a single nest (Robinson
1992). In this case, cowbirds are probably not
ß r = -0.72
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
80
70 * ß
4O
30
20
10
ß
0 ß '
0 20 40 60 80 100
% forest cover in landscape
FIGURE 4. Correlation of the amount of forest cover
in a 10-km radius with cowbird relative abundance and
level of brood parasitism in the Midwestern United
States. Data and figures are adapted from Thompson
et al. 2000.
food limited but may be constrained by the num-
ber of available host nests.
Cowbird abundance and levels of parasitism
are closely correlated with landscape statistics
reflecting the amount of forest fragmentation,
the percent of forest cover, and the amount of
potential feeding habitat (agricultural land uses)
in the landscape. For example the number of
cowbirds and level of brood parasitism are both
highly negatively correlated with the amount of
forest cover in a 10-km radius (Fig. 4). Land-
scapes have been defined by 5- to 10-km radii
in these studies (Robinson et al. 1995a, Donovan
et al. 2000, Thompson et al. 2000), which relates
well to the distances most cowbirds commute
between breeding and feeding areas (<5 km;
Thompson 1994, Thompson and Dijak 2000).
Hochachka et al. (1999) combined numerous
data sets from across the United States to test
the generality of the midwestern pattern at two
different spatial scales. They found that increas-
ing amounts of forest cover within 10 km of
study sites was correlated with reduced parasit-
ism rates across the continent. In contrast, when
they analyzed the data using forest cover within
50 km of the study site, they found that increas-
ing forest cover resulted in slightly increased
parasitism rates in sites west of the Great Plains.
14 STUDIES IN AVIAN BIOLOGY NO. 25
Although there are still details that we do not
understand, it appears quite clear that there are
landscape-level effects on cowbird densities that
affect parasitism rates throughout the range of
the Brown-headed Cowbird.
We have suggested that the importance of
landscape composition in limiting cowbird num-
bers is constrained by biogeographic location. Is
there evidence that landscape composition con-
strains the importance of local-scale effects such
as host density, nest concealment, or other fac-
tors? Several studies suggest that cowbirds se-
lect habitats with high host densities (Verner and
Ritter 1983, Rothstein et al. 1986, Thompson et
al. 2000). However, this relationship may de-
pend upon whether landscapes offer both breed-
ing and feeding opportunities for cowbirds. In
Missouri, cowbirds are more abundant in frag-
ments than in contiguous forest with a compar-
atively greater abundance of hosts (Donovan et
al. 2000). We found evidence that cowbird and
host abundances were correlated in fragmented
landscapes, but not in contiguous forest land-
scapes, suggesting that landscape composition
may constrain the influence of local host abun-
dance on local cowbird abundance. If food or
host resources are scarce at the landscape scale,
local habitat characteristics may not explain ei-
ther cowbird abundance or parasitism levels.
Landscape composition may also constrain
the importance of local-scale habitat features
such as edge or patch size in determining cow-
bird numbers and parasitism levels. For exam-
ple, in a heavily forested landscape in Vermont
(94% forest cover), cowbird distribution at the
patch level was best explained by examining one
local-scale habitat characteristic (patch area) and
two landscape-scale habitat characteristics (dis-
tance to the closest opening and the number of
livestock areas [known feeding areas] within 7
km of the patch; Coker and Capen 1995). Sim-
ilarly, in Missouri the distribution of cowbirds
is not as well correlated with patch level statis-
tics such as area or the ratio of perimeter to area,
but by landscape-level measures that encompass
the known daily movements of cowbirds (Don-
ovan et al. 2000).
HABITAT-SCALE EFFECTS
Hypothesis: Habitat-scale factors affect the
probability a nest is depredated or parasitiged
because of effects on predator and cowbird
abundance and activity patterns or nest detect-
ability. The strength of these effects depends on
the biogeographic and landscape context.
Within a given biogeographic and landscape
context, nest predation and brood parasitism
should be related to habitat effects. Species de-
mographics vary among habitats as a reflection
of habitat quality. The question of interest here
is whether there are consistent features or pro-
cesses at the habitat scale, or interactions with
landscape and biogeographic processes that el-
evate predation and parasitism. Several possibil-
ities of habitat effects are patch size, proximity
to edge, forest management, and nest conceal-
ment. These effects have been widely studied,
yet there are substantial gaps in our knowledge
and inability to explain known effects within a
conceptual model. Recent reviews (Martin 1993,
Paton 1994, Robinson and Wilcove 1994, Faa-
borg et al. 1995, Heske et al. 2001) have ad-
dressed these topics to various degrees. Here we
address edge and forest management effects and
how they fit within our general model.
EDGE EFFECTS
Edge effects are not uniform within or among
regions (cf. Bolger this volume). Many studies
show no edge effects or only such effects very
close (<50 m) to edges (Paton 1994, Hartley and
Hunter 1998). Parasitism levels remain high in
forest far from edge in some landscapes (Marini
et al. 1995, Thompson et al. 2000), and in at
least one landscape parasitism in forest declined
gradually from 70% to 5% over a gradient of
1500 m from an agricultural edge (Morse and
Robinson 1999).
At least four hypotheses have been suggested
for higher predation rates near edges: (1) pred-
ators may be attracted to edges because of abun-
dant prey (a functional response; e.g., Gates and
Gysel 1978, Ratti and Reese 1988); (2) predator
density may be greater near edges than in forest
interiors (a numerical response; e.g., Bider 1968,
Angelstam 1986, Pedlar et al. 1997); (3) the
predator community may be richer near edges
(Bider 1968, Temple and Cary 1988, Marini et
al. 1995); and (4) predators may forage along
travel lanes such as edges (Gates and Gysel
1978, Yahner and Wright 1985, Small and Hunt-
er 1988, Marini et al. 1995).
Results of edge-effects studies have been in-
consistent and comparisons among studies have
been confounded by lack of experimental con-
trol of landscape or habitat context, differences
in predator communities, and methodological bi-
ases. Problems associated with artificial nests
exist (e.g., nest appearance, lack of parental and
nestling activity), but even the types of eggs
used in artificial nests may bias results. Large
eggs (i.e., quail or chicken) exclude predation
by some small predators and predation rates are
greater when small eggs are used (Haskell
1995a, DeGraaf and Maier 1996). Lack of a
mechanistic approach that addresses hypotheses
for why predation should be higher near edges
FRAGMENTATION IN EASTERN FORESTS--Thompson et al. 15
has also hampered research. A more mechanistic
approach requires studies of predator activities
or abundances, not just nest predation patterns.
Equally variable are the results of nest place-
ment studies (i.e., ground vs. shrub/elevated
nests). Major and Kendal (1996) reported higher
predation at elevated nests in six studies, higher
predation at ground nests in four studies, and
equal predation rates in three studies. Ground
nests containing Japanese Quail (Coturnix spp.)
and plasticine eggs exhibited increased preda-
tion along farm edge and interior in Saskatche-
wan, but there were no detectable differences in
predation rate between ground and shrub nests
in logged edge, in logged interior, or in contig-
uous forest (Bayne and Hobson 1997). Although
two studies in the northeastern U.S. did not de-
tect any difference in predation rates between
ground and shrub nests (Vander Haegan and
DeGraaf 1996, Danielson et al. 1997), DeGraaf
et al. (1999) found a strong placement effect
(high predation on ground nests) using small
eggs, as did Marini et al. (1995).
Our perspective on edge effects is from stud-
ies in eastern forests that largely investigated
predation of forest bird nests by medium sized
mammals such as raccoons and opossums, and
corvids such as Blue Jays and American Crows
(Corvus brachyrhynchos). Based on our studies
and others, we offer two predictions that may
help account for the variability among previous
studies.
Edge effects are dependent on landscape and
habitat context
The importance of landscape context is
emerging as perhaps one of the few generalities
that can be made concerning edge effects. Our
hypothesis is that the occurrence of local edge
effects is dependent on landscape composition
and pattern because of dependence of predators
and cowbirds on landscape-level factors. Some
evidence exits to support this hypothesis. Edge
effects tend not to exist in mostly forested land-
scapes (Heske 1995, Marini et al. 1995, Bayne
and Hobson 1997, Hartley and Hunter 1998,
DeGraaf et al. 1999, Chalfoun et al. 2002).
Some level of forest fragmentation is necessary
to support high numbers of generalist predators
in eastern forests. At moderate levels of frag-
mentation elevated predation rates will be lim-
ited to edges because predators depend on ag-
ricultural habitats or human settlements. At ex-
treme levels of fragmentation all forest habitat
is within close proximity to these habitats and
predation is high throughout the forest. We be-
lieve edge effects are a result of increases in
abundance of predators due to landscape effects
(fragmentation) and activity patterns of preda-
tors in fragmented landscapes (Andrn 1995,
Chalfoun et al. 2002).
As previously discussed, Donovan et al.
(1997) directly tested this hypothesis with a rig-
orous field experiment using artificial nests, and
found strong support for it. Hartley and Hunter
(1998) detected the same effects in a meta-anal-
ysis of artificial nest studies. In a different meta-
analysis Chalfoun et al. (2002) determined that
predator responses to edges, patch size, or frag-
mentation were not independent of landscape
context. Predator abundance or activity was re-
lated to edge, patch area, or fragmentation in
66.7% of tests when adjacent land use was ag-
ricultural, 5.6% when forest, 16.7% when grass-
land, 5.6% when clearcut forest.
In addition to the effect of landscape context
on predator abundance, landscape and habitat
contexts also affect the species of predators pre-
sent. The variability in results among studies of
egg predation may reflect diflrences in nest
predator communities or the abundance of par-
ticular species in study areas (e.g., Picman
1988). For example, in New England Blue Jays
and raccoons were predominant predators of ar-
tificial nests in suburban forests, whereas fishers
(Mattes pennanti) and black bears (Ursus amer-
icanus) were important in extensive forest
(DeGraaf 1995, Danielson et al. 1997), and no
avian nest predators were detected in the inte-
riors of extensive forest (DeGraaf 1995).
Attempts to identify egg predators include
characterizations of predation remains of real
eggs (Gottfried and Thompson 1978; but see
Marini and Melo 1998), impressions in plasti-
cine (Bayne et al. 1997) and clay eggs (Donovan
et al. 1997), hair catchers (Baker 1980), and re-
motely triggered cameras (DeGraaf 1995). The
most promising technique, however, may be the
use of subminiature video cameras with infrared
illumination at real nests (Thompson et al. 1999,
Bolger this volume). For example, F. Thompson
and D. Burhans (pers. comm.) used this tech-
nique and determined 85% of nest predation
events in old fields were by snakes, whereas
60% of predation events in forests were by rac-
coons.
Not all edges are the same
We suggest that negative edge effects are
most likely to occur where land-use patterns or
topography concentrate activities of predators,
and are therefore a functional response by pred-
ators. Edge effects are most likely to occur
where forest abuts habitats that provide key re-
sources for predators. Agricultural edges gener-
ally have stronger edge effects than other types
of edge (e.g., regenerating forest, grassland) on
nesting success (Hanski et al. 1996, Hawrot and
16 STUDIES IN AVIAN BIOLOGY NO. 25
Neimi 1996, Darveau et al. 1997, Hartley and
Hunter 1998, Marzluff and Restani 1999, Morse
and Robinson 1999; but see King et al. 1996,
Suarez et al. 1996) and on predators (Chalfoun
et al. 2002). Differences in results among studies
likely are due at least partly to differences in
habitat use among predators.
In one of the few studies of predator distri-
butions relative to edges, Dijak and Thompson
(2000) showed that raccoons respond differently
to different edge types. Raccoon activity was
significantly greater in forest adjacent to agri-
cultural fields and riparian areas than in forest
adjacent to roads, clearcuts, or forest interior.
Studies of raccoon foraging behavior show that
the degree of nest cover is much less important
than local habitat heterogeneity in preventing
depredation (Bowman and Harris 1980). In Illi-
nois Blue Jays used edges differently and pre-
ferred gradual shrubby edges (J. Brawn, unpubl.
data). Avian predators were more abundant in
forest-dividing corridors composed of shrub-
sapling vegetation than grass in New Jersey
(Rich et al. 1994). Heske (1995), however, found
no significant difference in predator activity ad-
jacent to and >500m from edges. Recent work
in New England oak forests showed that six spe-
cies of small mammals represented 99% of cap-
tures at both forest edge and interior and their
abundance and nest predation rates did not differ
between edge and interior (DeGraaf et al. 1999).
We believe these differences in edge effects are
a result of differences in predator species, type
of edge, and landscape context.
SILvICULTURAL PRACTICES
Silvicultural practices such as tree harvest and
regeneration of stands (habitat patches) dramat-
ically affect habitat scale characteristics. Bird
communities can change greatly in response to
these practices, and balancing the needs of spe-
cies with diverse habitat needs in managed for-
ests is a challenge for land managers and plan-
ners (see review by Thompson et al. 1995). Here
we focus on two aspects of silvicultural practices
that are related to concerns for forest fragmen-
tation: fragmentation of old forests by young
forests, and creation of edges between old and
young forests.
Fragmentation of mature forest by young
forest
Fragmentation of mature forest by young for-
est created by timber harvest has raised conser-
vation concerns because of the loss of mature
forest habitat and potential fragmentation ef-
fects. Both even-aged forest management and
uneven-aged forest management result in chang-
es in the bird community (Thompson et al. 1992,
Annand and Thompson 1997, Robinson and
Robinson 1999). These changes in the bird com-
munity can be interpreted as good or bad de-
pending on management objectives. Habitat
needs of forest breeding birds need to be ad-
dressed by identifying conservation objectives
and then evaluating the effects of land manage-
ment practices on these. Young forests in the
East provide habitat for at least some species
acknowledged as management priorities (e.g.,
Kirtland's Warbler [Dendroica kirtlandii], Prai-
rie Warbler [Dendroica discolor], Golden-
winged Warbler [Vermivora chrysoptera]);
therefore the needs of early and late successional
species need to be addressed in forest manage-
ment plans.
We are aware of no evidence in eastern forests
that fragmentation of mature forest by young
forest creates the type of negative fragmentation
effects that fragmentation by agricultural or de-
veloped land uses do. We have suggested that
cowbirds and generalist predators benefit from
interspersion of agricultural and developed land
use in forests because they provide rich food
sources, but this would not seem to apply to
young forests. For example, in extensively for-
ested northern New England, predation rates on
artificial ground and shrub nests were not dif-
ferent among timber size-classes (DeGraaf and
Angelstam 1993). Likewise, predation rates on
artificial ground and shrub nests were similar in
managed and reserved large forest blocks
(DeGraaf 1995).
Edge eJfkcts between mature and young forest
Not many studies have directly addressed
edge effects in managed eastern forests. The ev-
idence for edge effects between mature forest
and recently harvested stands is highly variable
and suggests results vary locally. In a study of
Ovenbird (Seiurus aurocapillus) reproductive
success in northern New Hampshire in relation
to clearcutting (King et al. 1996), nests, territo-
ries, and territorial males obtaining mates were
equally distributed in edge (0-200 m) and inte-
rior (201-400 m) mature forest. Nest survival
was higher in forest interior in year 1, but not
in year 2. The proportion of pairs fledging at
least one young, fledgling weight, and fledgling
wing-chord did not differ between edge and in-
terior in either year, nor did the number of young
fledged per pair. In another study artificial nests
were placed in edge areas (0-5 m from edges)
and interior areas (45-50 m from edges) adja-
cent to clearcuts and groupcuts. The probability
of a nest being depredated was higher in edge
than interior, and was independent of nest con-
cealment, nest height, or whether adjacent to
clearcuts or group-selection cuts (King et al.
FRAGMENTATION IN EASTERN FORESTS--Thompson et al. 17
1998). In Illinois forest predation of Kentucky
Warbler (Oporornis formosa) nests was not re-
lated to clearcut edges (Morse and Robinson
1999). Nest predation, however, was significant-
ly higher in clearcuts than adjacent older forests,
suggesting differences in vegetation structure
were important while edge was not. Edge effects
can differ among species nesting in the same
habitat patch as well. Woodward et al. (2001)
determined that nest success of songbirds nest-
ing in regenerating forests and cedar glades var-
ied with distance to mature forest edge, but that
patterns were different among species and did
not generally increase monotonically with dis-
tance from edge.
Given that edge effects seem to vary locally
it is important to remember the top down nature
of our model. Landscape level fragmentation of
forests by habitats that elevate predator and
cowbird numbers is likely a more important de-
terminant of nest success at a population level
than are local edge effects. While some studies
have demonstrated edge effects, no studies have
shown a population-level effect on viability.
POPULATIONS ARE STRUCTURED AS
SOURCES AND SINKS
Hypothesis: Top-down spatial constraints lim-
it reproductive success in some fragmented
landscapes in the Midwest to the point where
populations in such landscapes will either de-
cline to extinction or will persist as part of a
larger, source-sink system The presence of sink
populations may or may not be a detriment to
the larger population, depending on the amount
of sink habitat in the landscape and to what de-
gree individuals select sink habitat for breeding.
AT A POPULATION SCALE, SINKS EXIST IN
HIGHI. Y FRAGMENTED HABITATS
Source-sink theory (Pulliam 1988) has be-
come a popular framework for describing the
population dynamics of organisms that are af-
fected by habitat fragmentation. Pulliam (1988)
used models based on births, immigration,
deaths, and emigration (BIDE models; Cohen
1969, 1971) to describe geographic subpopula-
tions that are connected by dispersal. All sub-
populations contribute individuals that make up
the greater population, or the entire source-sink
system. At equilibrium, a subpopulation is a
source when B > D and E > I; and is a sink
when B < D but E < I. The greater population
is at dynamic equilibrium (not changing) when
B (all the births) + I (all the immigrants from
outside the greater population) - D (all the
deaths) - E (all the emigrants that leave the
greater population) = 0. If habitat fragmentation
subdivides populations into more or less inde-
pendent breeding subpopulations, then source-
sink structure may be an appropriate demo-
graphic model.
Is there any evidence that forest passerines
exhibit source-sink population structure that is
linked to the degree of habitat fragmentation?
Several field studies document that reproductive
success of neotropical migrant birds varies
across a species' range (Probst and Hayes 1987,
Robinson et al. 1995a), but few studies examine
the interaction of subpopulations from a source-
sink viewpoint. One must know the BIDE pa-
rameters of each subpopulation to evaluate
source-sink dynamics. Measurement of these pa-
rameters is extremely field intensive and poten-
tially unachievable with current techniques be-
cause of the dispersal capabilities of birds. Sur-
veys of bird abundance may not be capable of
establishing source-sink status (Brawn and Rob-
inson 1996).
Most empirical studies documenting sink pop-
ulations use nesting data and mortality data from
the subpopulation, and model population persis-
tence over time in the absence of immigration
or emigration (Ricklefs 1973, King and Mewaldt
1987, Stacey and Taper 1992, Pulliam and Dan-
ielson 1991, Donovan et al. 1995b). Without im-
migration, sink populations decline over time
and go extinct. With immigration, however,
sinks can persist with no detectable declines in
numbers over time (Pulliam 1988).
What evidence is there, then, that birds are
structured as sources and sinks, and that source-
sink status is related to level of landscape-scale
fragmentation? The evidence is very weak at
this time, in part because we do not yet know
the geographic scale that encompasses dispersal
movements among sources and sinks. However,
there is evidence that reproductive success in
fragmented landscapes is too low to compensate
for adult mortality (e.g., Donovan et al. 1995b,
Trine 1998), and that dispersal occurs among
habitat patches. For example, Trelease Woods is
an isolated woodlot in central Illinois where bird
populations have been censused since 1927
(Kendeigh 1982). In most years, several breed-
ing pairs of Wood Thrush occurred in the wood-
lot, but three extinction events were recorded
that were followed by three colonization events,
suggesting that the colonists of unknown origin
were not produced locally (Brawn and Robinson
1996).
Although direct evidence to support source-
sink structure is weak, predictions generated
from population modeling may offer some sup-
porting evidence. Source-sink models suggest
that sinks should show relatively higher year to
year variation in abundance than source popu-
lations (Davis and Howe 1992). As predicted,
18 STUDIES IN AVIAN BIOLOGY NO. 25
recent empirical studies demonstrate that popu-
lations in fragmented landscapes have greater
annual variation than populations in continuous
landscapes, which may also affect turnover rates
and local extinction (Boulinier et al. 1998).
However, it is still unclear whether such vari-
ability is due to local processes (such as vari-
ability in source-sink status over time), to
source-sink dispersal dynamics, or other causes.
THERE IS NO EVIDENCE THAT SINKS OR EDGES
FUNCTION AS ECOLOGICAL TRAPS AT A
LOCAL SCALE
Although reproductive and survival rates are
too low to maintain numbers in sinks, these hab-
itats may benefit the greater source-sink system
by "housing" a large number of individuals at
any given time. Additionally, a significant num-
ber of young may be produced in low-quality
habitats, depending on the number of individuals
breeding there (Pulliam 1988, Howe et al. 1991).
Is there evidence, however, that maintenmce
of sink habitat is a detriment to population per-
sistence? Animals often have the opportunity to
select among a variety of habitats that vary in
quality; preferred habitats are those that are se-
lected disproportionately to other available habi-
tats (Johnson 1980). If individuals avoid low-
quality areas, the presence of low-quality habitats
may not negatively influence population persis-
tence. However, if individuals select low-quality
habitats over available, high-quality habitats for
reproduction and survival, then low-quality hab-
itats may function as ecological traps, and their
presence may lead to population extirpation
(Gates and Gysel 1978, Ratti and Reese 1988,
Pulliam md Dmfielson 1991).
Edges have been suggested to be an ecologi-
cal trap because they are potentially food rich
and have high abundances and diversity of birds,
which in turn potentially attract predators
searching for food-rich areas (Gates and Gysel
1978, Ratti and Reese 1988). Woodward et al.
(2001) examined the ecological trap hypotheses
for several species of shrubland-nesting song-
birds, and while nesting success varied with dis-
tance to edge, they found no evidence that edges
acted as ecological traps. Observations of high
densities of Wood Thrushes in fragmented Mid-
west landscapes (Donovan et al. 1995b) have led
us to speculate that fragments are similarly act-
ing as traps. High densities of birds in poor-qual-
ity fragmented landscapes and low densities in
high-quality contiguous landscapes may be the
result of: (1) absence of suitable habitat features
such as nest sites in contiguous landscapes; (2)
displacement of individuals from high quality
contiguous landscapes through interspecific
competition; or (3) innate preference for habitat
characteristics that more commonly occur in
fragmented landscapes, such as edge.
Population models suggest that when individ-
uals in the population selected high- and low-
quality habitats in proportion to habitat avail-
ability in the landscape, landscapes could con-
tain up to 40% low-quality habitat and still pro-
mote population persistence. However, when
individuals preferred low-quality habitats over
high-quality habitats, populations on landscapes
containing > 30% low-quality habitat were ex-
tirpated, and the low-quality habitat functioned
as an ecological trap (Donovan and Thompson
2001). Clearly, much more work is needed to
determine the effect of sink habitats on popula-
tion persistence.
POPULATIONS STRUCTURED AS SOURCES AND
SINKS CAN GROW OR DECLINE
Populations structured as sources and sinks
can grow or decline depending on the amount
of sink habitat, the selection and use of sinks for
breeding, and the magnitude of spatial and tem-
poral variation in demographic parameters. It is
critical that we examine how our observations
of reduced fecundity or density in fragmented
landscapes may impact population trends of a
source-sink system. We believe our observations
of correlations between nesting success and for-
est cover at the landscape level in the Midwest
(e.g., Robinson et al. 1995a) have been uncriti-
cally cited as strong evidence that habitat frag-
mentation causes bird populations to decline.
The negative correlation between fragmentation
and nesting success offers support for the hy-
pothesis that fragmentation of breeding habitat
is causing declines in some songbird population.
No one, however, has attempted to evaluate the
number of source and sink populations and their
effect on a regional population.
For example, Ovenbirds in the Midwest U.S.
are thought to be impacted by habitat fragmen-
tation in several ways: they are area-sensitive
(Hayden et al. 1985, Burke and Nol 1998), their
pairing success on fragments is often signifi-
cantly lower compared with larger, contiguous
patches (Gibbs and Faaborg 1990, Villard et al.
1993), and they have higher daily nest-mortality
and parasitism levels in fragments compared
with larger patches (Donovan et al. 1995b, Rob-
inson et al. 1995a). Yet, Breeding Bird Survey
data suggest that Ovenbirds are maintaining
numbers and even increasing in many areas in
the Midwest (Sauer et al, 1997). Overall popu-
lation growth (the growth rate of the entire
source-sink system on the landscape) may not
be impacted by the poor reproductive success of
birds in fragments if breeding individuals gen-
erally avoid small patches or if the landscape is
FRAGMENTATION IN EASTERN FORESTS--Thompson et al. 19
dominated by larger patches that are used for
breeding.
We have used modeling approaches to test
how landscape composition, habitat selection,
and nesting success interact to produce popula-
tion increases or declines at a regional scale
(Donovan and Lamberson 2001). The model
combined (1) the frequency distribution of patch
sizes in the landscape (e.g., highly fragmented
landscapes vs. continuously forested land-
scapes), (2) the distribution of individuals across
the range of patches in the landscape (e.g., area
sensitive vs. area insensitive vs. edge distribu-
tion patterns), and (3) the fecundity of individ-
uals as a function of patch size in the landscape
(e.g., fragmentation effects on fecundity vs. no
fragmentation effects on fecundity). We used
this model to examine population growth under
various landscape, distribution, fecundity, and
survival scenarios.
Results from the model indicate that the high-
ly cited observation that fecundity decreases as
patch size decreases does not necessarily cause
landscape level population declines in songbirds.
When total habitat in the landscape is held con-
stant, reduced fecundity associated with patch
size could lead to population declines when
landscapes are highly fragmented, or when land-
scapes are more continuous, but individuals oc-
cur in high densities in small patches and low
densities in large patches. Thus, when land-
scapes offer both large and small patches for
breeding (a more contiguous landscape), area-
sensitive species can maintain population sizes
in spite of decreased fecundity in small patches
because birds achieve their highest densities in
patches where fecundity is greatest, and high re-
production in such source habitats can maintain
sinks within the landscape (Donoran and Lam-
berson 2001). Two recent large scale analyses of
Breeding Bird Survey data have linked popula-
tion change to fragmentation. Donoran and
Flather (2002) found a significant negative cor-
relation between the proportion of a population
occupying fragmented habitat and population
trend. Boulinier et al. (2001) found that richness
of forest area-sensitive species was lower, and
year-to-year rates of local extinction higher, on
Breeding Bird Survey routes surrounded by
landscapes with lower mean forest-patch size.
RESEARCH AND CONSERVATION
IMPLICATIONS
We believe there is adequate corroborative ev-
idence for this multi-scale approach to fragmen-
tation to use this as a working model for re-
search and conservation. We believe one of the
most important conclusions from our work in
eastern forests is that landscape composition is
an important determinant of reproductive suc-
cess, even at a local scale. In eastern forests
where concerns are focused on the effects of
cowbird parasitism and on generalist predators
associated with agricultural and other human-
dominated land uses, fragmentation of forests
and a reduction in the amount of forest in the
landscape results in increased levels of predation
and parasitism. Future research should directly
test our hypotheses of top-down constraints on
reproductive success as well as hypothesized
mechanisms for effects at each scale. Research
should address the larger scale context of studies
and potential differences among predators.
There is already evidence that landscape level
effects of fragmentation differ between the west-
ern and eastern United States (Tewksbury et al.
1998), which is further indication of the impor-
tance of top-down constraints and a multi-scale
approach.
This model has important conservation impli-
cations as well. The importance of large-scale
effects suggests that at high levels of fragmen-
tation, conservation efforts should be focused on
restoration of the landscape matrix and a reduc-
tion in fragmentation. At some level, where the
landscape-level effects of fragmentation are no
longer critical, local habitat management prac-
tices become important. Local management con-
siderations could include management practices
to provide appropriate habitat types, minimize
edge, or manage habitat structure. Finally, while
we believe fragmentation is a major conserva-
tion issue in eastern forests, we caution that not
all fragmentation needs to be mitigated. Frag-
mentation of one habitat provides other habitats,
and source-sink dynamics suggest that some
proportion of a population can reside in sink
habitat. A challenge for researchers, land man-
agers, and policy-makers is to determine when
fragmentation at a regional or population level
is severe enough to drive population declines,
and to balance competing species conservation
objectives and land use.
ACKNOWLEDGMENTS
We thank the numerous graduate students, techni-
cians, colleagues, and supporting agencies who have
assisted or supported the work that led to the ideas
presented in this paper.
Studies in Avian Biology No. 25:20-29, 2002.
WHAT IS HABITAT FRAGMENTATION?
ALAN B. FRANKLIN, BARRY R. NOON, AND T. LUKE GEORGE
Abstract. Habitat fragmentation is an issue of primary concern in conservation biology. However,
both the concepts of habitat and fragmentation are ill-defined and often misused. We review the habitat
concept and examine differences between habitat fragmentation and habitat heterogeneity, and we
suggest that habitat fragmentation is both a state (or outcome) and a process. In addition, we attempt
to distinguish between and provide guidelines for situations where habitat loss occurs without frag-
mentation, habitat loss occurs with fragmentation, and fragmentation occurs with no habitat loss. We
use two definitions for describing habitat fragmentation, a general definition and a situational definition
(definitions related to specific studies or situations). Conceptually, we define the state of habitat frag-
mentation as the discontinuity, resulting from a given set of mechanisms, in the spatial distribution of
resources and conditions present in an area at a given scale that affects occupancy, reproduction, or
survival in a particular species. We define the process of habitat fragmentation as the set of mechanisms
leading to that state of discontinuity. We identify four requisites that we believe should be described
in situational definitions: what is being fragmented, what is the scale of fragmentation, what is the
extent and pattern of fragmentation, and what is the mechanism causing fragmentation.
Key Words: forest fragmentation; habitat; habitat fragmentation; habitat heterogeneity.
Habitat fragmentation is considered a primary
issue of concern in conservation biology (Meffe
and Carroll 1997). This concern centers around
the disruption of once large continuous blocks
of habitat into less continuous habitat, primarily
by human disturbances such as land clearing and
conversion of vegetation from one type to an-
other. The classic view of habitat fragmentation
is the breaking up of a large intact area of a
single vegetation type into smaller intact units
(Lord and Norton 1990). Usually, the ecological
effects are considered negative (Wiens 1994). In
this paper, we propose that this classic view pre-
sents an incomplete view of habitat fragmenta-
tion and that fragmentation has been used as
such a generic concept that its utility in ecology
has become questionable (Bunnell 1999a).
In attempting to quantify the effects of habitat
fragmentation on avian species, there is consid-
erable confusion as to what habitat fragmenta-
tion is, how it relates to natural and anthropo-
genic disturbances, and how it is distinguished
from terms such as habitat heterogeneity. Here,
we attempt to provide sufficient background to
define habitat fragmentation adequately and, as
a byproduct, habitat heterogeneity. This paper
was not intended as a complete review of the
existing literature on habitat fragmentation but
merely as a brief overview of concepts that al-
lowed us to arrive at working definitions.
There are two ways to define habitat frag-
mentation. First, there is a conceptual definition
that is sufficiently general to include all situa-
tions. We feel a conceptual definition is needed
for theoretical discussions of habitat fragmenta-
tion. Second, there is a situational definition that
relates to specific studies or situations. In this
paper, we review current definitions and offer a
revised conceptual definition of habitat fragmen-
tation. In addition, we propose four requisites
for building situational definitions of habitat
fragmentation: (1) what is being fragmented, (2)
what is the scale(s) of fragmentation, (3) what
is the extent and pattern of fragmentation, and
(4) what is the mechanism(s) causing fragmen-
tation. To define habitat fragmentation, it is first
necessary to review current understanding of
how habitat is defined, and to contrast fragmen-
tation and heterogeneity.
FRAGMENTATION--THE HABITAT
CONCEPT
Prior to understanding fragmentation of hab-
itat, the term habitat must be properly defined
and understood. Habitat has been defined by
many authors (Table 1) but has often been con-
fused with the term vegetation type (Hall et al.
1997; see Table 1). As Hall et al. (1997) point
out, habitat is a term that is widely misused in
the published literature. The key features of the
definitions of habitat in Table I are that habitat
is specific to a particular species, can be more
than a single vegetation type or vegetation struc-
ture, and is the sum of specific resources needed
by a species. Habitat for some species can be a
single vegetation type, such as a specific seral
stage of forest in a region (e.g., old forest in Fig.
1 a). This might be the case for an interior forest
species where old forest interiors provide all the
specific resources needed by this species. How-
ever, habitat can often be a combination and
configuration of different vegetation types (e.g.,
meadow and old forest in Fig. lb). In the ex-
ample shown in Figure lb, a combination of old
forest and meadow are needed to provide the
specific resources for a species. Old forest may
2O
WHAT IS HABITAT FRAGMENTATION?--Franklin et al. 21
¸
¸
22
STUDIES IN AVIAN BIOLOGY NO. 25
POOR
Old forest
Meadow
Non-habitat
e,, IG m
FIGURE 1. Example of habitat represented as (a) a single vegetation type, (b) a mosaic of different vegetation
types, and (c) different mosaics of vegetation types representing different degrees of habitat quality.
provide some resources necessary for survival,
whereas meadow might provide resources nec-
essary for reproduction.
In addition to considering habitat versus non-
habitat (the intervening matrix), habitat can have
a gradient of differing qualities (Van Horne
1983) where habitat quality is defined as the
ability of the environment to provide conditions
appropriate for individual and population persis-
tence (Hall et al. 1997). The idea that habitat
can be a specific combination and configuration
of vegetation types can be extended further to
different combinations and configurations rep-
resenting different levels of habitat quality (Fig.
lc). Poor habitat quality may result from too
much of one vegetation type relative to another.
Returning to the example from Figure lb, too
much meadow may provide sufficient resources
for reproduction, but not enough for survival
(Fig. lc). Habitat quality is influenced by the
mix and configuration of the two vegetation
types (Fig. lc).
An important consideration in both defining
and understanding habitat fragmentation is that
it ultimately applies only to the species level be-
cause habitat is defined with reference to a par-
ticular species. Habitat is proximately linked to
communities and ecosystems only because these
levels are composed of species. There is no con-
cept of community or ecosystem habitat. For ex-
ample, one cannot take a vegetation map and
assess habitat fragmentation without reference to
a particular species. Therefore, habitat fragmen-
tation must be defined at the species level and
those levels below (e.g., populations and indi-
viduals within species).
FRAGMENTATION VERSUS HETEROGENEITY
Based on existing definitions (Table 1), frag-
mentation can be viewed as both a process (that
which causes fragmentation) and an outcome
(the state of being fragmented; Wiens 1994).
The definitions in Table 1 suggest that fragmen-
tation represents a transition from being whole
to being broken into two or more distinct pieces.
The outcome of fragmentation is binary in the
sense that the resulting landscape is assumed to
be composed of fragments (e.g., forest) with
something else (the non-forest matrix) between
the fragments. In contrast, heterogeneity implies
a multi-state outcome from some disturbance
process. For example, contiguous old-growth
forest can be transformed into a mosaic of dif-
ferent seral stages by some disturbance such as
fire (e.g., Fig. lb). If each seral stage, as viewed
by a species, is a distinct habitat, then the result
of the disturbance is an increase in habitat het-
erogeneity. In addition, if habitat is a combina-
WHAT IS HABITAT FRAGMENTATION?--Franklin et al. 23
tion of different vegetation types, then hetero-
geneity in vegetation types may influence habitat
quality (e.g., Fig. lc), but does not represent
fragmentation.
Habitat fragmentation is heterogeneity in its
simplest form: the mixture of habitat and non-
habitat. However, the effects of habitat fragmen-
tation is also dependent on the composition of
non-habitat. The matrix of non-habitat may have
a positive, negative, or neutral effect on adjacent
habitat. For example, non-habitat consisting of
agricultural fields may have a very different ef-
fect than non-habitat consisting of younger for-
est. The key point is whether intervening non-
habitat affects the continuity of habitat with re-
spect to the species. We argue that habitat frag-
mentation has not occurred when habitat has
been separated by non-habitat but occupancy, re-
production or survival of the species has not
been affected. Under this argument, key com-
ponents in defining habitat fragmentation are
scale, the mechanism causing separation of hab-
itat from non-habitat (i.e., the degree to which
connectivity is affected), and the spatial arrange-
ment of habitat and non-habitat. For example, a
narrow road dividing a large block of habitat
may not affect occupancy, reproduction or sur-
vival for a wide-ranging species, such as a rap-
ton However, the road may affect a species with
a narrower range, such as a salamander. Thus,
fragmentation is from the species' viewpoint and
not ours. We discuss these points in more detail
further on.
The analogy of habitat fragmentation as
equivalent to the breaking of a plate into many
pieces (Forman 1997:408)is of limited utility.
First, habitat fragmentation generally occurs
through habitat loss; unlike the broken plate, the
sum of the fragments is less than the whole. For
example, in a uniform landscape composed en-
tirely of a single habitat, fragmentation is only
possible if accompanied by habitat loss. Thus,
fragmentation usually involves both a reduction
in area and a breaking into pieces (Bunnell
1999b). Second, the transition from being whole
to being in pieces may lead to a change in qual-
ity of one or more of the fragments if habitat
quality is a function of fragment size. For ex-
ample, fragmentation of continuous forest (ac-
companied by an inescapable reduction in forest
area) may change the quality of the fragments;
habitat quality may increase for edge species
and decrease for forest interior species (Bender
et al. 1998).
When the effects of habitat loss and fragmen-
tation are addressed independently, habitat loss
has been suggested as having the greatest con-
sequences to species viability (e.g., McGarigal
and McComb 1995, Fahrig 1997). This obser-
vation led Fahrig (1999) to suggest the need to
distinguish three cases: (1) habitat loss with no
fragmentation; (2) fragmentation arising from
the combined effects of habitat loss and break-
ing into pieces; and (3) fragmentation arising
from the breaking apart but with no loss in hab-
itat area. These three cases are illustrated in Fig-
ure 2. It is possible to illustrate these cases with
reference to a common landscape only if the ref-
erence landscape is composed of at least one
habitat and a surrounding matrix within the
bounded landscape (Fig. 2). This occurs because
case (3) requires the ability to shift the location
of the focal habitat within the landscape bound-
aries. If there was no matrix within the land-
scape boundaries (e.g., the landscape was com-
posed entirely of the single habitat), then only
cases (1) and (2) in Fig. 2 would apply.
The possibilities illustrated in Fig. 2 are not
artificial constructs. Conservation planning usu-
ally occurs in a context of habitat mosaics with
a diversity of land uses and land ownerships. As
such, case 3 is a common result of conservation
tradeoffs. For example, wetland mitigation in the
U.S. often requires no net loss in wetland area
but allows a change in the spatial pattern and
location of wetlands. Thus, it is possible to break
one large wetland into two or more pieces, mit-
igate this loss somewhere else on the landscape
by creating additional wetlands, and claim no
net loss in area.
Fragmentation arising from habitat loss un-
avoidably leads to an increase in heterogeneity
in habitat quality because the fragments may un-
dergo a change in state either directly (through
conversion) or indirectly through edge effects
(see Bolger this volume, Sisk and Batten this
volume). In light of the previous discussion, this
possibility suggests that we need another case in
addition to those discussed by Fahrig (1999).
This case (case 4 in Fig. 2) includes changes in
the spatial pattern of a habitat that are, or are
not, accompanied by a change in the quality of
the habitat. Case (4) would occur as a byproduct
of case (2) depending on the habitat require-
ments of the species in question.
We attempt to capture these differences in
outcome in a dichotomous flow diagram (Fig.
3). Following the diagram from top to bottom
requires the investigator to answer a series of
questions: "Has there been a reduction in area
of the focal habitat? .... Has there been a change
in spatial continuity of the habitat? .... Has there
been a change in quality of the focal habitat?"
Answering this progression of questions allows
one to discriminate habitat loss from fragmen-
tation, and to recognize cases where habitat
quality has changed.
A final point is that fragmentation of vegeta-
24 STUDIES IN AVIAN BIOLOGY NO. 25
Original habitat boundary /'1 i __ ',
................... Landscape boundary/i ! _ _ _
Original Landscape / [,/ ...... "/ I L __
with Focal Habitat | .a.ja.t/"'x,
1. Habitat loss +
no fragmentation
2. Habitat loss +
fragmentation
3. No habitat loss +
fragmentation
4. Habitat loss +
fragmentation +
change in habitat quality
FIGURE 2. Four cases illustrating the relationship between habitat loss, habitat fragmentation, and change in
habitat quality in a bounded landscape.
tion type and habitat fragmentation are often
considered synonymous (e.g., the definition by
Faaborg et al. (1993) in Table 1). However, the
extent and effects of fragmentation can be very
different when habitat is considered a single
vegetation type or a combination of vegetation
types (Fig. 4). Starting with the landscape in
Figure 4, forest fragmentation would only be
I Contiguous Habitat
Area Reductin?
YES Aea Re] NO
I
Ch; in Spatial Continuity?) (chane in Spatial Continuity?)
YES NO NO
ß YES i
Fragmented I Habitat I Fragmented I I Contiguous
(in Quality?) (in Ouality?/ inQ
YES NO YES % NO YES NO
Habitat Loss Habitat Loss Habitat Loss Habitat Loss Fragmentation Fragmented
+ + + + Habitat
Fragmentation Fragmentation Change in Quality Change in Quality
+
Change in Quality
FIGURE 3. Flow diagram to differentiate between landscapes experiencing habitat loss, habitat fragmentation,
and changes in habitat quality.
WHAT IS HABITAT FRAGMENTATION?--Franklin et al. 25
I Old forest
Forest Fragmentation
Meadow
Habitat Fragmentation
i .ance
FIGURE 4. Schematic differences in forest fragmentation and habitat fragmentation in a landscape composed
of a habitat consisting of two vegetation types (old forest and meadow).
considered as habitat fragmentation for a species
whose habitat was solely defined as interior old
forest (a single vegetation type). However, for
the hypothetical example used previously where
a species' habitat is composed of two vegetation
types (meadow and old forest), habitat fragmen-
tation would occur when some disturbance (such
as a flood) disrupted the continuity in the con-
figuration of these two vegetation types (Fig. 4).
Thus, to define habitat fragmentation adequately,
habitat must first be defined at a scale relevant
to the species being examined.
WHAT IS THE SCALE OF FRAGMENTATION. 9
The second requisite for defining habitat frag-
mentation is determining the scale at which frag-
mentation is occurring. Wiens (1973) and John-
son (1980) recognized different scales in under-
standing distributional patterns and habitat se-
lection, respectively. For example, Johnson
(1980) proposed first-order selection at the geo-
graphical range of a species, second-order at the
home range of individuals or social groups, and
third-order at specific sites within individual
home ranges. A similar hierarchical scaling can
be used in defining and understanding habitat
fragmentation. For example, habitat tYagmenta-
tion could be considered at a range-wide scale
for fragmentation that occurs throughout a spe-
cies geographic distribution, a population scale
where fragmentation occurs within populations
connected by varying degrees by animal move-
ment, and a home-range scale for fragmentation
that occurs within home ranges of individuals
(Fig. 5). While this scaling can be subdivided
into finer intermediate levels, the idea remains
the same; habitat tYagmentation is scale-depen-
dent with different processes predominating at
the different scales for a given species. For ex-
ample, lYagmentation at the range-wide scale
can affect dispersal between populations, frag-
mentation at the population scale can alter local
population dynamics, and fragmentation at the
home range scale can affect individual perfor-
mance measures, such as survival and reproduc-
tion. Clearly, the different scales are not mutu-
ally exclusive, but provide a unifying nested re-
lationship that allows for understanding mecha-
nisms and processes at different levels (Johnson
1980).
Rather than a hierarchical scale. Lord and
Norton (1990) proposed a continuous gradient
of scale. At one end of the gradient, they defined
geographical fragmentation where fragments
are large relative to the scale of the physiognom-
ically dominant plants (Fig. 6a) and. at the op-
posite end, they defined structural fragmentation
where tYagments are individual plants or small
26 STUDIES IN AVIAN BIOLOGY NO. 25
Range-wide Scale
Population Scale
FIGURE 5.
Home Ranme Scale
Example of three different scales at which habitat fragmentation can occur.
groups of plants (Fig. 6b). While this gradient
puts fragmentation on a continuous scale, it
lacks the biological connection of the species-
centered, hierarchical approach advocated by
Johnson (1980). The ideal would be a gradient
that is continuous and that has a biological con-
text. Regardless of how scale is measured, a sit-
uational definition should include scale because
inferences to population and distributional pro-
cesses for a given species are limited to what-
ever scale is being examined. Fragmentation tha!
affects processes at the home range scale (i.e.,
individual survival and reproduction) do not
necessarily affect processes at a population or
range-wide scale (i.e., dispersal between popu-
lations of home ranges). For example, fragmen-
tation that affects foraging sites within the home
range of an individual may not impede the abil-
ity of the offspring of that individual to disperse
across a wider area.
WHAT IS THE EXTENT AND PATTERN OF
FRAGMENTATION?
Here, we refer to the extent of habitat frag-
mentation as the degree to which fragmentation
has taken place within a specified spatial scale,
whereas the pattern of fragmentation describes
patch geometry, e.g., size, shape, distribution,
and configuration. Extent describes how much
fragmentation has taken place (Fig. 7) whereas
geometry describes the pattern of habitat frag-
mentation. For example, the patterns of frag-
mentation in Figure 8 appear very different even
though the total amounts of remaining habitat
are the same. Various spatial parameters and sta-
tistics (e.g., Turner and Gardner 1991, Mc-
Garigal and Marks 1995) can be used to describe
the different patterns in Figure 8. A considerable
literature exists on how to describe the extent
and pattern of habitat fragmentation and we will
not review these quantitative methods here.
However, a situational definition should include
some measure of extent and pattern of fragmen-
tation to place it in context.
WHAT IS THE MECHANISM CAUSING
FRAGMENTATION?
Habitat fragmentation often occurs because of
some disturbance mechanism. However, habitat
fragmentation can be static, such as resulting
from topographic differences (Forman 1997:
412). For example, habitat used by Mexican
WHAT IS HABITAT FRAGMENTATION?--Franklin et al. 27
as
\
I
I
/
!
!
Do
FIGURE 6. Example of (a) geographical fragmenta-
tion as illustrated by patches of sagebrush and (b)
structural fragmentation as illustrated by the distribu-
tion of individual sagebrush plants on a plot within
one of the patches (after Lord and Norton 1990).
Spotted Owls (Strix occidentalis lucida) is dis-
tributed on a range-wide scale in a highly frag-
mented manner across four states in the U.S.
(Keitt et al. 1997; see Fig. 5). This distribution
is essentially fixed over an ecological time
frame.
Dynamic mechanisms occur with some fre-
quency within a time frame that is applicable to
the ecology of the species and the habitat they
use. These mechanisms can be "natural" (fire,
wind, etc.) or anthropogenic (logging, agricul-
ture, urbanization, etc.; Forman 1997:413). In a
given area at a given scale, these mechanisms
can simultaneously fragment habitat for some
species while creating habitat for others. In con-
servation issues, the mechanisms causing habitat
fragmentation are often of primary concern, es-
pecially when these mechanisms are human-in-
duced.
A complete description of fragmentation must
include an understanding of how the matrix in-
fluences the ability of the habitat to support a
species. If the matrix differs substantially from
the original habitat, the impacts on the species
may be more severe than if the matrix differs
little. That is, fragmentation is also a function of
the degree of contrast in quality between the fo-
cal habitat and its neighborhood. For example,
both selective logging and building homes may
cause tYagmentation of unharvested forest but
the consequences may be very different for the
species that inhabit the landscape. Most mea-
sures of habitat fragmentation do not consider
the effects of the matrix on the survival and re-
production of individuals or populations within
the remaining patches.
Understanding what mechanisms are contrib-
uting to habitat fragmentation is important for
placing habitat fragmentation into the context of
either an acceptable ecological process (i.e., re-
sulting from natural mechanisms) or a required
conservation action (i.e., fragmentation resulting
from anthropogenic mechanisms). Current dog-
ma on habitat fragmentation is value-biased to-
ward a negative connotation (Wiens 1994, Meffe
and Carroll 1997); use of the term currently im-
plies that the biological effects are negative.
However, habitat fragmentation can be value-
neutral or positive, depending on the species.
FRAGMENTATION--A CONCEPTUAL
DEFINITION
We propose that the state (or outcome) of hab-
itat fragmentation can be defined conceptually as
the discontinuity, resulting from a given set of
mechanisms, in the spatial distribution of re-
sources and conditions present in an area at a
given scale that affects occupancy, reproduc-
tion, or survival in a particular species. From
this, the process of habitat fragmentation can be
defined as the set of mechanisms leading to the
discontinuity in the spatial distribution of re-
sources and conditions present in an area at a
given scale that affects occupancy, reproduc-
tion, and survival in a particular species. In de-
veloping these definitions, we incorporated def-
initions proposed by Lord and Norton (1990)
and Hall et al. (1997; Table 1) and included
three of the four requisites that we previously
outlined. The fourth requisite, the extent and
pattern of fragmentation, was not included be-
cause it hampers the ability of the definition to
be general. However, scale and mechanism are
included in the definition to avoid, even in gen-
eral terms, misleading statements. The term hab-
itat fragmentation has acquired a negative con-
notation over the years (Wiens 1994). Habitat
fragmentation can occur naturally and the term
should not be interpreted solely in terms of its
potential negative impacts. Our definition re-
28 STUDIES IN AVIAN BIOLOGY NO. 25
None -" High
Extent of Fragmentation
FIGURE 7. Schematic representation of changes in the extent of fragmentation (after Curtis 1956).
moves the value-bias that currently is attached
to the phrase "habitat fragmentation."
How does our definition differ from previous
definitions? We believe our definition is more
specific than the definition proposed by Morri-
son et al. (1992) and explicitly incorporates the
concept of continuity (Lord and Norton 1990)
that is lacking in the definitions of Wiens (1989)
and Forman (1997) (Tablel). The definition by
Faaborg et al. (1993) does not fit the definitions
of habitat by Block and Brennan (1993) and Hall
et al. (1997), and is more applicable to vegeta-
tion type fragmentation than to habitat fragmen-
tation.
8ITUATIONAL DEFINITIONS
To state that "the habitat is fragmented" is
insufficient for understanding the scope of a par-
ticular conservation problem or the potential ef-
fects on the status of a given species in a given
area. When defining fragmentation for a given
situation (say, within a particular study, conser-
vation plan, or for a given species), statements
a
FIGURE 8. Examples of different patterns of habitat
fragmentation for an area having equal habitat amounts
but (a) fewer large patches with higher edge to interior
ratio versus (b) greater number of small patches with
lower edge to interior ratio.
about habitat fragmentation should include the
four requisites discussed earlier. The first requi-
site, what is being fragmented, requires an un-
derstanding of a species' habitat. The second
requisite, scale, is essentially a statement as to
where inferences are being made and the level
of habitat description being considered (e.g.,
stands of vegetation versus structure of vegeta-
tion within stands). The third requisite, extent
and pattern of fragmentation, provides a descrip-
tion of the magnitude and type of habitat frag-
mentation. The fourth requisite, mechanisms,
puts habitat fragmentation into a temporal scale
(how rapidly changes occur over time) and also
into an ecological and conservation context
("natural" versus anthropogenic, or situations in
between).
A situational definition for habitat fragmen-
tation will not necessarily be limited to a com-
pact statement as is the conceptual definition.
Rather, it should be considered as a series of
paragraphs, or even an entire manuscript that in-
cludes the four requisites. However, the four req-
uisites should be identified and stated clearly to
put habitat fragmentation for a particular situa-
tion into its appropriate context.
CONCLUSIONS
By defining habitat fragmentation as we have
proposed here, people will have to think more
clearly about the characteristic attributes of frag-
mentation. While some may consider our at-
tempts at defining habitat fragmentation as an
over-emphasis on semantics, we agree with Pe-
ters (1991) and Hall et al. (1997) that vague and
inconsistent terminology in the ecological sci-
ences leads to ineffective and misleading com-
munication, poor understanding of concepts, and
WHAT IS HABITAT FRAGMENTATION?--Franklin et al. 29
generally sloppy science. Habitat is a unifying
concept in ecology (Block and Brennan 1993)
and central to many of the conservation prob-
lems that ecologists face. We believe that de-
veloping precise definitions for key concepts at
the interface between ecology and conservation
is paramount before these concepts become so
muddled that ecologists become ineffective in
their ability to deal with problems and to com-
municate those problems to others.
ACKNOWLEDGMENTS
We thank R. A. Askins and J. A. Wiens for their
thoughtful reviews of this manuscript. We also thank
D. Dobkin and J. Rotenberry for their useful comments
and for editing this volume.
Studies in Avian Biology No. 25:30-48, 2002.
HABITAT EDGES AND AVIAN ECOLOGY: GEOGRAPHIC
PATTERNS AND INSIGHTS FOR WESTERN LANDSCAPES
THOMAS D. $ISK AND JAMES BATTIN
Abstract. Habitat edges are an important feature in most terrestrial landscapes, due to increasing rates
of habitat loss and fragmentation. A host of hypothesized influences of habitat edges on the distri-
bution, abundance, and productivity of landbirds has been suggested over the past 60 years. Never-
theless, "edge effects" remains an ill-defined concept that encompasses a plethora of factors thought
to influence avian ecology in heterogeneous landscapes. The vast majority of research on edge effects
has been conducted in the broad-leafed forests of northeastern and midwestern North America. In
general, many western habitats are more heterogeneous and naturally fragmented than their eastern
counterparts, and habitat edges are a ubiquitous component of most western landscapes. These dif-
ferences in landscape structure suggest that edge effects, and the mechanisms underlying them, may
differ markedly in the West. We examined over 200 papers from the peer-reviewed literature on edge
effects, focusing our efforts on empirical results and trends in research approaches. The relative dearth
of western studies makes geographic comparisons difficult, but it is clear that mechanistic understand-
ing of edge effects has lagged behind pattern identification. Bird responses to edge effects tend to
vary markedly among species and among different edge types, while no clear pattern emerges re-
garding species diversity. In the context of the review, we discuss research and modeling approaches
that could move our understanding of edge effects toward a more mechanistic and predictive frame-
work.
Key Words: core area model; density; edge effects; effective area model; habitat edge; habitat frag-
mentation; heterogeneity; species diversity.
Habitat fYagmentation increases landscape het-
erogeneity as continuous patches of native hab-
itats are broken into numerous smaller, isolated
patches surrounded by a matrix of different, of-
ten heavily disturbed or anthropogenic habitats
(Wilcox 1980, Wilcove et al. 1986, Wiens 1994,
Franklin et al. this volume). The loss of native
habitat cover and the increasing isolation of the
resulting patches from one another have been
the subject of numerous empirical and theoreti-
cal studies and several reviews (e.g., Saunders
et al. 1991, Faaborg et al. 1995). Since the early
1970s these two factors have dominated debates
about conservation planning in increasingly
fragmented landscapes (e.g., Diamond 1976;
Simberloff and Abele 1976, 1982; Terborgh
1976).
Another result of habitat fragmentation is an
increase in the amount of edge habitat, as well
as the proliferation of new types of edges, as
anthropogenic habitats (e.g., agriculture, logged
forest, and urbanized areas) replace native hab-
itats and abut the remaining fragments. The in-
creasing number of smaller patches, and the lin-
ear or irregularly shaped patches that often result
from fragmentation (Feinsinger 1997), contrib-
ute to the rapid, often exponential increase in the
amount of edge habitat in the landscape (Fig. 1).
Implications of the proliferation of edge hab-
itat for bird populations are numerous, ranging
from the alteration of microclimatic conditions
to changes in interspecific interactions, such as
competition, predation, and nest parasitism.
These and other edge effects are often distinct
from the effects associated strictly with the loss
of habitat and the increasing isolation of the re-
maining patches. By influencing the quality of
nearby habitat in the remaining fragments, edges
may also directly affect the amount of available
suitable habitat (Temple 1986, Sisk et al. 1997).
Thus, edge effects constitute a class of impacts
that are of increasing importance as fragmenta-
tion advances and the heterogeneity and struc-
tural complexity of the landscape increases.
Despite over 60 years of active research, our
understanding of edge effects remains diffuse
and largely site-specific. Interestingly, the liter-
ature on "edge effects" predates research on
habitat fragmentation by some 45 years, and be-
cause of this long history, a summary of the lit-
erature on edge effects parallels the development
of avian ecology in general. In fact, edge effects
can be viewed as the earliest attempt to study
avian ecology at the landscape scale, a perspec-
tive that received less attention as the focus of
field ecology shifted to population dynamics and
community ecology in the 1950s through the
1970s. The conservation imperative that
emerged in the seventies, driven by the recog-
nition of rapid habitat loss and fragmentation,
returned consideration of edge effects to the
forefront of avian research, but in a very differ-
ent context.
Our overview of edge effects traces the de-
velopment of conceptual approaches through
field studies, experiments, and modeling ap-
30
EDGE EFFECTS AND AVIAN ECOLOGY--Sisk and Battin 31
NUMBER OF PATCHES
% DEFORMATION
FIGURE h Edge habitat proliferates with increasing
fragmentation, due both to the increased edge per unit
area as the number of patches increases (top), and as
individual patches become, on average, more linear or
irregularly shaped, as represented here as an increas-
ingly flattened patch (bottom). From Sisk and Mar-
gules (1993).
proaches. The paper focuses on patterns in the
literature, particularly the disparity in the level
of research in the eastern and western United
States and the emphasis upon certain habitat
types. We list working hypotheses derived from
the literature, and we provide brief summaries
of supporting and refuting evidence. Finally, we
examine more predictive approaches to the study
of edge effects so that the accumulated knowl-
edge might be put to work in efforts to predict
the impacts of ongoing fragmentation. Our ulti-
mate goal is to incorporate a consideration of
edge effects into efforts to reverse the negative
impacts of fragmentation and improve reserve
designs, restoration efforts, and management
plans for the conservation of avian biodiversity.
EDGE EFFECTSAN ILL-DEFINED
"LAW" OF ECOLOGY
"Edge effect" is among the oldest surviving
concepts (some would say "buzz-words") in
avian ecology. In 1933, Leopold referred to "the
edge effect" to explain why quail, grouse, and
other game species were more abundant in
patchy agricultural landscapes than in larger
fields and forested areas (Fig. 2). He hypothe-
sized that the "desirability of simultaneous ac-
cess to more than one (habitat)" and "the great-
er richness of (edge) vegetation" supported
higher abundances of many species and higher
species richness in general (Leopold 1933). This
common-sense definition drew on years of ex-
perience as a forester and game manager, and
reflects the focus of early wildlife managers on
game species, many of which utilize early suc-
cessional and/or edge habitats preferentially.
Lay (1938) provided some of the earliest empir-
ical evidence supporting both increased abun-
dance and greater species richness at woodland
edges. His interpretation of these patterns also
began a long tradition of deriving management
guidelines from studies of bird abundances and
species diversity at edges. His claim that the
"maximum development of an area for wildlife
requires ... small but numerous clearings" was
accepted by many wildlife managers and found
its way into many textbooks over a period of
several decades, culminating in what has been
called the "law of edge effect" (Odum 1958,
Harris 1988). General acceptance of the hypoth-
esis that diversity and abundance are higher near
edges led wildlife biologists to advocate the cre-
ation of edge under the assumption that it would
benefit biodiversity (e.g., Giles 1978, Yoakum
1980, Dasmann 1981). This understanding of the
beneficial nature of edge effects influenced land
management practices for decades and served as
a de facto prescription for habitat fragmentation
in the name of wildliI management. Even to-
day, land managers frequently advocate the cre-
ation of edges via (for example) forest clearing
and prescribed fire, with the intention of increas-
ing avian abundance and diversity.
More recently, the relationship between forest
fragmentation and both nest predation and par-
asitism has spawned a different view of edge
effects. Edges have been shown to support high-
32 STUDIES IN AVIAN BIOLOGY NO. 25
INTERSPERSION OF TYPES - RELATION TO MOBILITY & DENSITY OF QUAIL
A.' Poor Inferspersion (I Cove,/)
... CULTIVATION
,,VEY
:,:.....I,. ,.- ...........
;*, t tt,.:s 3? :.. :?::':
FIGURE 2. Leopold (1933) coined the term "edge effect" to explain increased abundance of game birds in
heterogeneous landscapes with many edges. In this figure, 160 ac (64.7 ha) blocks of 4 habitat types, each 40
ac (16.2 ha), are displayed in the two panels. Panel (a) has 2 mi (3.2 km) of edge, while panel (b) has 10 mi
(16 km). Leopold argued that greater bird abundances are associated with the heterogeneous landscapes, such
as (b).
er rates of nest predation and parasitism (Wil-
cove 1985, Paton 1994, Andrdn 1995). Current
texts are likely to present evidence that edge ef-
fects are "bad" and that the creation of edge
habitat by fragmentation leads to the decline of
"interior species" that are particularly suscep-
tible to nest parasites and predators (e.g., Meffe
and Carroll 1997). Again, the focus on certain
aspects of edge effects (in this case nest preda-
tion and parasitism rates) has led to a widely
accepted, general rule of edge effects. However,
in this case, the supposedly beneficial effects are
often ignored, while the adverse effects, dem-
onstrated for a subset of species in particular
habitats and in certain geographic areas, are
highlighted.
Thus, perceptions of the relationship between
edge effects and habitat fragmentation are often
contradictory, and the reality is almost always
more complex than perceptions. In some cases,
edges are thought to benefit birds; in others they
are seen as the primary threat to bird diversity.
And in cases where edges support high bird den-
sity but low nest productivity, edge effects on
population persistence may be particularly neg-
ative (Ratti and Reese 1988). Nevertheless, the
term continues to be applied with little discrim-
ination, and the assumption that all influences of
habitat edges can and should be grouped into a
uniform class of ecological impacts persists in
the literature. The complexity and diversity of
the responses of different species to differing
edge types, combined with the lack of an inclu-
sive theoretical framework for organizing the
plethora of field observations reported in the lit-
erature, has turned "edge effects" into a grab-
bag term, one that too often is used casually to
explain anomalous or inconclusive results. In-
deed, the term edge effect has become so widely
accepted in the management literature that it is
commonly used to explain diametrically op-
posed observations.
Part of the confusion may result from changes
in the scale at which species diversity is as-
sessed. Historically, biologists and planners have
focused on alpha (local) diversity, which is often
high near habitat edges. As conservation plan-
ning has shifted to larger areas, and scientists
have assessed regional and global patterns in
biodiversity, the focus on species diversity has
shifted to the gamma (regional) level, which
may be lower in fragmented landscapes due to
the loss of edge-avoiding species. Until scien-
tists and managers are able to adopt a multi-
scaled approach to assessing biodiversity (see
Noss 1990), confusion over edge effects is likely
to persist.
HISTORICAL PERSPECTIVES: RESPONSE
VARIABLES, FOCAL SPECIES, AND
GEOGRAPHIC PATTERNS
METHODS
We reviewed the literature on edge effects dating
back to the mid-1930s in an attempt to synthesize the
large and diverse body of published work in arian
ecology and wildlife management. Drawing from on-
line searches, published abstracts, examination of lit-
erature cited in all papers reviewed, and inquiries with
colleagues, we created an annotated bibliography to
facilitate analysis of patterns from published studies of
edge effects. We limited our review to the peer-re-
viewed literature after initial attempts to include un-
published reports and other "gray literature" demon-
EDGE EFFECTS AND AVIAN ECOLOGYSisk and Battin 33
TABLE 1. ANALYSIS OF THE EDGE EFFECTS LITERA-
TURE BASED ON PARAMETERS LISTED BELOW, RECORDED
FOLLOWING REVIEW OF 215 PAPERS PUBLISHED OVER A
66-YR PEPrOD
Study Type-observational, experimental, theoretical,
or modeling
Location-country, state/province
Focal habitat type
Adjacent habitat
Edge definition (e.g., is the edge treated as a gradient
or separate habitat type)
Focal species
Study design
Replication
Response variable(s)
Explanatory variable(s) measured
Results and Conclusions
strated a tremendous volume of work of highly vari-
able quality. Inclusion of gray literature would have
substantially increased our sample size, particularly in
the West, but that literature could not be accessed in
any consistent manner, and a haphazard sampling of
material would have compromised our analyses. In this
article we attempt to present an unbiased review of the
peer-reviewed literature, and we invite the reader to
critically explore the voluminous gray literature for ad-
ditional site- and species-specific information on edge
effects.
A total of 215 publications were examined for this
chapter. Of these, we eliminated from further consid-
eration any field studies that did not explicitly address
avian response to edges (for example, studies that em-
ploy edge as one of many possible explanatory vari-
ables in multivariate analyses of fragmentation effects;
see citations in other chapters in this volume). This left
us with 125 studies, providing a comprehensive per-
spective on the development of the edge effects con-
cept in the primary literature, current understanding of
edge effects in the context of habitat fragmentation,
and the application of this knowledge in the manage-
ment of avian populations. Of the 125 publications re-
viewed, 90 presented original research results involv-
ing avian subjects (Appendix), and these are included
in the analyses presented below. For this subset of the
edge literature, we quantified aspects of each study
pertaining to the location, focal habitats, species stud-
ied, key results, and several related parameters (Table
1). Conceptual and theoretical treatments of edge ef-
fects are discussed in subsequent sections of this chap-
ter.
Unlike the nest predation literature (see recent re-
views by Paton 1994, Andrrn 1995, HartIcy and Hunt-
er 1998), the literature on patterns of bird density and
diversity with respect to habitat edges has not under-
gone a recent review. For this reason, we analyze this
body of literature in detail. We report the density and
species richness response(s) for every treatment con-
sidered in each study (Appendix). For multi-year stud-
ies, we consider a treatment to show a response if a
statistically significant response (increased or de-
creased density or species richness at edges) was ob-
served in at least one year, and a non-significant trend
in the same direction was observed in other years.
GEOGRAPHIC PATTERNS AND RESPONSE
VARIABLES
The majority of published studies of edge ef-
fects in avian ecology (88%, N -- 60) are from
the eastern half of North America (Figs. 3, 4a).
Furthermore, the West has produced less than
half as much research on this topic than has
FIGURE 3 Map of North America showing number of studies addressing edge effects in landbirds.
34
a) 5
18
53
STUDIES IN AVIAN BIOLOGY
c) s 7
B Eastern NA 29
nWestern NA 8/'
B Scandinavia 4 '...._._--
Tropics
13 Other 4
9
15
9
ß Agriculture
nClearcut
ß Road/Trail
ß Powedine
ß Urban
ß Other Induced
[3 Natural-Water
ß Natural--Other
ß Undifferentiated
NO. 25
5
b) 6 3 4 d) 5
9b5 [] Forest Predation: Artificial
[] Agriculture 37
9 9 [] Predation: Natural
[3 Native Open Habitat Parasitisrn
ß Clearcut
[3 Wetland ß Density
Species Richness
[] Powerline Corridor 40
[] Urban 10 ß Nest Density
7
FIGURE 4. The number of edge studies (a) by region, N = 90; (b) by habitat type, N = 90; (c) by adjacent
(matrix) habitat, forest edges only, N = 75; (d) by response variable, N = 112 (some studies involved more
than one edge type).
Scandinavia, where conditions are, arguably,
more similar to eastern North America (Fig. 4a).
Clearly, as measured by the number of peer-re-
viewed publications, studies in Europe and east-
ern North America have had a tremendous influ-
ence on our understanding of edge effects.
Not surprisingly, since forests are the domi-
nant natural habitats in these regions, 73% of all
empirical studies focused on forest edges (Fig.
4b), and 33% of these were edges with agricul-
tural habitats (Fig. 4c). Again, there is a geo-
graphic bias, as conversion of forested habitats
to agriculture (and the reverse) has been a pre-
dominant land-use trend in the East and Mid-
west, whereas edges in western habitats are most
often due to timber harvest and a range of fac-
tors that degrade, but less often radically trans-
form, native habitats. When this distribution of
research effort is viewed in the context of the
overall habitat diversity of North America, and
when the range of natural and anthropogenic
factors that modify habitats and create edges is
considered, it is apparent that our understanding
of edge effects is largely the product of research
focused on a small subset of edge types in east-
ern, midwestern, and northern European forest
edges.
Examination of the response variables mea-
sured in empirical edge studies reveals a strong
tendency to focus on patterns in species abun-
dance (44% of all studies) and species richness
(17%; Fig. 4d). This work highlights patterns in
avian distribution near edges but typically does
not examine the factors creating the patterns.
Fifty-two per cent of all studies quantified rates
of nest predation, but of these only 21% looked
at natural nests. The remainder manipulated the
placement of artificial nests to estimate relative
rates in the wild. Nest parasitism, a topic men-
tioned at least parenthetically in most recent
publications on edge effects, was quantified in
only 7 of the papers that we reviewed (8%; Fig.
4d). Many other potentially important variables,
including competitive interactions, pairing suc-
cess, movement and dispersal rates, and edge
permeability have received scant attention in
empirical studies of avian edge effects.
EDGES AND NEST PREDATION
Three recent reviews that have examined the
relationship between forest edges and predation
have found that, while evidence exists for higher
predation rates at edges, this pattern is far from
universal (Paton 1994, Andrn 1995, Hartley
and Hunter 1998). These reviews addressed not
only the question of how frequently predation
edge effects occur, but also looked for explana-
tions regarding why some studies found edge ef-
fects and others did not. Landscape context was
the primary explanatory variable used by all au-
EDGE EFFECTS AND AVIAN ECOLOGY--Sisk and Battin 35
thors, but they drew markedly different conclu-
sions about its importance.
Paton (1994) examined edge effects in nest
predation on artificial nests and in both preda-
tion and parasitism on natural nests. He found
that 10 of 14 studies using artificial nests
showed evidence of differential nest predation at
edges, compared with 4 of 7 studies of natural
nests. Of the 14 studies showing differences,
most showed higher predation at edges. Just un-
der half of the 32 studies examined by Andrdn
(1995) showed higher predation rates near edg-
es, while only 5 of the 13 North American stud-
ies examined by Hartley and Hunter (1988)
found a difference in predation rates between
habitat edges and interiors. These reviews indi-
cate that high nest predation rates occur near
edges, but not consistently. Some studies re-
viewed by Andrdn (1995) and Paton (1994) even
found lower predation near edges.
In seeking to explain this variable pattern of
edge effects, the three reviews draw strikingly
different conclusions, though they consider
many of the same papers. Paton (1994) conclud-
ed that "significant edge effects were as likely
to occur in forested as in unforested habitats."
Andrdn (1995) concluded that predation near
edges was more likely in agricultural than in for-
ested landscapes. Hartley and Hunter (1998),
who conducted a substantially more rigorous
meta-analysis of the association between forest
cover and edge effects, found a marginally sig-
nificant (P = 0.095) pattern of higher predation
in unforested than in forested landscapes. Un-
fortunately, the power of their analysis was lim-
ited, as they considered only two studies from
unforested landscapes.
One possible explanation for the inconsisten-
cies in the findings of these different studies is
that Andrdn (1995) considered both edge effects
and patch size effects in a single analysis, while
Paton (1994) and Hartley and Hunter (1998) an-
alyzed edge effects and patch size effects sepa-
rately. In contrast to their equivocal findings on
the relationship between landscape context and
the presence of edge effects, both Paton (1994)
and Hartley and Hunter (1998) found a very
strong relationship between nest predation rate
and patch size. This result suggests that Andrdn
(1995) may have confounded effects by lumping
patch size and edge effects in his analysis, and
that the strong pattern that he detected could be
due to patch size rather than edge effects per se.
Another difficulty in interpreting these results
is that most of the studies of edge effects on nest
predation have been conducted using artificial
nests. Hartley and Hunter (1998) used only ar-
tificial nest studies in their analysis, while An-
drdn combined artificial and natural nests. Paton
considered artificial and natural nest studies sep-
arately, but he found only 7 natural nest studies.
The use of artificial nests has been questioned
repeatedly in recent years (see Willebrand and
Marcstrom 1988; Haskell 1995a,b; Major and
Kendal 1996, Yahnet 1996), and Haskell
(1995a,b) suggested that there is a systematic
bias toward increased predation on artificial
nests in smaller fragments, a finding that could
be especially misleading in studies of predation
near edges.
While evidence of increased predation rates
near edges does exist, it is not clear that this is
a widespread phenomenon, or that it is pro-
nounced in the West. We found only two studies
of nest predation in the West, one that used ar-
tificial nests (Ratti and Reese 1988) and one that
used natural nests (Tewksbury et al. 1998). Nei-
ther study found a significant edge effect in nest
predation.
PATTERNS IN COMMUNITY ORGANIZATION
For several decades, "edge effects" referred
almost exclusively to the increase in species di-
versity and/or density commonly observed near
the edge (Johnston 1947, MacArthur et al. 1962,
Giles 1978). A total of 21 studies, with 34 sep-
arate treatments, examined density or species
richness of the entire bird community (Appen-
dix). Of these, 21 treatments reported higher
bird densities near edges, while 10 reported no
edge response and 3 showed a decrease. The
vast majority of these studies (19 studies, ad-
dressing 27 treatments) were conducted in for-
ested habitats, so we restrict our more detailed
analyses to these results.
Overall, forest studies showed a strong pattern
of higher density at edges but a weaker pattern
with regard to species richness. Sixteen treat-
ments recorded higher bird abundance near edg-
es, with 8 showing no significant response and
3 a negative response. Nine treatments found
higher species richness at edges, while 10 found
no difference, and 2 found a decrease. While an
unequivocal pattern of higher bird density and
species richness at edges does not emerge from
this analysis, it seems clear that, in the recent
literature, negative responses to edges are rela-
tively rare and positive responses are common.
This could be a manifestation of a general eco-
logical principle (i.e., density and species rich-
ness increase at most edges) or the result of a
bias in the literature (edge responses in areas
where studies have been done are different from
those in unstudied areas). Because, as we have
shown, there is a strong geographical bias in the
literature, this second explanation cannot be
ruled out.
All studies (9 studies, 9 treatments) conducted
36 STUDIES IN AVIAN BIOLOGY NO. 25
in temperate zone forests that examined total
bird abundance at edges between native forests
and large anthropogenic openings (matrix = ag-
riculture, clearcut, clearing, anthropogenic
grassland; see Appendix) found higher bird den-
sities near the edge. Of the 7 studies that also
looked at species richness, 3 found an increase
while 4 found no significant pattern. On the oth-
er hand, the only study that looked at the dif-
ference in overall bird density and species rich-
ness along an anthropogenic edge gradient in the
tropics found that both decreased near the edge
(Lovejoy et al. 1986). Another tropical study,
which analyzed edge response by foraging guild,
found that two guilds did not differ in abundance
and one (insectivores) decreased at the edge
(Canaday 1997). These results suggest that even
the strongest patterns detected in temperate for-
ests may not generalize well to other habitats
and geographic regions.
The effects of linear drivers of habitat frag-
mentation (roads and powerlines) and natural
edges appear to be less consistent. While no
studies of road or powerline edges found com-
munity-level decreases in avian density, 4 of 7
treatments showed increases and 3 of 7 showed
increased species richness. Of the studies that
examined natural edges (6 studies, 8 treatments),
3 treatments showed increased density, 4
showed no change, and 1 showed a decrease.
Four treatments showed increased species rich-
ness at natural edges, with 2 showing no change,
and one showing a decrease.
Aside from the suggestion that edge responses
may differ between the tropics and the temperate
zone, no clear geographical patterns of edge re-
sponse were evident. No studies from eastern
North America recorded decreases in total bird
abundance (Fig. 5a) or species richness (Fig. fib)
at edges, but almost as many treatments showed
no response in overall bird density (6) as showed
an increase (9). As many treatments showed no
response in species richness (7) as showed a
positive response near edges (7). The only study
from western North America had one treatment
that showed increased density and species rich-
ness at the forest edge and one that showed no
change in either variable (Sisk 1992). Two Scan-
dinavian studies showed decreases in density at
edges, while I reported no change and 2 found
increases. We were surprised at the small num-
ber of studies that reported on the entire avian
community, especially considering the widely
held "rule of thumb" associating edges with
higher densities and/or species richness. Many
of the studies most commonly cited to support
this idea examine only part of the bird commu-
nity present at the study site.
Many explanations for the reported trends in
FIGURE 5. Numbers of treatments from studies con-
ducted in eastern and western North America finding
positive, negative, or neutral edge responses in total
bird density (a) md species richness (b).
avian abundance and diversity near edges have
been proposed, and few are mutually exclusive.
Few studies have attempted to distinguish
among them, and many authors have invoked
"edge effects" when discussing any of the myr-
iad influences of habitat fragmentation on dis-
turbance-sensitive species. From this broad
range of uses, four general categories of edge
effects can be identified:
ß Habitat interspersion. Species diversity may
increase at habitat edges due solely to the
proximity of diflrent habitats (Leopold 1933,
Giles 1978). At the habitat edge, each com-
munity contributes, on average, more than
half of its fauna, resulting in higher species
diversity at the edge where the two commu-
nities mix (MacArthur and MacArthur 1961,
Wiens 1989).
ß Resource availability. Many authors have
suggested that birds may utilize more than
one habitat type during different activities
(e.g., nesting and foraging) or during different
life stages. Allocating different activities to
the most appropriate habitat may allow some
species to maintain higher population densi-
ties near edges. It also may provide suitable
habitat for species that require more than one
habitat type (Kendeigh 1944, MacArthur et al.
1962, Yoakum 1980, Dasmann 1981).
ß Edge as a unique habitat. Edges may support
higher densities of species characteristic of
both the adjoining communities, due to in-
EDGE EFFECTS AND AVIAN ECOLOGY--SiNk and Battin 37
creased diversity of the vegetation that typi-
cally occurs where two habitats intergrade.
Many workers have shown correlations be-
tween foliage height diversity and bird species
diversity (e.g., MacArthur 1958, Cody 1968,
Karr and Roth 1971; but see also Willson
1974). Other studies have shown that floriNtic
composition and the presence or absence of
particular plant species are good predictors of
both diversity and density of birds (Wiens
1989). Vegetation structure and floriNtic com-
position are generally more diverse at edges,
so increases in both species diversity and avi-
an density might be expected, even without
the addition of edge-dependent species.
ß Interspecific interactions and cascading biotic
efkcts. Edges, especially those associated
with habitat conversion and fragmentation,
may permit edge-dependent or habitat-specific
species to penetrate some distance into adja-
cent habitats where they normally do not oc-
cur. Their presence can influence the abun-
dance of species in the adjacent habitat, gen-
erating cascading effects that penetrate further
than the direct environmental changes asso-
ciated with the edge (Diamond 1978, 1979;
Pulliam and Danielson 1991, Fagan et al.
1999). Such secondary effects, including
competition, predation, and nest parasitism,
are thought to result in the exclusion of forest
species from otherwise suitable habitat near
habitat edges (Ambuel and Temple 1983, Wil-
cove et al. 1986, Harris 1988).
SPECIES-LEVEL RESPONSES UNDERLYING
COMMUNITY PATTERNS
Each of the definitions of edge effects pre-
sented above implies that population densities of
some species will change as a function of the
distance from the habitat edge. However, few
authors have stated explicitly which species they
expect to be influenced by habitat edges or how
they will respond. In fact, many early studies
that support the hypothesis of elevated diversity
at edges do not report which species contribute
to the diverse assemblages found there. Those
that do often show that the increase in species
richness is due to the addition of common, cos-
mopolitan, or disturbance-tolerant species,
which may mask the loss or decline of sensitive
species.
A better understanding of the dynamics in
community organization near edges emerges
from studies of the responses of individual spe-
cies near habitat edges (Giles 1978, DaNmann
1981, Harris 1988, Reese and Ratti 1988, NoNs
1991, Bolger this volume). Many studies have
shown that certain species reach their highest or
lowest abundance at particular habitat edges
(e.g., Kendeigh 1944, Johnston 1947, Hansson
1983, Kroodsma 1984b, NoNs 1991, Bolger et
al. 1997, Germaine et al. 1997, King et al.
1997). Species that are encountered more com-
monly near the edge are often termed "edge spe-
cies" (e.g., Johnson 1975, Giles 1978, Reese
and Ratti 1988), and those whose densities are
low near the edge are considered to be habitat-
interior species (e.g., Brittingham and Temple
1983, Wilcove et al. 1986, Thompson 1993, Bol-
ger et al. 1997). A more quantitative approach
to understanding how species respond to habitat
edges involves measurement of a species-specif-
ic edge response, defined as the pattern of
change in population density at incremental dis-
tances from the habitat edge (NONs 1991, SiNk
and Margules 1993).
SiNk and Margules (1993) proposed a classi-
fication scheme for population-level edge re-
sponses based on changes in density along a
transect from one interior habitat, across the
edge, and into the adjacent habitat (hereafter the
edge gradient). For some species, the edge itself
has no effect on population density (null re-
sponses), and changes in density are attributable
to differences between the two adjoining habi-
tats. Other species reach their highest density
("edge exploiters'*) or lowest density ("edge
avoiders") near edges (see also Bolger this vol-
ume). While classification schemes differ among
the published studies reviewed here, it is clear
that a diversity of responses is manifest in any
particular avian community. Four studies from
eastern North America show that edge-exploit-
ing responses are generally more common than
edge-avoiding responses, with neutral responses
(i.e., no edge effect) more common than either
in 3 out of 4 studies (Fig. 6a). The small number
of Western studies showed similar patterns, ex-
cept that edge-exploiting responses outnumbered
edge-neutral responses (Fig. 6b).
Villard (1998) compared the edge responses
of forest-interior neotropical migrants reported
in 4 studies from the eastern seaboard stretching
from Florida to New Hampshire. He found that
there was little consistency in the way that the
authors classified responses for the same spe-
cies. We extended this analysis to all species that
occurred in two or more of the studies (Table 2).
While there is considerable variability in the re-
sponses reported for these species, some patterns
do emerge. Most neotropical migrants are edge
avoiders, and all disagreements among authors
have to do with whether a species shows a neu-
tral response or a positive or negative response;
no species is considered an edge-exploiter by
one author and an edge-avoider by another. Con-
versely, species that are not latitudinal migrants
showed neutral or edge-exploiting responses.
38 STUDIES IN AVIAN BIOLOGY NO. 25
FIGURE 6. Numbers of bird species in four studies
showing positive, negative, or neutral responses to
habitat edges. Eastern studies (a) were conducted in
Vermont (Germaine et al. 1997), New Hampshire
(King et al., 1997), Florida (Noss, 1991), and Tennes-
see (Kroodsma, 1982). Western studies (b) are from
California redwood stands (Brand and George this vol-
ume) and California oak woodlands (Sisk 1992, Sisk
et al. 1997).
Again, no species was assigned a positive re-
sponse by one author and a negative response
by another (Table 2). Unfortunately, there are
not enough studies of western birds to make
similar comparisons, and there is little overlap
in species among the few published studies.
Three studies from California do, however, seem
to show greater variation in the responses of
both neotropical migrants and resident species
(Sisk et ai. 1997, Brand and George this volume,
Bolger this volume).
Ecologists and wildlife managers have often
assumed that birds will show consistent, char-
acteristic patterns of habitat selection at edges,
even when the adjoining habitats differ in veg-
etation structure and/or species composition. Im-
plicit in this assumption is the idea that edges of
all types share some intrinsic qualities, and that
their influence on the distribution of organisms
and the composition of assemblages is similar.
There is little evidence to support these views.
Few studies have measured edge responses at
more than one type of edge in a given region,
and those that have report differences in the con-
sistency of arian responses at different edge
types. Noss (1991) found considerable variation
among species and among sites in longleaf pine
(Pinus palustris) bird communities. Sisk et al.
(1997) showed that over half of the breeding
birds in oak woodland showed different respons-
es at edges with grassland versus edges with
chaparral, and Kristan et al. (in press) found sig-
nificant site-to-site variation in edge response in
several southern California coastal sage scrub
bird species. Brand and George (this volume)
found general consistency at redwood forest
edges adjoining habitats as different as logged
forest and grassland.
In summary, our examination of empirical
studies of edge effects did not identify a simple
pattern in avian responses, but it did uncover
several important points regarding patterns in
community organization and population re-
sponses to habitat edges:
ß "Edge effects" is an ambiguous term in arian
ecology and conservation. Its usefulness is
limited by widely varying assumptions that
permeate its history.
ß Edge effects do not contribute to species di-
versity in a consistent manner that is easily
generalized among sites.
ß The abundances of many species change dra-
matically near habitat edges.
ß Edge responses vary markedly among spe-
cies.
ß A given species often responds very differ-
ently at different types of edges (but a few
studies show consistency).
MECHANISMS UNDERLYING SPECIES-LEVEL
RESPONSES
Mechanisms underlying edge effects are
many, but few have been adequately investigat-
ed (Bolger this volume). Sisk and Haddad (2002)
hypothesize that several basic driving factors
may underlie the broad range of responses typ-
ically grouped together under the term ':edge ef-
fects". These include:
ß Edges influence movement. Edges may influ-
ence behavior, creating barriers to movement
even when animals are clearly capable of
crossing them (Ries 1998, Haddad 1999). The
influence of edges may prevent dispersal
through complex landscapes and isolate ani-
mals. Sisk and Zook (1996) have shown that
"passive accumulation" of migrating birds
may generate widely reported increases in
density observed near forest edges.
© Edges influence mortality. Particularly for
habitat interior species, edges may lead to
higher mortality in plants and animals. Higher
mortality may occur in three different ways.
First, edges create greater opportunity for loss
EDGE EFFECTS AND AVIAN ECOLOGY--Sisk and Battin 39
TABLE 2. VARIATION IN SPECIES-SPECIFIC EDGE RESPONSES REPORTED IN DIFFERENT EMPIRICAL STUDIES FROM
THE EASTERN USA
New
Tennessee Hampshire Vermont
(Kroodsma Florida (King et al. (Germaine
Common name Scientific name 1984) (Noss 1991) I997) et al. 1997)
Neotropical Migrants
Yellow-billed Cuckoo Coccyzus americanus 0 +
Acadian Flycatcher Empidonax virescens - -
Wood Thrash Hylocichla mustelina 0
Hermit Thrash Catharms guttatus 0 - -
Red-eyed Vireo Vireo olivaceus 0 - -
Black-and-white Warbler Mniotilta varia + 0 0
Black-throated Blue Warbler Dendroica caerulescens 0 +
Black-throated Green Warbler Dendroica virens 0 +
Hooded Warbler Wilsonia citrina 0 -
Ovenbird Seiurus aurocapillus - 0 0 -
American Redstart Setophaga ruticilla 0 0
Summer Tanager Piranga rubra + +
Scarlet Tanager Piranga olivacea 0 0 0
Temperate Migrants
American Robin Turdus migratorius 0 0 +
Residents
Red-bellied Woodpecker Melanerpes catolinus + 0
Downy Woodpecker Picoides pubescens 0 0
Carolina Chickadee Parus ctirolinensis 0 +
Northern Cardinal Cardinalis cardinalis + +
Note: Results from four studies allowed the classification of 12 species according to their density responses near edges: '+' for edge-exploiting
response; '0' lbr no edge response; '-' for edge-avoiding response; ' ' if not reported (after Viilard 1998).
of dispersers into unsuitable habitat. For ex-
ample, plants with wind-dispersed seeds that
are near the edge will lose more of their prop-
agules into unsuitable habitat. Second, edges
alter microclimate, including temperature,
light, and moisture (Sisk 1992, Chen et al.
1993, Young and Mitchell 1994, Camargo and
Kapos 1995). In doing so, edges impact com-
petitive interactions between species. Third,
edges provide points of entry for predators
and parasites, such as the Brown-headed
Cowbird (Molothrus ater; Wilcove et al.
1986, Murcia 1995).
ß Edges provide feeding or reproductive subsi-
dies. From the edge, species may be able to
obtain a greater quantity and quality of food
resources from each of the habitats that create
the edge, leading to positive effects on pop-
ulation sizes (MacArthur et al. 1962, Fagan et
al. 1999).
ß Edges define the boundary between two sep-
arate habitats, creating new opportunities for
species to mix and interact. By their very na-
ture, edges influence species interactions be-
cause they bring into close proximity species
that would not normally be present in the
same habitat. Species that are brought togeth-
er at the edge, including predators and prey,
new competitors, and mutualists, generate
novel interactions and create new communi-
ties of species.
Despite the diversity of hypothesized and doc-
umented mechanisms underlying edge effects,
surprisingly few studies have attempted to iden-
tify the mechanistic basis for edge response and
patterns in community organization reported in
the literature. Of the 90 field studies considered
in this review, most were observational, typical-
ly involving some count of individuals or nests
in unmanipulated landscapes. The vast majority
of experimental studies involved manipulation
of artificial nests for the purposes of examining
nest predation and parasitism rates; few involved
the experimental manipulation of bird habitats
(but see Lovejoy et al. 1986).
Forty studies focused on estimates of abun-
dance or species richness, but few examined the
mechanisms driving the observed patterns. Don-
ovan et al. (1997) noted that little work has been
devoted to exploring the mechanisms underlying
observed patterns of edge effects in nest preda-
tion and parasitism. This is even more pro-
nounced for studies examining patterns in bird
density and species richness. Clearly, the eluci-
dation of mechanisms driving edge effects has
lagged far behind pattern identification. In-
creased attention to the mechanistic drivers un-
40 STUDIES IN AVIAN BIOLOGY NO. 25
derlying edge effects and their relative contri-
bution to observed patterns of distribution and
abundance is a fruitful area for future research.
PREDICTIVE APPROACHES TO
MODELING EDGE EFFECTS
Despite recent advances in understanding the
general consequences of fragmentation, the de-
velopment of tools for predicting specific im-
pacts has progressed slowly. A growing body of
research is demonstrating that edges are often
highly influential in determining habitat suit-
ability and population persistence in fragmented
landscapes (Robinson et al. 1995a, Donovan et
al. 1997, Howell et al. 2000). Like the work fo-
cusing explicitly on edges, this landscape-scale
research is showing that the importance of hab-
itat edges varies from species to species and
from landscape to landscape. Thus, it is increas-
ingly clear that informed habitat management
will necessitate the incorporation of our increas-
ing understanding of the role of habitat edges in
fragmented landscapes into predictive models
that will allow assessment of alternative man-
agement options in novel landscapes. Most mod-
eling efforts addressing birds in fragmented hab-
itats have focused on the loss of habitat area and
the isolation of remnant patches, typically fo-
cusing on a single species (e.g., Thomas 1990,
Noon and Sauer 1992, Pulliam et al. 1992).
However, models that focus on habitat patches
in isolation from matrix and edge effects olen
prove to be disappointing in management situ-
ations (see Saunders et al. 1991). An integrated
approach for assessing edge responses and pre-
dicting the impacts of increasing edge habitat is
needed before the influence of habitat edges can
be incorporated into assessments of the effects
of habitat fragmentation.
Effective management of habitat edges re-
quires knowledge of population-level responses
and a conceptual framework for linking this un-
derstanding to spatially explicit information
about the landscape. Area-based approaches that
treat the edge as an area influenced by adjacent
habitats, rather than as a separate habitat type,
show some promise for guiding management de-
cisions. In addition, predictive models oflr a
powerful means for advancing our understand-
ing of the mechanisms that drive observed pat-
terns. The generation of explicit predictions
based on empirical measures of species-specific
edge responses, followed by field tests and mod-
el revision, offer the possibility of more rapid
progress in understanding edge effects.
Temple (1986) presented a simple, straight-
forward approach for including edge effects into
a patch-based model of arian abundance. He as-
sumed that the effects of nest predators and par-
a. Total area 47 ha,
core area 20 ha
b. Total area 39 ha,
core area 0 ha
FIGURE 7. Temple's (1986) original core area model
of edge effects used sensitivity to edge as a predictor
of habitat use by forest-interior birds. The model as-
sumed that edge effects, in general, penetrate 100 m
into a forested patch, dramatically infuencing the
"core area" of suitable habitat within a forest patch
(contrast panels a, b). The approach motivated a series
of efforts that placed edge effects in landscape context
and considered edge effects in predictions of the im-
pacts of habitat fragmentation.
asites penetrate about 100 m into remnants of
midwestern forest and woodland patches, and
that the abundances of species that are "sensi-
tive to fragmentation" would be low or zero
within 100 m of the edge patch. He found that
linear regressions of species' abundances against
the "core area" of the patch--the area greater
than 100 m from the edge--were significantly
stronger than regressions against total patch
area. This idea provided a conceptual foundation
for incorporating the effects of edges and patch
shape into patch-based approaches to estimating
habitat suitability (Fig. 7). Subsequent work re-
laxed some of the assumptions of the core area
model, allowing the distance of edge penetration
to vary among species (Temple and Cary 1988)
and to vary monotonically with distance from
the edge (Laurance and Yensen 1991), adding
realism to the approach.
Extension of the core area approach to ad-
dress all species--those with edge-exploiting as
well as edge-avoiding responses--and multiple
habitat and edge types, led to the effective area
model (EAM; Sisk and Margules 1993, Sisk et
al. 1997, Sisk and Haddad 2002). EAM ap-
proaches predict species abundances (or other
variable of interest) in any number, size, or
EDGE EFFECTS AND AVIAN ECOLOGY--Sisk and Battin 41
Patch-specific
population
estimate:
N = E(A, d,)
150m 50m EDGE 50m 150m
Chaparral Oak Wood/and
FIGURE 8. Schematic of the effective area model
(EAM). Sisk et al. (1997) extended the core area ap-
proach to multiple habitat and edge types, using digital
habitat maps to describe landscape pattern. The EAM
incorporates variation in edge responses among species
and at different edge types to estimate the abundances
of the breeding bird community in any number of
patches of any shape.
shape of habitat patches by projecting density
estimates from species-specific edge response
curves onto digitized maps of all the habitat
patches within the focal landscape. The predict-
ed density of each species within each patch
varies with distance from the edge. In the dis-
crete approach illustrated in Figure 8, the patch
is divided into sub-regions. These sub-regions
correspond to the distance intervals used for
field surveys of species abundances, which are
used to define species-specific edge responses,
illustrated here by the bar graph for Spotted To-
whee (Pipilo maculatus). Multiplying the area of
each sub-region by the corresponding estimate
of population density, and then summing the
products for all sub-regions, gives a predicted
population size for the species in a particular
patch (Fig. 8). The degree to which the predicted
density differs from predictions that assume
equal abundance throughout the patch reflect the
importance of "edge effects." Sisk et al. (1997)
reported that the EAM performed significantly
better than a null model that ignored edge effects
and estimated bird abundances based on patch
area alone. Other applications of the EAM are
presented in Sisk and Haddad 2002.
Several practical considerations influence how
the core area and effective area models are ap-
plied. First, the spatial resolution of the edge re-
sponse measured (i.e., the magnitude of the re-
sponse at various distances from the edge) de-
termines the spatial resolution of the edge ef-
fects modeled. Therefore, the sampling design
and survey techniques for measuring the edge
response should be scaled to the life history
characteristics (e.g., territory size, vagility) of
the animals being studied. Logistic and meth-
odological limitations often constrain sampling
designs somewhat, but the variety of proven
methods for sampling avian populations pro-
vides flexibility in quantifying edge responses
and facilitates the application of these patch-
based models to birds operating at different spa-
tial scales. In complex, heterogeneous land-
scapes, detailed habitat maps reflecting species-
specific requirements are needed. Advances in
mapping technologies and the application of re-
motely sensed data to habitat mapping (e.g.,
Scott et al. 1993, Imhoff et al. 1997), offer
promise for rapid and cost-efficient methods for
mapping habitats across large regions.
EDGE EFFECTS IN THE WEST:
IMPLICATIONS FOR STUDIES OF
HABITAT FRAGMENTATION
After 60 years of attention and relatively little
progress toward articulating general principles
pertaining to edge effects, it might be tempting
to conclude that the topic is intractable. Indeed,
the early adoption of simplistic rules of thumb
regarding habitat edges--for example, that more
edge leads to higher diversity--may have led to
poor habitat management and stalled progress in
identifying the mechanisms underlying edge ef-
fects. However, slow progress in the past is not
a reason to ignore the compelling reasons for
expanding mechanistic and management-rele-
vant research in the future.
Why study edge effects? First, anthropogenic
disturbances are rapidly increasing the preva-
lence of edges in most terrestrial landscapes.
This process is sure to continue, and ignoring
edge effects will become increasingly debilitat-
ing to conservation efforts. Edge effects may
compound the effects of habitat loss and the iso-
lation of fragments on the distribution, abun-
dance, and persistence of many sensitive bird
species. Second, edges are amenable to manage-
ment. The area of habitat protected and its lo-
cation are often the result of societal decisions
based on many factors that often lie outside the
purview of conservation biologists. However,
management of boundaries often is left to the
discretion of the manager. Better understanding
of the influences of edges on bird populations
will lead to more effective strategies for man-
aging habitat fragments. Third, edges are inher-
ently dynamic environments and, therefore, they
offer opportunities for studying avian responses
to changing landscape pattern.
What do we know? Not nearly enough, but
42 STUDIES IN AVIAN BIOLOGY NO. 25
the numerous studies from eastern North Amer-
ica offer some important lessons tbr those pur-
suing studies in western landscapes undergoing
fragmentation.
ß Our understanding of the many biological
phenomena associated with habitat edges is
dominated by the description of patterns from
eastern forests.
ß Western landscapes are, in general, more nat-
urally heterogeneous than their eastern coun-
terparts, and edges are common components
in many landscapes (e.g., riparian corridors).
ß The relationship between natural heterogene-
ity and avian sensitivity to the increased prev-
alence of edge due to habitat fragmentation is
not well understood.
ß Mechanistic explanations for avian responses
near habitat edges are, in general, poorly de-
veloped and inadequately tested. Work in the
West should pursue mechanistic understand-
ing and predictive capabilities of use to hab-
itat managers.
These lessons, derived from our review of an
extensive literature on edge effects and aug-
mented by landscape-scale studies of avian re-
sponses to habitat fragmentation, argue that edge
effects occur commonly in many habitats, that
they are of increasing importance as habitats be-
come more fragmented, and that we currently
know too little about what causes them to pre-
dict accurately where and to what degree they
will influence bird populations. This knowledge
should be sufficient to inspire a more focused,
and hopefully more fruitful, effort to understand
the many driving factors underlying edge effects
and to incorporate this knowledge into strategies
for avian conservation.
ACKNOWLEDGMENTS
We are indebted to L. Ries whose role in designing
the edge review was fundamental to our efforts. We
also thank P. Paton and J. Faaborg for insightful com-
ments on an earlier version of this manuscript. Our
work was supported by the Strategic Environmental
Research and Development Program (project CS-
1 00).
EDGE EFFECTS AND AVIAN ECOLOGY--Sisk and Battin 43
I oo+++o+++++oo+++ - I o +
¸ ¸ ¸
44 STUDIES IN AVIAN BIOLOGY NO. 25
+++
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EDGE EFFECTS AND AVIAN ECOLOGY--Sisk and Battin 45
+ ++ +++ I
46 STUDIES IN AVIAN BIOLOGY NO. 25
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EDGE EFFECTS AND AVIAN ECOLOGY--Sisk and Battin 47
48 STUDIES IN AVIAN BIOLOGY NO. 25
<<<
Studies in Avian Biology No. 25:49-64, 2002.
EFFECTS OF FIRE AND POST-FIRE SALVAGE LOGGING ON
AVIAN COMMUNITIES IN CONIFER-DOMINATED FORESTS OF
THE WESTERN UNITED STATES
NATASHA B. KOTLIAR, SALLIE J. HEJL, RICHARD L. HUTTO, VICTORIA A. SAAB,
CYNTHIA P. MELCHER, AND MARY m. MCFADZEN
Abstract. Historically, fire was one of the most widespread natural disturbances in the western United
States. More recently, however, significant anthropogenic activities, especially fire suppression and
silvicultural practices, have altered fire regimes; as a result, landscapes and associated communities
have changed as well. Herein, we review current knowledge of how fire and post-fire salvaging
practices affect avian communities in conifer-dominated forests of the western United States. Specif-
ically, we contrast avian communities in (1) burned vs. unburned forest, and (2) unsalvaged vs.
salvage-logged burns. We also examine how variation in burn characteristics (e.g., severity, age, size)
and salvage logging can alter avian communities in burns.
Of the 41 avian species observed in three or more studies comparing early post-fire and adjacent
unburned forests, 22% are consistently more abundant in burned forests, 34% are usually more abun-
dant in unburned forests, and 44% are equally abundant in burned and unburned forests or have varied
responses. In general, woodpeckers and aerial foragers are more abundant in burned forest, whereas
most foliage-gleaning species are more abundant in unburned forests. Bird species that are frequently
observed in stand-replacement burns are less common in understory burns; similarly, species com-
monly observed in unburned forests often decrease in abundance with increasing burn severity. Gran-
ivores and species common in open-canopy forests exhibit less consistency among studies. For all
species, responses to fire may be influenced by a number of factors including burn severity, fire size
and shape, proximity to unburned forests, pre- and post-fire cover types, and time since fire. In addition,
post-fire management can alter species' responses to burns. Most cavity-nesting species do not use
severely salvaged burns, whereas some cavity-nesters persist in partially salvaged burns. Early post-
fire specialists, in particular, appear to prefer unsalvaged burns. We discuss several alternatives to
severe salvage-logging that will help provide habitat for cavity nesters.
We provide an overview of critical research questions and design considerations crucial for evalu-
ating the effects of prescribed fire and other anthropogenic disturbances, such as forest fragmentation.
Management of native avifaunas may be most successful if natural disturbance regimes, including fire,
are permitted to occur when possible. Natural fires could be augmented with practices, such as pre-
scribed fire (including high-severity fire), that mimic inherent disturbance regimes.
Key Words: burn severity; cavity-nesters; fire effects; fire suppression; passerine birds; prescribed
fire; salvage logging; silviculture; snags; wildland fire; woodpeckers.
Understanding the consequences of anthropogen-
ic activities that alter natural systems requires a
thorough knowledge of the natural disturbance re-
gimes that shape communities and landscapes.
Often, the ecological consequences of anthropo-
genic activities have been evaluated in the con-
text of relatively undisturbed, mature forest (e.g.,
Whitcomb et al. 1977, Mladenoff et al. 1993,
King et al. 1997, Morse and Robinson 1999).
However, this approach may be inadequate for
systems that evolved with major and persistent
disturbances, such as fire. In the West, fire has
played a dominant role in shaping communities
and landscapes. Thus, one of the greatest threats
to the ecological integrity of western forest sys-
tems may be alteration of natural disturbance re-
gimes and landscape structure through livestock
grazing, fire suppression, logging in burned for-
ests (hereafter "salvaging" or "salvage log-
ging"), and other silvicultural activities.
Concern that decades of fire suppression may
lead to more frequent, larger wildfires has
prompted government agencies to expand pre-
scribed-burning programs and fire-management
policies to diminish the chances of large, severe
wildfires (U.S. Dept. of Interior and U.S. Dept.
of Agriculture 1998). Unfortunately, our under-
standing of historical fire regimes remains rudi-
mentary and may be inadequate for setting such
goals (Tiedemann et al. 2000). Furthermore, the
new government-sanctioned program of prescrip-
tion burning focuses on reducing fuel loads, with
relatively little consideration given to the efikcts
on wildlife (Tiedemann et al. 2000). In part, this
problem stems from a paucity of rigorous field
studies that have evaluated the eflkcts of fire on
wildlife communities. Without a better under-
standing of how historical fire regimes influenced
communities (Bunnell 1995) and landscapes, as
well as how anthropogenic activities have altered
fire regimes, programs of prescription burning
and other mitigation measures could be as mis-
guided as widespread fire suppression.
In the review and discussion that follow, we
49
50 STUDIES IN AVIAN BIOLOGY NO. 25
examine avian communities in post-fire forests
in conifer-dominated systems of the West, and
compare them to those in unburned forests. We
focus in particular on the responses of wood-
peckers and passefine birds. Because avian re-
sponses to fire may vary with burn severity and
size, time since fire, ecological contexts of
burns, and post-fire salvage logging, these issues
are also discussed. We preface our review by
providing an overview of historical fire regimes
of western forests and how human activities,
particularly fire suppression, may have altered
those regimes. This background is essential for
understanding the patterns observed among avi-
an communities using unburned and burned for-
ests. We conclude with a discussion of compel-
ling management implications that arise from
this review, and we identify essential research
questions for improving and enlarging our un-
derstanding of how fire shapes and perpetuates
avian communities in western forests.
FIRE REGIMES IN CONIFEROUS FORESTS
OF THE WESTERN UNITED STATES
Although current knowledge of historical fire
regimes in western forests remains somewhat ru-
dimentary, it is possible to place those systems
into broad fire-regime categories. The regime
that characterizes any one system is an interplay
between gradients in burn severity and fire fre-
quency (i.e., fire-return interval). Generally,
burn-severity gradients are divided into three
levels, based on vegetation responses to fire: (1)
low-severity fires kill or temporarily remove
above-ground portions of herbaceous and un-
derstory layers and sometimes scorch the lower
portions of mature trees, typically without kill-
ing them; (2) moderate-severity fires may kill
but usually do not consume leaves of canopy
trees, although some tree mortality may result;
and (3) high-severity fires usually burn the can-
opy, killing the majority of trees (Agee 1993).
One level of burn-severity may dominate a giv-
en burn, but most burns are mosaics of various
fire sevefities (Agee 1993, Turner et al. 1994).
Furthermore, there is variation among tree spe-
cies' responses to fire intensity (e.g., heat). For
example, the thick, fire-retardant bark of mature
ponderosa pines (Pinus ponderosa) generally
provides them protection from understory fires,
whereas subalpine firs (Abies lasiocarpa) are of-
ten killed by understory fires (Agee 1993). Un-
derstory fires also typically kill the above-
ground biomass of quaking aspen (Populus tre-
rnuloides) stands, although lateral roots readily
respond to fire by resprouting vigorously (Agee
1993). Thus, variations in burn severity can have
profound effects on the composition and struc-
ture of plant communities.
For simplicity, most forest systems of the
West can be characterized by one of three fire-
regimes based on the effects of fire intensity on
the dominant tree species: high frequency/low
severity, moderate frequency and moderate to
high severity, or low frequency/high severity
(Agee 1993, 1998). High frequency/low severity
fires (i.e., 1- to 40-yr fire-return intervals) are
characteristic of many dry, warm forests. The
combination of dry conditions and pervasive
surface fuels (grasses and duff) allows fire to
recur frequently. Many tree species in these sys-
tems are adapted to fire (e.g., fire-retardant bark,
seedling germination requires bare substrates).
Generally, fires in these systems are restricted to
herbaceous and understory layers, thereby elim-
inating the majority of saplings and perpetuating
a discontinuous forest canopy. Examples of such
systems include ponderosa pine forests of foot-
hills along the Rocky Mountains and Sierra Ne-
vada (Arno 1980, Verner and Boss 1980,
McKelvey et al. 1996).
In forests characterized by intermediate mois-
ture and temperatures, fire regimes are generally
moderate in severity and frequency, although in
many cases severity can be high (Agee 1993,
1998). The mix of burn severities often results
in heterogeneous burns and multiple-age struc-
tures of dominant trees (Agee 1993, 1998). Fire-
return intervals tend to be longer (40-150+ yr)
than those in drier sites, but can be quite variable
(Agee 1993). Examples of this type of system
include red fir (Abies magnifica) and coastal red-
wood (Sequoia sernpervirens) in California
(Agee 1993, 1998).
Low frequency/high severity fire regimes typ-
ically result in stand-replacement events. Because
of the long fire intervals, trees in these systems
often lack the ability to withstand fire (Agee
1993), although some species have reproductive
adaptations to fire (e.g., serofinous cones of lod-
gepole pine, Pinus contorta; Agee 1993). Typi-
cally, climatic conditions (e.g., severe drought
and strong winds) necessary for these systems to
bum occur only several times per century, and
fires spread only if sufficient fuels have accu-
mulated (Romme 1982). Once started, fires in
these systems often burn vast areas and may last
for months (Agee 1993). Regeneration in larger
bums can take decades if viable seed sources are
distant (Agee 1993). Fire return intervals range
from 200-300 years in lodgepole pine forests
(Romme 1982, Veblen 2000) to more than 1000
years for some cedar/spruce/hemlock forests of
the Pacific Northwest (Agee 1993).
Local factors, such as elevation, topography,
and climate, can modify the general fire regimes
described above. For example, surface fires may
occur less frequently in naturally dense systems
FIRE EFFECTS ON AVIAN COMMUNITIES--Kotliar et al. 51
of ponderosa pine with limited herbaceous cov-
er; in turn, canopy fuels may become sufficiently
dense to support crown fires (Shinneman and
Baker 1997, Brown et al. 1999, Veblen 2000).
Especially high probabilities of lighting strikes
in mountainous terrain may result in small, fre-
quent surface fires that often perpetuate open
meadows in moist forests (Agee 1993, Veblen
2000). Overall, the complex mosaic of western
forest systems has been shaped by an equally
complex mosaic of fire regimes.
CHANGES IN FIRE REG1MES
Attempts to understand how contemporary
human activities have altered natural fire re-
gimes are fraught with difficulties. Fire regimes
are inherently dynamic, largely due to variations
in climate, both long-term (Clark 1988, Romme
and Despain 1989, Johnson et al. 1990) and
short-term (e.g., E1 Nifio-driven events; Swet-
nam and Betancourt 1990, Veblen et al. 2000).
In ponderosa pine systems, the degree to which
severe fires result from the long-term accumu-
lation of fuels due to fire suppression or the
short-term accumulation and desiccation of fine
fuels following E1 Nifio/Southern Oscillations is
poorly understood and can vary among sites
(Veblen et al. 2000). Likewise, decades of fire
suppression at Yellowstone National Park, which
may have delayed the onset of extensive fires,
were apparently overshadowed by severe
drought and high winds in August 1988 (Rom-
me and Despain 1989). Thus, the relative con-
tributions of fire suppression and climate on ex-
treme fire behavior remains unclear.
The relatively ephemeral nature of fire records
(e.g., fire scars, stand cohorts) limits our recon-
struction of fire histories for most locations (but
see Agee 1998). Charcoal deposits in lake-bed
sediments have revealed longer histories (Mills-
paugh and Whitlock 1995), but they are influ-
enced strongly by prevailing winds and water-
shed dynamics so that the overall area they rep-
resent may be quite limited. Historic accounts of
fire behavior and forest conditions during Euro-
American settlement can also be biased (Wagner
et al. 2000). Furthermore, humans have influ-
enced fire regimes in North America for at least
6,000-10,000 years. Native Americans used fire
in warfare and for driving game (Stewart 1956),
and Euro-American settlers used fire to clear
land for mining, logging, and even in land dis-
putes (Veblen and Lorenz 1991); settlers also
caused many accidental fires (Johnson et al.
1990). Extensive livestock grazing after the mid-
1800s coupled with effective fire suppression
(particularly after World War II) led to structural
changes in forest stands (Saab et al. 1995),
which altered fire regimes further (Madany and
West 1983, Covington and Moore 1994; but see
Swetnam et al. 1999). Thus, it is difficult to de-
termine what constitutes "natural" or "anthro-
pogenic" changes to fire regimes. For the pur-
poses of this review, we focus on anthropogenic
changes that began in the mid 1800s, including
grazing, unprecedented fire suppression, and
large-scale silvicultural activities (e.g., wide-
spread clearcutting, salvage logging).
Effects office suppression
Given the complexity and limited understand-
ing of historical fire regimes, the full ramifica-
tions of fire suppression remain unknown. Cer-
tainly, the long-term, global-scale effects of fire
suppression and their potential interactions with
climate changes caused by anthropogenic activ-
ities are cause for concern (Leenhouts 1998). On
a continental scale, however, it is clear that fire
suppression over the last six or seven decades
has reduced the number of fires and the total
area burned across the U.S. (Ferry et al. 1995).
Using satellite imagery, maps of potential natu-
ral vegetation, and estimated fire regimes, Leen-
houts (1998) concluded that only 8-14% of the
area that burned annually in the conterminous
United States 200-500 yr ago still burns today.
In western forest systems, effects of fire sup-
pression vary with forest type and inherent fire
regime, as well as accessibility (Romme 1982). In
many systems adapted to high-frequency/low-se-
verity fire regimes (e.g., ponderosa pine), changes
in forest structure since Euro-American settlement
have included increased stem densities resulting
from decreased mortality of saplings and increased
recruitment, and changes in species composition
(Gruell 1983, Veblen and Lorenz 1991, Covington
and Moore 1994, Swetnam and Baisan 1996, Bel-
sky and Blumenthal 1997, Allen 1998). Accumu-
lation of fuels may promote more extensive, severe
fires than those that occurred prior to Euro-Amer-
ican settlement (Barrett 1988, Covington and
Moore 1994, Lissoway 1996, Covington et al.
1997, Fule et al. 1997, Veblen et al. 2000). How-
ever, wetter climates post-settlement may also con-
tribute to a decrease in fire frequency (Veblen et
al. 2000, Wagner et al. 2000).
The consequences of fire suppression in forests
characterized by infrequent fires of high severity
(e.g., high-elevation spruce-fir forests of the central
Rockies) are less apparent, in part because the lon-
ger fire-return intervals may delay, or reduce, the
effects of fire suppression (Romme 1982, Romme
and Despain 1989, Veblen 2000). Even in regions
where the frequency of fires has declined, burn
severity may not have changed (Romme and Des-
pain 1989). Although the relative contribution of
climate and fire suppression is debatable, clearly
52 STUDIES IN AVIAN BIOLOGY NO. 25
the effects of both have influenced fire regimes
across western landscapes.
Other human activities may amplify or con-
found the effects of fire suppression. Overgrazing
by livestock or elevated populations of native un-
gulates protected from wolf predation may di-
minish fire frequency (Hess 1993, Belsky and
Blumenthal 1997). For example, during the late
1800s to early 1900s, livestock grazing in many
ponderosa pine systems led to decreased surface
fuels and increased areas of exposed soil; the re-
sult was diminished fire frequencies and in-
creased germination and survival of tree seed-
lings (Swetnam and Baisan 1996, Veblen 2000).
In addition, the combined effects of fire suppres-
sion, grazing, and contemporary silvicultural
practices in many western forests has promoted
the growth of dense, monospecific, even-aged
stands (Swetnam et al. 1995, Fule et al. 1997). In
turn, this stand structure is believed to present
opportunities for more extensive outbreaks of
tree-damaging insects than would have occurred
prior to the mid-1800s when stands were ofien
more open and complex in structure (Swetnam et
al. 1995, Veblen 2000, Veblen et al. 2000). Wide-
spread tree mortality resulting from insect out-
breaks can increase a given stand's susceptibility
to fire. Although our current knowledge of the
interactive effects of fire suppression and other
factors is limited, it has become clear that these
factors can alter fire regimes significantly.
EFFECTS OF FIRE AND SALVAGE
LOGGING ON AVIAN COMMUNITIES
Understanding fire regimes in western forests
is essential to understanding forest structure,
overall landscape patterns, and the responses of
bird communities to fire. Fire affects avian nest-
ing and foraging activities by generating snags,
altering insect communities, eliminating foliage,
and altering the size, abundance, and distribution
of tree species across the landscape (Finch et al.
1997, Huff and Smith 2000). The degree to which
fire affects any of these factors depends, in part,
on the severity and ecological context of a par-
ticular burn. A thorough understanding of the in-
fluence of fire and fire-management activities,
such as prescribed burning and post-fire salvage
logging, on avian communities is essential to both
conservation biology and sound management.
Here, we summarize the best current knowl-
edge about the influence of fire and salvage log-
ging on avian communities in conifer-dominated
forests (which often include quaking aspen) of
the West. Most of the relatively few published
studies were conducted in the northern Rocky
Mountains. Because these studies encompassed
many cover types and were usually poorly rep-
licated, many of our conclusions are prelimi-
nary. However, some general patterns, as well
as a number of questions, have emerged from
four comparisons: (1) avian abundance in
burned and unburned forests, (2) avian abun-
dance among different fire severities, (3) chang-
es in avian-community structures associated
with post-fire forest succession, and (4) nesting
patterns of cavity-nesting birds in salvaged and
unsalvaged, burned forests.
AVIAN ABUNDANCE IN RECENTLY BURNED AND
UNBURNED FORESTS
We summarized the results of 11 studies that
compared the abundance of breeding bird spe-
cies in early post-fire burns and adjacent mature,
unburned forests (Tables la-lc; Fig. 1). Al-
though "unburned" forests may have burned
previously, these forests were largely mature
(i.e., late-successional). All 23 burns surveyed
were severe (predominantly stand-replacement)
and less than 10 yr old (most were <4 yr old).
All but a few burns were greater than 400 ha,
and four burns were greater than 1400 ha. Co-
nifers, including ponderosa pine/Douglas-fir
(Pseudotsuga menziesii), Jeffrey pine (Pinus jef-
fryi)/white fir (Abies concolor), lodgepole pine,
spruce/fir, and mixed conifers, were the domi-
nant cover types. The studies covered seven
western states; seven studies were conducted in
the northern Rocky Mountains, one was in the
southern Rocky Mountains, two were in the Pa-
cific Northwest, and one was in the Pacific
Southwest (Fig. 1). Studies of post-fire bird
communities that were older than 10 yr, were
predominantly aspen or riparian, or sampled
only burn edges were excluded from analysis.
For each species present in >--3 of the 11 stud-
ies, we classified abundance patterns into three
response classes by study: (1) occurred only in
burns or abundance was >-50% higher in burns
than in unburned forest; (2) occurred only in un-
burned forest or abundance was >-50% higher in
unburned than in burned forest; and (3) results
varied among samples or there were similar
abundances in burned and unburned forest (Ta-
bles la-lc). Because only one study (Johnson
and Wauer 1996) included both pre- and post-
fire surveys, we used this comparison of abun-
dance patterns to infer response to fire.
Many species showed remarkably consistent
patterns, despite the wide geographic area and va-
riety of cover types surveyed. Species that com-
monly occurred in burns, but were uncommon or
absent in unburned forests (Table la), included
Black-backed Woodpecker, Three-toed Wood-
pecker, Olive-sided Flycatcher, and Mountain
Bluebird (see Appendix for species' scientific
names). Species that used unburned forests, but
rarely occurred in early post-fire forests (Table
FIRE EFFECTS ON AVIAN COMMUNITIES--Kotliar et al.
TABLE 1. SUMMARY OF AVIAN ABUNDANCES IN BURNED AND UNBURNED FORESTS
53
Response categories (number of studies)
Similar
abundance
More abundant or response
Species in burns mixed
More abundant
in unbumed
(A) Typically more abundant in burns
Three-toed Woodpecker 8 a, b, d, e, g, h, i, j
Black-backed Woodpecker 6 b, d, e, i, j, k
Olive-sided Flycatcher 8 a, c, d, f, g, h, i, k
Mountain Bluebird 9 a, b, c, d, g, h, i,j, k
Western Wood-Pewee 7 a, c, d, g, h, i, j
Hairy Woodpecker 8 a, b, c, e, f, g, h, j 2 d, i
House Wren 5 a, b, d, g, j 1 h
Tree Swallow 4 b, h, i, j
Northern Flicker 5 a, c, f, i, j 3 b, g, h
(B) Typically exhibited mixed or neutral response to burns
Mourning Dove 2 d, h
Common Nighthawk 2 c, h
Cassin's Finch 4 c, h, i, j
Pine Siskin 3 c, f, i
Chipping Sparrow 2 a, c
Dark-eyed Junco 3 c, f, i
American Robin 4 a, f, J, k
Townsend's Solitaire 1 f
Hammond's Flycatcher 1 f
Clark's Nutcracker 2J, h
Red-naped Sapsucker I h
Western Tanager 1 c
White-breasted Nuthatch I a
Evening Grosbeak lg
Pygmy Nuthatch I a
Yellow-rumped Warbler
WilliamsoWs Sapsucker 1 a
Red Crossbill
(C) Typically more abundant in unburned forests
Steller's Jay 1 g
Plumbeous/Cassin's Vireo lg
Warbling Vireo lg
Gray Jay 2 , h
Ruby-crowned Kinglet 2g, h
Brown Creeper 2 f, g
Red-breasted Nuthatch 1 g 2 h, i
Hermit Thrush 1 c
Mountain Chickadee
Golden-crowned Kinglet
Townsend's Warbler
Swainson's Thrush
Varied Thrush
1 g
3a, d, g
3d, g, h
4g, h, i, j
5a, d, g, h, j
5c, d, g, h, i
5a, c, d, g, h
3d, g, h
2 d, g
lg
4d, g, h,
lg
1 h
5a, c, g, i, k
lg
2g, h
1 ½
1 c
I d
l i
2 a, b
2a, J
1 d
1 d
2g , h
3 d, h,j
2 h, i
l d
3a, f, h
2 a, h
2 d, h
3 f, i,j
3d, i, j
5a, d, h, i, j
6a, b, d, f, j, k
5a, g, h, i, j
6a, g, h, i, j, k
6a, d, f, h, j, k
3d, f, k
3d, J, k
3d, 1', k
Notes: Only species observed in three or more studies were included. More abundant in burns - only occurred in bums or abundance was >50%
higher in early post fire forests than unburned forest; similar or mixed - abundance was similar in burned and unburned forest or results varied
among samples; more abundant in unburned occurred only in unburned forest or abundance was >50% higher in unburned than early post-fire
forests.
aBock and Lynch 1970.
b Caton 1996.
c Davis 1976.
d Hairis 1982.
e Hoffman 1997.
t Huff 1984, Huff et al. 1985.
g Johnson and Wauer 1996.
h N. Kotliar and C. Melcher, unpubl. data.
Pfister 1980.
Taylor and Bannore 1980.
k R. Sallabanks and J. Mclver, unpubl. data.
54 STUDIES IN AVIAN BIOLOGY NO. 25
FIGURE 1. Approximate location of study sites re-
ferred to in Table 1. Center location of study area is
indicated in cases where multiple burns were surveyed.
References (dominant cover type; number of burns;
survey years post-fire): A--Bock and Lynch 1970 (Jef-
frey pine/white fir; 1 burn; 6-8 yrs); B--Caton 1996
(lodgepole pine; 1 bum; 2-4 yrs); C--Davis 1976
(lodgepole pine; 2 burns; 6 yrs, 9 yrs); D--Harris 1982
(ponderosa pine/Douglas fir; 2 burns; 2-4 yrs, 2 yrs);
E-Hoffman 1997 (lodgepole pine; 2 bums; 1-2 yrs);
F--Huff 1984, Huff et al. 1985 (w. hemlock/Douglas
fir; I burn; 1-3 yrs); G--Johnson and Wauer 1996
(ponderosa pine; 1 bum; 1 yr pre-fire; 3 yrs); H--N.
Kotliar and C. Melcher, unpubl. data (ponderosa pine;
lodgepole; spruce/fir; mixed conifer; 8 burns; varied
from 0-8 yrs); IPfister 1980 (lodgepole pine; 2
burns; 2 yrs, 4 yrs); J Taylor and Barmore 1980
(lodgepole pine; spruce/fir; 2 burns; 1-3 yrs, 5/7 yrs);
K--R. Sallabanks and J. Mclver, unpubl. data (mixed
conifers; I burn; 1-3 yrs).
lc), included Mountain Chickadee, Golden-
crowned Kinglet, Hermit Thrush, Varied Thrush,
and Townsend's Warbler. Generally, wood drillers
and aerial insecfivores were more abundant in
early post-fire forests, whereas foliage and bark
gleaners were usually more abundant in unburned
forests. However, there were several exceptions
to this generalization. Overall, these results sug-
gest that species with either the strongest affinity
for, or aversion to, young burns are responding
primarily to the dramatic changes in structural
characteristics (e.g., increased availability of
snags, decrease in canopy coverage) and/or den-
sities of insect prey brought about by burning.
Numerous species showed more varied, or ap-
parently neutral, responses to bums (Table lb).
For example, Townsend's Solitaire, American
Robin, Dark-eyed Junco, Chipping Sparrow, and
Cassin's Finch were common in both burned and
unburned forests, indicating that both types of
forests often may provide suitable habitat for
these species. Many species, including Red-
breasted Nuthatch, Brown Creeper, Yellow-rom-
ped Warbler, and Western Tanager, were fre-
quently observed in burns, but typically reached
their highest abundance levels in unburned for-
ests. Many granivores, bark gleaners, and spe-
cies that prefer a mixed, open canopy had a var-
ied responses. The mixed results may be due, in
part, to the influence of site-specific character-
istics (see FACTORS THAT AFFECT SPECIES' RE-
SPONSES TO BURNS).
Several species observed in fewer than three
studies exhibited higher abundances in burned
compared to unburned forests, including Lewis's
Woodpecker (V. Saab, unpubl. data), Rock Wren,
Western Bluebird (N. Kotliar and C. Melcher, un-
publ. data), Lazuli Bunting (Bock and Lynch
1970), and White-crowned Sparrow (Pfister 1980;
N. Kotliar and C. Melcher, unpubl. data). Our
personal observations of these species suggest
that they readily use bums in certain contexts.
Although the generality of these observations is
unknown, the apparent suitability of burned for-
ests for these species warrants further study.
A comparison of bird abundances in more than
30 fires that burned in the northern Rockies in
1988, with bird abundances derived from the lit-
erature for nine other major Rocky Mountain for-
est cover types (Table 3 in Hutto 1995), generally
corresponds to the results of our review. Most of
the species that exhibited higher abundances in
burned forests (Table l a) were more commonly
observed in recently burned forests than in all
other mature forest types (Hutto 1995). Likewise,
species that exhibited higher abundances in un-
burned forests (Table lc) commonly occurred in
one or more mature forest types but were infre-
quently observed in recently burned forests (Hut-
to 1995); however, Mountain Chickadee and Red-
breasted Nuthatch occurred in a relatively high
percentage (52-74%) of the 1988 bums surveyed
by Hutto (1995). Many of the species that showed
a mixed or neutral response to bums (Table la)
also had a higher frequency of occurrence in ear-
ly post-fire forests compared to mature forest
types (Table 3 in Hutto 1995).
Some of the species that showed mixed pat-
terns across studies may use forest edges as well
as forest interiors (e.g., Mountain Chickadee,
Hermit Thrash; N. Kotliar and C. Melcher, un-
publ. data), and because some are rather nomad-
ic (e.g., Red Crossbill), the degree to which
bums represent suitable habitat cannot be in-
ferred easily from surveys that abut the edges of
bums. Further research is needed to determine
how various factors can alter the relative suit-
ability of burned and unburned forests for such
species (see next section).
FACTORS THAT AFFECT SPECIES' RESPONSES TO
BURNS
The suitability of bums for birds often will
depend on bum characteristics (e.g., severity,
FIRE EFFECTS ON AVIAN COMMUNITIES--Kotliar et al. 55
time since fire, burn geometry) and landscape
context (e.g., forest cover types), as well as re-
gional variation (Finch et al. 1997, Huff and
Smith 2000). To begin to address these issues,
we summarized the results of several studies that
evaluated how burn severity and time since fire
influenced bird communities. To provide impe-
tus for future studies, we also speculate (based
on personal observations and a few limited stud-
ies) about the ways in which burn characteristics
and context may contribute to variation in re-
suits among studies.
Burn severity
Three studies compared avian abundances
across various burn severities in reference to un-
burned forests. Taylor and Barmore (1980) ex-
amined two burn severities (moderate, severe) for
the first three yr post-fire in a 1414-ha burn in
lodgepole pine and spruce/fir forests in Grand Te-
ton and Yellowstone National Parks. Preliminary
results (first three yr post-fire) are available from
a study of a 9283-ha burn in Oregon in which
three burn severities (low, moderate, severe) were
examined in mixed coniferous forests (R. Salla-
banks, unpubl. data; R. Sallabanks and J. Mclver,
unpubl. data). In addition, preliminary results are
available for a comparison of two understory-pre-
scribed (1 yr post-fire, 200 ha, and 1-3 yr post
fire, 1200 ha) and two stand-replacement burns
(1 yr post fire, 200 ha, and 3 yr post-fire, 4450
ha) in ponderosa pine/Douglas-fir forests in Col-
orado (N. Kotliar and C. Melcher, unpubl. data).
The trends observed in the burn-severity studies
generally are consistent with the patterns we
found in our review of severely burned versus
unburned forest, which represented the extremes
of the burn-severity gradient (Tables la-c). The
general patterns presented here should be viewed
as preliminary and in need of further testing, giv-
en that two of the studies are unpublished and
only six burns were studied.
Many bird species whose abundances were
consistently higher in burned compared to un-
burned forests (Table l a) also appeared to use
stand-replacement burns more readily than low-
and moderate-severity burns. These species in-
cluded Black-backed Woodpecker (R. Sallabanks,
unpubl. data), Three-toed Woodpecker and Cas-
sin's Finch (Taylor and Barmore 1980; N. Kotliar
and C. Melcher, unpubl. data), Olive-sided Fly-
catcher (R. Sallabanks and J. McIver, unpubl.
data; N. Kotliar and C. Melcher, unpubl. data),
Mountain Bluebird (Taylor and Barmore 1980; R.
Sallabanks, unpubl. data; N. Kotliar and C.
Melcher, unpubl. data), and Western Bluebird (N.
Kotliar and C. Melcher, unpubl. data). Dark-eyed
Juncos occurred at similar abundances across all
burn severities (Taylor and Barmore 1980; N. Ko-
tliar and C. Melcher, unpubl. data).
Several species reached their highest abun-
dances in moderate-severity burns. Brown
Creeper and Chipping Sparrow exhibited highest
abundances in moderate-severity and severe
burns (Taylor and Barmore 1980). Townsend's
Solitaire was fairly abundant across all severi-
ties, but was most abundant in moderately se-
vere burns (N. Kotliar and C. Melcher, unpubl.
data). Western Tanager occurred at similar abun-
dances in moderately burned and unburned for-
ests, but was less abundant in severely burned
forests (Taylor and Barmore 1980). Cavity nest-
ing species that usually glean the bark of live
trees (e.g., nuthatches, Brown Creeper) may re-
spond positively to moderate-severity burns that
increase availability of snags for nesting, but re-
tain live trees for foraging. Species common in
open canopy forests (e.g., Townsend's Solitaire,
Western Tanager, Chipping Sparrow) may use
the mixed open canopy of moderate-severity
burns, whereas they may avoid large areas of
stand-replacement burns. Thus, the varied re-
sults observed for these species in our review of
severely burned and unburned forests (Table 1 b)
may reflect, in part, the heterogeneity of burn
severities within and across studies.
Species that were consistently more abundant
in unburned than in burned forests (Table 1 c) also
decreased in abundance with increasing burn se-
verity. These species include Plumbeous Vireo,
Steller's Jay, and Hammond's Flycatcher (N. Ko-
tliar and C. Melcher, unpubl. data), Gray Jay
(Taylor and Barmore 1980); Mountain Chickadee
(Taylor and Barmore 1980; R. Sallabanks, un-
publ. data; N. Kotliar and C. Melcher, unpubl.
data); Ruby-crowned and Golden-crowned king-
lets (Taylor and Barmore 1980; R. Sallabanks,
unpubl. data); Townsend's Warbler and Varied
Thrush (R. Sallabanks, unpubl. data). Many of
these species are foliage gleaners; thus their abun-
dance patterns probably reflect the incremental
loss of foliage area with increasing burn severity.
Several species showed slightly different pat-
terns across the three studies. Red-breasted Nut-
hatch and Yellow-rumped Warbler were least
abundant in severe burns across all three studies,
but their abundances varied across other severi-
ties (Taylor and Barmore 1980; R. Sallabanks,
unpubl. data; N. Kotliar and C. Melcher, unpubl.
data). Western Wood-pewee increased in abun-
dance with burn severity in a lodgepole pine burn
(Taylor and Barmore 1980), but was most abun-
dant in low-severity ponderosa pine burns (N.
Kotliar and C. Melcher, unpubl. data). Again, var-
iation in results among studies may be due to the
heterogeneity of burn severities both within and
among studies. Furthermore, if patches of low-
56 STUDIES IN AVIAN BIOLOGY NO. 25
I Open Canopy I
.................. [Closed Canopy ]
e-
Low High
Fire Severity
FIGURE 2. Conceptual model of the interactive ef-
fects of burn severity and forest structure on the den-
sity of avian species preferring open forest structure.
In open-canopy forests (e.g., ponderosa pine) avian
densities are high in unburned forests but may be low
in severely burned forests. In closed-canopy forests
(e.g., lodgepole pine), avian densities are low, but may
increase as fire opens up the forest canopy. Thresholds
responses to degree of burn severity may result in de-
parture from linear relationships depicted here.
and moderate-severity burns occur along the burn
periphery, as is often the case, it may be difficult
to differentiate between the influence of burn se-
verity and edge effects (i.e., the juxtaposition of
burned and unburned forest).
Interactions between burn severity and pre-
fire forest structure also may lead to mixed re-
sponses to burn severity, particularly for bird
species that are sensitive to differences in can-
opy coverage (Fig. 2). Some species that occur
in open-canopy forests (e.g., Western Wood-pc-
wee, Western Tanager) are common in unburned
ponderosa pine forests but uncommon in stand-
replacement burns in this cover type (N. Kotliar
and C. Melcher, unpubl. data). In contrast, these
species may be uncommon in dense lodgepole
pine (Pinus contorta) forests, but common im-
mediately following stand-replacement fires in
lodgepole pine forests (N. Kotliar, unpubl. data).
Such interactions makes it difficult to predict
how a species will respond to burns without a
better understanding of how context (e.g., cover
type, canopy closure, regional differences, pre-
vious silvicultural treatments) can alter suitabil-
ity of burned forests for a particular species.
Post-fire succession and associated changes in
.[orest structure and arian communities
No studies have followed bird communities
from early through late successional stages after
fire (but see Bock and Lynch 1970, Bock et al.
1978, Raphael et al. 1987, Johnson and Wauer
1996); therefore, to examine changes in bird
communities from early successional to mature
forests we also rely on comparisons of stands
that vary in time since fire (e.g., Peterson 1982,
Huff et al. 1985). In general, forest structure and
avian communities change fairly rapidly after
fire, although the rates of change depend, in part,
on burn severity as well as pre- and post-fire
cover type. Because tree mortality is low, and
ground cover often rapidly resprouts, evidence
of fire in understory burns may be minimal with-
in a few years after fire. In contrast, stand-re-
placement burns may persist as a forest of snags
for decades. The structure of burned snags typ-
ically changes within the first few years. First,
needles (if remaining) and smaller branches are
shed, then bark and larger branches slough
away. Smaller snags typically decay faster than
larger snags (Morrison and Raphael 1993, Bull
et al. 1997). Factors such as topography, root
depth, moisture regime, wind, and tree species
can all influence how long snags remain stand-
ing, which may exceed a century.
Early post-fire forests and associated insect
outbreaks attracts cavity-nesting birds due to in-
creases in nest sites and food supplies (e.g.,
Blackford 1955, Koplin 1969, Lowe et al. 1978,
Raphael and White 1984, Bock et al. 1978, Saab
and Dudley 1998). Duration of occupancy, how-
ever, varies among bird species, presumably due
to differences in preferred prey availability, as
well as the size, distribution, and age of snags.
Black-backed and Three-toed woodpeckers rap-
idly colonize stand-replacement burns within
one to two years of a fire; within five years,
however, they become rare, presumably due to
declines in bark and wood-boring beetles (Ko-
plin 1969, Bock and Lynch 1970, Bock et al.
1978, Bull 1980, Taylor and Barmore 1980, Ap-
felbaum and Haney 1985, Dixon and Saab
2000). In contrast, Lewis's Woodpecker is re-
ported to be abundant both in recent burns (2-4
yr; Saab and Dudley 1998) and older burns (10-
25 yr; Bock 1970, Linder and Anderson 1998).
Hairy Woodpecker and Northern Flicker exhibit
more mixed responses, but usually decline with-
in the first 25 yr post-fire (Bock and Lynch
1970, Bock et al. 1978, Taylor and Barmore
1980, Huff et al. 1985, Raphael et al. 1987).
Mountain and Western bluebirds are secondary-
cavity nesters that commonly nest in recently
burned forests (e.g., Hutto 1995, Saab and Dud-
ley 1998; Table la), but they typically decline
in mid-successional stages (Bock and Lynch
1970, Bock et al. 1978, Pfister 1980, Peterson
1982, Raphael et al. 1987).
Vegetation regrowth after fire also can lead to
increases in flower, seed, and insect abundance,
which attracts nectarivores, granivores, and ae-
FIRE EFFECTS ON AVIAN COMMUNITIES--Kotliar et al. 57
rial and ground insectivores (Lowe et al. 1978,
Apfelbaum and Haney 1981, Huff et al. 1985).
Olive-sided Flycatcher may appear immediately
after fires (Table la; Hutto 1995; N. Kotliar and
C. Melcher, unpubl. data) and can persist as long
as snags are available and canopy cover remains
low (Huff et al. 1985; N. Kotliar and C. Melcher,
pers. obs.). Seed-eating birds exhibit a mixed re-
sponse to burns, but there is some evidence that
several species readily use burns, Clark's Nut-
cracker, Pine Siskin, Cassin's Finch, and Red
Crossbill in particular (Table lb; Hutto 1995).
Whether theses species are responding to in-
creased seed availability (e.g., serotinous cones),
minerals in the ashes (C. W. Benkman, pers.
comm.), or other factors remains unclear. Fur-
thermore, these species are rather nomadic, or
have large home ranges, and may use burned
forests opportunistically.
Many species absent or uncommon immediate-
ly post-fire begin to increase in mid-successional
stages as snags decay or fall, shrubs and saplings
become well-developed, and canopy cover in-
creases. Although Cordilleran and Dusky fly-
catchers may appear at the edges of early post-
fire forests (N. Kotliar and C. Melcher, unpubl.
data), they sometimes reach peak abundances at
mid-successional stages (Peterson 1982, Raphael
et al. 1987; N. Kotliar and C. Melcher, unpubl.
data). Resprouting aspen stands can attract spe-
cies commonly associated with deciduous sys-
tems (e.g., Warbling Vireo, Dusky Flycatcher; N.
Kotliar and C. Melcher, pers. obs.). Red-naped
Sapsucker also has been observed drilling holes
in lodgepole pine and aspen saplings within 5-10
years following disturbances (N. Kotliar and C.
Melcher, pers. obs.). Lewis's Woodpecker may
use burned forests 10-20 yr after fires, presum-
ably in response to improved conditions for aerial
foraging following a decrease in snag density and
an increase in flying arthropods associated with
shrub regrowth (c.f., Bock 1970, Linder and An-
derson 1998). Species such as Mountain Chick-
adee, Ruby-crowned Kinglet, and Swainson's and
Varied thrushes reach peak abundance in late-suc-
cessional forests (Bock and Lynch 1970, Bock et
al. 1978, Peterson 1982, Huff et al. 1985, Raphael
et al. 1987). In contrast, species that favor open
canopies (e.g., American Robins) begin to decline
in mid- to late-successional stages (Peterson
1982, Huff et al. 1985, Raphael et al. 1987).
Several species that occur in early post-fire
forests also may occur in later successional stag-
es. Hammond's Flycatcher occasionally has
been detected in young post-fire forests (Harris
1982, Huff et al. 1985, Hutto 1995, Johnson and
Wauer 1996; N. Kotliar and C. Melcher, unpubl.
data), but they typically reach peak abundance
in mature forests (Peterson 1982, Sedgwick
1994; N. Kotliar and C. Melcher, unpubl. data).
However, its occasional occurrence immediately
after fire suggests that Hammond's Flycatcher
may temporarily exhibit site-fidelity. Several
species, such as Olive-sided Flycatcher, Brown
Creeper, and Dark-eyed Junco, initially may de-
cline in mid-successional stages, but may in-
crease as canopy gaps and snags are created
(Huff et al. 1985, Carey et al. 1991).
Fire geometry
Although no studies have explicitly examined
how birds respond to burn size or shape, one
study examined whether bird abundance was af-
fected by differing patch sizes created by the
extensive fires of 1988. Of the 87 species pres-
ent, only Plumbeous Vireo and Townsend's Sol-
itaire decreased with increasing patch size (Hut-
to 1995). However, the relatively large minimum
patch size surveyed (40 ha) may have masked
important area effects at lower size ranges. Thus,
the response of birds to total burn area needs
additional study.
Given that area effects have been found to be
important in other ecosystems, we should con-
sider these effects as they relate to fires as well.
For example, post-fire specialists may require a
minimum burn size. In contrast, some species
may select openings created by small burns and
avoid larger burns. Increase in burn size may
also lead to increased heterogeneity of bums
(e.g., variation in burn severity).
The proportion of burn to edge area is also
affected by burn size and shape. Thus, species
that show positive responses to burns may be
attracted to the juxtaposition of burned and un-
burned forest. For example, Olive-sided Fly-
catcher and Townsend's Solitaire (Table la)
reached their highest abundances at burn edges
(N. Kotliar and C. Melcher, unpubl. data). In ad-
dition, fire damaged trees (not killed outright by
fire), which often occur along the periphery of
crown fires, are used by several post-fire wood-
pecker species (Murphy and Lehnhausen 1998).
Many of the species showing mixed response to
burns (e.g., American Robin, Townsend's Soli-
taire, Western Tanager, Dark-eyed Junco, Chip-
ping Sparrow, Pine Siskin, and Cassin's Finch;
Table lb) reached their highest abundances
within 50 m of the edges of burns (N. Kotliar
and C. Melcher, unpubl. data).
Many crown fires also contain "peninsulas"
and "islands" of unburned forest remnants,
which can increase edge habitats or retain un-
burned forest well inside of large burns. For ex-
ample, the moist microclimate of riparian areas,
which may inhibit fire or limit burn severity, can
result in riparian remnants. Thus, species not
typically associated with early post-fire forests
58 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 2. NUMBER OF CAVITY-NESTING SPECIES IN UNLOGGED AND SALVAGE-LOGGED POST-FIRE FORESTS DURING
THE BREEDING SEASON 1N THE NORTHERN ROCKY MOUNTAINS
Number of nesting species
Partially Severely
Forest type Unsalvaged salvaged salvaged Totals Study
Mixed conifer/deciduous 16 12 4 17 Caton 1996 a
Mixed conifer/deciduous 18 -- 8 18 Hitchcox 1996 b
Ponderosa pine/douglas-fir 9 9 -- 10 Saab and Dudley 1998 c
Mixed conifer 8 9 -- 9 S. Hejl and M. McFadzen, unpubl. data d
a Salvage logging of entire 4000-ha burn included clearcuts (all trees were removed except for a few snags) and partial cuts (individual trees or small
groups of trees were logged).
b Salvage logging of entire 500-ba burn created an interspersion of harvest treatments with unlogged control plots, In severely salvaged areas, all
merchantable (>15 cm dbh, >4.5 m tall) fire-killed trees were harvested.
c In salvage-logged units, about 50% of all trees >23 cm dbh, and 70% of trees >53 cm, were harvested.
d Salvage logging varied among three bums (bin'ns ranged from 494 3,321 ha). The salvaged portions of burns were partially logged with several
areas of severe salvage logging. A portion of each burn was left unbarvested.
(e.g., Wilson's Warbler, Lincoln's Sparrow; N.
Kotliar and C. Melcher, pers. obs.) may be ob-
served in remnant patches immediately post-fire.
In burns, detections of birds more typically as-
sociated with unburned forest may be artifacts of
study design. Few studies explicitly control for
distance from survey points in burned habitats to
unburned edges and remnant patches. Yet, some
species characteristic of unburned forests (e.g.,
Mountain Chickadee, Ruby-crowned Kinglet,
Hermit Thrush) may use live trees along burn
edges (N. Kotliar and C. Melcher, unpubl. data).
Thus, these species, which also have highly de-
tectable songs, may appear to use recently burned
forests if survey points are too close to edges.
Conclusions: effects of fire on avian communities
Although there are relatively few studies that
address the effects of fire on avian communities,
the consistent presence of many woodpeckers
and aerial insectivores in early post-fire forests,
and the near absence of many foliage-gleaning
species associated with closed-canopy forests,
appear to be robust patterns. Many additional
species appear to use post-fire forests in certain
contexts. For most species, however, we still
have a poor understanding of how fire alters
habitat suitability. We clearly need more infor-
mation about how species' responses to fire can
be altered by burn severity (including within-
burn heterogeneity), fire geometry, proximity to
unburned edges and remnants, pre- and post-fire
cover types (e.g., tree species, forest structure,
previous silvicultural treatments), and time since
fire. Finally, because most burns outside national
parks are salvaged, information about the effects
of post-fire salvage logging is also critical.
EFFECTS OF POST-FIRE SALVAGE LOGGING ON
AVIAN COMMUNITIES
Salvage logging following stand-replacement
fires has occurred since the early 1900s (D. At-
kins, pers. comm.). Initially, salvage logging
was uncommon due to limited access to burned
forests (K. McKelvey, pers. comm.). In the
1950s, however, the demand for lumber in-
creased greatly, and subsequent road-building in
national forests provided opportunities to har-
vest more burns (D. Arkins, pers. comm.). Typ-
ically, salvage logging was implemented imme-
diately post-fire, leaving few, if any, standing
snags. Only within the past two decades have
forest managers begun to retain snags within sal-
vaged areas to benefit wildlife.
The effects of salvaging on avian communities
remain poorly understood. Only four studies, all
of which were restricted to coniferous and mixed
coniferous/deciduous (hereafter "mixed") forests
of the northern Rocky Mountains (Montana and
Idaho), specifically examined the effects of sal-
vage logging on cavity-nesting bird communities
(Caton 1996, Hitchcox 1996, Saab and Dudley
1998; S. Hejl and M. McFadzen, unpubl. data;
Table 2). Two other studies evaluated salvaged
burns (Blake 1982, Raphael and White 1984) but
did not replicate treatments, thus they were not
emphasized in this review. As a result, we focus
our discussion on cavity-nesting species in the
northern Rocky Mountains.
Effects of salvage logging on birds
Severely salvaged burns (Table 2) may de-
crease the suitability of post-fire forests for most
cavity-nesting species. However, the effects of
partial salvaging are more equivocal (Table 2).
In general, species richness declined only in the
most severely salvaged burns, although even
partial salvaging altered species composition
(Table 2; Raphael and White 1984).
Several cavity nesters showed consistent pat-
terns of abundance in logged or unlogged con-
ditions across studies. Black-backed and Three-
toed woodpeckers were most abundant in unsal-
vaged burns and rarely nested in salvaged areas
FIRE EFFECTS ON AVIAN COMMUNITIES--Kotliar et al. 59
of burns (Hitchcox 1996, Saab and Dudley
1998; S. Hejl and M. McFadzen, unpubl. data).
In contrast, nesting Lewis's Woodpeckers were
most abundant in partially salvaged burns (Saab
and Dudley 1998; S. Hejl and M. McFadzen,
unpubl. data). Mountain Bluebird and Hairy
Woodpecker nested in both unsalvaged and sal-
vaged portions of burns, but tended to nest more
often in unsalvaged portions (Hitchcox 1996,
Saab and Dudley 1998; S. Hejl and M. Mc-
Fadzen, unpubl. data).
The responses of several species to salvage
logging varied among studies. Red-breasted
Nuthatch and Williamson's Sapsucker nested
primarily in partially salvaged burns in conifer-
ous forest (S. Hejl and M. McFadzen, unpubl.
data), whereas in mixed forest they nested only
in the unsalvaged portions of severely salvaged
burns (Hitchcox 1996). These mixed responses
to salvage logging may be due to differences in
salvage severity or cover type. In general, it ap-
pears that species most closely tied to early suc-
cessional post-fire forests (Table la) may be the
most sensitive to salvage logging.
The effects of salvage logging on nesting suc-
cess also varied among species and studies. In
the three studies that examined nesting success
(>20 nests per treatment per species), Hairy
Woodpecker (Saab and Dudley 1998), Northern
Flicker (Hitchcox 1996), and Mountain Bluebird
(S. Hejl and M. McFadzen, unpubl. data) expe-
rienced significantly higher nesting success in
unsalvaged treatments. Three-toed Woodpeck-
ers, House Wrens, and Western Bluebirds had
similar nesting success among treatments.
Variation in characteristics of snags used for
nests sites and foraging
Salvage-logging practices often call for the
harvest of larger, more economically valuable
tree species. By altering species composition,
sizes, and densities of snags, salvaging may alter
resource availability for birds. Therefore, we de-
scribe characteristics of post-fire forests required
for foraging and nesting cavity-nesting birds and
relate those needs to management practices.
Although tree species selected for nest sites
varied among bird species and studies, some gen-
eral patterns were evident. In three studies of
mixed forests (both salvaged and unsalvaged)
dominated by conifers (95% conifers, 5% Popu-
lus spp.), a disproportionate percentage of nests
(35-80%) were located in deciduous trees (Hutto
1995, Caton 1996, Hitchcox 1996). Most nests
were located in snags. In two other studies of
coniferous and mixed conifer forests, birds nested
in snags of western larch (Hitchcox 1996; S. Hejl
and M. McFadzen, unpubl. data) and ponderosa
pine (S. Hejl and M. McFadzen, unpubl. data)
Williamson's Sapsucker
Lewis's Woodpecker
Northern Flicker
Brown Creeper
White-headed Woodpecker
Hairy Woodpecker
Western Bluebird
Mountain Bluebird
Red-breasted Nuthatch
Black-backed Woodpecker
Three-toed Woodpecker
Increasing Snag Density at Nest Sites
FIGURE 3. General distribution of cavity-nesting
birds in burned forests (unsalvaged and salvage
logged) as a function of nest-tree diameter (DBH) and
snag density at nest sites (Saab and Dudley 1998; S.
Hejl and M. McFadzen, unpubl. data).
more often than expected. In one study in Idaho
and Montana, 45% of all nests were in Douglas-
fir (S. Hejl and M. McFadzen, unpubl. data).
Such variation in nest-tree selection among stud-
ies may result from variation in species compo-
sition and the relative availability of preferred
trees (S. Hejl and M. McFadzen, unpubl. data).
The extent of snag decay influences which
snags woodpeckers select for nesting. For ex-
ample, strong excavators such as Black-backed,
Three-toed, Hairy, and Downy woodpeckers,
nested in snags with intact tops (Caton 1996,
Hitchcox 1996, Saab and Dudley 1998; S. Hejl
and M. McFadzen, unpubl. data). Weak excava-
tors such as Lewis's Woodpecker, White-headed
Woodpecker, and Northern Flicker, nested more
frequently in broken-topped snags (many broken
pre-fire) that were presumably more decayed than
intact snags (Hitchcox 1996, Saab and Dudley
1998; S. Hejl and M. McFadzen, unpubl. data).
Because the extent of decay influences nest-tree
selection, selective salvaging of less decayed
snags likely affects bird species differentially.
Cavity nesters also respond to differences in
the sizes and spatial distribution of snags (Fig.
3), which, in turn, could be affected by different
salvage prescriptions (Saab et al. 2002). In both
coniferous and mixed burns, most cavity nesters
selected large-diameter trees more often than ex-
pected (Caton 1996, Hitchcox 1996, Saab and
Dudley 1998; S. Hejl and M. McFadzen, unpubl.
data). Black-backed and Three-toed woodpeck-
ers nested in medium-sized snags (Hitchcox
1996, Saab and Dudley 1998; S. Hejl and M.
McFadzen, unpubl. data). This size class was
among the smallest used by any woodpecker
species, but is within the size-range targeted for
salvaging. In general, cavity nesters selected
dense patches of snags more often than dis-
60 STUDIES IN AVIAN BIOLOGY NO. 25
persed or isolated snags (Raphael and White
1984, Saab and Dudley 1998, Saab et al. 2002).
Despite the paucity of foraging studies in post-
fire forests, some general patterns regarding pref-
erences of woodpeckers for certain tree species
and sizes emerged from our review. Woodpeckers
selectively foraged on large snags in both winter
(Kreisel and Stein 1999) and summer (Hutto
1995, Powell 2000; S. Hejl and M. McFadzen,
unpubl. data). However, use of tree species in
summer varied among studies (Hutto 1995, Caton
1996, Powell 2000; S. Hejl and M. McFadzen,
unpubl. data), among habitats within one study
(Caton 1996, Powell 2000), and among Picoides
woodpeckers within a study (S. Hejl and M.
McFadzen, unpubl. data). In northeastern Wash-
ington during winter, Downy, Hairy, Three-toed,
and Black-backed woodpeckers selectively for-
aged on western larch and ponderosa pine, which
are also preferentially salvage logged. Thus, by
altering the size, distribution, and species com-
position of post-fire snags, salvage logging dif-
ferentially affects cavity-nesting species.
Co-occurring species of woodpeckers some-
times select different prey, which could influ-
ence avian diversity in post-tire habitats. For ex-
ample, in a recent study of an unsalvaged burn
in Alaska, Murphy and Lehnhausen (1998) an-
alyzed the contents of 33 woodpecker stomachs
and found that Three-toed Woodpeckers con-
sumed bark beetle larvae (Scolytidae) almost ex-
clusively, whereas Black-backed and Hairy
woodpeckers primarily consumed wood-boring
beetles (Buprestidae and Cerambycidae). In an
unsalvaged burn in east-central idaho, Black-
backed Woodpeckers were observed feeding
their nestlings the larvae and pupae of wood-
boring beetles approximately 65% of the time
(Powell 2000). Beal (1911), however, reported
that 65-75% of the prey consumed by Three-
toed and Black-backed woodpeckers were
wood-boring beetles. Differences among studies
could be due to prey availability (Powell 2000),
which in turn is affected by tree species com-
position, burn severity, and salvage severity.
Conclusions: effects of post-fire salvage
logging on cavity-nesting birds
Overall, salvage logging in burned forests can
have pronounced effects on cavity-nesting species
that use post-fire habitats. In conjunction with a
substantial reduction in fire-killed trees due to fire
suppression, salvage logging has resulted in dra-
matic reductions in the availability of snags in
these ephemeral habitats. The effects of such re-
ductions have serious implications for the viability
of Black-backed and Three-toed woodpeckers,
which rarely use even partially- logged post-tire
forests. Although forest managers have begun to
retain some snags (including large snags) in sal-
vaged areas, this is not sufficient for species that
prefer high densities of snags that characterize un-
salvaged bums. Some types of partial salvaging
may actually benefit a few species, but historically
such species may have been more closely associ-
ated with later successional stages of burns after
snag densities had decreased naturally, with forests
kept open by frequent, low-severity rites, or open
post-tire forests. Retention of a diversity of snag
species, sizes, and spatial distributions, as well as
snags in various stages of decay, in burned forests
is essential to the conservation of avian diversity
in northern Rocky Mountain forests. The applica-
bility of these conclusion across western forests or
other avian communities (e.g., open-cup nesting
species) requires further research.
MANAGEMENT IMPLICATIONS
FIRE MANAGEMENT
Given the importance of fire to many bird spe-
cies, restoration of natural fire regimes may be
critical to the ecological integrity of western for-
ests. However, the problems associated with re-
producing the complexity and diversity of fire
processes at multiple scales pose great challeng-
es (Baker 1993). The recent emphasis on pre-
scribing frequent, low-intensity fires in low-el-
evation forests of the Rocky Mountains is a
good start toward. reintroducing fire in systems
where frequent understory burns maintained
open, old-growth stands (but see Covington and
Moore 1994, Tiedemann et al. 2000), but this
treatment will not be adequate for bird species
that associate with stand-replacement burns. For
example, prescribed fire may alter the availabil-
ity of large snags, depending on fire severity
(Horton and Mannan 1988, Tiedemann et al.
2000). In general, the effects of prescribed fire
on avian communities are poorly understood
(Finch et al. 1997, Tiedemann et al. 2000); the
few studies of prescribed fire have been plagued
by methodological problems, and thus the con-
clusions of these studies are suspect (Finch et al.
1997). Furthermore, incorrectly applied pre-
scribed fire can alter landscape structure (Baker
1993). Fire-management practices that include
allowing wildland fires of all severities to bum,
when and where they are appropriate, may help
re-create natural conditions (Hejl et al. 1995).
Given the uncertainty about specific, local fire
regimes (Baker 1994, Tiedemann et al. 2000,
Veblen et al. 2000) and the variation among bird
species in response to fire characteristics (Hutto
1995), managers may wish to mimic natural var-
iation in fire regimes (e.g., size, severity, fre-
quency, timing) that may have occurred within
a given cover type and geographic area (Baker
FIRE EFFECTS ON AVIAN COMMUNITIES Kotliar et al. 61
1992, Hejl et al. 1995, Veblen et al. 2000). This
approach will help to avoid overemphasis on
any particular prescription.
Post-fire forests can be altered significantly by
salvage logging. Although bird species will vary
in their responses to different management op-
tions, few cavity-nesting species, if any, will ben-
efit from severe salvaging (i.e., clearcut, or re-
moval of most medium and large snags). Here,
we evaluate several alternatives to severe salvage
logging based on our knowledge of nesting re-
quirements for six cavity-nesting birds in the
northern Rocky Mountains: (1) leave the burn un-
salvaged; (2) lightly salvage throughout the burn
(e.g., leave many of the biggest snags); (3) sal-
vage the burn (e.g., light or partial) after a delay
of several years (Murphy and Lehnhausen 1998,
Kreisel and Stein 1999); (4) salvage part of the
burn severely and leave the remainder unsalvaged
(Hutto 1995); and (5) apply different salvage
treatments across the burn (including variation in
tree distributions, sizes, and species left uncut).
The species most likely to benefit from unsal-
vaged burns, or unsalvaged portions of burns, are
those most-closely tied to early post-fire condi-
tions. Because Black-backed and Three-toed
woodpeckers appear to depend on the short-lived
availability of prey resources that quickly invade
post-fire habitats, a delay in salvaging may be
warranted (Murphy and Lehnhausen 1998). Some
species (e.g., American Kestrel, Lewis's Wood-
pecker) may tolerate or benefit from partial or
light salvage logging provided the large snags
and tree species (e.g., deciduous trees, Douglas-
fir, ponderosa pine, western larch) they tend to
select are left uncut (Saab and Dudley 1998; S.
Hejl and M. McFadzen, unpubl. data).
Species may inhabit partially salvaged burns
(Saab and Dudley 1998; S. Hejl and M. Mc-
Fadzen, unpubl. data) because they resemble the
later successional stages of burns (when snags
begin to thin out naturally) or open forests. Giv-
en our limited understanding of the cumulative
effects of fire suppression and post-fire salvage
logging, and their effects on post-fire habitat
availability across western landscapes, allowing
succession to proceed naturally in unsalvaged
burns may benefit the most species.
MIMIC NATURAL DISTURBANCE REGIME
Many bird species are adapted to, and may de-
pend upon, natural disturbance such as fire. Over
the last century, however, logging has supplanted
fire as the dominant process shaping coniferous
forests in many regions of the West. Yet, the con-
sequences of this shift for avian communities is
poorly understood (Hansen et al. 1991). It has been
suggested that the disturbance created by logging
may create adequate habitats for some fire-depen-
dent species in areas where severe fires are im-
practical (Hutto 1995). Indeed, fire and logging
could have similar effects on western landscapes
if logging were modified to mimic natural fires
more closely (Hunter 1993, Hejl 1994). However,
there are profoundly different ways in which past
fire and silvicultural activities have affected west-
em forest systems. First, they often operate on
vastly different spatial and temporal scales (e.g.,
disturbance size and frequency), which, in turn,
will lead to different landscape structure (Hansen
et al. 1991, Gluck and Rempel 1996). Second,
there are many unique features produced by fire
(e.g., a high density of snags and consequent in-
creases in wood-boring beetles) that may not be
replicated readily by current logging practices
(Hansen et al. 1991, Hutto 1995). Finally, selective
logging often removes larger trees whereas low-
severity fires typically kill smaller trees (Finch et
al. 1997). Thus, natural disturbances may provide
useful models for developing logging and salvag-
ing techniques that would diminish the negative
impacts on birds (Hunter 1993, Hejl et al. 1995).
Our understanding of how birds respond to
silvicultural activities is based primarily on com-
parisons of logged versus relatively undisturbed,
mature forests (Hejl et al. 1995). However, as-
sessments that include comparisons of logged
and naturally disturbed forests with similar dis-
turbance severities (e.g., thinned forests might
be compared to moderate or understory burns)
would be valuable. For example, a recent study
of 16 burned and 16 logged conifer forests in
Colorado found that severely logged forests (i.e.,
logged areas contained few, if any, live or dead
trees) were generally unused by most species as-
sociated with stand-replacement burns (N. Kot-
liar and C. Melcher, unpubl. data). Overall, avi-
an species richness was much higher in burns
than in logged forests. The pattern was espe-
cially salient when comparing clearcuts (i.e., no
retention trees) to unsalvaged burns. Of the spe-
cies that did occur in clearcuts, most also oc-
curred in burns, whereas the reverse was not ob-
served. Hansen et al. (1995b) also found that
retaining canopy trees benefits many bird spe-
cies in the west Cascades of Oregon. In general,
clearcut conifer forests do not function as sub-
stitutes for burned forests. In many respects, the
effects of logging on avian communities in un-
burned forests may be similar to those of salvage
logging in stand-replacement burns.
The high density of snags in burns is the most
obvious distinction between burned and clearcut
forests. However, the edges of these disturbanc-
es can also differ dramatically. For example,
clearcut forests often have well-defined edges
with few, if any standing snags. In contrast, burn
edges are often a heterogeneous mix of burned
62 STUDIES IN AVIAN BIOLOGY NO. 25
and unburned trees, except along fire breaks
where burn edges are usually more abrupt. The
juxtaposition of live and dead forests may be
important to many species, such as Olive-sided
Flycatcher, which generally sings and conducts
foraging sallies from dead trees in open areas
but nest in nearby live, mature trees (Altman and
Sallabanks 2000). In Colorado, Olive-sided Fly-
catcher only occurred in cuts that contained both
snags and live trees (i.e., not clearcuts; N. Kot-
liar and C. Melcher, unpubl. data). The com-
plexity of burn edges may also help to diminish
deleterious edge effects (e.g., increased nest pre-
dation and parasitism) in adjacent undisturbed
forests that could result from high-contrast edges
of clearcuts. Thus, silvicultural practices that in-
corporate structural elements of burns (e.g., re-
talning or creating high densities of snags and
patches of live trees, and increasing the com-
plexity of edges) may improve the suitability of
logged forests for many post-fire bird species.
There are also important differences between
natural and anthropogenic disturbances at larger
spatial and temporal scales. For example, in both
conifer- and aspen-dominated forests, differenc-
es in bird communities among burned and cut
forests were most evident in early successional
stands, but were still apparent in mid-succes-
sional forests (Hutto 1995, Hobson and Schiek
1999). We explore this idea further by compar-
ing the fragmenting effects of severe disturbanc-
es: stand-replacement fire, silvicultural activities
(e.g., post-fire salvage, clearcuts), and forest
conversion. Here, we restrict the meaning of for-
est fragmentation to the fragmenting effects of
anthropogenic disturbance relative to the natural
heterogeneity of the landscape. Fragmentation
can alter several landscape-scale parameters, in-
cluding the number, size, and spatial distribution
of forest patches, the degree of contrast between
disturbed and adjacent undisturbed forests, and
the persistence of the disturbed patches. By def-
inition, natural disturbance regimes, such as
stand-replacement fires, create and reinforce nat-
ural heterogeneity (e.g., spatial configuration of
forest patches, variation in successional stages
among patches). Because most post-fire forests
eventually resemble pre-fire forests (e.g., cover
type), persistence and contrast are relatively low
compared to the highly persistent patches that
result from forest conversion in agricultural or
suburban landscapes. The fragmenting effects of
silvicultural practices will generally fall some-
where between these two extremes, depending
on logging severity (e.g., thinning vs. clearcut-
ting) and frequency (e.g., cut rotation). For some
species, however, the negative effects resulting
from alteration of landscape structure and dy-
namics through fire suppression may rival the
negative consequences of forest fragmentation
in some western forests. However, few studies
have evaluated the consequences of fire sup-
pression or other alterations of fire regimes on
avian communities (Lyon et al. 2000).
The degree to which anthropogenic disturbance
results in forest fragmentation depends on differ-
ences between the scale, intensity, and frequency
of natural and anthropogenic disturbance, as well
as the natural heterogeneity of the landscape. Spe-
cies adapted to frequent natural disturbance may
tolerate or even prefer the conditions created by
disturbance over undisturbed forests. The Pygmy
Nuthatch, for example, which is endemic to pon-
derosa pine forests (relatively short fire return in-
tervals), had higher abundance in prescribed un-
derstory bums than in adjacent unburned forests,
and was absent in stand-replacement bums (N.
Kotliar, unpubl. data). In contrast, species such as
the Golden-crowned Kinglet, Varied Thrush, and
Townsend's Warbler, which are most often found
in association with spruce-fir and cedar-hemlock
cover types (relatively long fire return intervals;
Hutto 1995), consistently occurred at lower abun-
dances in burned forests (Table l c). Although
many species may tolerate, or be adapted to, nat-
ural disturbance, we expect that most bird species
(except for some generalists and introduced spe-
cies) will be extremely sensitive to the high degree
of persistence and contrast of forest conversion,
regardless of inherent disturbance regimes. Super-
imposed on these factors are other landscape-scale
issues such as local cowbird abundance or the
composition of predator communities. Thus, local,
landscape, and regional diftErences need to be ad-
dressed when basing silvicultural practices on nat-
ural disturbance regimes.
RESEARCH RECOMMENDATIONS
SPECIFIC RESEARCH QUESTIONS
Based on our review of past research, we have
identified some general patterns regarding the
responses of avian communities to fire. How-
ever, the studies have raised more questions than
they have answered. Thus, applications of man-
agement prescriptions involving fire and fire-re-
lated silvicultural practices should be considered
experimental and be designed to increase our
knowledge about fire effects. For example, we
need more information about the basic ecology
of post-fire forests, including:
ß how various fire characteristics (e.g., severity,
size, successional stage, and season of burn-
ing), landscape contexts, and cover types
(both pre- and post-fire types) affect avian
communities;
ß the extent to which avian use of burns is pred-
FIRE EFFECTS ON AVIAN COMMUNITIES--Kotliar et al. 63
icated on the juxtaposition of burned and un-
burned forest;
ß the effects of fire on life histories (foraging
behavior, nest site selection) and demograph-
ics, particularly reproductive success, survi-
vorship, and recruitment for both breeding
and wintering populations (Finch et al. 1997,
Lyon et al. 2000);
ß variation in avian use of fire-generated snags
for nest, foraging, or perch sites compared to
use of snags generated by other process (e.g.,
lightning, disease, insects);
ß how avian communities differ in naturally dis-
turbed forests compared to managed forests
across successional stages;
ß the effects of seed-eaters, flycatchers, and oth-
er specialists on seed dispersal, forest regen-
eration, and overall forest health;
ß the manner in which snag characteristics and
distributions affect insect prey and, in turn,
foraging birds; and
ß whether or not there is geographic variation
in avian responses to disturbances such as fire.
We also need to understand the ways in which
fires differ from other natural disturbances (e.g.,
blowdowns, insect kills) that can be extensive and
severe. In Colorado, for example, a recent wind-
storm uprooted or damaged trees across 10,000
ha (Flaherty 2000) and, in 1939, an outbreak of
spruce beetles (Dendrocotonus rufipennis) killed
nearly 290,000 ha of trees (Veblen et al. 1991).
Information required for sound management in-
cludes:
ß improved information on the range of natural
variation both within, and among, historic
fires;
ß the effects of fire suppression on forest and
landscape structure and wildlife communities;
ß the ecological tradeoffs between wildland,
prescribed fire, and mechanical treatments (in-
cluding thinning and burning; Tiedemann et
al. 2000, Wagner et al. 2000);
ß appropriate management of post-fire forests,
including how salvage treatments affect spe-
cies that require post-fire habitats;
ß how wildlife species respond to different stag-
es of succession and whether or not those
stages are similar across disturbance types;
ß the responses of forests and wildlife to re-
peated management treatments in the same lo-
cation (Andersen et al. 1998);
ß the effects of severity in natural compared to
anthropogenic disturbances;
ß differences and similarities among fire and
forest harvesting practices and how these dis-
turbances affect avian communities; and
ß which management treatments are most likely
to conserve the biological integrity of forest
systems.
RESEARCH DESIGN
The inherent nature of fire limits the opportu-
nities to conduct well-replicated, controlled ex-
periments that evaluate the full spectrum of fire
characteristics across all western forest types.
Rather, we must rely on several complementary
approaches, including: (1) unplanned compari-
sons of wildfires (e.g., Finch et al. 1997); (2)
meta-analyses that combine data from numerous
studies to generate larger datasets and greater sta-
tistical power (e.g., Hutto 1995); and (3) con-
trolled experiments using prescribed (planned)
burns, logged, logged and burned, and unburned
controls. The collective results of all approaches
should help us develop a greater overall under-
standing of how fire affects wildlife.
Most studies of fire effects on avian communi-
ties have been unplanned comparisons of wildfires
(Finch et al. 1997). Although variation among
wildfires (e.g., forest type, burn characteristics) and
post-fire management strategies, plus the lack of
pre- and post-fire treatments, has limited the scope
of inference provided by unplanned comparisons,
they nonetheless provide unique opportunities to
study extensive, severe wildfires. This approach is
most useful immediately after years with extensive
fire, when researchers can establish numerous,
similar-age replicates across regions and in many
forest types. Intensive studies of single sites can
provide useful information as well, especially in
large burns. For example, the effects of burn se-
verity could be studied in one large burn by strat-
ifying survey points across severities (e.g., R. Sal-
labanks and J. Mclver, unpubl. data). In addition,
single-site studies can generate data for use in
meta-analyses.
Meta-analyses provide excellent opportunities
for improving the results of multiple studies that
have little or no replication (Brett 1997). Even
non-statistical compilations of unplanned com-
parisons can reveal biologically meaningful
trends, as we found in our review that Three-
toed and Black-backed woodpeckers were either
restricted to, or more abundant in, burned forests
(Table la). In order for meta-analyses to be pos-
sible, however, researchers must publish detailed
study protocols, and they must cooperate with
one another to the extent possible to standardize
protocols and share data.
To complement and expand the existing knowl-
edge gained from unplanned comparisons and
meta-analyses, we need more experiments that
control for and test variations among fire charac-
teristics, forest type, and landscape context (e.g.,
Breininger and Schmalzer 1990). Because annual
variation in bird populations can be considerable,
64 STUDIES IN AVIAN BIOLOGY NO. 25
several years of pre- and post-treatment data ide-
ally should be collected. Whenever possible, re-
searchers should incorporate the full range of fire
characteristics provided by natural fire regimes in
the systems of interest (Andersen et al. 1998). It
will be difficult to find sites for conducting severe
bums, but there is increasing support for conduct-
ing such studies in national parks (J. Connor, pers.
comm.) and wildemess areas. In general, it will be
more feasible to conduct experiments of low- to
moderate-severity burns in systems that typically
experience lower-severity fires.
Research programs must also take into ac-
count some important design and interpretation
problems that are often ignored in fire studies.
Because burn edges and burn severity may have
pronounced effects on avian use of burns, sur-
vey points must be stratified across burn edges,
adjacent unburned forest, and distant unburned
forest, and over a range of burn severities to
control for these sources of variation. In addi-
tion, to determine whether avian species use of
post-fire habitats immediately after fire repre-
sents a preference for burns, or site-tenacity for
breeding territories, studies need pre- and post-
fire measures of abundance, as well as measures
of reproductive success and recruitment over
several years.
Finally, researchers need to implement long-
term studies to develop a full picture of post-fire
successional changes and how they affect avian
communities. Although habitat loss may be the
immediate effect of severe fire on species that typ-
ically inhabit mature forests (e.g., Golden-crowned
Kinglet, Spotted Owl), the long-term effects (e.g.,
decades or centuries later) may be habitat improve-
ment. Thus, clearing forests of fuels to prevent se-
vere fires that could decrease Spotted Owl habitat
in the short term could preclude more significant
habitat improvements that would benefit Spotted
Owls in the future. Overall, researchers will need
to consider a wide variety of research approaches,
as well as the full spectrum of fire characteristics
and forest types, both unmanaged and managed,
to understand how proposed management strate-
gies may affect the future health and integrity of
western-forest systems.
ACKNOWLEDGMENTS
We thank W. L. Baker, W. H. Romme, and T T.
Veblen for their gracious assistance in helping us un-
derstand the finer points of fire terminology and ecol-
ogy. H. D. Powell's expertise on insects and wood-
pecker foraging were instrumental in drafting related
sections of the manuscript. W. L. Baker, D. S. Dobkin,
T. L. George, and J. E. Roelle all provided valuable
suggestions and improvements to earlier drafts of the
manuscript. J. Connor contributed to numerous discus-
sions regarding the effects of fire management on bird
communities in national parks.
APPENDIX. SCIENTIFIC NAMES OF BIRD SPECIES
Species
American Kestrel (Falco sparverius)
Spotted Owl (Strix occidentalis)
Mourning Dove (Zenaida macroura)
Common Nighthawk (Chordeiles minor)
Northern Flicker ( Colaptes auratus)
Lewis's Woodpecker (Melanerpes lewis)
White-headed Woodpecker (Picoides albolarvatus)
Black-backed Woodpecker (Picoides arcticus)
Downy Woodpecker (Picoides pubescens)
Three-toed Woodpecker (Picoides tridactylus)
Hairy Woodpecker (Picoides villosus)
Red-naped Sapsucker (Sphyrapicus nuchalis)
Williamson's Sapsucker (Sphyrapicus thyroideus)
Olive-sided Flycatcher ( Contopus cooperi)
Western Wood-Pewee (Comopus sordidulus)
Hammond's Flycatcher (Empidonax hammondii)
Dusky Flycatcher (Empidonax oberholseri)
PlumbeDus Vireo (Vireo plumbeus)
Cassin's Vireo (Vireo cassinii)
Warbling Vireo (Vireo gilvus)
Tree Swallow (Tachycineta bicolor)
Steller's Jay (Cyanocitta stelleri)
Clark's Nutcracker (Nucifraga columbiana)
Mountain Chickadee (Poecile gambeli)
Red-breasted Nuthatch (Sitta canadensis)
White-breasted Nuthatch (Sitta carolinensis)
Pygmy Nuthatch (Sitta pygmaea)
Brown Creeper ( Certhia americana)
Rock Wren (Salpinctes obsoletus)
House Wren (Troglodytes aedon)
Ruby-crowned Kinglet (Regulus calendula)
Golden-crowned Kinglet (Regulus satrapa)
Hermit Thrush (Catharus guttatus)
Swainson's Thrash ( Catharus ustulatus)
Varied Thrush (Ixoreus naevius)
Townsend's Solitaire (Myadestes townsendi)
Mountain Bluebird (Sialia currucoides)
Western Bluebird (Sialia mexicana)
American Robin (Turdus migratorius)
Yellow-rumped Warbler (Dendroica coronata)
Townsend's Warbler (Dendroica townsendi)
Wilson's Warbler (Wilsonia pusilia)
Western Tanager (Piranga ludoviciana)
Lazuli Bunting (Passerina amoena)
Dark-eyed Junco (Junco hyemalis)
Lincoln's Sparrow (Melospiza lincolnii)
Chipping Sparrow (Spizella passerina)
White-crowned Sparrow (Zonotrichia leucophrys)
Pine Siskin (Carduelis pinus)
Cassin's Finch (Carpodacus cassinii)
Red Crossbill (Loxia curvirostra)
Pine Grosbeak (Pinicola enucleator)
Evening Grosbeak (Coccothraustes ve,72ertinus )
Studies in Avian Biology No. 25:65-72, 2002.
GEOGRAPHIC VARIATION IN COWBIRD DISTRIBUTION,
ABUNDANCE, AND PARASITISM
MICHAEL L. MORRISON AND D. CALDWELL HAHN
Abstract. We evaluated geographical patterns in the abundance and distribution of Brown-headed
Cowbirds (Molothrus ater), and in the frequency of cowbird parasitism, across North America in
relation to habitat fragmentation. We found no distinctive parasitism patterns at the national or even
regional scales, but the species is most abundant in the Great Plains, the heart of their original range,
and least common in the southeastern U.S. This situation is dynamic, because both the Brown-headed
and two other cowbird species are actively expanding their ranges in the southern U.S. We focused
almost entirely in this paper on the Brown-headed Cowbird, because it is the only endemic North
American cowbird, its distribution is much wider, and it has been much more intensively studied. We
determined that landscape is the most meaningful unit of scale for comparing cowbird parasitism
patterns as, for example, in comparisons of northeastern and central hardwood forests within agricul-
tural matrices, and suburbanized areas versus western coniferous forests. We concluded that cowbird
parasitism patterns were broadly similar within all landscapes. Even comparisons between prominently
dissimilar landscapes, such as hardwoods in agriculture and suburbia versus coniferous forest, display
a striking similarity in the responses of cowbirds. Our review clearly indicated that proximity of
feeding areas is the key factor influencing presence and parasitism patterns within the landscape. We
considered intensity of landscape fragmentation from forest-dominated landscapes altered in a forest
management context to fragmentation characterized by mixed suburbanization or agricultural devel-
opment. Our review consistently identified an inverse relationship between extent of forest cover across
the landscape and cowbird presence. Invariably, the variation seen in parasitism frequencies within a
region was at least partially explained as a response to changes in forest coven The most salient
geographic aspect of cowbirds' response to landscape fragmentation is the time since fragmentation
occurred. Eastern landscapes generally experienced 200 years ago the development and fragmentation
that western landscapes experienced less than 75 years ago. Consequently, there is a broad east-west
contrast in which more numerous human settlements and smaller unbroken forest stands are found in
the East, a difference that permits cowbirds to be more pervasive and ubiquitous. The locality of
suitable feeding areas is a hallmark trait of the cowbirds' strategy in exploiting specific forest frag-
ments. Host abundance influences parasitism patterns only secondarily at the landscape scale. These
two limiting factors come into play differently in different landscapes. For example, cowbird abun-
dance in unbroken forested landscapes are limited primarily by the availability of foraging areas rather
than by host density, whereas cowbirds are limited primarily by host availability in landscapes that
are extensively fragmented with feeding areas.
Key Words: Brown-headed Cowbird; cowbird parasitism; fragmentation; geographic variation; host
defense; Molothrus ater.
The laying of eggs by one species in the nests
of another species, allowing the host species to
raise their young, is a fascinating evolutionary
story (e.g., Rothstein and Robinson 1988, Or-
tega 1998:37-63). In North America, the
Brown-headed Cowbird (Molothrus ater) is the
primary nest parasite, although two other species
are expanding their ranges in the southern U.S.
(Cruz et al. 1998, Ortega 1998). The trait of par-
asitizing nests apparently developed in the
Brown-headed Cowbird in the Great Plains. As
reviewed below, this cowbird species expanded
its range eastward in the 1800s and westward in
the 1900s, and now occupies most states and
provinces in North America (Rothstein 1994,
Peterjohn et al. 2000). Parasitism, along with the
cowbird's range expansion, has caused scientists
to consider the role that cowbirds might be hav-
ing in population declines of certain of their host
species. Thus, the goal of our paper is to review
cowbird abundance, distribution, and parasitism
frequencies across North America so a better un-
derstanding of cowbird ecology and its impact
on host species can be gained.
In this paper we assumed no difference in
cowbird parasitism behavior by geographic lo-
cation. We reviewed the literature (including un-
published manuscripts and reports) in order to
characterize the relationship between host and
parasite. Given the striking differences in envi-
ronmental conditions across North America--in-
cluding the distribution of bird species--we can
presuppose that one can easily find some amount
of difference in the frequencies of cowbird par-
asitism just by looking for it. And, in fact, we
know this to be the case (see reviews by Ortega
1998, Trine et al. 1998). We were primarily in-
terested in examining the process of parasitism.
That is, are there fundamental differences in
cowbird behavior in different regions that have
ecological implications and evolutionary expla-
65
66 STUDIES IN AVIAN BIOLOGY NO. 25
nations? In our review we considered both feed-
ing behavior and host selection behavior.
VALIDITY OF AN EAST-WEST
COMPARISON OF BROOD PARASITISM
Our perception of geographic location is
based in part on historic context and tradition. It
is also difficult to lump large geographic areas
under a common descriptor. Where does the East
begin and the West end; where does the East
becomes the Southeast? These geographical
terms are frequently used subjectively and an-
thropocentrically in ways that are not supported
by ecological characteristics that affect birds.
Thus, dividing North America into "East" and
"West" is an inappropriate means of examining
an ecological relationship such as parasitism and
fragmentation. This does not mean, however,
that geographic differences do not occur in land-
use practices and ecological processes and in the
response of animals to these practices and pro-
cesses. But establishing a priori boundaries con-
strains the analysis to preconceived categories
and notions.
THE RESPONSE OF COWBIRD HOSTS TO
FOREST FRAGMENTATION
In this section we set the stage for evaluating
regional differences in cowbird parasitism by
defining fragmentation and placing this concept
into an ecological framework. The emphasis of
this volume is on fragmentation, and from the
perspective of cowbirds, the most important as-
pects of fragmentation are, first, that it affects
the abundance and distribution of host species
by altering their habitat and, second, that it alters
the abundance and distribution of feeding areas
associated with developments. These twin
themes about the influence of fragmentation on
hosts' breeding habitat and on feeding areas of
cowbirds associated with human development
recur throughout our review.
The classic description of fragmentation im-
plies extensive landscapes of homogeneous veg-
etation, but this conception is an artifact of
graphic art framed at a large spatial scale. Ex-
amined at finer resolutions, most ecological sys-
tems are actually a mosaic of different plant as-
sociations. Even changes of a few meters can
change soils, slope, and aspect, and thus the as-
sociated plants. Further, these mosaics are dy-
namic and change, often rapidly, through suc-
cession, catastrophic events (e.g., fire, flood,
wind), or development activities such as crop
plantings or settlements (Meffe and Carroll
1997:274-275; Franklin et al. this volume).
The definition of "fragmented" habitat de-
pends upon the spatial scale of observation. Our
analyses use fragmentation at a scale relevant to
selection of habitat by birds, particularly song-
birds. Briefly, habitat selection is often viewed
as a hierarchical process where individuals first
select a broad geographic range, a decision that
is largely innate. Within the geographic range
the individual then makes a series of decisions
based on increasingly refined combinations of
vegetation structure, floristics, food resources,
and nest sites (Johnson 1980, Hutto 1985).
Thus, in an analysis of brood parasitism, frag-
mentation is an ambiguous concept unless it is
defined in spatial terms relevant to the series of
responses a host makes. There are changes that
take place in the environment at several scales
of resolution (see also Angelstam 1996). Such
descriptions of the environment and habitat se-
lection are not restricted geographically, but
should apply across eastern and western envi-
rons. Consequently, we would not expect diffEr-
ent behavioral processes in either host species or
cowbirds to be operating geographically. The
proportion of birds that show a particular re-
sponse to fragmentation (e.g., area sensitive, en-
hanced by edge) may differ geographically de-
pending on the historic factors that formed the
initial bird assemblage (e.g., Morrison et al.
1998:16-26). For example, fewer Dendroica
warblers occur in the West than in central and
eastern locations. This is apparently the result of
Pleistocene and post-Pleistocene events (Mengel
1964, Morrison et al. 1998:18-21). Thus, there
is simply a greater opportunity for fragmentation
to cause negative impacts on these warblers in
more eastern locations, and perhaps a propor-
tionally more apparent impact to the bird assem-
blage due to fragmentation.
Fragmentation in managed forests can be con-
sidered dynamic in that stands are cut and re-
forested; stands are not retained in early succes-
sional conditions. This means the songbird com-
munities that cowbirds parasitize continue to
have extensive natural breeding habitat although
the vegetation communities are less stable than
they would be in unmanaged forest. In contrast,
disturbances due to human development activi-
ties result in permanent or static fragmentation
(McGarigal and McComb 1995). This eradicates
some host-breeding habitat, leaving disjunct
fragments separated by patches that have food
for cowbirds. They concluded that it is unlikely
that the empirical findings on forest lYagmenta-
tion from urban and agricultural landscapes ex-
tend to the dynamic forest landscapes of the Pa-
cific Northwest and elsewhere. Likewise, Keller
and Anderson (1992) concluded that fragmen-
tation in Wyoming could not be directly com-
pared with fragmentation occurring in the Pacif-
ic Northwest. Freemark et al. (1995) also noted
that most studies in the West have been con-
GEOGRAPHICAL VARIATION IN COWBIRDS Morrison and Hahn 67
TABLE 1. COMPARISON OF THE EFFECTS OF LANDSCAPE STRUCTURE ON NEOTROPICAL MIGRATORY SPECIES BREED-
ING IN NORTHEASTERN AND CENTRAL HARDWOOD FORESTS WITHIN AGRICULTURE AND SUBURBANIZED LANDSCAPES
VERSUS WESTERN FORESTS
Landscape structure Northeastern and central vs. western comparison
Landscape composition
Forest type Same
Forest cover Same; less severe in west
Habitat proportion Same
Landscape configuration
Patch size Same; perhaps less severe in west
Patch shape N/A a
Interpatch distance Same
Nonforest edge N/A
Habitat juxtaposition Same
Note: Information summarized from Freemark et al. (1995).
a N/A - comparison not iliade or conlparable.
ducted in forested landscapes fragmented by sil-
vicultural activities--which usually do not have
rich food sources for cowbirds--rather than in
agricultural and urban landscapes as in the East,
which do include sources of food (see also Hejl
et al. this volume).
Yet, Freemark et al's. (1995) extensive liter-
ature review of the response of breeding com-
munities of neotropical migrants to landscape
structure across much of North America does
show similarities in songbird responses. A sub-
jective comparison of communities nesting in
northeastern and central hardwood forests within
agricultural and suburbanized areas with com-
munities nesting in western coniferous forests
revealed similar responses of birds to broad
measures of landscape structure (Table 1). Par-
ticularly because this is a comparison among
very dissimilar landscape settings (i.e., hard-
woods within agriculture and suburbia versus
managed coniferous forest), the similarity in re-
sponse by breeding birds is striking.
Although there are similarities in the respons-
es of host communities in different regions to
fragmentation, Freemark et al. (1995) concluded
that birds in western (coniferous) forests have
not shown as strong a negative response to frag-
mentation as have birds in northeastern and cen-
tral hardwood forests. They attributed this sev-
eral factors: fragmentation is a more recent oc-
currence in the West; fragmentation has rarely
resulted in habitat isolation; and western forests
are naturally fragmented and human-induced
fragmentation has not had time to negatively im-
pact birds. The key insight here is that there are
not inherent differences in the response of bird
communities to forest fragmentation. The earlier
stage of fragmentation typical of western forest
means that many western coniferous forests are
actually "perforated" rather than fragmented
(Forman and Collinge 1996), or, as Freeman et
al. (1995) described them, "punctuated" by
clearcuts. Of course there are also numerous ex-
amples of both extensively forested areas and
forests perforated by logging and agriculture
outside of western environs (e.g., Robinson et
al. 1995a, Robinson and Robinson 1999).
McGarigal and McComb (1995), working in
the Oregon Coast Range, found that landscape
structure (composition and configuration) ex-
plained <50% of the variation in each species'
abundance among the landscapes. Species'
abundances were generally greater in areas with
a relatively fragmented distribution of habitat.
Note that from the cowbird's perspective this
means host abundance increases as fragmenta-
tion progresses. They cautioned, however, that
species sensitive to fragmentation at the scale of
their study may have been rare already and
therefore not subject to the approach they used.
Again from the cowbird's perspective the spe-
cies that drop out do not reduce the number of
host individuals available to cowbirds. They
concluded, however, that their results were gen-
erally similar to studies conducted in forest-
dominated landscapes in New Hampshire, Mis-
souri, Maine, and Wyoming. Thus, when com-
parisons are made between similar vegetation
types, birds respond in a similar manner across
broad geographic regions. They noted that ef-
fects of fragmentation in forest-dominated land-
scapes altered in a forest management context is
not comparable with fragmentation caused by
urbanization or agricultural development, which
is typically how eastern and western regions
have been compared in the literature.
In conclusion, the same ecological processes
associated with fragmentation seem to operate
regardless of geographic region. It is the longev-
ity of those land-use changes that precipitated
fragmentation that causes any geographic differ-
ences in current responses by birds. Verner
68 STUDIES IN AVIAN BIOLOGY NO. 25
(1986) concluded that in western forests frag-
mentation was in the early stage and tended to
produce two-dimensional islands (clearcuts) in
three-dimensional seas (forests), while in eastern
forests (as in European forests) the later stages
of fragmentation have resulted in three-dimen-
sional islands (forest fragments) in two-dimen-
sional seas (e.g., agricultural lands). Askins et
al. (1990) likewise concluded that the longer his-
tory of fragmentation in Europe has resulted in
the extirpation of most area-sensitive species, a
situation now in progress in North America. The
localized abundance, breeding success, and sur-
vival of birds is related primarily to factors of
habitat quality such as resource availability and
predator-competitor activity, but these factors
can be overridden when patches becomes very
small (<10-20 ha) and isolated.
In summary, landscape fragmentation affects
the songbird communities that cowbirds parasit-
ize. At one level of intensity, fragmentation re-
fers to the transformation of extensive forests
into smaller stands, with the consequence for
cowbird hosts of smaller, often shifting, breed-
ing areas, and habitats with a greater edge to
interior ratio. As fragmentation progresses, it
evolves to a heterogeneous landscape composed
of a mix of patches of breeding habitat with
patches of development activities such as agri-
culture and settlements. With these twin aspects
of fragmentation--smaller forest stands and in-
creasing food sources associated with develop-
ment--an increase in cowbird abundance and
parasitism is likely.
HISTORIC DISTRIBUTION OF
BROWN-HEADED COWBIRD AND
POPULATION TRENDS
Peterjohn et al. (2000) described the continen-
tal decline in cowbird numbers in North Amer-
ica since the mid-1960s. Maximum cowbird
abundance occurs in the northern Great Plains.
Regionally, numbers are declining in the south-
ern plains and throughout most of the East. The
decline in the East is attributed to substantial
increases in forest cover. There appears to be an
overall steady abundance of cowbirds in the
West. Within the region there is perhaps a slight
decrease in the Pacific Northwest, while the
Central Valley of California showed perhaps the
greatest proportional increase in cowbird num-
bers in North America.
While there is consensus that the ancestral
range of cowbirds in the Great Plains is still the
area of their greatest abundance, other aspects
of the extent and timing of their range expan-
sions both eastward and westward are less cer-
tain. Rothstein (1994) suggested that cowbirds
have been in the East in small numbers since at
least the 1700s, the earliest era of European col-
onization. In the West, cowbirds may not be re-
cent additions to the avifauna. While their col-
onization up the Pacific Coast from southern
California to Oregon and Washington has been
well documented over the course of the 20th
century, there is also evidence of earlier popu-
lations in the northwest (Rothstein 1994). They
apparently occurred historically, however, across
the Great Basin to the eastern edge of the Sierra
Nevada (Rothstein 1994). Thus, contrary to pop-
ular belief, the cowbird did occur historically in
western North America. The Sierra Nevada-Cas-
cade mountain ranges may have served as a bar-
rier to widespread expansion onto the Pacific
slope. There is also fossil evidence that cowbirds
(of unknown breeding behavior) occurred along
the edges of the species' current range in Cali-
fornia, Oregon, and Florida in the late Pleisto-
cene (Lowther 1993). Chace and Cruz (1999)
suggested that cowbirds formerly ranged to near
timberline in the Rocky Mountains because of
the historic presence of bison (Bison bison).
Cowbirds retreated from these elevations with
the extirpation of bison from these mountains.
The addition of cattle to former bison range is
now allowing cowbirds to return to the moun-
tains. If this is the case, we would expect that
birds in at least some regions of the Rocky
Mountains have had a longer exposure to cow-
birds than our recent data indicate, and they may
still express behavioral traits that evolved during
the bison-cowbird period.
SUBSPECIES DIFFERENCES
Differences among the three subspecies of the
Brown-headed Cowbird have been little studied.
Rothstein (1994) speculated that the smaller
southwestern subspecies, the "dwarf" cowbird,
M. a. obscurus, might be more vagile or more
competitive than M. a. artemisia, forrod to the
north, east of the Rockies, because the westward
range expansion of the species to the Pacific md
up the west coast seems to have been driven by
obscurus. At some point later artemisia appears
also to have crossed the Rockies into northern
California such that the two have subsequently
intermixed as cowbirds moved north into
Oregon and Washington.
Recent evidence of the range expansion of the
eastern subspecies M. a. ater into the Florida
peninsula makes it feasible that ater may be as
successful as obscurus was in colonizing the Pa-
cific west coast. Cruz et al. (1998) noted that
ater has spread rapidly since the 1950s and now
has breeding records confirmed halfway down
the peninsula, with non-breeding sightings re-
ported throughout the state. The expansion of
the Brown-headed Cowbird into Florida is ex-
GEOGRAPHICAL VARIATION IN COWBIRDSMorrison and Hahn 69
pected to have significant negative consequences
for the indigenous breeding passerines, many of
which are patchily distributed and breeding in
small populations. The character of natural hab-
itats and human settlements in Florida consists
of mangrove on the west coast and dunes and
beach on the east coast, with relentless human
settlement along both coasts. The central section
of the peninsula is higher and drier and agricul-
tural and livestock developments are pervasive.
Two mangrove-obligate species, the Black-whis-
kered Vireo (Vireo altiloquus) and the Florida
subspecies of Prairie Warbler (Dendroica dis-
color), are already reflecting local population
extirpation due to parasitism (W. Pranty, pers.
comm.).
OTHER COWBIRD SPECIES: RECENT NORTH
AMERICAN INVADERS
While it is only speculative to compare the
invasive character of Shiny (Molothrus bonar-
iensis) and Bronzed (M. aeneus) cowbirds to
Brown-headed Cowbirds at this stage, recent de-
velopments in their respective range expansions
suggest that both may be successful and increas-
ingly widespread in the United States. Both are
also host generalists, although perhaps not as ex-
treme as the Brown-headed Cowbird (Rothstein
et al. 2002). The rapid and impressive northward
range expansion of the Shiny Cowbird across
the Caribbean and into North America makes it
a likely candidate to become established in the
southeastern U.S. in the next few decades. While
no breeding records have yet been recorded in
Florida, the Shiny Cowbird is expected to be-
come established there with little difficulty (Ste-
venson and Anderson 1994; W. Pranty, pers.
comm.). Nothing is known about the extent of
habitat specialization for either Brown-headed or
Shiny cowbird within Florida.
The Bronzed Cowbird has only recently
shown marked range expansion, apparently in
association with loss of songbird breeding hab-
itat in lower Rio Grande Valley in Texas. How-
ever, it has expanded both eastward and west-
ward and could thus become a factor in regions
of the U.S. (Cruz et al. 1998). In Texas, the
Bronzed Cowbird parasitizes over 23 species,
and at this stage it appears to prefer larger host
species than does M. ater. The bronzed is
thought to have contributed to the extirpation of
Audubon's Oriole (lcterus graduacuada) in por-
tions of lower Rio Grande Valley. Together with
the brown-headed, the bronzed may also have
contributed to declines of the Orchard (1. spur-
ius), Hooded (I. cucullatus), and Northern (1.
galbula) orioles in south Texas (Cruz et al.
1998).
HOST BEHAVIOR AND GEOGRAPHY
Much interest has focused on the question
why most host species of the Brown-headed
Cowbird do not show effective anti-parasite be-
havior. Rothstein's (1975) early experimental
study of twelve eastern species used artificial
eggs colored to resemble cowbird eggs and
showed that only a few species regularly ejected
the parasite eggs. Since then a large number of
studies have been conducted in a variety of sites
both east and west, showing that parasitism de-
fenses (i.e., egg ejection, egg burial, or nest de-
section) occur occasionally and unpredictably
among species.
Some western-residing species and subspecies
show eftkctive anti-parasite behaviors that pre-
vent or minimize deleterious eftcts of parasit-
ism, which may have developed after contact
with cowbirds, or which may have been present
as pre-adaptation. For example, the Black-
throated Gray Warbler (Dendroica nigrescens)
regularly buried cowbird eggs in its nests in the
Inyo-White mountains of eastern-central Cali-
fornia (J. Keane and M. Morrison, unpubl. data),
and Rich and Rothstein (1985) showed that Sage
Thrashers regularly rejected cowbird eggs
throughout their western range.
Egg-ejection behavior is one of the best-stud-
ied anti-parasite behaviors, yet a thorough sum-
mary of the proportion of acceptor and rejecter
species by geographic region is still lacking be-
cause that would require systematic comparative
studies of dirtbrent populations of a large num-
ber of host species. Although evidence for egg
rejection exists for many species, the quantita-
tive estimates of frequency of this behavior can
usually only be confirmed through experimen-
tation, usually with artificial eggs (Ortega 1998:
19). Of the >225 species known to be parasit-
ized by Brown-headed Cowbirds, fewer than 20
are known to regularly eject parasitic eggs (Or-
tega 1998:19-20). Despite the obvious advan-
tages to hosts of removing cowbird eggs, there
are also many reasons why birds accept them
(Ortega 1998:23-27). The most prominent rea-
son is that parents risk breaking their own eggs
when they try to move the cowbird egg.
Little is known about the degree to which
egg-ejection behavior is genetically based or
learned. Briskie et al. (1992) concluded that
some anti brood-parasitic defenses are probably
genetically determined. Robertson and Norman
(1977) thought that the presence and intensity of
aggression should vary widely geographically
depending on the length of exposure to brood
parasitism. For example, they compared aggres-
sion in an area of long-term host-cowbird sym-
patry (Manitoba) with an area (Ontario) of more
70 STUDIES IN AVIAN BIOLOGY NO. 25
recent sympatry. They found that the Manitoba
host populations showed more aggression to-
wards a model cowbird, and concluded that this
was because of the longer history of sympatry.
Hobson and Villard (1998) studied the response
of American Redstarts to model cowbirds in
western Canada and found that they exhibited
more vigorous nest defense in fragmented for-
ests where cowbirds are more common than in
extensively forested landscapes.
There is a widespread assumption that all
hosts would evolve measurable anti-parasite be-
haviors given long enough sympatry with cow-
birds. According to this hypothesis, some spe-
cies along the Pacific slope may not have had
adequate exposure to parasitism to evolve reg-
ular ejection behavior (Rothstein 1975). As dis-
cussed above, however, additional evidence
must be gathered before any analysis of geo-
graphic trends in egg-rejection behavior. We
suggest that the variability and relative rarity of
anti-cowbird defenses reflects the inconsistent
selection pressure exerted by cowbird parasitism
in those landscapes where parasitism is relative-
ly low and where the level of parasitism on in-
dividual species and communities varies from
year to year. In several areas where long-term
studies of cowbird parasitism have been con-
ducted and where parasitism pressure is both
high and consistent on particular species in the
community (such as central Illinois, the Edwards
Plateau in Texas and Oklahoma, and southern
California), the study populations should be
tracked for the emergence of anti-parasite be-
haviors. Similarly, the evolution of defenses by
forest interior birds should be watched in the
context of fragmentation in both east and west.
COWBIRD PARASITISM AND
GEOGRAPHY
We present a summary of patterns of cowbird
parasitism in relation to vegetation structure,
host community, and degree of landscape de-
velopment based on studies conducted across
North American a variety of vegetation types in
different geographic regions (Table 2).
Our review indicates that proximity of feed-
ings areas is the key factor influencing which
host community a local cowbird population will
parasitize. Although Payne (1973, 1977) dis-
cussed the importance of temporal mismatch of
breeding seasons (i.e., differing lengths of ex-
posure, sensu Mayfield 1965) and documented
the phenomenon for the birds of northern Cali-
fornia, temporal mismatch is often overlooked.
It is a notable phenomenon in eastern and west-
ern locations. The local abundance of cowbirds
resulting from fragmentation and feeding oppor-
tunities further correlated with parasitization
(Payne 1973, 1977).
It is commonly stated that the heavily para-
sitized riparian communities in the western and
southwestern United States are physiographical-
ly unique because of the often abrupt change
from the relatively roesic riparian vegetation and
the xeric surrounding landscape (Ortega 1998:
267, Farmer 1999). However, cowbirds fre-
quently use riparian areas in eastern and central,
as well as western regions for passage, nesting,
and foraging. Riparian corridors allow passage
by cowbirds into an otherwise less suitable land-
scape matrix, including both eastern and western
forests. The primary development impact to
western riparian areas is loss of area and frag-
mentation (isolation), which is the same pattern
seen in eastern deciduous forests (i.e., isolated
patches of forest in a matrix of different vege-
tation). Several riparian obligate species in the
West and Southwest have been nearly extirpated
because of habitat loss. The isolation of these
species into small patches exacerbated the effect
of cowbird parasitism on their host populations.
This situation, however, is not restricted to ri-
parian vegetation of the West and Southwest. In
three eastern regions where small and restricted
species or subspecies occur in conjunction with
a unique and limited habitat, development has
created the classic situation in which cowbird
parasitism (and nest predation) accelerate the de-
cline of the resident species. In northern Mich-
igan, in jack pine (Pinus banksiana) habitat, the
species at risk is the Kirtland's Warbler (Den-
droica kirtlandii). In the coastal mangrove for-
ests of Florida, the species at risk are Black-
whiskered Vireo and Prairie Warbler (Cruz et al.
1998, Stevenson and Anderson 1994). In Central
Texas and Oklahoma, on the Edwards Plateau,
the species at risk are the Golden-cheek Warbler
(Dendroica chrysoparia) and Black-capped Vir-
eo (Vireo atricapillus).
VALIDITY OF GEOGRAPHICAL COMPARISONS OF
COWBIRD PARASITISM
One of the most important aspects of geog-
raphy in analyzing the impact of cowbirds is the
use of different spatial scales. Robinson (1999)
noted that cowbird ecology can be analyzed at
continental, regional, and landscape scales as
much as at a local scale in relation to factors
such as distances from edges. In this section, we
discuss the findings of investigators who ana-
lyzed patterns at different scales. Hochachka et
al. (1999) emphasized that investigators must
define the scale they are using when predicting
cowbird abundance and parasitism level.
Several investigators have considered whether
aspects of cowbird parasitism vary on a conti-
GEOGRAPHICAL VARIATION IN COWBIRDS--Morrison and Hahn
TABLE 2. FACTORS CORRELATED WITH INCREASED COWBIRD PRESENCE, ABUNDANCE, OR PARASITISM
71
Factor Location Source
Temporal mismatch
Proximity of feeding
Local stand factors a
Presence of riparian corridor
Host density
Species richness
Fragmentation
Original range
E. Washington 1
Arizona/California 11
E. Washington 1
N. Rockies 2, 3, 5
Sierra Nevada 6, 10
N. Michigan 7
Midwest 8, 13, 14, 15
Vermont 9
Florida 16, 17
New Mexico 18
Texas 19
Pennsylvania 20
Virginia 21
N. Michigan 7
New York 22
N. Rockies 2, 3, 5
Coastal California 4
Southern California 23
Sierra Nevada 10
Missouri 12
N. Rockies 2, 5
Midwest 13
Nationally 24
Sierra Nevada 6
Illinois 8
Arizona/California 11 a
Florida 17
Tennessee 25
Nationally 26
Northeast 27
Sources: 1: Vander Haegen and Walker (1999); 2: Young and Hutto (1999); 3: Hejl and Young (1999); 4: Farmer (1999); 5: Tewksbury et al. (1999);
6: Purcell and Verner (1999); 7: Striblcy and Haultier (1999); 8: Robinson et al. (1995a); 9: Coker and Capen (1995. 1999); 10: Lynn ctal. (1998);
11: Rosenberg et al. (1991:265, 335); 1 la: Rosenberg et al. (1991:282-283); 12: Thompson et al. (1992); 13: Donowm et al. (1997); 14: Thompson
(1994); 15: Trine et al. (1998); 16: Cruz et al. (1998); 17: W. Pranty, pets. comm.; 18: Gogucn and Mathews (1999); 19: Eckrich et aL (1999); 20:
E. Morton, pets. COlrim.; 21: J. Kan; pets. comm.; 22: Hahn and Hatfield (1995); 23: Kus (1999); 24: Hahn and O'Connor (2(X)2); 25: Miles and
Buehler (1999); 26: Smith and Myers-Smith (1998); 27: Hoover and Brittingham (1993).
a When in close proximity to feeding areas.
nental scale (Smith and Myers-Smith 1998,
Robinson 1999). At a national scale, Hahn and
O'Connor (2002) found that the most important
factor predicting cowbird abundance is the pres-
ence of their preferred mix of host species (i.e.,
the seventeen most common hosts identified by
Friedmann [1963]; Table 2). Landscapes in
which host communities are found in close prox-
imity to feeding areas typically occur where
considerable habitat fragmentation occurs, that
is, intrusion of agricultural activities, including
concentrated livestock grazing, into a formerly
undisturbed area. When they examined ancestral
versus invaded ranges separately, they found
that the predictive value of these host species
actually operated only in the invaded ranges.
Robinson et al. (1995b) suggested that because
some western coniferous forests are more open
than eastern forests, it was unclear whether or
not western and eastern cowbirds differed in
their preferences for forests, or if host distribu-
tion or some other factors influenced habitat oc-
cupancy by cowbirds. Our review indicates that
the relationship between the openness of forests
and cowbird abundance holds regardless of re-
gion. In fact, the variation seen in parasitism
rates within a region was at least partially ex-
plained as a response to changes in forest cover.
Further, many western forests have interlocking
canopies with dense understories (e.g., Pacific
Northwest, many western riparian forests).
Again, sweeping generalizations regarding East
and West seem unwarranted.
Hochachka et al. (1999) evaluated the rela-
tionship between torest coverage and parasitism
among eastern, central, and western regions of
the United States to provide a biological expla-
nation for differences in the relationship
tween forest coverage and rates of cowbird par-
asitization across the continent. They also ex-
amined if variation in forest coverage was as-
sociated with the presence or absence of
72 STUDIES IN AVIAN BIOLOGY NO. 25
cowbird parasitization in a study area, and,
where cowbirds were present, if the frequency
at which nests were parasitized was associated
with forest coverage. They obtained data on par-
asitization rates of forest birds from the Breed-
ing Biology Research and Monitoring Database
(BBIRD), with data from 23,448 individual
nests being analyzed. There were 26 study sites
on which the nesting success of forest-nesting
birds was monitored.
Hochachka et al. (1999) reported that the con-
clusions of previous research suggested that
larger proportions of forest cover will result in
a lower impact of Brown-headed Cowbirds on
their hosts. They further suggested that the re-
lationship between forest coverage and parasiti-
zation might differ away from the Midwest for
a number of reasons. They offered that variation
in cowbird abundance may not only affect ab-
solute rates of parasitization, but also the pattern
of variation in parasitization rate with varying
forest coverage. Cowbirds in different parts of
the continent encounter communities of hosts
with different lengths of exposure (e.g., May-
field 1965) and responses (e.g., Briskie et al.
1992) to parasitization, and host species with
longer exposure to cowbirds may be resistant to
parasitization regardless of the proportion of for-
est in a landscape. This appears true, but we do
not see any evidence of this varying predictably
by region in our review--all host responses are
seen across the country, and all responses were
seen within different localities within a region.
Hochachka et al. (1999) continued that the re-
lationship between cowbird parasitization and
forest coverage may also vary as a function of
the local area over which forests were measured.
Within local areas, forest coverage varied in its
power to predict parasitization, depending on the
size of the area over which forest coverage was
measured (Tewksbury et al. 1998, Donovan et
al. 2000). It is clear that vegetated patches sur-
rounded by agriculture are different than those
surrounded by more forest; this holds regardless
of region.
Hochachka et al. (1999) failed to find any
substantial differences in the behavior and hab-
itat requirements among the races of Brown-
headed Cowbirds (Lowther 1993). They con-
cluded that although cowbird abundance de-
clined westward--away from the center of the
cowbird's range--the lower abundance of cow-
birds in the West should result in a lower rate
of parasitization, but not in a complete reversal
of the relationship between parasitization rate
and forest coverage. In the analyses by Ho-
chachka et al. (1999), we see the importance of
examining parasitization in a spatially explicit
manner. Local factors, such as presence of ag-
riculture and patch size, will usually override
relatively region-wide factors, such as absolute
forest coverage and host density, in determining
parasitization rates. Our review shows that the
major factors determining the impacts of cow-
birds on hosts operate continent-wide (Table 2).
Fragmentation increases the degree of local
sympatry between cowbird and host. Peterjohn
et al. (2000) found no evidence to suggest that
changes in cowbird populations differentially in-
fluenced population changes in cowbird hosts
and rejecter species. Trends from BBS data
showed that both cowbird host species and spe-
cies rarely parasitized showed the same pattern
of direct association with trends in cowbird
abundance, and all of the correlations were low.
The general direct relationship between cowbird
trends and trends of neotropical migrants reflect-
ed the broad regional patterns of increasing bird
populations in western North America and de-
clines in the southern United States. They con-
cluded that large-scale changes in weather pat-
terns, land use practices, and habitat availability
were primarily responsible for the direct asso-
ciations they found between population trends in
cowbirds and their host species. The strong in-
fluence of weather was also used by Johnson
(1994) to explain the numerous range expan-
sions of western birds.
Lowther (1993) concluded that fragmentation
of eastern deciduous forest leads to increased
parasitism by cowbirds. Further, he summarized
that similar patterns were becoming evident in
western montane areas as human settlement ex-
pand. We agree, and conclude that geographic
differences in the response of birds to fragmen-
tation-and thus our characterizations of the as-
semblage of birds in different locations (e.g.,
species richness)--are largely determined by the
time since fragmentation occurred, rather than
any inherent differences in the response. Cow-
birds respond in distribution to fragmentation
first by the location of suitable feeding areas,
and secondarily to host abundance. As aptly
summarized by Robinson et al. (1995a), cow-
birds in heavily forested landscapes appear lim-
ited primarily by the availability of foraging ar-
eas rather than by host density. In fragmented
landscapes, however, cowbirds appear limited
primarily by host availability because feeding
areas are readily available as a result of the frag-
mentation.
ACKNOWLEDGMENTS
We thank the editors of this volume for inviting our
presentation and for critical reviews of several drafts.
We also thank additional comments provided by sev-
eral anonymous referees.
Studies in Avian Biology No. 25:73-80, 2002.
EFFECTS OF FOREST FRAGMENTATION ON BROOD
PARASITISM AND NEST PREDATION IN EASTERN AND
WESTERN LANDSCAPES
JOHN E CAVITT AND THOMAS E. MARTIN
Abstract. The fragmentation of North American forests by agriculture and other human activities
may negatively impact the demographic processes of birds through increases in nest predation and
brood parasitism. In fact, the effects of fragmentation on demographic processes are thought to be a
major underlying cause of long-term population declines of many bird species. However, much of our
understanding of the demographic consequences of fragmentation has come from research conducted
in North America east of the Rocky Mountains. Thus, results obtained from these studies may not be
applicable to western landscapes, where habitats are often naturally heterogeneous due to topographic
variation and periodic fire. We utilized data from a large database of nest records (> 10,000) collected
at sites both east and west of the Rocky Mountains to determine if the effects of fragmentation are
consistent across broad geographic regions. We found that forest fragmentation tended to increase the
frequency of brood parasitism by Brown-headed Cowbirds (Molothrus ater) east of the Rockies but
we were unable to detect a significant difference in the West. Within the eastern United States, nest
predation rates were consistently higher within fragmented sites relative to unfragmented sites. Yet,
in the West, fragmentation resulted in a decrease in nest predation relative to unfragmented sites. This
is perhaps accounted for by differential responses of the local predator community to fragmentation.
Our results suggest that the effects of fragmentation may not be consistent across broad geographic
regions and that the effects of fragmentation may depend on dynamics within local landscapes.
Key Words: brood parasitism; forest fragmentation; nest predation; Western North America.
Forest fragmentation occurs when large, contin-
uous, forested tracts are converted to other veg-
etation types or land uses so that only a few
scattered fragments remain (Faaborg et al.
1995). Fragmentation is a characteristic feature
of most human dominated landscapes (Burgess
and Sharpe 1981) and is particularly evident in
portions of northern Europe and eastern North
America (east of the Rocky Mountains) where
agricultural production and urban development
have reduced once contiguous forests into small,
and often isolated patches (Andrn 1992, Don-
ovan et al. 1995b, Robinson et al. 1995a).
For the past several decades considerable at-
tention has been given to the effects of forest
fragmentation on avian populations within North
America because of widespread population de-
clines (Gates and Gysel 1978, Ambuel and Tem-
ple 1983, Wilcove 1985, Askins et al. 1990,
Robinson et al. 1995a). The fragmentation of
once continuous forests may result in both a
quantitative and qualitative loss of habitat for
species (Faaborg et al. 1995). Fragmentation can
negatively influence avian populations by reduc-
ing the total area of native vegetation resulting
in the extinction of some species. In addition, as
an area is fragmented into increasingly smaller
patches, the amount of edge relative to interior
area increases. This exposes populations to the
conditions of a different surrounding ecosystem
and consequently to what are known as "edge
effects" (Murcia 1995). Research conducted to
date suggests several characteristics of forest
fragments that may negatively affect avian pop-
ulations. Small forest patches with a high edge
to interior ratio have: (1) High rates of nest pre-
dation. The abundance of avian and mammalian
nest predators (avian and mammalian) often are
higher along forest edges than within the forest
interior (e.g., Gates and Gysel 1978, Chasko and
Gates 1982, Hanski et al. 1996). (2) High rates
and intensities of brood parasitism. The Brown-
headed Cowbird (Molothrus ater) is often more
abundant along forest edges, and nests adjacent
to edges typically have higher rates of parasitism
(Donovan et al. 1995b, Robinson et al. 1995a,
Young and Hutto 1999). (3) Reductions in pair-
ing success. Several species within forest frag-
ments and near forest edges have a reduced
chance of attracting mates than when in large
continuous forests and within the forest interior
(Wander 1985, Gibbs and Faaborg 1990, Villard
et al. 1993, Burke and Nol 1998). (4) Lower
food availability for breeding birds. Burke and
Nol (1998) demonstrated that invertebrate bio-
mass was lower within forest fragments than
large continuous forests.
These fragmentation effects are thought to be
a major underlying influence of long term pop-
ulation declines of many birds, particularly for-
est-interior species within eastern North Ameri-
ca (Whitcomb et al. 1981, Robbins et al. 1989b,
Sauer and Droege 1992, Ball et al. 1994). Con-
sequently, many small forest fragments in east-
ern North America support few if any forest-
73
74 STUDIES IN AVIAN BIOLOGY NO. 25
interior species (Robbins et al. 1989b, Freemark
and Collins 1992).
Concern over avian population declines and
the potential demographic consequences to frag-
mentation have led to numerous studies de-
signed to examine the potential effects of forest
fragmentation on avian productivity. Previous
studies have suffered from two major problems.
First, studies of fragmentation effects have often
depended on data from artificial nests, which of-
ten do not reflect rates or patterns of predation
on real nests (e.g., Major and Kendal 1996).
Studies using artificial nests also cannot provide
information on the rates and patterns of cowbird
parasitism. Second, much of our current under-
standing of the demographic consequences of
fragmentation has come from research conduct-
ed east of the Rocky Mountains (George and
Dobkin this volume). Because most fragmenta-
tion studies are conducted over a relatively small
geographical area (but see Donovan et al. 1995b,
Robinson et al. 1995a), often with no replica-
tion, the results cannot be generalized to other
locations or regions. The effects of forest frag-
mentation within eastern North America may
not automatically be applied to the West for sev-
eral reasons. Unlike once contiguous eastern for-
ests, forests west of the Rocky Mountains have
a naturally heterogeneous pattern due to topo-
graphic variation, periodic fire, flooding and oth-
er climatic events (Franklin et al. this volume,
Hejl et al. this volume). Thus, human induced
fragmentation in the West (e.g., logging) may
not have yet created sufficiently different land-
scape patterns to affect avian populations (Hejl
1992, Freemark et al. 1995, Hejl et al. this vol-
ume). Unlike fragmentation in eastern North
America, fragmentation in the West is a rela-
tively recent phenomenon and thus there may
not have been sufficient time for birds to re-
spond (Rosenberg and Raphael 1986). Addition-
ally, the pattern of nest predation may not be
comparable between regions because local pred-
ator communities likely diffen Large predators
found in western North America, but largely ab-
sent in the East, may keep mesopredator popu-
lations in check (Soulfi 1988, Rogers and Caro
1998). Thus, the effects of fragmentation on avi-
an demographic processes in the East may not
apply to western North America.
In this paper, we utilized data from 20 repli-
cated study sites to examine the effects of forest
fragmentation on the reproductive success and
nest predation rates of a suite of forest nesting
species breeding at sites east and west of the
Rocky Mountains. We also examined if forest
fragmentation affects the frequency (number of
nests parasitized) and intensity (number of par-
asite eggs laid per nest) of brood parasitism dif-
ferently in eastern versus western sites. Finally,
we review the available literature on the effects
of fragmentation on nest predation by geograph-
ic region (east vs. west).
METHODS
We used nesting data from 10,446 nests (103,855
days of exposure) of 23 species of open nesting pas-
serines (Table 1). The data used in these analyses come
from the Breeding Biology Research and Monitoring
Database, a collaborative effort in which researchers
monitor avian breeding productivity and habitat con-
ditions using standardized sampling protocols (Martin
et al. 1997) at sites located throughout the continental
U.S. Data were utilized from 20 study sites located east
and west of the Rocky Mountains (Fig. 1). Examina-
tion of Figure 1 illustrates that sites were not evenly
distributed across North America and include a group-
ing centered along the Mississippi River and a group-
ing along the western side of the Rocky Mountains.
For simplicity we refer to sites east of the Rocky
Mountains as eastern sites and those along the western
side of the Rockies as western sites. Each site utilized
was replicated and composed of 4 to 30 separate study
plots. Sites were chosen from the database for this
analysis if the principal investigator designated them
as either largely fragmented by human activities (ag-
riculture or logging), or unfragmented. Because our
classification of sites is subjective, we also calculated
the proportion of forest within a 10-km radius of each
study plot from a GIS layer produced by the USDA
Forest Service covering the entire United States. A 10-
km radius was chosen because this area relates well to
distances most cowbirds commute between breeding
and feeding areas (Thompson 1994, Thompson and
Dijak 2000), and previous studies have used this area
as a simple measure of forest fragmentation (Robinson
et al. 1995a, Donovan et al. 1995b, Hochachka et al.
1999, Thompson et al. this volume). Forest coverage
was calculated using FRAGSTATS (McGarigal and
Marks 1995).
Three unfragmented sites in the east and three in the
west were paired with a nearby fragmented site to ex-
amine local landscape-level effects of fragmentation
on daily mortality rates (Table 2). Species were chosen
for the analysis if they satisfied all three of the follow-
ing criteria: (l) they are open nesting passerines that
primarily nest in forest habitats, (2) the total number
of nests available for each species was greater than 50,
and (3) the species were recorded breeding at more
than one site. All statistical analyses were conducted
using PC-SAS (SAS Institute 1998). Tests were para-
metric unless transformations of the data could not
meet assumptions of normality and homogeneous var-
iances. Results from statistical tests are referred to as
significant when P < 0.05. Values reported in the RE-
SULTS section are means + SE.
REPRODUCTIVE SUCCESS
We examined the effects of fragmentation on com-
ponents of reproductive success by performing paired
t-tests on mean clutch size and mean number of off-
spring fledged per nest, blocking by species and testing
for habitat diftbrences. Because cowbirds often remove
host eggs before parasitizing nests (Nolan 1978), we
PARASITISM, PREDATION, AND FRAGMENTATION--Cavitt and Martin
TABLE 1. FOCAL SPECIES USED IN ANALYSES
75
Colllnlon nanle Scientific name Nest placement Number of nests
Eastern Wood-pewee Contopus virens Tree 169
Western Wood-pewee Contopus sordidulus Tree 264
Acadian Flycatcher Empidonax virescens Tree 1624
Blue-gray Gnatcatcher Polioptila caerulea Shrub 210
Wood Thrush Hylocichla mustelina Shrub 814
Swainson's Thrush Catharus ustulatus Shrub 162
Veery Catharus fuscescens Shrub 100
American Robin Turdus migratorius Shrub 1461
Cedar Waxwing Bombycilla cedrorum Tree 163
Warbling Vireo Vireo gilvus Tree 468
Red-eyed Vireo Vireo olivaceus Shrub 673
Yellow Warbler Dendroica petechia Tree 1276
Kentucky Warbler Oporornis formosus Ground 115
Hooded Warbler Wilsonia citrina Shrub 363
Worm-eating Warbler Helmitheros vermivorus Ground 286
Ovenbird Seiurus aurocapillus Ground 411
American Redstart Setophaga ruticilla Tree 335
Northern Cardinal Cardinalis cardinalis Shrub 307
Indigo Bunting Passerina cyanea Shrub 492
Black-headed Grosbeak Pheucticus melanocephalus Tree 180
Song Sparrow Melospiza melodia Shrub 218
Northern Oriole Icterus galbula Tree 65
Western Tanager Piranga ludoviciana Tree 291
included only unparasitized nests in the analysis of
clutch size.
BROOD PARASITISM
The frequency of brood parasitism was calculated
by determining the number of nests containing cow-
bird eggs or young for a species within each study site.
We calculated parasitism frequency for a species only
when evidence of cowbird parasitism could be found
within the database. The intensity of cowbird parasit-
ism was calculated by determining the mean number
of cowbird eggs laid within each species' nest, within
each study site. Each species was classified according
to nest placement as either a ground, shrub, or tree
nester (Table 1 ) to determine if nest placement affected
a species' response to forest fragmentation. The clas-
sification of nest placement was based on Ehrlich et
al. (1988) and Baicich and Harrison (1997). Differenc-
es in the frequency of cowbird parasitism between
fragmented and unfragmented sites were examined us-
ing Friedman's nonparametric analysis of variance
(ANOVA) for randomized blocks (Sokal and Rohlf
1981) and differences in intensity of cowbird parasit-
ism were examined by using parametric ANOVAs. For
each analysis we blocked by species and tested for
habitat affects. Nonparametric Wilcoxon 2-sample
tests (Sokal and Rohlf 1981) were performed on the
arcsine transformed proportion of nests parasitized for
each nesting classification to determine if nest place-
ment affected a species' response to fragmentation.
NEST PREDATION
The daily mortality rate of nests and their associated
standard errors were estimated using the Mayfield
(1961, 1975) method as modified by Johnson (1979)
and Hensler and Nichols (1981). We calculated the dai-
ly mortality rate for nests of each species as the total
number of failures divided by the total number of days
nests were observed, pooled across all nests within
each study site. Differences in daily mortality rates be-
tween fragmented and unfragmented sites were ex-
amined using analysis of variance blocking by species
and testing for habitat affects. We also partitioned daily
mortality rates into cause-specific components (pre-
dation and parasitism) to determine the mechanisms
that may influence reproductive success in fragmented
versus contiguous sites. As in the parasitism analyses,
we classified each species according to its nest place-
ment. Differences in predation rates between paired
fragmented and unfragmented sites were examined us-
ing the program CONTRAST (Hines and Sauer 1989).
This program uses chi-square statistics to test for ho-
mogeneity of mortality rates by creating a linear con-
trast of the rate estimate (Sauer and Williams 1989).
LITERATURE REVIEW
We also reviewed the available literature to sum-
marize the effects of forest fragmentation and edge ef-
fects on nest predation rates between sites east and
west of the Rocky Mountains. We limited our review
to studies conducted in forested systems and to those
that examined the effects of anthropogenic fragmen-
tation (e.g., agriculture and forestry practices). Be-
cause most nest predation studies have used artificial
nests, we have included them in our review, but rec-
ognize that there are inherent weaknesses in their use
(Haskell 1995a, Ortega et al. 1998).
RESULTS
Sites classified by investigators as fragmented
had significantly lower proportion of forest cov-
76 STUDIES IN AVIAN BIOLOGY NO. 25
FIGURE 1. Locations of study sites used in analyses. Squares indicate sites designated as "eastern" and circles
as "western." Open symbols indicate fragmented sites and closed unfragmented. Each site plotted on the map
is composed of several independent study plots.
er within a 10 km radius (0.45 _+ 0.10) relative
to unfragmented sites (0.90 _+ 0.04, t = -4.199,
df = 6.2, P = 0.005).
REPRODUCTIVE SUCCESS
We found no difference in clutch size of un-
parasitized nests between fragmented and un-
fragmented sites (East 0.01 +_ 0.10, t =
-0.091, df = 1, P = 0.930; West 0.10 _+ 0.07,
t = 1.46, df = 1, P - 0.194). Yet, the mean
number of offspring fledged per nest attempted
was significantly greater in unfragmented rela-
tive to fragmented sites in the east (-0.23 _+
0.08, t = -2.72, df = 1, P = 0.02), but we found
no difference between fragmented and unfrag-
mented sites west of the Rocky Mountains (0.09
_+ 0.08, t - 1.06, df = 1, P = 0.314).
BROOD PARASITISM
The frequency of parasitism by Brown-head-
ed Cowbirds was significantly higher in eastern
fragmented sites relative to unfragmented sites
(X 2 = 317.34, df = 1, P < 0.001) but there were
no significant differences among western sites
(X 2 = 2.29, df = 1, P > 0.1; Fig. 2). In addition,
fragmentation resulted in a significantly higher
frequency of brood parasitism for all eastern
TABLE 2. LOCATIONS OF PAIRED FRAGMENTED AND UNFRAGMENTED SITES
Site Landscape Latitudelongitude Location
Columbia Frag 38.95-92.11
Mofep Unfrag 37.04-91.12
SE Forest I Frag 43.61-91.25
SE Forest 2 Unfrag 43.61-91.25
St. Croix Frag 45.36-82.72
Cheque. NF Unfrag 46.06-91.11
Bitterroot I Frag 46.10 114.23
Bitterroot 2 Unfrag 46.10-114.23
South Fork 1 Frag 43.62-111.63
South Fork 2 Unfrag 43.62-111.63
PNFF Frag 44.67-116.20
PNFU Unfrag 44.67-116.20
Columbia, MO
Ozarks, MO
Southeastern MN
Southeastern MN
Eastern MN, Western WI
Chequemegon NE WI
Bitterroot Valley, MT
Bitterroot Valley, MT
South Fork of Snake River, ID
South Fork of Snake River, ID
Payette National Forest, ID
Payette National Forest, ID
PARASITISM, PREDATION, AND FRAGMENTATION--Cavitt and Martin 77
0.4
E o.3
, 0.2
._
o
P o.1
n
i Fragmented
Unfragmented
East
FIGURE 2. Mean frequency of brood parasitism (_+
SE) by Brown-headed Cowbirds in fragmented and un-
fragmented eastern and western sites. A * indicates P
< 0.05.
West
nest placement classifications, but no differences
were found among western sites (Table 3).
The intensity of brood parasitism was not af-
fected by forest fragmentation east (F = 0.07, df
= 1, 10, P = 0.80) or west (F = 0.14, df = 1,
2, P = 0.75) of the Rockies. Within nest place-
ment classifications, shrub nesters at fragmented
western sites had a significantly higher intensity
of cowbird parasitism relative to unfragmented
sites (Table 3). There were no other differences
in parasitism intensity by nest placement clas-
sification (Table 3).
DAILY MORTALITY
Eastern fragmented sites tended to have high-
er daily mortality rates than unfragmented sites
(F = 3.03, df = 1, 47, P = 0.08) but the differ-
ence was not significant (Fig. 3). However, west-
ern unfragmented sites had significantly higher
daily mortality rates relative to fragmented sites
(F = 3.87, df = 1, 30, P = 0.05; Fig. 3). Eastern
shrub nesting birds suffered significantly higher
daily mortality rates on fragmented than on un-
fragmented sites, but no other differences by
nest placement classification were observed (Ta-
ble 3).
The daily mortality rate due to nest predation
was not significantly different between eastern
fragmented (0.031 -+ 0.002) and unfragmented
sites (0.030 _+ 0.003; F = 0.10, df = 1, 31, P =
0.76), but was significantly higher in western
unfragmented sites (0.038 -+ 0.003; F = 4.04, df
= 1, 30, P = 0.05) relative to fragmented loca-
tions (0.029 _+ 0.003). The daily mortality rate
due to parasitism was significantly greater in
TABLE 3. EFFECTS OF HABITAT FRAGMENTATION ON THE FREQUENCY (PERCENTAGE OF NESTS) AND INTENSITY
(NUMBER OF EGGS) OF BROWN-HEADED COWBIRD PARASITISM AND DAILY MORTALITY RATES WITHIN NEST PLACE-
MENT CLASSIFICATIONS FOR SITES EAST AND WEST OF THE ROCKY MOUNTAINS
Nest
Region placement Statistics Fragmented Unfragmented
Frequency of Cowbird Parasitism
Intensity of Cowbird Parasitism
Daily Mortality Rate
Z, dr, P Median, Median,
Upper-Lower Upper-Lower
Quartiles Quartiles
East Ground 2.33, 1, 0.02 28.5, 50.0-20.2 2.0, 13.3-0.9
Shrub 2.01, 1, 0.05 30.1, 62.7-26.5 6.4, 34.8-0.0
Tree 1.94, 1, 0.05 9.6, 17.0-8.0 1.6, 5.6-0.07
West Shrub 0.44, 1, 0.66 35.3, 52.6-0.0 3.1, 19.0-1.4
Tree 0.0, 1, 1.00 8.6, 21.1-0.0 1.8, 32.0-0.0
F, dfmode I error, P Mean -+ SE Mean -+ SE
East Ground 1.16, 1, 1, 0.48 1.7 + 0.4 1.0 +- 0.5
Shrub 1.25, 1, 6, 0.31 1.7 -+ 0.2 1.4 -+ 0.3
Tree 1.07, 1, 2, 0.41 1.1 _+ 0.05 1.0 _+ 0.1
West Shrub 21.36, 1, 2, 0.04 1.6 + 0.06 1.2 _+ 0.06
Tree 2.2, 1, 2, 0.27 1.2 +_ 0.08 1.4 _+ 0.08
Z, df, P Median, Median,
Upper-Lower Upper-Lower
Quartiles Quartiles
East Ground 1.3, 1, 0.20 0.4, 0.06-0.04 0.03, 0.05-0.03
Shrub -2.1, 1, 0.04 0.043, 0.05-0.04 0.037, 0.04-0.03
Tree 0.14, 1, 0.89 0.039, 0.04-0.03 0.034, 0.04-0.03
West Shrub 0, 1, 1.0 0.041, 0.04-0.03 0.04, 0.06-0.03
Tree -0.3, 1, 0.77 0.031, 0.04-0.03 0.037, 0.06-0.03
78 STUDIES IN AVIAN BIOLOGY NO. 25
0.06
656
Fragmented
Unfragmented
0.05
0.04 -
0.03
0.02
0.01
0.00
1463
East
1122
West
FIGURE 3. Mean daily mortality rate (2 SE) of nests
in fragmented and unfragmented eastern and western
sites. The total number of nests used in analyses are
given above each bar. A * indicates P < 0.05.
eastern fragmented sites (X 2 = 29.04, df = 1, P
< 0.001; median, upper-lower quartiles of frag-
mented sites 0.005, 0.01-0; unfragmented sites
0, 0.003-0) but not among western sites (X 2 =
0.278, df = 1, P > 0.5).
In two of the three paired eastern sites, daily
mortality rates were significantly higher on frag-
mented relative to unfragmented plots (Fig. 4).
This pattern was reversed in the west where two
of the three paired sites had significantly higher
daily mortality rates on unfragmented plots rel-
ative to fragmented ones.
LITERATURE REVIEW
Our review consisted of 39 studies; the vast
majority (33) were located east of the Rockies,
with only six studies in the West (Table 4). The
results of eastern studies were based on 53 field
seasons with a mean duration of 1.6 field sea-
sons per study. Western studies were based on
only 11 field seasons with a mean of 1.8 field
seasons per study. Of the studies that have tested
for edge effects, 56% of 16 studies detected an
eflct in the East, whereas only one of four stud-
ies observed an edge eflct in the West. Eastern
studies that examined the eflct of fragmentation
on nest predation rates typically found negative
relationships. A negative relationship between
fragmentation and nest predation was found in
68% of 19 studies, no relationship in 21%, and
two studies (--10%)reported a positive relation-
ship. Only three western studies reviewed tested
for fragmentation eflcts; two of three studies
found a positive relationship between nest pre-
dation rates and fragment size with the third
demonstrating no relationship.
MO
wI MN
East
MT
Unfragmented
N-ID S-ID
West
FIGURE 4. Comparison of fragmentation effects on
the daily mortality rates (+ SE) of paired local sites
east and west of the Rocky Mountains. The number of
nest records utilized in each comparison is indicated
above each bar. A * indicates P < 0.001; other com-
parison P > 0.05.
It has been suggested that forest fragments
embedded in different matrices may differen-
tially affect patterns of nest predation (Andr6n
1995, Bayne and Hobson 1997). According to
the "Eastern Paradigm," birds nesting in forest
patches imbedded in an agriculture or urban/sub-
urban matrix are expected to have lower repro-
ductive success relative to those nesting in more
natural settings (Thompson et al. this volume).
Thus, we classified studies according to the ma-
trix of the surrounding landscape (e.g., agricul-
ture and forest dominated). Six studies in the
East tested for edge effects within an agricultur-
ally dominated matrix and nine within a forested
matrix. Five of the six forest-agricultural edge
studies demonstrated an increase in nest preda-
tion, whereas only four of eight found edge ef-
fects within a forested matrix. We were unable
to review any western studies that tested for
edge effects within an agricultural matrix. Brand
and George (2000), however, compared preda-
tion rates on artificial nests between sites with
different types of adjoining habitat. In contrast
to predictions of the "Eastern Paradigm," Brand
and George (2000) found predation rates were
lower in patches adjacent to urban/suburban ar-
eas than those adjacent to natural grasslands.
Three of four western studies within forest-dom-
inated landscapes failed to demonstrate an edge
eflct.
Ten of the eastern studies reviewed tested for
fragmentation effects within an agricultural ma-
trix. Two of ten found no relationship between
forest area and nest predation rates but the re-
maining eight reported significant and negative
relationships. The results of eastern studies con-
ducted within a logging matrix are not as ap-
parent; of the nine studies reviewed, five report-
PARASITISM, PREDATION, AND FRAGMENTATION--Cavitt and Martin 79
TABLE 4. SUMMARY OF STUDIES EXAMINING THE EFFECTS OF EDGE AND FOREST FRAGMENTATION ON NEST PRE-
DATION RATES EAST AND WEST OF THE ROCKY MOUNTAINS
Nest Duration Edge Fragnlentation
Reference Location type a Matrix of stud?' effect effect c
Eastern Studies
Bayne and Hobson 1997 SK A Agriculture 2 no
Burger 1988 MO A Agriculture I yes
Donovan et al. 1995 Midwest R Agriculture 3 -
Donovan et al. 1997 Midwest A Agriculture I -
Fauth 2000 IN R Agriculture 3 no 0
Gates and Gysel 1978 MI R Agriculture 2 yes
Haskell 1995 NY A Agriculture I 0
Hobson and Baynes 2000 SK R Agriculture 4 -
Hoover et al. 1995 PA R Agriculture 2 -
Linder and Bollinger 1995 IL A Agriculture 1 yes
Marini et al. 1995 IL A Agriculture 1 yes
Robinson et al. 1995 Midwest R Agriculture 5 -
Saracco and Callazo 1999 NC A Agriculture 1 yes
Sargent et al. 1998 SC A Agriculture 1 -
Seitz and Zegers 1993 PA A Agriculture 1
Weinberg and Roth 1998 DE R Agriculture 2 -
Wilcove 1985 MD, TN A Agriculture I -
Bayne and Hobson 1997 SK A Forested 2 no
DeGraaf and Angelstam 1993 NH A Forested 1 0
Fenske-Crawford and Niemi 1999 MN A Forested 1 no
Gale et al. 1997 CT R Forested 2 0
Hanski et al. 1996 MN R Forested 1 no
King et al. 1996 NH R Forested 2 yes
King et al. 1998 NH A Forested 1 yes
Niemuth and Boyce 1997 WI A Forested 2 yes
Rudnicky and Hunter 1993 ME A Forested 2 no 0, +
Small and Hunter 1988 ME A Forested 1 no -
Vander Haegen and DeGraaf 1996 ME A Forested 1 yes -
Vander Haegen and DeGraaf 1996 ME A Forested 1 +
Yahner and Mahan 1996 PA A Forested 1 -
Yahner and Scott 1988 PA A Forested 1 -
Yahner and Wright 1985 PA A Forested 1 no
Keyser et al. 1998 AL A Residential I -
Western Studies
Hannon and Cotterill 1998 AB A Agriculture 2 0, +
Tewksbury et al. 1998 MT R Agriculture 2 +
Brand and George 2000 CA A Forested I yes
Cotterill and Hannon 1999 AB A Forested 3 no 0
Ratti and Reese 1988 ID A Forested 1 no
Song and Hannon 1999 AB A Forested 2 no
a R - study monitoring the effect on real nests, A - study monitoring effect on artfficial nests.
b Number of field seasons on which results are based.
c This column indicates the direction of the relationship between forest area and nest predation rates. A "0" indicates no relationship, a .... indicates
a negative relationship and a "+" indicates a positive relationship. Studies with more than one symbol represent annual variation in response.
ed negative relationships between forest area
and nest predation rate, two reported a positive
relationship, and two reported no relationship.
Only two western studies reviewed tested for
fragmentation effects within an agricultural ma-
trix, and both of these studies found a positive
relationship between nest predation rates and
fragment size.
DISCUSSION
We found that the patterns of brood parasitism
were not consistent between sites east and west
of the Rocky Mountains. The frequency of
brood parasitism was significantly higher in
eastern fragmented sites relative to unfragment-
ed sites, but not in the West. In addition, all nest
placement classifications within fragmented
eastern sites had a higher frequency of parasit-
ism relative to unfragmented sites, but we were
unable to detect a difference in the West. It ap-
pears this differential response may, in part, be
due to greater variation in the frequency of par-
asitism among western sites. For example, some
fragmented western sites reported no cowbird
80 STUDIES IN AVIAN BIOLOGY NO. 25
parasitism for shrub and tree nesting species and
others reported rates as high as 52%, a rate com-
parable to the most severely affected eastern
fragmented sites. This higher variability among
western sites in their response to brood parasit-
ism may be attributed to lower cowbird abun-
dance in the West as compared to the East
(Sauer et al. 2000). Morrison and Hahn (this vol-
ume), in an extensive review of the literature,
did not find evidence to suggest that cowbird
parasitism varied by region. Rather, they suggest
that the major factors determining the impacts
of cowbirds on their hosts operate continent-
wide. The frequency and intensity of cowbird
parasitism may be difficult to predict across
large geographic regions and may depend pri-
marily on local factors such as the presence of
agriculture and patch size (Hahn and Hatfield
1995, Hochachka et al. 1999, Morrison and
Hahn this volume).
It is clear from this study that the effects of
forest fragmentation on nest predation rates are
not necessarily consistent across the continent.
We found that eastern fragmented sites had few-
er offspring fledged per nest attempted, and
tended to have higher daily mortality rates rel-
ative to unfragmented sites. These results are in
agreement with the "Eastern Paradigm" (e.g.,
Thompson et al. this volume). In contrast, west-
ern unfragmented sites had significantly higher
daily mortality rates due to nest predation rela-
tive to fragmented ones. Paired sites east and
west of the Rockies also tended to follow this
same general pattern, higher daily mortality
rates in fragmented eastern sites and unfrag-
mented western sites (see Fig. 4).
Studies reviewed for this paper also suggest
that forest fragmentation may not be generalized
between sites east and west of the Rockies. East-
ern studies typically reported a negative rela-
tionship between forest area and nest predation
rates (68%). This generality is improved when
only studies conducted within an agricultural
matrix are examined (80%). Unfortunately, only
two western studies could be located, and thus
any conclusions regarding the effects of frag-
mentation on nest predation in the West are
speculative. However, both of these studies re-
ported a positive relationship between forest
area and nest predation rates and both studies
explained their results on the basis of a differ-
ential response of nest predators. Tewksbury et
al. (1998) demonstrated that nest predation was
higher on unfragmented sites relative to sites
fragmented by agriculture and human develop-
ment within the Bitterroot Valley of Montana.
They suggested this pattern was due to the re-
sponse of nest predators to fragmentation. Red
squirrels (Tamiasciurus hudsonicus), important
nest predators in their system, were more abun-
dant in forested landscapes and declined with
increasing forest cover (but see Bayne and Hob-
son 2000). Similarly, an artificial nest study con-
ducted in woodlots surrounding agricultural land
in Alberta, Canada, found higher rates of nest
predation within larger woodlots during one
breeding season and no difference during anoth-
er (Hannon and Cotterill 1998). They suggested
that forest interior predators, such as small mam-
mals, were important in driving this response.
Any attempt to uncover patterns associated
with nest predation is difficult because predation
is an inherently complex phenomenon. Each
study site will have a particular suite of reptilian,
mammalian, and avian predators (e.g., Miller
and Knight 1993, Fenske-Crawford and Niemi
1997, Thompson et al. 1999; Cavitt 1999, 2000)
and these predators will either take nests inci-
dentally (Vickery et al. 1992) or deliberately for-
age for nests (Sonerud and Fjeld 1987). Fur-
thermore, this suite of nest predators will vary
from site to site across North America and will
likely respond to fragmentation differently
(Bayne and Hobson 1998, 2000).
Unfortunately, few studies have been con-
ducted within the western U.S. that examine the
effects of forest fragmentation on nest predation
rates. Our analyses and literature review are
based on only a handful of western sites in com-
parison to the numerous studies conducted in the
East. Consequently, we are not certain of the
generality of our results throughout the West.
However, these results do suggest that (1) suf-
ficient evidence exists to question the applica-
tion of patterns observed in the eastern U.S.
across broad geographic regions, (2) more stud-
ies on the effects of fragmentation are needed
throughout the western U.S., particularly studies
that simultaneously monitor both the fates of
real nests and the response of the predator com-
munities, and (3) long-term studies are needed
to separate real effects from stochastic process-
es.
ACKNOWLEDGMENTS
The results presented here are the products of an
extensive list of investigators and their field assistants.
Without their collective efforts and generous contri-
butions of data to the BBIRD (Breeding Biology Re-
search and Monitoring Database) project this research
would not have been possible. We also wish to thank
T. L. George, D. Dobkin, and an anonymous reviewer
for comments and suggestions on drafts of this man-
uscript, and N. Summers for editorial assistance. This
research was supported by the BBIRD program under
the Global Change Research Program of the USGS
Biological Resources Division.
Studies in Avian Biology No. 25:81-91, 2002.
EFFECTS OF FOREST FRAGMENTATION ON TANAGER AND
THRUSH SPECIES IN EASTERN AND WESTERN
NORTH AMERICA
RALPH S. HAMES, KENNETH V. ROSENBERG, JAMES D. LOWE, SARA E. BARKER, AND
ANDRI A. DHONDT
Abstract. It is likely that selective forces on forest-specialist birds differ by region across the North
American continent, and closely related species that evolved under presumably differing selective
regimes may show markedly different responses to human-caused habitat fragmentation. We report
the results of research by the Cornell Laboratory of Ornithology that used volunteers to gather data
on the effects of habitat fragmentation on forest tanager and thrush species across their ranges and
the continent. This large-scale approach permits the comparison of effects between regions within
species as well as between species. Although forested landscapes in western North America are often
naturally fragmented compared to historically contiguous forests in eastern North America, an identical
set of principal components described forest fragmentation in both regions. Response by the Western
Tanager (Piranga ludoviciana) to overall fragmentation was very similar to that of the Scarlet Tanager
(P. olivacea) in eastern regions; probability of breeding dropped significantly for both species in highly
fragmented landscapes. The Hermit Thrush (Catharus guttatus), with both eastern and western pop-
ulations, is highly affected by fragmentation, with no geographic variation. Additionally, both the
Swainson's Thrush (C. ustulatus) in the West and the Veery (C. Jhscescens) in the East showed similar
strong effects of fragmentation. Predation and parasitism pressures as estimated by detections of mam-
malian and avian predators or of Brown-headed Cowbirds (Molothrus ater) differed between eastern
and western study sites, as did the response by cowbirds to fragmentation gradients in different regions.
Overall, however, we found that closely related species and populations showed similar responses to
habitat fragmentation, regardless of the historic configuration of the forests in which they occurred.
Key Words: Catharus fuscescens; Catharus guttams; Catharus ustulatus; geographic variation; Hy-
locichla rnustelina; Molothrus ater; Piranga ludoviciana; Piranga olivacea; predators; principal com-
ponents analysis.
Selective forces on forest-specialist birds differ
by region across the North American continent,
with differing levels of disturbance, nest para-
sitism, and of predation by a variable suite of
predators. Further, closely related species, or
populations within widely distributed species,
that have evolved under differing selective re-
gimes may show markedly different responses
to human-caused habitat fragmentation. How-
ever, testing whether presumably different selec-
tive regimes have indeed led to different re-
sponses to fragmentation in western and eastern
North America is not a trivial matter. It requires
several things that, heretofore, have not been
combined in one research project (or even in a
series of research projects); these include a large
geographic extent, a large sample size, standard-
ized data collection, and a widely applicable
measure of fragmentation. Further, the species to
be studied must have continent-wide distribu-
tions, or comparisons must be made between
closely related species with primarily eastern or
western geographic ranges. We report the results
to date from the Cornell Lab of Ornithology's
Birds in Forested Landscapes (BFL) project,
which used volunteers to gather data on the ef-
fects of habitat fragmentation on forest tanager
and thrush species across their ranges and across
North America.
Several authors have pointed out the differ-
ences between western, often coniferous, forest
and eastern deciduous forest landscapes as se-
lective environments for obligate forest-nesting
birds (Hejl 1992, Freemark et al. 1995, Tewks-
bury et al. 1998). For example, western and
eastern forests differ both in their original con-
figuration and in their subsequent use by humans
(Hejl 1992). Western forests are naturally
patchy, and in many areas are confined by mois-
ture regimes to riparian zones or to topographic
"islands" (Tewksbury et al. 1998). Further, hu-
man-caused fragmentation in western North
America has often been due to logging (Hejl
1992), and is of fairly recent origin. In contrast,
the formerly contiguous eastern hardwood for-
ests have been cleared for agriculture as long as
200 years before present (Smith et al. 1993,
Yahner 1997), and are now increasing from his-
torical lows as abandoned farms revert to forest.
In addition to disturbances caused by humans,
naturally occurring disturbances also play a
large role in shaping the selective environment
in which forest bird species evolve, and it is
clear that the type, scale, and frequency of dis-
turbance are different in the two regions. In
81
82 STUDIES IN AVIAN BIOLOGY NO. 25
western North America, the rainiest months oc-
cur in winter and spring, with relatively little
rain occurring during the summer and fall (Perry
1994). There are also extensive stands of early-
successional, serotinous tree species (lodgepole
pine, Pinus contorta; jack pine, P. banksiana;
and black spruce, Picea mariana) in boreal and
temperate montane forest (Perry 1994). Further,
dryer forests throughout the West are dominated
by the equally fire-adapted ponderosa pine (Pi-
nus ponderosa; Perry 1994). This combination
of seasonal droughts and fire-adapted vegetation
is reflected in frequent disturbance by fire (Free-
mark et al. 1995). In contrast, eastern deciduous
forests are relatively free of fire because of fre-
quent rains during the summer and fall, and be-
cause the combination of warmth and high mois-
ture levels leads to rapid decomposition of fallen
trees and other potential fuels (Perry 1994).
Other selective forces such as predation and
rates of nest parasitism also appear to differ be-
tween western and eastern North America. Both
the suites of predator species present, nest par-
asites, and their abundance (Donovan et al.
1995a), appear to combine to alter the selection
regimes in the two regions (Tewksbury et al.
1998, Rosenberg et al. 1999). For example, red
squirrels (Tamiasciurus hudsonicus), which are
the most common nest predator in some western
landscapes (Bayne and Hobson 1997, Darveau
et al. 1997, Tewksbury et al. 1998), are relative-
ly rare in the East where avian predators such
as corvid species are much more common (Ho-
grefe et al. 1998). Moreover, rates of nest para-
sitism by the Brown-headed Cowbird (Moloth-
rus ater) also vary with region, with highest
rates in the Midwest region (42.1% of Wood
Thrush, Hylocichla mustelina, nests) and lower
rates in the Mid-Atlantic (26.5%) and Northeast
(14.7%) (Hoover and Brittingham 1993). Final-
ly, the responses of both nest predators and par-
asites to fragmentation has also been shown to
vary across physiographic regions (Robinson et
al. 1995b, Trine 1998, Rosenberg et al. 1999).
These large differences between eastern and
western forest vegetation, historical land uses,
disturbance, and between parasitism and preda-
tion regimes provide ample grounds to suspect
differences in responses to fragmentation be-
tween eastern and western landscapes (Freemark
et al. 1995). The question becomes how to test
for these hypothesized differences. The first re-
quirement is for a measure of fragmentation that
is applicable across the continent, and in land-
scapes with differing conformations of habitat.
Habitat fragmentation implies loss of habitat,
a reduction in mean habitat patch size, increases
in the mean isolation of patches, and increases
in the mean amount of forest/non-forest edge
(Andr6n 1994). Most workers agree that loss of
habitat is one of the primary mechanisms by
which human-caused habitat fragmentation af-
fects populations of birds; some even suggest
that habitat loss is the primary (Trzcinski et al.
1999) or only (Fahrig 1997, 1998) mechanism.
Others have cited the effects of increased edge
(Paton 1994, Hoover et al. 1995, Donovan et al.
1997) and isolation (Robbins et al. 1989a, Vil-
lard and Taylor 1994, Villard et al. 1995, Des-
rochers and Hannon 1997), or of decreased
patch size (Schieck et al. 1995, Bellamy et al.
1996a, Keyser et al. 1998, Trine 1998) as also
playing an important role. However, it seems
most likely that both habitat abundance and con-
figuration (McGarigal and McComb 1995, Vil-
lard et al. 1999) play important roles, with the
effect of configuration increasing in importance
below a critical threshold in abundance (Turner
1989, Andrn 1994, Andrn et al. 1997, With et
al. 1997, Andrn 1999). What is needed is a
composite measure of habitat fragmentation that
captures a large proportion of the information
contained within these variables. Such a com-
posite measure should include information cap-
tured at the level of the surrounding landscape,
as well as at the patch (Freemark et al. 1995),
to afford a more complete understanding of the
factors affecting the distribution of sensitive spe-
cies (Hinsley et al. 1995). The Cornell Labora-
tory of Ornithology's BFL project provides both
the fragmentation data needed to calculate such
a composite measure, as well as data on species
occurrence from across the continent that are
necessary to test the hypothesis of different re-
sponses to fragmentation in eastern and western
landscapes.
BFL is a natural continuation of the Cornell
Lab of Ornithology's Project Tanager, which be-
gan as a National Science Foundation (NSF) Na-
tional Science Experiment. Project Tanager used
volunteers across North America (north of Mex-
ico) to study the effects of forest fragmentation
on four species of tanagers (Rosenberg et al.
1999). BFL uses the same methodology to study
the effects of fragmentation on seven species of
forest thrushes and two species of Accipiter
hawks. BFL was undertaken during the 1997
and 1998 breeding season in cooperation with
Partners in Flight, an umbrella organization of
government agencies, conservation organiza-
tions, and industry working together to promote
the conservation of birds in the Americas. Birds
in Forested Landscapes was continued during
the 1999 and 2000 field seasons in cooperation
with the United States Department of Agricul-
ture (USDA) Forest Service. For simplicity's
sake, we will refer to both Project Tanager and
TANAGERS AND THRUSHES IN EAST AND WEST--Hames et al. 83
Birds in Forested Landscapes as BFL hereinaf-
ter.
METHODS
DATA COLLECTION
The data-collection protocol for both Project Tana-
ger (Rosenberg et al. 1999) and BFL were essentially
identical. Each protocol consisted of four stages: the
unbiased selection of one or more study sites; repeated
visits to the study sites with the playback of conspe-
cific vocalizations to elicit responses from territorial
birds so that they could be counted; the estimation of
a number of patch- and landscape-scale measures of
fragmentation; and the coding of data onto computer-
readable bubble-forms, which were returned to the Lab
of Ornithology for collation and analysis.
In both studies, the volunteer participants selected
study sites in suitable wooded habitat (e.g., trees >6
m tall, canopy coverage 30%). The instructions
stressed that almost any patch of relatively mature for-
est or woodland was acceptable, and participants were
urged to find a range of patch sizes in similar habitat.
To avoid bias, participants were cautioned to select
their study sites based only on apparent habitat suit-
ability and to not select sites where the species of in-
terest was known to nest (Rosenberg et al. 1999). Each
study site was defined as a circle of 150-m radius;
point-counts and playbacks were conducted at the cen-
ter of each study site. Participants made two visits to
each site to census for territorial males of the focal
species. During a ten-minute point count on each visit,
participants looked and listened for territorial individ-
uals of the species of interest within the study site.
Participants also recorded the presence of avian and
mammalian predators, as well as any detections of
Brown-headed Cowbirds during the two point-counts.
The two required visits were timed to coincide with
pair bonding or nest building, and with the nestling/
fledgling stages of the breeding cycle. If no individuals
of the species of interest were detected within the point
count period, participants used playback of conspecific
territorial vocalizations to elicit a response from any
previously silent birds in order to verify that no terri-
torial males were present (Viilard et al. 1995, Rosen-
berg et al. 1999). Based on the behavior of birds that
were detected, each site was scored as missing, pres-
ent, possible, probable, or confirmed breeding using
breeding atlas codes (Anonymous 1986, Butcher and
Smith 1986, Rosenberg et al. 1999). To avoid counting
birds passing through on migration, we scored study
sites as "possible" breeding sites only if a singing
male of the focal species was detected on both visits.
While in the field, participants also used simple
techniques to estimate canopy height and amount of
canopy closure and noted other site characteristics
such as the forest type (coniferous, deciduous or
mixed), three most common tree species, and presence
or absence of surface water (streams or ponds) at each
site. After completion of the fieldwork, participants
used USGS topographic maps in conjunction with a
clear acetate grid overlay to estimate a number of mea-
sures of fragmentation for each site. (The grid was
intended for use with 1:24000 maps or aerial photos,
and was divided into 1 ha squares at that scale.) Esti-
mated fragmentation measures included the size of the
forest patch surrounding the study site, the isolation of
that patch from other patches, and the proportion of
forest and edge density (amount of forest/non-forest
edge corrected for the amount of forest) in the sur-
rounding 1000 ha block. The site's elevation above
mean sea level (MSL) was also recorded, as was an
estimate of the canopy height. A number of other data
were also collected at each site, but were not used in
this analysis. For further details on the development of
this protocol see Rosenberg et al. (1999). Participants
then coded these data onto computer-readable forms
and returned the forms to the Lab of Ornithology. At
the Lab, we edited each form by hand to ensure it had
been correctly completed; simple checks were also
performed when the SAS (SAS Institute 1989) dataset
was constructed to ensure that each datum was within
possible ranges. We excluded all sites with missing
data from subsequent analyses.
ANALYSES
At each site participants collected a number of data,
including measures of forest fragmentation. We
checked the distributions of all fragmentation variables
on normal probability plots and transformed variables
as needed before analysis began. Many of the mea-
sures of fragmentation are highly significantly inter-
correlated (Hames et al. 2001). To avoid multicolli-
nearity and the fitting of complicated models with dif-
ficult-to-interpret interaction terms, we used principal
component analysis (PCA) on the transformed data to
simplify the dataset by yielding fewer uncorrelated
factors (principal components), which explained a high
proportion of the variance in the original dataset (John-
son and Wichern 1982, Villard et al. 1995, Rosenberg
et al. 1999). We then used multiple logistic regression
to model the probability that territorial birds would be
found, based on the principal component values at
each site. We also used logistic regression to model
the probability of occurrence of the Brown-headed
Cowbird. To test the hypothesis that the effects of frag-
mentation varied between eastern and western land-
scapes, we compared the magnitude of the fragmen-
tation coefficients derived from logistic regression for
each region.
Principal components analysis
To conduct the PCA we combined all unique study
points from the 1995, 1996, 1997, and 1998 field sea-
sons of BFL into one dataset. We then used PROC
FACTOR (SAS Institute 1989) with the orthogonal
varimax rotation option to ensure that there was max-
imal separation (Johnson and Wichern 1982) and no
intercorrelation between the resulting principal com-
ponents. These rotated factors were then standardized
to a mean of zero and a standard deviation of one (SAS
Institute 1989) to facilitate comparison of estimated
coefficients, before they were used as predictor vari-
ables in the logistic regression.
We included a number of transformed variables
from each study site in the PCA. These variables were
the natural log of the forest patch size (Ln Size), edge
density (Ln Edge Density), elevation above msl (Ln
Elevation) and canopy height (Ln Canopy Height), as
well as the arcsine square-root transformed proportion
of forest (Asqrt %Forest; Table 1). The natural log of
84 STUDIES IN AVIAN BIOLOGY
TABLE 1. CORRELATION MATRIX FOR VARIABLES INCLUDED IN PRINCIPAL COMPONENTS ANALYSIS
NO. 25
Ln(size) Asqrt(%forest) Ln(edge density) Ln(eIevatiol) Ln(canopy height)
Ln(Size) 1.000 0.556** -0.386** 0.114** 0.064**
Asqrt(%Forest) 1.000 -0.740** 0.151 ** 0.029
Ln(Edge Density) 1.000 -0.156** -0.033
Ln(Elevation) 1.000 -0.031
Ln(Canopy Height) 1.000
Notes: Ln(Size) is the natural log of the patch size; Asqrt(% Forest) is the arcsine square-root transformed % forest in the surrounding 10130 ha;
Ln(Edge Density) is the linear measure of forest/non-forest in nffha; Ln(Elevation) is the natural log of distance above Mean Sea Level, in m;
L(Canopy Height) is the natural log of canopy height, in m. * P < 0.01, ** P < 0.001.
isolation, measured as distance to the nearest forest
patch of 40 or 200 ha, was not included in the PCA
because these data were missing from a substantial
number of records. As this variable was highly signif-
icantly correlated with Ln Size (r = -0.228, P --<
0.001), Ln Edge Density (r = 0.413, P < 0.001), and
Asqrt %Forest (r = -0.567, P < 0.00l), we felt that
the increase in sample size gained by omitting this
variable more than compensated for any loss of ex-
planatory power caused by its omission.
Logistic regression analysis
We used PROC LOGISTIC (SAS Institute 1996) to
model the probability that a singing male of the species
of interest would be detected on the two required vis-
its, either vocalizing spontaneously or in response to
playback of conspecific territorial calls, based on the
level of fragmentation at each site. We fit multiple lo-
gistic regressions using all of the calculated predictor
variables (Principal Components), and used manual
backward elimination of non-significant (Wald chi-
square P > 0.1 ) variables to fit the best model. Models
were compared using the G 2 statistic (difference in -2
log-likelihood between two nested models; Agresti
1996) and Akaike Information Criterion (AIC; Agresti
1996). The model chosen in each case was the most
parsimonious one that minimized the AIC and had a
G 2 that was not significant at the P < 0.05 level.
Comparison of fragmentation effects
To compare the effects of fragmentation in eastern
and western landscapes, we first subset our data into
two parts at the 98th meridian, a natural break in the
dataset that coincides roughly with the Great Plains.
We focused our analyses on widespread species that
had both eastern and western populations (e.g., Hermit
and Swainson's, Catharms ustulatus, thrushes and Vee-
ry, C. fuscescens) or congeneric species pairs (e.g.,
Western, Piranga ludoviciana, and Scarlet, P. oliva-
cea, tanagers) with one eastern and one western mem-
ber. In addition to these focal species, we compared
the effects of fragmentation on the presence of Brown-
headed Cowbird across North America. Additionally,
we used contingency table analysis to test for differ-
ences in the frequency of occurrence of several species
of predators in eastern and western landscapes.
We fit separate regression models for each member
of species pairs, and tested for differences in the
strength of regression coefficients between the pair us-
ing a large sample t-test. We rejected the null hypoth-
esis of no differences if P < 0.05. However, because
we had very large sample sizes for several species, we
also compared 95% confidence intervals for the frag-
mentation coefficient in each model, to avoid rejecting
the null hypothesis based on differences that were sta-
tistically, but not biologically, significant. We accepted
the null hypothesis of no difference in the effects of
fragmentation between species pairs if the 95% con-
fidence intervals for the mean estimated effect of frag-
mentation overlapped substantially. For single species,
we fit regression models that included an east/west
dummy or indicator variable, and region by factor in-
teraction terms. We rejected the null hypothesis of no
difference in effects of fragmentation for widespread
species if P < 0.05 (Wald chi-square) for the region
by fragmentation interaction term.
Comparison of predator and nest parasite pressure
To characterize differences in predation and nest
parasitism pressures between eastern and western land-
scapes, we used contingency table analysis to test for
differences in frequency of occurrence for the Brown-
headed Cowbird and for several species of predator.
Predator species included nest predators such as squir-
rels, chipmunks, and corvid species, as well as pred-
ators of fledglings and adult birds such as Accipiter
hawks.
RESULTS
DATA COLLECTION
Volunteers collected data at a total of 1840
sites during the 1995 and 1996 field seasons
(tanager species) and at an additional 1298 sites
during the 1997 and 1998 field seasons (thrush
species), for a total of 3138 sites (Fig. 1). These
sites spanned North America, covering 50 states
and provinces, and 55 physiographic regions
(Robbins et al. 1986). However, many sites were
missing required data, and we based subsequent
analyses only on sites for which complete data
were available. The proportion of sites which
contained a territorial male of the focal species
on both visits varied from 0.15 for the Swain-
son's Thrush to 0.325 for the Scarlet Tanager.
ANALYSES
Principal component analysis
Our principal component analysis was based
on 2515 unique study sites. These sites included
1933 sites with complete data east of the 98th
meridian (East), and 582 west of the 98th me-
TANAGERS AND THRUSHES IN EAST AND WEST--Hames et al. 85
FIGURE 1. Locations of the approximately 2500 study sites on which this analysis is based. Because of the
large size of the symbols representing study sites relative to distances on the map, one study site may cover
several others.
ridian (West). The correlation matrix for the in-
cluded variables showed highly significant cor-
relations between patch size, proportion of for-
est, and edge density (Table 1), which was re-
moved by the orthogonal varimax rotation, thus
yielding uncorrelated and easily interpretable
principal components (Table 2).
The first three principal components ex-
plained 83% of the variance in the data set (Ta-
ble 2). The first principal component (PC1) had
high positive loadings (coefficients >0.5) for
patch size and proportion of forest, and high
negative loading for edge density in the sur-
rounding landscape; we interpreted this principal
component as an overall measure of fragmen-
tation. PC1 varies from negative values for small
patches in a landscape with little forest and a
large amount of forest/non-forest edge, to posi-
TABLE 2. FACTOR LOADINGS DERIVED FROM PRINCIPAL COMPONENTS ANALYSIS OF 2515 FORESTED SITES
Variable PC 1 PC2 PC3
Ln(Size) 0.742 0.029 0.082
Asqrt(%Forest) 0.921 0.067 -0.041
Ln(Edge Density) -0.850 -0.090 0.178
Ln(Elevation) 0.093 0.995 -0.016
Ln(Canopy Height) 0.032 -0.016 0.997
Eigenvalue 2.187 1.027 0.923
Cumulative variance explained 0.437 0.643 0.827
86 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 3. COMPARISONS OF FRAGMENTATION VALUES (PC1) AT SITES SAMPLED IN EASTERN AND WESTERN NORTH
AMERICA FOR BIRDS IN FORESTED LANDSCAPES PROJECT
Geographic
region N Mean SD Minimum Maximum Range
East 1933 0.036 1.0069 -2.440 2.819 5.259
West 582 -0.127 0.9820 -2.591 2.393 4.984
Notes: Data were included from both the 1997 and 1998 field season of BFL. The mean fragmentation values from eastern and western landscapes
were not significantly different (pooled test of H0: iz I - Iz2 = 0, z - 0.366, df - 2513, P - 0.373).
tive values for large patches in a landscape with
high proportions of forest and little edge. Inter-
pretations of the second and third principal com-
ponents were straightforward: PC2 had a high
loading only for elevation and PC3 had a high
loading only for canopy height. PC3 was re-
tained in the PCA despite an eigenvalue (0.92),
which was less than the commonly accepted cut-
off of 1.0, because other studies have suggested
that the height of the canopy plays an important
role in habitat selection by forest-obligate birds
(Cody 1985, Hames 2001). Hereinafter PC1,
PC2, and PC3 will be referred to by their inter-
pretations as overall fragmentation, elevation,
and canopy height, respectively.
Overall, there was little difference between
western and eastern sites in the PCA-derived
overall fragmentation values (PC1). The mean
overall fragmentation values were not signifi-
cantly different for western and eastern sites (z
= -0.158, df = 2347, P = 0.874) and the min-
ima, maxima, and ranges were very similar (Ta-
ble 3).
Logistic regression analysis
The effect of fragmentation was a very similar
decrease in the probability of detection with in-
creasing habitat fragmentation for both tanager
species. Both the Scarlet Tanager in the East,
and the Western Tanager in the West, showed a
strong, highly significant increase in probability
of "possible" breeding as the fragmentation
measure PC1 increased (Table 4). This resulted
in an approximately five-fold decrease in the es-
timated probability of occurrence from the least
to the most fragmented site. The probability of
detection also increased with increasing eleva-
tion in the Scarlet (Fig. 2), but not the Western,
tanager (Fig. 3).
Sample sizes for the eastern populations of
the Swainson's Thrash, and for western popu-
lations of the Veery, were insufficient to make
within-species comparisons for these species.
We therefore treated these as a species pair and
restricted the regression analyses to eastern sites
for the Veery and to western sites for the Swain-
son's Thrush. Both of these thrushes displayed
similar highly significant increases in the prob-
ability of "possible" breeding as PC1 increased,
and fragmentation decreased (Table 4). As in the
tanager species, this resulted in an approximate-
ly five-fold decrease in probability from the least
to most fragmented sites. In both species the
probability of detection also decreased with in-
creasing elevation (Figs. 4, 5). The Hermit
Thrush (Table 5) also showed a highly signifi-
cant negative response to fragmentation of ap-
proximately the same magnitude as that dis-
TABLE 4. STRENGTH OF THE EFFECTS OF FRAGMENTATION (PC1), ELEVATION (PC2), AND CANOPY HEIGHT (PC3)
ON THE PROBABILITY OF DETECTING TERRITORIAL BIRDS, SHOWN AS ESTIMATED COEFFICIENTS DERIVED FROM MUL-
TIPLE LOGISTIC REGRESSION
ScarIet Tanager Western Tanager Veery Swainson's Thrush Wood Thrush
Intercept -0.6174'** - 1.4866'** - 1.5899'** -0.8660*** -0.7545***
PC 1/east 0.3648 a*** -- 0.5755 b** -- -0.1668**
PC1/west -- 0.5954 a*** -- 0.7315 b** --
95% CI low 0.2304 0.2765 0.3747 0.3054 -0.3089
95% CI high 0.5016 0.9299 0.7835 1.1902 -0.0453
PC2/east 0.3148'* -- -0.2061' -- ns
PC2/west -- ns -- -0.3184* --
PC3/east ns -- ns -- 0.3245***
PC3/west -- ns -- ns --
Notes: The PCA was calculated using all data from across North America; the notations "east" and "west" refer to the region in which each species
was studied; denotes that the corresponding coefficient was not calculated; ns indicates that the coefficient was not significant at the P <- 0.05
level.
a Test of H0: no difference between coefficients, z - 1.2812, P - 0.176, ns.
b Test of H0: no difference between coefficients, z - 0.5968, P = 0.334, ns.
* P <- 0.10, ** p < 0.01, *** P <- 0.001.
TANAGERS AND THRUSHES IN EAST AND WEST Hames et al. 87
. 1.00 1 n = 934
0.05 ....
O= 0.00_7.1fi 1
PC2 Higher Fragmention
Elevation
FIGURE 2. The effects of fragmentation (PC1) and
elevation (PC2) on the probability of detecting a sing-
ing or ca]ling male Scaler Tanager on both required
visits. Probability of occuence increases as agmen-
tation decreases and elevation increases. Model is
highly significant ( 2 log-likelihood = 39.876, df =
2, P (0.001).
n = 659
õ 1.00 '/
0.50 L ....
:' 0.25 ' F;mentation
- 0. ..... PC1
-1.87
Lower - ' 0 94
Elev:;i' Higher
PC2 Higher Fragmentation
Elevation
FIGU 4. The effects of fragmentation (PC1) and
elevation (PC2) on the probability of detecting a sing-
ing or ca]ling male Veery on both required visits. Prob-
ability of occuence increases as fragmentation and
elevation decrease. Model is highly significant (-2
log-likelihood 35.932, df - 2, P < 0.001).
played by the other thrushes. In addition, the
Hermit Thrush showed a highly significant in-
crease in the probability of "possible" breeding
with increases in elevation. The best model also
contained a significant region by canopy height
interaction term, so that we can conclude that
the effect of canopy height differed between
eastern and western populations. The uniform
response to fragmentation across species and
also across genera was striking, and somewhat
troubling. To test if this trend was universal and
potentially an artifact of our analytic design, we
also fit a logistic regression model to data for
the Wood Thrush, a purely eastern species. The
Wood Thrush showed the opposite trend (Table
4), a somewhat weaker but still significant in-
crease in probability of "possible" breeding
with increases in fragmentation. The Wood
Thrush was also more likely to be detected in
forests with higher canopies (Fig. 6).
In both the East and the West, the Brown-
headed Cowbird likewise showed an increase in
the probability of occurrence with increases in
fragmentation (Table 6). The best model for the
cowbird also contained a significant effect of
year, an indicator variable used to partition var-
iance due to slight differences in the Project
Tanager and BFL protocols as to when cowbirds
could be counted. In addition, there was a highly
significant year by region interaction term,
g 1.00 n = 339
0.75
0.50¾
0.25 2.23
a. 0.00_ p2.1'/'; 1
PC2 Higher Fragmentation
FIGURE 3. The effect of fragmentation (PC 1) on the
probability of detecting a singing or calling male West-
em Tanager on both required visits. Probability of oc-
currence increases as fragmentation decreases. Model
is highly significant (-2 log-likelihood = 13.757, df
= 1, P < 0.001). Note there is no significant effect of
elevation; elevation is only included for comparison
between graphs.
n = 140
._(2
0.75
'5 0.50 Lower
Fragmenlation
0.25 ' 2.0s
O 73
a. 0.00
-O.9O
Elevation Higher
PC2 Higher Fragmentation
Elevation
FIGURE 5. The effects of fragmentation (PC1) and
elevation (PC2) on the probability of detecting a sing-
ing or calling male Swainsoh's Thrush on both re-
quired visits. Probability of occurrence increases as
fragmentation and elevation decrease. Model is highly
significant ( 2 log-likelihood = 12.588, df = 2, P =
0.002).
88 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 5. RESULTS OF LOGISTIC REGRESSION OF GEOGRAPHIC REGION, FRAGMENTATION, ELEVATION, VEGETATION
STRUCTURE, AND THEIR INTERACTIONS, ON THE PRESENCE OF THE HERMIT THRUSH
Variable Parameter estimate df SE Wald X2 p
Intercept - 1.7284 1 0.1724 100.5300 <0.001
West -0.5680 1 0.3253 3.0498 0.081
PC 1 0.6793 I 0.1270 28.6187 <0.001
PC2 0.4099 1 0.1517 7.3037 0.007
PC3 -0.3452 I 0.1432 5.8130 0.016
West*PC3 0.3968 1 0.2245 3.1245 0.077
Notes: Regression based on data from 617 study sites censused for BFL from 1997 to 1998. "West" is an indicator variable: West - 0 east of the
Great Plains and West - I west of the Gmat Plains. Overall model X 2 = 57.879, df - 5, P < 0.001. Concordant pairs = 71.8%.
which showed that fewer cowbirds were detect-
ed in the West during the 1997 and 1998 BFL
field seasons. Further, there were other highly
significant region by fragmentation, and region
by elevation interactions, as well as a region by
elevation by year three-way interaction.
East/West comparisons
Because we used a standardized measure of
fragmentation that included both patch size and
the landscape measures proportion of forest and
of edge, and because this variable had similar
distributions in the East and West, we were able
to directly compare fragmentation coefficients
from logistic regressions. We tested for differ-
ences in the strength of fragmentation between
species using a large sample, two-tailed t-test, or
between populations within species by using the
Wald chi-square for the region by fragmentation
interaction term from the logistic regression. We
also directly compared the relative strengths of
the effects of fragmentation across species by
comparing 95% confidence intervals for the es-
1.00 n = 1089
0.50
._.., Higher
0'2511 I I -F2r.:: mentatiøn
a. 000
' . 0. PC1
1.95 -058
Higher " Lower
Canopy PC3 Lower Fragmentation
Canopy
FIGURE 6. The effects of fragmentation (PCI) and
canopy height (PC3) on the probability of detecting a
singing or calling male Wo Thrash on both required
visits. (Note that fragmentation axis is reversed from
other graphs.) Probability of occuence increases as
fragmentation increases and canopy height increases.
Mode] is highly significant (-2 log-likelihood =
26.381, df = 2, P < 0.001).
timated fragmentation coefficients. We found
that the strength of the negative effects was not
significantly different (z = - 1.281, P = 0.176)
in the Scarlet and the Western tanagers (Table
4) and that their 95% confidence intervals
showed considerable overlap. Likewise, there
was no significant difference in the strength of
fragmentation effects (z = 0.597, P = 0.334)
between the Veery in the East and the Swain-
son's Thrush in the West (Table 4), and the 95%
confidence interval for the Veery was complete-
ly contained within that of the Swainson's
Thrush. Logistic regression for the Hermit
Thrush (Table 5) did not yield a significant re-
gion by fragmentation interaction term (Wald X 2
= 0.099, P = 0.753), indicating that there was
no significant difference in the strength of frag-
mentation effects between eastern and western
populations. Thus, neither objective hypothesis
testing, nor a more subjective examination of the
degree of overlap in confidence intervals, pro-
vided strong evidence to reject the null hypoth-
esis of no difference in eastern and western re-
sponses to fragmentation, at least in these tana-
ger and thrush species.
Conversely, although the Brown-headed Cow-
bird, like the Wood Thrush, showed an overall
increase in probability of detection with increas-
es in fragmentation, a significant region by frag-
mentation interaction term showed that the re-
sponse to fragmentation was stronger in the
West than in the East (Table 6). Additionally,
contingency table analysis of the number of sites
at which the Brown-headed Cowbird was de-
tected (Table 7) showed a somewhat higher fre-
quency of occurrence in the East than the West,
although this difference was not significant (P
0.058). For predators, however, the picture is
more straightforward. Overall the East had a sig-
nificantly higher proportion of sites with at least
one mammalian (49.3%) or at least one avian
(64.4%) predator, than did the West (39.3% and
25.4%, respectively.) In fact, the West signifi-
cantly surpassed the East only in the frequency
of occurrence for the red or Douglas (Tamias-
TANAGERS AND THRUSHES IN EAST AND WEST Hames et al. 89
TABLE 6. RESULTS OF LOGISTIC REGRESSION OF PROTOCOL, GEOGRAPHIC REGION, FRAGMENTATION, ELEVATION
AND THEIR INTERACTIONS, ON THE PRESENCE OF BROWN-HEADED COWBIRDS
Variable Parameter estimate df SE Wald X 2 P
Intercept -0.8756 I 0.0747 137.37 <0.001
Year -0.2883 I 0.1259 5.24 0.022
West -0.3474 1 0.2210 2.47 0.116
PC1 -0.1998 1 0.0571 12.22 <0.001
PC2 0.1398 1 0.0999 1.96 0.162
Year*West -0.7813 1 0.3562 4.81 0.028
Year*PC2 -0.2965 1 0.1516 3.83 0.050
West*PC1 -0.5577 1 0.1604 12.09 <0.001
West*PC2 -0.7654 1 0.1798 18.12 <0.001
West*PC2*Year 0.8415 1 0.2944 7.65 0.006
Notes: Regression based on data from 2068 study sites certsused for Project Tanager and BFL from 1995 to 1998. "Year" is an indicator variable
that partitions variation due to differences in the protocols of the two projects. "West" is an indicator variable: West = 0 east of the Great Plains
and West = 1 west of the Great Plains. Overall model X 2 = 101.25, df = 9, P < 0.001. Concordant pairs = 63.0%.
ciurus douglasii) squirrels and for Accipiter spe-
cies. For all other predators the proportion of
sites with detections was significantly higher in
the East than in the West (Table 7).
DISCUSSION
Despite regional differences in topology, veg-
etation structure, suites of predators, and land
uses past and present, compounded by differ-
ences in phylogeny, there is a surprising unifor-
mity in the strength and direction of the respons-
es to fragmentation across the regions and the
species studied. This is particularly surprising
because Rosenberg, et al. (1999) showed clear
regional differences in the strength of responses
to fragmentation in the Scarlet Tanager. This
lack of regional effects in the present study may
be due to the "lumping" of variation occurring
at smaller scales, due to the extremely large re-
gions defined for the current study. However, as
measured by presence/absence of singing males,
for at least the tanager and thrush species we
studied, increasing fragmentation is strongly
correlated with decreasing probability of detec-
tion. What is perhaps not intuitively clear is the
correct interpretation of our results.
Our study measured the distribution (presence
or absence) of the focal species in relation to
fragmentation, not the demographic consequenc-
es of that fragmentation. However, demonstrated
sensitivity to fragmentation alone (shown as
changes in distribution of sensitive species) is
sufficient to infer that the tanager and thrush
species studied are adversely affected by frag-
mentation (Winter and Faaborg 1999). For ex-
ample, in a recent study of fragmentation effects
on grassland birds, Winter and Faaborg (1999)
make a clear distinction between the distribu-
tional consequences (lower densities, lower
probability of occurrence) and the demographic
consequences (lower nesting success) of frag-
mentation. Further, their results demonstrate that
some area-sensitive species may show distribu-
tional effects such as absence from small patch-
es (Robbins et al. 1989a), while other species
may show demographic effects such as lower
nesting success in fragments (Donovan et al.
1995a, Winter and Faaborg 1999). This useful
partitioning of the adverse effects of fragmen-
tation can equally well be applied to forest-
dwelling species. This is important because di-
rectly determining the demographic consequenc-
es of fragmentation requires a skilled field crew
and is extremely labor-intensive, making it im-
TABLE 7. PERCENTAGES OF SITES, BY REGION, AT WHICH NEST PREDATORS OR BROWN-HEADED COWBIRDS WERE
DETECTED DURING THE 1995, 1996, 1997 OR 1998 FIELD SEASON
Brown- Chipmunk Red or Gray Crow Jay Accipiter
headed (any Douglas or fox (any (any (any Mammalian Avtan
Cowbird species) squirrel squirrel species) species) species) predator predator
N 644 783 388 685 1148 1222 161 1429 1838
East % 21.88 29.94 9.86 26.83 44.54 45.59 4.38 49.28 64.40
West % 18.66 12.87 20.98 9.40 16.99 23.42 6.82 39.25 25.41
A 3.22 17.07 --11.12 17.43 27.55 22.17 -2.44 10.03 38.99
X2 3.603 88.687 64.622 101.356 187.665 118.740 5.058 23.390 69.124
P --< 0.058 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001
Notes: N = Total number of sites at which predators or Brown-headed Cowbird detected; 6, = difference in percentage detected (East - West).
90 STUDIES IN AVIAN BIOLOGY NO. 25
practical for an extensive, volunteer-based study
such as this one.
In the future, repeated sampling over several
breeding seasons will allow us to use rates of
site occupation or turnover (Villard et al. 1992,
Winker et al. 1995, Bellamy et al. 1996b), rather
than simple presence/absence in one season, as
a measure of the effects of fragmentation. For
example, Hames et al. (2001) have demonstrated
that the proportion of breeding seasons a site is
occupied by a territorial male Scarlet Tanager
over several years is inversely proportional to
the degree of fragmentation. Thus, we eagerly
await analyses of multiple-year BFL data, which
will allow us to make stronger inferences by us-
ing rates of territory occupancy as a currency
for the effects of fragmentation on habitat qual-
ity and reproductive success. However, although
direct demographic data are necessary for a
complete understanding of these effects, already
documented changes in distribution due to frag-
mentation are sufficient to demonstrate adverse
effects on sensitive species.
Our requirement that singing males be de-
tected on both visits to the study sites reduces
the probability that migrant males would be
counted as "possible" breeders; that is, as resi-
dent males displaying territoriality. However, al-
though the participants were charged to find as
many nests of focal species as possible, and to
monitor any nests found to determine reproduc-
tive success, very few nests were in fact found
(Rosenberg et al. 1999). This lack of direct mea-
sures of reproductive success, per se, limits our
ability to determine the processes that lead to the
observed patterns, and hence our ability to make
inferences about population effects of fragmen-
tation. In particular, Van Horne (1983) pointed
out that the use of density alone as a measure
of habitat quality could give rise to misleading
results, especially where territorial behavior lim-
its access to high quality habitat. Others (Maurer
1986, Hobbs and Hanley 1990, Winker et al.
1995) have supported her conclusion, and still
others (Vickery et al. 1992, Donovan et al.
1995b, Winter and Faaborg 1999) have also
pointed out that density does not necessarily
track reproductive success. However, although
density (measured as number of birds per area)
is mathematically equivalent to probability of
occurrence (with the same units), probability of
occurrence based on presence/absence data is a
special case of density measures with density
bounded by zero and one. In fact, the only re-
liable evidence of the effects of fragmentation
available from census data is arguably based on
the presence or absence of a species (Freemark
et al. 1995, Winter and Faaborg 1999). Further,
Boyce and McDonald (1999) point out that hab-
itat usage involves both active habitat selection
and passive persistence in a habitat. The fitness
consequences of utilizing that habitat, expressed
as selection on survival or reproduction (South-
wood 1977), is what gives rise to the perceived
patterns of distribution (Boyce and McDonald
1999). Thus, in most cases, extent of habitat use
(or presence/absence) reflects fitness in those
habitats (Fretwell and Lucas 1970). The patterns
described above (Van Horne 1983, and others)
may be exceptions to this generalization (Boyce
and McDonald 1999).
Thus, at first glance, it is somewhat surprising
that the high sensitivity to fragmentation shown
in most of the species studied was not correlated
with population trends as measured by the
Breeding Bird Survey. For example, while the
Veery showed a significant decline survey-wide
between 1966 and 1996 (trend = -1.4%, P <
0.01; Sauer et al. 1997), the Hermit Thrush,
which displayed approximately the same level of
fragmentation sensitivity as the Veery, showed
a survey-wide significant increase over the same
period (trend = +1.4%, P = 0.01; Sauer et al.
1997). The equally sensitive Swainson's Thrush
displayed no significant trend at all survey-wide.
Finally, the Wood Thrush, whose probability of
occurrence increased with increasing fragmen-
tation, has shown a strong and highly significant
negative trend (trend = -1.8%, P < 0.01) over
the same 30 years (Sauer et al. 1997). However,
this is perhaps not a total surprise.
As migrant species, the thrushes' and tana-
gers' population trends reflect influences on the
birds on their breeding grounds, during migra-
tion, and on their wintering grounds. In the case
of the Wood Thrush, population decreases co-
incide with deforestation in their tropical win-
tering grounds (Morton 1989) and a decrease in
the survival of non-territorial "floaters" while
over-wintering (Rappole et al. 1989). In contrast,
the Hermit Thrush, which is the only thrush ex-
hibiting an increasing population trend, is also
the only species we studied that does not winter
in the tropics. Thus, demonstrated sensitivity to
fragmentation on the breeding grounds alone
may not be sufficient for prediction of popula-
tion trends of these neotropical migrant species.
Data from all portions of the annual cycle are
important to understand changes in migratory
bird demography (Danielson et al. 1997). How-
ever, at least in the case of the Wood Thrush,
the preponderance of recent evidence suggests
that declining trends are due, in large part, to
poor reproductive success in fragmented land-
scapes on the breeding grounds (Robinson and
Wilcove 1994, Hoover et al. 1995, Trine 1998).
Another surprising result of our analysis was
the uniformly negative correlation between the
TANAGERS AND THRUSHES IN EAST AND WEST--Hames et al. 91
degree of fragmentation and presence of our fo-
cal species (with the exception of the Wood
Thrush), which held across western and eastern
regions. As recently as five years ago, Freemark
et al. (1995) pointed to differences between the
landscape contexts of studies of fragmentation
in the East and the West as a means to explain
the clear differences in levels of response be-
tween the regions. They pointed to the fact that
most western studies had taken place in forested
regions fragmented by silviculture, as opposed
to most eastern studies that took place in land-
scapes where forests were fragmented by agri-
culture and urbanization (Freemark et al. 1995).
Our current analysis did not take the nature and
extent of adjacent habitat into account because
these data were not always available, but instead
made comparison based on patch and landscape
configuration alone. Further, Freemark et al.
(1995) cited an earlier study by Rosenberg and
Raphael (1986), which suggested that the lack
of strong reaction by western species may also
be due to relatively recent fragmentation com-
bined with a time-lag in response by sensitive
birds, as well as a lack of truly isolated forest
patches. It is possible that the intervening 16
years was a sufficient time for a time-lagged re-
sponse to become apparent, or for levels of par-
asitism by Brown-headed Cowbirds to increase
with increasing human populations throughout
the West (Tewksbury et al. 1998). It seems just
as likely, however, that our study was simply the
first that undertook a large scale comparison of
fragmentation effects in the East and West using
the same methodology and measures of frag-
mentation in both regions, and that the nature of
adjacent habitat has a far from negligible effect
on sensitive species' response to fragmentation.
In summary, it is clear that the trends in prob-
ability of detecting tanager or thrush species in
landscapes with varying proportions of fragmen-
tation are the same, in both direction and
strength, in both western and eastern landscapes.
Further, this similarity in response to fragmen-
tation occurs despite differences in both the
suites and abundances of predators and of nest
parasites, and despite significant regional differ-
ences shown in other analyses (Rosenberg et al.
! 999). The Brown-headed Cowbird increased in
all landscapes with increases in the level of frag-
mentation, and this effect was stronger in the
West. However, all the focal species except the
Wood Thrush showed strong negative effects of
fragmentation on possible breeding, whatever
their distribution and whatever the history of
landuse in their ranges. Finally, this study dem-
onstrates that the use of volunteer citizen sci-
entists in conjunction with explicit, rigorous pro-
tocols using playback to verify the absence of
the species of interest, can be effective at ad-
dressing a large-scale question such as this by
gathering detailed distributional data about spe-
cies of interest across North America.
ACKNOWLEDGMENTS
This research was conducted with funding from the
National Science Foundation, the National Fish and
Wildlife Foundation, the USDA Forest Service, Archie
and Grace Berry Charitable Foundation, Florence and
John Schumann Foundation, and the Packard Foun-
dation. We also gratefully acknowledge helpful statis-
tical advice from C. E. McCullough, W. M. Hochach-
ka, and fieldwork by hundreds of dedicated volunteers.
We also thank the editors, S. T. Knick, and an anon-
ymous reviewer for comments that improved the paper.
Studies in Avian Biology No. 25:92-102, 2002.
THE EFFECTS OF HABITAT FRAGMENTATION ON BIRDS IN
COAST REDWOOD FORESTS
r. LUKE GEORGE AND L. ARRIANA BRAND
Abstract. Human activities in the redwood (Sequoia sempervirens) region over the last 150 years
have changed what was once a relatively continuous old-growth forest ecosystem into a highly frag-
mented mosaic of young, mature, and old-growth forest patches, agricultural land, and human settle-
ments. We summarize recent studies on the eflcts of forest fragmentation on diurnal landbirds in
redwood forests and present new analyses of the effects of forest patch size on the distribution and
abundance of breeding birds. Analyses of the relative abundance of 31 bird species in 38 patches of
mature and old-growth redwood forest indicate that six species were positively correlated with forest
patch area and may be sensitive to fragmentation: Pileated Woodpecker (Dryocopus pileams), Pacific-
slope Flycatcher (Empidonax difficilis), Steller's Jay (Cyanocitta stelleri), Brown Creeper (Certhis
americana), Winter Wren (Troglodytes troglodytes), and Varied Thrush (lxoreus naevius). These spe-
cies (except the Steller's Jay) have been identified as sensitive to forest fragmentation in other studies
of wet coniferous forests in the western U.S. The American Robin (Turdus migratorius), Orange-
crowned Warbler (Vermivora celata), Dark-eyed Junco (Junco hyemalis), and Song Sparrow (Melos-
piza melodia) were negatively correlated with patch area. Song Sparrows and Orange-crowned War-
blers are more abundant in young second-growth than mature redwood forests, and American Robins
and Dark-eyed Juncos are generally associated with forest openings. Thus, these four species are
associated with and likely responding to habitats surrounding forest patches. Previous analyses have
shown that four of the species that were positively associated with patch area, Pacific-slope Flycatch-
ers, Brown Creepers, Winter Wrens, and Varied Thrushes, were less abundant at forest edges than the
forest interior, suggesting that edge avoidance may be responsible for their sensitivity to fragmentation.
Two species, Steller's Jay and Swalnson's Thrush (Catharus ustulatus), were more abundant along
forest edges. In a previous study, we found that predation on artificial nests increased with proximity
to forest edge and that Steller's Jays were observed preying on some of the nests. These and other
studies suggest that several bird species are sensitive to fragmentation of old-growth and mature
second-growth coast redwoods possibly due to changes in microclimate along forest edges or to
increased nest predation and subsequent avoidance of forest edges. Implementation of forest practices
that reduce the amount of forest edge on the landscape may reduce the potential impacts of fragmen-
tation on bird species in redwood forests.
Key Words: area effects; artificial nests; diurnal landbirds; edge effects; forest fragmentation; nesting
success; redwoods; Sequoia sempervirens.
Numerous studies have documented the negative
effects of forest loss and fragmentation on birds
breeding in forests of the midwestern and east-
ern United States (Ambuel and Temple 1982,
Askins et al. 1990, Robinson and Wilcove 1994,
Walters 1998, Thompson et al. this volume) and
Europe (Andrdn 1992, 1994). Furthermore, a
consensus is emerging among scientists working
in these regions that habitat fragmentation re-
suits in increased nest predation and parasitism,
thereby reducing breeding productivity and pos-
sibly leading to population declines. Thompson
et al. (this volume) have proposed a "top-down"
hierarchical model that includes regional, land-
scape-level, and local effects to explain variation
in nesting success across the landscape. How-
ever, there is substantial variation among studies
and some results in western forests seem to con-
tradict the general pattern (e.g., Tewksbury et al.
1998). This has led to suggestions that the
"Eastern Paradigm" may not be applicable to
western forests.
Over the last 150 years, Westside forests (for-
ests west of the Sierra Nevada/Cascade crest)
have been extensively logged, resulting in a
fragmented pattern of late-seral stage forest in a
sea of younger forest (Garmen et al. 1999). Be-
cause forest fragmentation has had such a dra-
matic impact on birds in other regions, it has
been suggested that similar effects may be oc-
curring in Westside forests. However, while
some species such as the Northern Spotted Owl
(Strix occidentalis caurina) and Marbled Mur-
relet (Brachyramphus marmoratus) show strong
negative responses to forest fragmentation, stud-
ies of passerines and other small bird species in
Westside forests have documented few effects of
forest fragmentation (Rosenberg and Raphael
1986, Lehmkuhl et al. 1991, McGarigal and Mc-
Comb 1995).
A number of hypotheses have been suggested
to explain the lack of response of birds to forest
fragmentation in Westside forests, including: (1)
insufficient time for species to respond (Rosen-
berg and Raphael 1986, Lehmkuhl et al. 1991),
(2) limited extent of forest loss (Rosenberg and
92
FRAGMENTATION EFFECTS IN REDWOOD FORESTS---George and Brand 93
Current and Historical Distribution Of Redwood Forests
l
1
FIGURE 1. Original distribution of coast redwood (Sequoia sempervirens) forests and current distribution of
old-growth and mature second-growth coast redwood forest north of Point Reyes National Seashore. Current
distributions are based on Landsat satellite imagery (Fox 1997).
Raphael 1986, Lehmkuhl et al. 1991), (3) the
matrix (generally young forest) is less detrimen-
tal to nesting birds (McGarigal and McComb
1995), and (4) the species are adapted to hetero-
geneous landscapes and thus to the kinds of
changes that logging has produced on the land-
scape (McGarigal and McComb 1995, Hejl et al.
this volume). The first two hypotheses do not
role out fragmentation effects but suggest that
effects may only be evident in forests that have
been logged extensively in the past. The latter
two hypotheses imply that forest fragmentation
due to logging will have little effect even in
heavily logged regions of the western United
States.
Coast redwood (Sequoia sempervirens) for-
ests have been heavily logged since the mid
1800s. Only about 3.5% of the pre-settlement
distribution remains as original growth, and the
current distribution of mature and old-growth
redwood forest habitat is highly fragmented
(Fig. 1; Larsen 1991). Logging began earlier and
has occurred more extensively in redwood than
in other Westside forests (Sawyer et al. 2000).
Thus, the effects of fragmentation may be more
evident in redwood than in other Westside for-
ests.
The birds of the redwood forest have not been
extensively studied. However, over the past sev-
eral years there have been a number of studies
that have examined the effects of forest frag-
mentation on the birds of the region. Our objec-
tives in this paper are to: (1) present new anal-
yses of bird response to patch size and nesfing
success of Winter Wrens and Swainson's
Thrushes (see Table 1 for scientific names of
bird species studied) with respect to distance
from forest edge, (2) summarize published and
unpublished studies on the effects of forest frag-
mentation on birds in redwood forests, and (3)
compare the effects of forest fragmentation on
94 STUDIES IN AVIAN BIOLOGY NO. 25
birds in redwood forests to those found in the
Midwest and the eastern United States.
METHODS
We describe the methods for the analysis of bird
response to patch size and nesting success of Winter
Wrens and Swainson's Thrushes in detail, as these
analyses have not been published. Methods for esti-
mates of relative bird abundance with respect to dis-
tance from forest edge and the artificial nest experi-
ments have been published elsewhere (Brand 1998;
Brand and George 2000, 2001).
STUDY AREA
We conducted our studies in redwood forest patches
in Humboldt County, California. Point counts that we
used for analysis of bird response to patch size were
conducted from I May to 15 July, 1994. Monitoring
of Winter Wren and Swainson's Thrush nests took
place during May-August 1998-1999. Study sites con-
sisted of old-growth as well as mature second-growth
(>80 years) coast redwood forests. The overstory of
all stands was dominated by redwoods (>50%), but
other tree species found in these stands included Doug-
las-fir (Pseudotsuga menziesii), Sitka spruce (Picea
sitchensis), western hemlock (Tsuga heterophylla),
grand fir (Abies grandis), red alder (Alnus rubra), Cal-
ifornia bay (Umbellularia californica), big-leaf maple
(Acer macrophyllum), and tan-oak (Lithocarpus den-
sifiorus). The understory was dominated by rhododen-
dron (Rhododendron rnacrophyllum), sword fern (Po-
lystichurn munitum), salal (Gaultheria shallon), Cali-
fornia huckleberry (Vacciniurn ovaturn), red huckle-
berry (Vaccinium parvifiorum), cascara (Rhamnus
purshiana), salmonben'y (Rubus spectabilis), Califor-
nia blackberry (Rubus ursinus), Himalayan blackberry
(Rubus discolor), and red elderberry (Sambucus race-
rnosa). The edge of each patch was defined by gaps
->100 m in the forest canopy occurring adjacent to
several features such as rivers, grasslands, young forest
(<30 years), residential development, and roads.
Study sites were located on public lands managed
by Humboldt Redwoods State Park, Redwood National
Park, Prairie Creek Redwoods State Park, the City of
Arcata (Arcata Community Forest), Humboldt State
University Wildlife Department (Wright Wildlife Ref-
uge), the City of Eureka (Sequoia Park), and Grizzly
Creek State Park. Study sites were also located on
Simpson Timber Company property and other private
lands. Stands on privately owned land have been in-
tensively managed in the past 100 years. Most of the
sites on public lands have never been logged; some
were logged once and are now mature stands (>100
years).
For the patch size study, we used orthophotographic
quadrangles of the region to identify potential forest
patches characterized by >50% redwood canopy and
a stand age of >80 years. From approximately 90 el-
igible patches, we randomly chose 38 forest patches to
survey. The size of patches ranged from 0.89 ha to
4252 ha. However, 35 of the 38 patches were <160
ha. The study sites were distributed over approximate-
ly 700 km 2, all within 50 km of the Pacific Ocean.
The fate of Winter Wren and Swainson's Thrush
nests was studied at the Wright Wildlife Refuge, the
Arcata Community Forest, and Redwood National
Park. Plots were established along forest edge (edge
plots) and in forest interior (interior plots, >400 m
from forest edge). One edge plot was established at the
Wright Wildlife Refuge, two interior and one edge plot
were established in the Arcata Community Forest, and
two interior plots were established in Redwood Na-
tional Park. Both the Wright Wildlife Refuge and the
Arcata Community forest bordered on suburban areas.
BIRD RESPONSE TO PATCH SIZE
To examine which passedfie bird species are sensi-
tive to forest patch size and shape during the avian
breeding season, we investigated the distribution and
relative abundance of birds in redwood forest patches
using point counts (Verner 1985). The location of the
first point in a patch was randomly selected. From that
point, a direction was randomly chosen to establish the
succeeding points placed 200 m apart, until no further
points could be placed within the patch or we had es-
tablished 4 points. Most points were > 100 m from the
edge of the patch. In some cases the size and shape of
the patch made this impossible, but in all cases points
were placed no closer than 50 m from the edge of the
patch.
Each patch was surveyed four times (twice by each
of two observers), approximately once every two
weeks. Point counts lasted 8 min, and were conducted
at least 5 min apart. Some patches were too small to
contain four points. In these patches, we established
fewer points but maintained equal sampling effort by
conducting additional counts at the points. If one point
was established in a patch, then four, 8-min point
counts spaced 5 min apart were conducted at one
point. If a patch contained two points, two point counts
were conducted 5 min apart at each point. If a patch
contained 3 points, two point counts were done at a
randomly chosen point, then one point count was con-
ducted at the two remaining points. If four points were
established in a patch, one point count was conducted
at each point. All point-counts were conducted within
four hours after sunrise.
Data were recorded separately for each 8-min point
count even if occurring 5 min apart in the same loca-
tion. During an 8-min point count, birds were not
counted twice unless there was a high certainty that it
was a different individual of the same species. The
number of birds counted at each point in each patch
across all visits to each patch was summed to get an
index of relative abundance for that patch.
To quantify the landscape variables of habitat patch
size and patch shape, we used a planimeter and ortho-
photoquads to measure the area (ha) of each forest
patch and a map wheel to measure the total perimeter
(m) of each patch. Because perimeter length is corre-
lated with area, we computed an index of patch shape
using the ratio of the perimeter (m) of a given forest
patch to the perimeter (m) of a circular forest patch of
equal area. Both patch area and patch shape were log
transformed for analysis.
Because the bird data are counts, we used Poisson
regression (McCullagh and Nelder 1989) to examine
the effect of patch area and shape on bird abundance.
Only species that were observed in at least 20% of the
patches were included in the analysis. We used the
FRAGMENTATION EFFECTS IN REDWOOD FORESTS--George and Brand 95
natural log of patch area to deal with wide disparity in
patch areas. The natural log of patch area and patch
shape were correlated (r 2 = 0.34, df = 36, P = 0.037)
and therefore we used only log patch area in the anal-
yses because it explained a higher proportion of the
variation in bird abundances than log patch shape, and
patch area is generally a better predictor of bird abun-
dance than patch shape (Galli et al. 1976. Blake and
Karr 1987, Askins et al. 1990). A scale parameter was
included in the model, which allows the variance to be
greater than the mean to allow for over-dispersion of
bird detections within patches compared to a standard
Poisson distribution (McCullagh and Nelder 1989).
Species that were positively associated with area were
considered sensitive to fragmentation. All analyses
were conducted using SAS statistical software (SAS
Institute 1999).
NATURAL NESTS
In 1998 and 1999 nests of Swainson's Thrushes and
Winter Wrens were monitored in plots established
along forest/suburban edges and at locations distant
(>400 m) from suburban edges (J. Kranz and T L.
George, unpubl, data). Nests were monitored at 3-4
day intervals until the nest failed or the young fledged.
Daily Survival Rate (DSR) was computed for edge
(<100 m from suburban edge) and interior (>100 m
from suburban edge) nests using the Mayfield method
(Hensler and Nichols 1981 ) and comparisons were per-
formed using program CONTRAST (Hines and Sauer
1989, Sauer and Williams 1989). Because of small
sample sizes of nests, we used a = 0.10 to reduce the
chance of a Type II error.
LITERATURE SURVEY
We surveyed the literature for studies of the re-
sponse of diurnal landbirds to forest fragmentation in
wet coniferous forests of the Pacific Northwest. We
classified a species as area sensitive if its abundance
increased with patch size (Schieck et al. 1995; this
study) or with the amount of mature or old-growth
forest within a surrounding buffer. Buffers differed in
extent fi'om 100 ha (Manuwal and Manuwal this vol-
ume) to 250-300 ha (McGarigal and McComb 1995).
Rosenberg and Raphael (1986) examined both patch
size and the amount of mature or old-growth in a
1,000-ha buffer surrounding the stand. Lehmkuhl et al.
(1991) examined three scales: patch size, the area ad-
jacent to the patch (within 400 m of the boundary),
and the landscape (circular 2,025 ha area centered on
the patch). Hejl and Paige (1994) compared bird rel-
ative abundance between a continuous stand of old-
growth forest, an old-growth forest with 1-8 year-old
clearcuts, and a selectively logged forest. A species
was classified as edge sensitive if its abundance de-
clined with proximity to edge (Brand and George
2001) or declined in abundance as the amount of edge
increased in a surrounding buffer area. Buffer areas
varied from 10 ha (Rosenberg and Raphael 1986), to
100 ha around each patch (Manuwal and Manuwal this
volume), to 400 m surrounding the patch (Lehmkuhl
et al. 1991). Thus there were seven studies that ex-
amined area effects and four that examined edge ef-
fects. We included fewer studies in our analysis than
Manuwal and Manuwal (this volume, Table 1) because
we only included studies that specifically addressed
area or edge sensitivity. Life history characteristics
(nest type, migratory status, and foraging mode) of
each species were obtained from the studies included
in the summary and from the literature (Ehrlich et al.
1988). Species that showed evidence of area effects in
two or more studies are included in Table 3.
RESULTS
Thirty-one species were included in the anal-
ysis of bird abundance and patch size (Table 1).
Three species, the Golden-crowned Kinglet, Pa-
cific-slope Flycatcher, and Wilson's Warbler,
were detected in all of the patches. The abun-
dances of six species, the Pileated Woodpecker,
Pacific-slope Flycatcher, Brown Creeper, Stell-
er's Jay, Winter Wren, and Varied Thrush, were
positively correlated with log forest patch size
(Table 2, Fig. 2). These species spanned the
whole range of frequency values, from species
that were detected in all of the patches (Pacific-
slope Flycatcher) to those that were detected in
a small proportion of the patches (Pileated
Woodpecker). American Robins, Orange-
crowned Warblers, Dark-eyed Juncos, and Song
Sparrows were negatively correlated with patch
size (Table 2, Fig. 2).
Varied Thrushes and Pileated Woodpeckers
showed a threshold response to patch area. Var-
ied Thrushes were detected in only 1 out of 17
patches below and 20 out of 21 patches above
16 ha. Pileated Woodpeckers were detected in 2
of 29 patches below and 6 of 9 patches above
48 ha. None of the other species showed evi-
dence of a threshold response (Fig. 2).
Twenty-three Swainson's Thrush and 48 Win-
ter Wren nests were monitored in the two years.
Nest success for both years combined was low
for Swainson's Thrushes (25%; DSR _+ sE =
0.940 _+ 0.016), whereas Winter Wrens had high
nest success (65%; 0.986 + 0.016). Daily sur-
vival rate of Swainson's Thrush nests close
(<100m) to forest edges was lower than interior
nests (0.92 -+ 0.023 vs. 0.974 _+ 0.018, respec-
tively; P = 0.065) but nest success of Winter
Wrens did not differ between edge and interior
locations (0.991 +_ 0.0053 vs. 0.977 _+ 0.009,
respectively; P = 0.17). None of the nests were
parasitized by Brown-headed Cowbirds (Mol-
othrus ater).
LITERATURE SURVEY
We found eight studies that had examined the
effects of forest fragmentation on diurnal land-
birds in Westside forests (Table 3). Because each
study used different methods to examine these
relationships and species composition varied
among sites, the results must be interpreted cau-
tiously. However, we felt this comparison was
96 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 1. B1RD SPEC1ES INCLUDED IN ANALYSES OF PATCH CHARACTERISTICS AND B1RD ABUNDANCE IN COASTAL
REDWOOD FORESTS
Proportion of patches
Species occupied (N - 38)
Golden-crowned Kinglet (Regulus satrapa)
Pacific-slope Flycatcher (Empidonax difficilis)
Wilson's Warbler ( Wilsonia pusilia )
Chestnut-backed Chickadee (Poecile rufescens)
Winter Wren (Troglodytes troglodytes)
Swainson's Thrush ( Catharus ustulatus)
Brown Creeper ( Certhia americana)
Steller's Jay (Cyanocitta stelleri)
American Robin (Turdus migratorius)
Hermit Warbler (Dendroica occidentalis)
Dark-eyed Junco (Junco hyemalis)
Song Sparrow (Melospiza melodia)
Orange-crowned Warbler (Vermivora celata)
Common Raven (Corvus corax)
Purple Finch ( Carpodacus purpureus)
Pine Siskin (Carduelis pinus)
Vaux's Swift (Chaetura vauxi)
Varied Thrush (Ixoreus naevius)
Hutton's Vireo (Vireo huttoni)
Band-tailed Pigeon (Columba fasciata)
Northern Flicker (Colapies auratus)
Red-breasted Nuthatch (Sitta canadensis)
Western Tanager (Piranga ludoviciana)
Cassin's Vireo (Vireo cassinii)
Hermit Thrush (Catharus guttatus)
Pileated Woodpecker (Dryocopus pileatus)
1.00
1.00
1.00
0.97
0.95
0.92
0.89
0.89
0.84
0.82
0.74
0.68
0.66
0.63
0.63
0.58
0.53
0.47
0.42
0.37
0.32
0.32
0.32
0.29
0.26
0.24
an important first step in identifying species that
consistently show evidence of sensitivity to frag-
mentation.
Out of seven studies that examined area sen-
sitivity, ten species were identified as being sen-
sitive to fragmentation in two or more and seven
in three or more studies (Table 3). There was no
tendency for species with particular nest types
or foraging modes to predominate, but the ma-
jority of the species were residents.
Eight of the ten species that were identified
as area sensitive also showed evidence of edge
sensitivity in one or more studies (Table 3).
Thus, there is high concordance between area
sensitive and edge sensitive species in these
studies. The association between edge sensitivity
and area sensitivity that we found, however,
must be viewed with caution. Only one of the
studies (Brand and George 2001) was specifi-
cally designed to examine response to forest
edge; the others were based on point counts,
which may be a poor indicator of edge effects
(Villard 1998).
DISCUSSION
Six of the 31 bird species we examined in the
forest patch size analysis showed a positive as-
sociation with forest patch area, suggesting that
a substantial portion of the avifauna is sensitive
to the effects of forest fragmentation in this re-
gion. Four species, American Robins, Orange-
crowned Warblers, Dark-eyed Juncos, and Song
Sparrows, were more abundant in small than in
large forest patches. This is consistent with the
habitat associations of these species. Song Spar-
rows and Orange-crowned Warblers are more
abundant in young second-growth than mature
redwood forests (Hazard and George 1999) and
therefore are likely to be associated with the
edges of mature stands. American Robins and
Dark-eyed Juncos are generally associated with
forest openings (Ehrlich et al. 1988) and there-
fore it is not surprising that they are more abun-
dant in smaller patches. Because of the extensive
loss and fragmentation of mature and old-growth
forest in this region, we will focus our discus-
sion on those species that may be negatively af-
fected by loss and fragmentation of mature and
old-growth forests.
Other studies in Westside forests have failed
to detect strong evidence for edge or area sen-
sitivity among diurnal landbirds (Rosenberg and
Raphael 1986, Lehmkuhl et al. 1991, McGarigal
and McComb 1995, Schieck et al. 1995). The
lack of evidence in other studies may have been
due to the landscapes studied and the approaches
FRAGMENTATION EFFECTS IN REDWOOD FORESTS--George and Brand 97
TABLE 2. POISSON REGRESSION RELATIONSHIPS BETWEEN BIRD RELATIVE ABUNDANCE AND PATCH AREA IN 38
REDWOOD FOREST PATCHES SURVEYED IN NORTHERN CALIFORNIA IN 1994
Species response to fragmentation Slope -+ SE P
Negative
Pileated Woodpecker 0.62 -+ 0.25 0.015
Pacific-slope Flycatcher 0.08 -+ 0.04 0.037
Steller's Jay 0.17 -+ 0.07 0.029
Winter Wren 0.30 -+ 0.05 <0.001
Brown Creeper 1.67 -+ 0.09 0.055
Varied Thrush 0.71 -+ 0.06 <0.001
Positive
American Robin -0.44 -+ 0.11 <0.001
Orange-crowned Warbler -0.76 -+ 0.26 0.004
Dark-eyed Junco -0.52 -+ 0.24 0.029
Song Sparrow -0.55 -+ 0.27 0.043
Notes: Species that were positively related to area were classified as showing a negative response to fragmentation. Those showing the opposite trend
were classified as being positively associated with fragmentation. Only thoc species that occurred in al least 20% of the patches were included in
the analysis.
that were used. Lehmkuhl et al. (1991) and Ro-
senberg and Raphael (1986) studied landscapes
that were far less fragmented than the redwood
forests we examined. The smallest stand exam-
ined by Lehmkuhl et al. (1991) was 51 ha, and
most of the area around the stands (2,025 ha)
consisted of less than 50% clearcut. Few (4/46)
of the stands that Rosenberg and Raphael (1986)
studied were true islands (isolated from other
mature stands by clearcuts or hardwood forest),
and the amount of clearcut forest in the sur-
rounding 1000 ha block varied from 0 to 44%.
Thus the lack of evidence for sensitivity to frag-
mentation in these studies may be because the
landscapes were not sufficiently fragmented to
affect the bird species they examined. Mc-
Garigal and McComb (1995) specifically ex-
amined landscapes (250-300 ha) encompassing
a wide range of landscape structure based on the
proportion of late-seral forest and the spatial
configuration of the forest. However, they did
not use a patch-centered approach, but rather ex-
amined the relationship between landscape char-
acteristics and average bird abundance in all ser-
al stages within those landscapes. Thus, the
scale of their analysis was much larger than our
study. Schiek et al. (1995) used a similar ap-
proach to ours but their sample of patches was
small (21), and therefore their ability to detect
eftcts of fragmentation may have been limited.
We found no association between sensitivity
to fragmentation and life history characteristics.
However, most of the species were residents,
which contrasts sharply with similar summaries
of birds in the midwestern and eastern United
States where species that have been identified as
sensitive to fragmentation are more often long-
distance migrants (Robbins et al. 1989b, Free-
mark et al. 1995). Thus, there does not appear
to be any suite of life history traits that makes
a species more likely to be negatively affected
by fragmentation in these forests. This suggests
that attempts to classify sensitivity to fragmen-
tation based on life history traits are likely to be
problematical (Hansen and Urban 1992, Hansen
et al. 1993).
Two species, Pileated Woodpeckers and Stell-
er's Jays, showed evidence of area sensitivity
but not edge sensitivity. Pileated Woodpeckers
have large territories (>300 ha) in western co-
niferous forests (Bull and Holthausen 1993), and
therefore small isolated forest patches may be
less suitable for nesting and foraging. Hejl
(1992) also found that Pileated Woodpeckers
showed a threshold response to forest patch area
in the northern Rockies and suggested that large
stands or aggregates of small stands of late-seral
forests are necessary to maintain suitable habitat
for this species. Brand and George (2001) found
that Steller's Jay abundance declined with dis-
tance from edge in redwood forests, which is
inconsistent with their area sensitivity. Rosen-
berg and Raphael (1986) also found that Steller's
Jays were more abundant along edges, and that
they were weakly negatively associated with an
index of insularity. Thus, the evidence for area
sensitivity in Steller's Jays is weak in both stud-
ies (Rosenberg and Raphael 1986; this study),
and therefore their designation as area sensitive
may be a statistical artifact.
Eight of ten species that showed sensitivity to
fragmentation also showed evidence of edge
sensitivity. This suggests that area sensitivity
may be related to edge avoidance in these spe-
cies. Although edge sensitivity is often assumed
to be associated with area sensitivity (Whitcomb
et al. 1981, Askins et al. 1990, Freemark and
Collins 1992), Villard (1998) found a poor cor-
98 STUDIES IN AVIAN BIOLOGY NO. 25
14
12
: 10
o
u 8
6
6 4
z
2
0
0.1
American Robin
Orange-crowned Warbler
9
ß 6
eeß ß ee
3
2
1 10 100 1000 10000 0.1 1 10 100 1000 10000
16
14
: 12
o
lO
8
Q 6
6 4
z
2
0
0.1
Dark-eyed Junco
ß
18
16
14
12
10
8
Song Sparrow
ß
ß ß
ß ß ß
ß ß ß
4 ß ß
2
0
1 10 100 1000 10000 0.1 1 10 100 1000 10000
Pileated Woodpecker Pacific-slope Flycatcher
3O
ß
3.5
3 25 ß eee ee ß
õ 2.5 20
..
2 ß 15 ß ß ß ß ß
1.5
6 1 # ee ß 10 ß
z 0.5 #--e 5 ß
0
0.1 1 10 100 1000 10000 0.1 1 10 100 1000 10000
FIGURE 2. Relationship between relative density and patch area for bird species in redwood (Sequoia sem-
pervirens) forest patches in northern California. Species that show a positive COlTelation between patch area and
relative abundance are considered area sensitive. Fitted Kine is best fit Poisson regression with log link function.
relation between edge- and area-sensitive spe-
cies in studies conducted in the eastern United
States.
There are many factors that change between
forest edges and interior locations that may in-
fluence bird abundance, such as differences in
predation (Paton 1994), microclimate (Chen et
al. 1993), vegetation structure (Ranney et al.
1981), and insect composition (Shure and Phil-
lips 1991). These factors may act singly or in
combination to make forest edges more or less
suitable to particular species. For instance, mois-
ture gradients may influence the abundance of
ground-dwelling arthropods, which in turn could
affect the distribution of ground foraging bird
species, as has been suggested for Ovenbirds
(Seiurus aurocapillus; Gibbs and Faaborg 1990).
Reduced moisture along forest edges may
play an important role in the edge avoidance for
several of the species. Winter Wrens breed in
moist coniferous forests and nest in dense brush,
especially along stream banks (Ehrlich et al.
1988). Barrows (1986) found that Winter Wrens
in California have broad habitat preferences in
fall and winter, but that habitat selection shifts
in the breeding season almost exclusively to old-
growth forest characterized by a dense, moist
understory. Likewise, McGarigal and McComb
(1995) found that Winter Wrens are associated
with riparian systems in Oregon. The Varied
Thrush breeds in moist coniferous forest
(George 2000) and song post locations are as-
sociated with large diameter trees, on steep
slopes, surrounded by a high density of trees
14
12
lO
o
, 8
c,, 6
4
2
0
0.1
FRAGMENTATION EFFECTS IN REDWOOD FORESTS--George and Brand 99
Steller's Jay Brown Creeper
1 10 100 1000 10000
10
8
7
6
5
4
3
2
1
0
0.1
1 10 100 1000 10000
30
.o 20
15
ß 10
o
z
5
0
0.1
FIGURE 2.
Winter Wren
1 10 100 1000 10000
Patch Area (ha)
Continued.
Varied Thrush
35
3O ß
25 ß ß
20 ß ß ß Jß
15
lO ß
o.1 1 lO lOO looo 10000
Patch Area (ha)
near streams (Beck and George 2000). Thus,
male thrushes prefer moist, shady locations for
song posts. The Pacific-slope Flycatcher breeds
in forests, especially near water (Ehrlich et al.
1988). Edges receive higher levels of incident
radiation (Chen et al. 1993), and thus the micro-
climate near edges may be unsuitable for these
species. Microclimate changes, in turn, could af-
fect vegetation composition and structure as well
as prey availability near edges.
Another factor that may cause bird species to
avoid edges is predation (Brittingham and Tem-
ple 1983). The mechanism is less clear in this
case but it could either be a direct response to
the presence of potential predators along edges
or occur indirectly as unsuccessful nesters move
TABLE 3. BIRD SPECIES IDENTIFIED IN Two OR MORE STUDIES AS SHOWING EVIDENCE OF SENSITIVITY TO FOREST
FRAGMENTATION IN WET CONIFEROUS FORESTS OF THE PACIFIC NORTHWEST
Nest Migratory Foraging Area Edge
Species type a status b mode c sensitive d sensitive d
Pileated Woodpecker Cavity R Drill 1, 3, 7
Pacific-slope Flycatcher Cup L Flycatch 6, 7 1, 8
Steller's Jay Cup R Omnivore 1, 7
Chestnut-backed Chickadee Cavity R Foliage 1, 3, 5, 6 1, 6
Red-breasted Nuthatch Cavity R Bark 3, 5, 6 1, 8
Brown Creeper Crevice R Bark 3, 4, 7 1, 8
Winter Wren Crevice R Ground 1, 2, 3, 4, 6, 7 1, 2, 8
Golden-crowned Kinglet Cup R Foliage 4, 6, 7 1
Varied Thrush Cup S Ground 3, 5, 6 8
Hermit/Townsend's Warbler Cup L/S Foliage 1, 6 1
a Cavity-nest in tree cavities; Crevice-nest in niches and behind bark; Cup-open cup nesters.
b L-long-distance migrant; R-resident; S-short distance migrant.
c Bark-bark gleaner; Drill-excavates insects from dead wood; Flycatch-sallies for insects from a perch; Foliage-gleans insects from foliage; Ground-
gleans insects from ground; Omnivore-leds on a variety of food types.
d Studies included: l-Rosenberg and Raphael (1986); 2-Lehmkuhl et al. (1991); 3-McGarigal and McComb (1995); 4-Hejl and Paige (1994); 5-
Schieck et al. (1995); 6-Manuwal and Manuwal (this volume, Table 6); 7-this study; 8-Brand and George (2001).
100 STUDIES IN AVIAN BIOLOGY NO. 25
7
6
asym
Relative 4
Density
3
2
1
Varied Thrush ] ø
510 160 1}0 260 2}0 360 3}0 460
Distance from Edge (meters)
FIGURE 3. Relative density with respect to distance from the forest edge and estimated edge width for the
Varied Thrush. The points represent the band-specific relative density. The smooth curve represents the relative
density based on an exponential regression model with one asymptote. The dash-dot line illustrates the edge
width, defined as the distance from edge at which 90% of the asymptotic interior relative density has been
achieved.
to new locations (Villard 1998). Brand and
George (2000) found that predation on artificial
nests that mimicked Varied Thrush and Winter
Wren nests declined with distance from edge in
redwood forest patches and that Steller's Jays
were observed preying on the nests on several
occasions. These results are consistent with the
hypothesis that Winter Wrens and Varied
Thrushes avoid forest edges because of higher
nest predation. Steller's Jays are also more com-
mon on forest edges than forest interior loca-
tions (Brand and George 2001) and thus their
presence could provide a proximate cue to nest-
ing birds.
Other studies of artificial and natural nests
have shown similar patterns with respect to dis-
tance from forest edge but there are many ex-
ceptions as well (Brand and George 2000, Sisk
and Battin this volume). In addition, some stud-
ies suggest that predation rates on artificial nests
may not reflect predation on real nests (Nour et
al. 1993, Haskell 1995a, Willebrand and Marc-
strom 1988, Wilson et al. 1998, Ortega et al.
1998, King et al. 1999). We found no difference
in nesting success between edge (< 100 m from
forest edge) and interior (>100 m) nests for
Winter Wrens, but nesting success of Swainson's
Thrushes was lower on edges. Thus the pattern
of decreasing nesting success with proximity to
forest edge appears to be species-specific and
more studies are needed to document the gen-
erality of this pattern.
Swainson's Thrush populations may be partic-
ularly vulnerable to increased predation along
edges because thrushes are more abundant along
edges in redwood forest patches (Brand and
George 2001). Thus, thrushes may be experi-
encing an ecological trap (Gates and Gysel
1978) in this region, which could have severe
effects on recruitment and population growth
(Donovan and Lamberson 2001). Swainson's
Thrush populations may be suffering poor re-
cruitment in other parts of their range. Bednarz
et al. (1998) found that Swainson's Thrushes are
experiencing low nesting success in central Ida-
ho, which they attributed to high levels of forest
fragmentation in the region. Swainson's Thrush-
es have also been included in a draft list of spe-
cies of special concern in California because of
declines and a shrinkage of their breeding range
in the Sierra Nevada mountains (T. Gardali, pers.
comm.).
Regardless of the mechanism, edge avoidance
has important implications for forest manage-
ment. Information on the distance over which
edge effects occur could provide important man-
agement guidelines for minimum widths of for-
est stands. Brand and George (2001) found that
the distance to 90% of asymptotic interior rela-
tive density varied from 85 m for the Brown
Creeper to 140 m for the Varied Thrush (Fig. 3).
The average distance to 90% asymptotic density
of the four forest interior species is approxi-
mately 115 m. The distance of 115 m from the
forest edge also corresponds with the distance at
which the probability of predation on artificial
FRAGMENTATION EFFECTS IN REDWOOD FORESTS--George and Brand 101
nests declines by half (Brand and George 2001).
The edge widths estimated in Brand and George
(2001) can be used to predict the patch sizes that
may be suitable for particular forest interior spe-
cies. For example, assuming that the average ter-
ritory size for Varied Thrushes is 4 ha (George
2000), a circular patch of 19.6 ha would provide
a 4 ha core with a 140 m buffer. Breeding Varied
Thrushes were found to require a minimum
patch size of approximately 16 hectares in coast
redwood forests (Hurt 1996), close to the pre-
dicted size.
Another pattern that has been observed in
studies in the eastern U.S. (Wilcove 1985) and
Europe (Andrdn et al. 1985, Angelstam 1986,
Andrdn and Angelstam 1988, Andrdn 1992), is
an increase in nest predation in forest fragments
embedded within urban or agricultural land-
scapes as compared to regenerating forest or
other more natural habitats. This may be due to
an increase in generalist predators in landscapes
that are dominated by agricultural or urban areas
(Thompson et al. this volume). In redwood forest
fragments, however, Brand and George (2000)
found that rates of predation on artificial nests
adjacent to rural (grassland) edge were signifi-
cantly higher than nests located adjacent to sub-
urbs, rivers, young forests, or roads. Thus, our
results suggest that landscape context has a very
different eflbct on rates of nest predation in the
redwood region than in the eastern U.S. and Eu-
rope. Our results are consistent with those of
Tewksbury et al. (1998) who found that rates of
nest predation in riparian forests in Montana
were higher in sites adjacent to undisturbed co-
nifer forests than those adjacent to agricultural
areas. Thus landscape context may not exert a
predictable influence on rates of nest predation
in western forests as it does in the eastern U.S.
and Europe, perhaps due to the diversity of hab-
itats and associated nest predators in the West.
It is also possible that the various landscapes
examined by Brand and George (2000) and
Tewksbury et al. (1998) were not sufficiently
different at the regional level to influence the
predator community (Thompson et al. this vol-
ume).
Predation on artificial nests appears to be sub-
stantially lower in redwood forests than other
forests. Approximately 69% of the artificial
ground nests and 55% of the arboreal nests were
intact after 14 days, which is substantially higher
than has been found for most other studies con-
ducted in fragmented forests of the eastern U.S.
(Wilcove 1985, Yahner and Cypher 1987, Rud-
nicky and Hunter 1993, Whelan et al. 1994, Fen-
ske-Crawford and Niemi 1997, Yahner and Ma-
han 1997). This difference may reflect lower
overall avian abundance as well as lower pred-
ator activity in mature and old-growth redwood
forests than in eastern deciduous forests.
Each of the species that showed evidence of
area sensitivity in our survey also has been iden-
tified as an old-growth associate in one or more
regions of the Pacific Northwest (Manuwal and
Manuwal this volume, Table 2). This suggests
that there may be an association between area
sensitivity and dependence on old-growth forest
habitat among the birds in this region. If this is
the case, loss and fragmentation of old-growth
forests may have a more severe impact on these
species than predictions based on the area of
old-growth forest alone.
EAST VS. WEST
The proportion of species showing evidence
of sensitivity to habitat fragmentation in red-
wood forests (6/31 or 19%) is lower than the
proportion that has been reported for studies in
the eastern U.S. For example, Freemark and
Collins (1992) reported that 34/70 or 49% of the
species they examined showed evidence of area
sensitivity, which is significantly higher than the
proportion we observed (X 2 = 7.67, df = 1, P =
0.006). The proportions may change depending
on what bird orders are included and the studies
considered, but the pattern of a higher propor-
tion of area sensitive species in forests of the
eastern and midwestern U.S. relative to redwood
forests is unlikely to change. In addition, given
the overlap in species identified as area sensitive
in the studies we examined, it is likely that this
pattern holds for all Westside forests. We also
found few long-distance migrants among the
species that are area sensitive, which is very dif-
ferent from the eastern and midwestern U.S.
where long-distance migrants predominate.
Our studies also suggest that the ecological
processes that are responsible for area sensitivity
among redwood forest birds may differ from
those in the eastern U.S. Thompson et al. (this
volume) have proposed a "top-down" hierarchi-
cal model where higher agricultural and human
habitation at the regional scale results in in-
creased predator and parasite numbers which in
turn reduces the nesting success of birds in these
landscapes. Contrary to the predictions of this
model, we found that predation on artificial nests
was significantly higher along natural grassland
edges than suburban edges or roads. In addition,
although predation on artificial nests declined
with distance from forest edge, this pattern dif-
fered among species when we examined natural
nests. Parasitism also was not a factor as none
of the nests we monitored were parasitized by
Brown-headed Cowbirds. Our studies suggest
that area sensitivity in some species may be a
result of edge avoidance and subsequent decline
102 STUDIES IN AVIAN BIOLOGY NO. 25
1800
1600
1400
1200
1000
800
600
400
200
0
0-10
10-20 20-30 3040 40-50 50-60 60-70 70-60 80-90 90-100 >100
Area (ha)
FIGURE 4. Size distribution of mature and old-growth redwood (Sequoia sempervirens) forest patches north
of Point Reyes National Seashore. Based on Landsat satellite images (Fox 1997).
in small forest patches. This suggests a "bottom-
up" mechanism where behavioral responses to
edge result in changes in abundance in different
sized patches.
MANAGEMENT IMPLICATIONS
Several bird species that breed in coast red-
wood forests are negatively affected by forest
fragmentation. This means that the regional
abundance of these species will be affected not
only by the amount of mature and old-growth
forest but also its distribution across the land-
scape. Most redwood forests are privately
owned and are intensively managed for timber
production, and it is unlikely that large amounts
of land will be added to parks and reserves
(Thornburgh et al. 2000). Thus, the abundance
of these species in the region will be greatly in-
fluenced by how forest practices affect the dis-
tribution of mature forests across the landscape.
Presently, 79% of the mature and old-growth
redwood forest patches north of Point Reyes Na-
tional Seashore are less than 10 ha (Fig. 4). This
is below the threshold for breeding occupancy
by Varied Thrushes, and many of these patches
may be poor or unsuitable habitat for the other
species that are sensitive to fragmentation.
Changes in forest practice rules that result in
larger patches of mature forest on the landscape
would greatly benefit these species and should
be encouraged.
ACKNOWLEDGMENTS
Special thanks go to M. Hurt, C. Campbell, K. Mel-
ody, M. Wuestehube, J. Powell, and D. Kwasny who
helped collect data. J. Kranz kindly provided data on
nesting success of Swainson's Thrushes and Winter
Wrens. S. Elliot helped with the preparation of the
manuscript. Public land managers of Prairie Creek
Redwoods State Park, Redwood National Park, Hum-
boldt Redwoods State Park, and the Arcata Commu-
nity Forest, as well as private landowners, were par-
ticularly helpful in granting permission to conduct this
research. This study was funded by the Humboldt Area
Foundation. Support for A. Brand during preparation
of this paper was provided by SERDP project CS-
1100.
Studies in Avian Biology No. 25:103-112, 2002.
EFFECTS OF HABITAT FRAGMENTATION ON BIRDS IN THE
COASTAL CONIFEROUS FORESTS OF THE PACIFIC NORTHWEST
DAVID A. MANUWAL AND NAOMI J. MANUWAL
Abstract. Few studies have been done in the Pacific Northwest on the effects of habitat fragmentation
on birds. Comparisons among studies is difficult because of different study designs and possible
regional variation in bird response. Timber harvesting and human settlements have greatly fragmented
the once vast amounts of old-growth forests. Forest patches of the Pacific Northwest are typically
surrounded by forests of different ages rather than agricultural lands, as is found in much of eastern
North America. In Washington, one three-year study showed that overall bird species richness and
abundance varied little in a managed coniferous forest despite differing degrees of fragmentation.
Some individual species, however, increased or decreased with the amount of clearcut area and other
landscape variables. Species associated with open habitats or edges increased, while those associated
with forests having a well-developed canopy decreased. There is substantial variation in avian response
to landscape variables that characterize watersheds. At the stand level, canopy dwellers and cavity
nesting species show the most negative response to increasing levels of canopy reduction, whereas
species associated with the ground or shrub layer are least affected. Cowbird parasitism is negligible
in the mountains of the Pacific Northwest, but apparently is more widespread in the large valleys such
as the Puget Sound lowlands and Oregon's Willamette Valley where more farmland and urban, non-
forest environments exist. More studies are needed on fragmentation effects on birds and cowbird
parasitism in the region.
Key Words: birds; habitat fragmentation; Pacific Northwest.
Natural forces such as fire, floods, and volcanic
eruptions have always created natural heteroge-
neity, but humans have accelerated fragmenta-
tion and caused reductions in suitable habitat in
some biomes. In the early days of wildlife man-
agement, managers were encouraged to create
fragmentation and edges since game species
thrived in this environment (Leopold 1933, Al-
len 1962). With more knowledge of the biology
of non-game species, we now know that there
are edge-sensitive species that often decline in
highly fragmented landscapes (Whitcomb et al.
1981, Ambuel and Temple 1983, Wilcove and
Whitcomb 1983). The increased concern over
the fate of neotropical migrant passerines has re-
sulted in numerous studies in eastern North
America (e.g., Howe 1984, Temple and Cary
1988, Robbins et al. 1989a, Terborgh 1989, Wil-
cove and Robinson 1990, Freemark and Collins
1992, Robinson 1992, Faaborg et al. 1995, King
et al. 1998, Friesen et al. 1999, Rosenberg et al.
1999). Thus, most of the published information
on this topic for the United States derives from
research done east of the Rocky Mountains.
Based on the many studies of birds in the
eastern portions of North America, the principal
effects of forest fragmentation on birds are: (1)
reduction in patch size and change of patch
shape appear to negatively affect area-sensitive
species, (2) species especially adapted to living
in edge habitats increase, and (3) depending on
landscape context, the increase in the amount of
edge results in elevated predation rates and in-
creased brood parasitism by the Brown-headed
Cowbird (Molothrus ater). Few studies have
been conducted on the effects of forest fragmen-
tation on birds in the Pacific states. Until re-
cently the emphasis has been on relating bird
populations to forest age and structural charac-
teristics (e.g., Manuwal and Huff 1987, Carey et
al. 1991, Gilbert and Allwine 1991, Hansen et
al. 1991, Manuwal 1991, Ralph et al. 1991; Han-
sen et al. 1995a,b). Our approach in this paper
is to evaluate the effects of forest fragmentation
on birds by reviewing published as well as un-
published studies of birds in the coniferous for-
ests of western Washington, western Oregon,
and northwestern California, and to present new
information from three studies in Washington
and Oregon.
RESULTS
CHARACTERISTICS OF FOREST FRAGMENTATION IN
THE PACIFIC NORTHWEST
Until Euro-American settlement of the area
about 150 years ago, forests in the Pacific North-
west were heterogeneous due to natural events
such as wildfires. Approximately 50-60% of the
forest land base was old-growth forest at the
time of settlement (Franklin and Spies 1984,
Booth 1991). Due to timber harvesting and other
land use activities, only about 20% of the pre-
settlement old-growth Douglas-fir (Pseudotsuga
menaiesii) forests remain (FEMAT 1993). Due
to different management goals, the remaining
forest is fragmented in a variety of ways (Figs.
1 and 2).
The forests of this region are under federal,
103
104 STUDIES IN AVIAN BIOLOGY NO. 25
FIGURE 1. Typical forest fragmentation in the Oregon and Washington Cascades, Willamette National Forest,
Oregon. Photo courtesy of U.S. Forest Service. Photo taken on 12 July 1987.
state, or private management. Private manage-
ment, which includes forests managed by timber
companies, forests owned by private ownership,
and forests on Indian lands, traditionally have
been harvested for profit as the major objective.
This has resulted in large clearcuts, some over
1,000 ha. These large clearcuts are in various
stages of regeneration, and some have been con-
vcrted into plantations, which typically have a
rotation time of 40-60 years (Garmcn ct al. in
press). This does not allow for development of
structure associated with mature or old-growth
forests (>200 years; FEMAT 1993). These lands
are regulated by state laws that mandate a ripar-
ian zone buffer, but this is generally narrow and
susceptible to edge effects such as windfall and
increased insect infestation due to stress on the
trees.
The federal lands are managed by agencies
with different mandates. The lands administered
by the National Park Service, and those desig-
nated as wilderness (which in this region are
managed by the Forest Service) have a policy
of no forest harvesting. Thus, they serve as a
refuge for large (>1,000 ha) patches of old-
growth forest. These protected forests are often
at high elevation, or are bordered by forests that
have undergone extensive cutting. The majority
of the lands managed by the Forest Service have
been harvested by cutting of small patches of
FRAGMENTATION AND BIRDS IN COASTAL FORESTS--Manuwal and Manuwal 105
FIGURE 2. Digitized satellite image of western Washington in the Mount Rainier National Park area. Arrow
denotes park boundary. Courtesy of C. Grue and K. Dvornich, Washington Gap Analysis.
forest within the old-growth matrix, which has
resulted in a checkerboard effect (Franklin and
Forman 1987). With time, further cuts between
these areas have resulted in different-aged seral
forests within the old-growth matrix, causing a
loss of large (>1,000 ha) continuous old-growth
areas. This technique also results in more edge
area than the harvesting practices of the private
sector (Spies et al. 1994). The Bureau of Land
Management harvesting policy results in mid-
sized patches.
The study conducted by Chen et al. (1992)
provides insights into the effect of clearcuts on
adjacent old-growth forests. They report that
these eflcts include: (1) reduced canopy cover,
(2) increased growth rates of Douglas-fir and
western hemlock (Tsuga heterophylla), (3) ele-
vated rates of tree mortality, and (4) more Doug-
las-fir and western hemlock seedlings but fewer
of Pacific silver fir (Abies amabilis; Chen et al.
1992). The eftcts of clear-cutting on vegetation
characteristics of old-growth Douglas-fir Ibrests
ranged from 16 to 137 m for variables related to
distance from the edge. Thus, some forest patch-
es, especially those less than 10 ha, may be too
small to preserve an interior forest environment
(Chen 1991 ).
In Washington, approximately half of the
9,971,625 ha classed as forest lands are admin-
istered by federal agencies (McGinnis et al.
1997). Of this, about 11% is wilderness. In
Oregon, Spies et al. (1994) clarified the diftring
rates of harvest in private and public ownership
on a 2,589-km 2 study area. Between 1972 and
1988 the closed forest canopy declined from
71% to 58%. In those areas under private own-
ership, the decrease was from 50% to 28%, for
a net loss of 45%. The non-wilderness lands un-
FRAGMENTATION AND BIRDS IN COASTAL FORESTS Manuwal and Manuwal 107
TABLE 2. FRAGSTATS INDICES USED IN LANDSCAPE ANALYSIS OF BIRD SPECIES ABUNDANCE AND COMMUNITY
CHARACTERISTICS
Index name (units) Description a
CCAREA (ha)
CCED (m/ha)
MAT_AREA (ha)
PATCHES
ED (m/ha)
MNN (m)
SHDI
IJI (percent)
CONTAC (percent)
Total area of clearcuts (3-8 yrs old)
Total amount of clearcut edge
Total area of mature forest (50-80 yrs old)
Number of patches
Edge density
Mean nearest neighbor index
Shannon's Diversity Index
Interspersion and juxtaposition index
Contagion index
a See McGarigal and Marks (1995) for a complete description and definition of each index.
dividual species abundance and six of the nine
FRAGSTAT indices. Nine bird species had a
positive and eight species had a negative rela-
tionship with total clearcut area (CCAREA; Ta-
ble 3). Virtually all species with a positive re-
sponse (Table 3) are known to be associated
with open, shrubby habitats, so even at the land-
scape level, these species tend to be most com-
mon in a landscape with a large amount of land
in clearcuts. All nine bird species typically for-
age or nest either on the ground or in shrubs and
small trees. These species are known as pioneer
species and typically are the first ones to colo-
nize recent clearcuts and fire sites. On the other
hand, species having negative responses, such as
the Winter Wren (Troglodytes troglodytes),
Golden-crowned Kinglet (Regulus satrapa) and
Chestnut-backed Chickadee (Poecile rufescens),
are most often associated with forests with a
well-developed canopy, so their response is
somewhat predictable.
Eight species were positively correlated with
total area of mature forest (MAT. AREA; Table
3). The Pacific-slope Flycatcher (Empidonax dif-
ficilis), Wilson's Warbler (Wilsonia pusilia),
Hermit-Townsend's Warbler (either Dendroica
occidentalis or D. townsendi or their hybrids;
see Rohwer and Wood 1998), Red-breasted Nut-
hatch (Sitta canadensis), Hairy Woodpecker (Pi-
comes villosus), and Evening Grosbeak (Coc-
cothraustes vespertinus) all had significant pos-
itive responses to the amount of mature forest in
the 100 ha circle. The Varied Thrush (Ixoreus
naevius) and Winter Wren also had negative re-
sponses to clearcuts, so these two species may
be attracted at the landscape level to more ex-
tensive stands of mature forests away from
clearcuts.
The Orange-crowned Warbler (Vermivora ce-
lata) was the only species associated with the
amount of clearcut edge. Chestnut-backed
Chickadees had a negative association with edge
density, indicating that this bird may be an area-
sensitive species. The Swainson's Thrush (Ca-
tharus ustulatus) was negatively associated with
an increasing number of habitat patches. Alter-
natively, the Dark-eyed Junco (Junco hyemalis),
White-crowned Sparrow (Zonotrichia leuco-
phrys), and Spotted Towhee (Pipilo maculatus)
were positively associated with interspersion and
juxtaposition. This seems to suggest that these
species are attracted to habitat patchiness.
At the community level, no significant rela-
tionships were found between bird species rich-
ness and area of clearcuts or area of mature for-
ests in any of the three years of the study. Sim-
ilarly, no significant relationships were found
between the number of bird detections and area
of clearcuts or area of mature forests.
Oregon
McGarigal and McComb (1995) investigated
bird community response to landscape structure
in the central Oregon Coast Range. They sam-
pled 10 landscapes (250-300 ha) in three basins.
Each landscape was characterized by the amount
of late-seral forest condition and relative frag-
mentation. Among the many bird species de-
tected, 12 species were strongly associated with
late seral forest condition but were also found in
other forest conditions. Three species, the Olive-
sided Flycatcher (Contopus borealis), Red-tailed
Hawk (Buteo jamaicensis), and Western Wood-
Pewee (Contopus sordidulus) were associated
with habitats where there was a sharp edge be-
tween late-seral and early seral forests. Five spe-
cies were positively associated with patch size:
Gray Jay (Perisoreus canadensis), Brown
Creeper, Winter Wren, Varied Thrush, and
Chestnut-backed Chickadee. The following spe-
cies were more abundant in fragmented land-
scapes: Red-breasted Sapsucker (Sphyrapicus
ruber), Western Wood-Pewee, Olive-sided Fly-
catcher, and Red-tailed Hawk. The Winter Wren
showed the most aversion to fragmented land-
scapes. Meyer et al. (1998) and Franklin and
Gutierrez (this volume) examine the relationship
108 STUDIES IN AVIAN BIOLOGY NO. 25
++++++++ I I I I I +++
FRAGMENTATION AND BIRDS IN COASTAL FORESTS--Manuwal and Manuwal 109
between habitat fragmentation and Spotted Owls
(Strix occidentalis).
In general, McGarigal and McComb (1995)
found a large amount of variation in response to
a wide variety of landscape variables. Part of the
difficulty in assessing species responses to hab-
itat variables is the scale at which the compari-
sons was made. Bird abundance was generally
greater in more fragmented landscapes. As is
true for many other studies, uncommon species
or those with large territories such as the Pile-
ated Woodpecker (Dryocopus pileatus), are gen-
erally undersampled and their relationship with
landscape variables could not be determined.
California
Raphael (1984) and Rosenberg and Raphael
(1986) assessed the effects of forest fragmenta-
tion in Douglas-fir forests of northwestern Cal-
ifornia by examining point count survey data
relative to 10 fragmentation measures at the plot
(N = 136), stand (N = 46), and landscape lev-
els. In general, bird species richness increased
in fragmented stands. They also found that bird
species richness at the plot and stand levels in-
creased with proximity and extent of adjacent
clearcut. They found 20 species associated with
edges and 20 other species that avoided edges.
Among the common species, only the Olive-sid-
ed Flycatcher was detected more often on the
edge than in the forest interion Birds showing
the most negative responses to forest fragmen-
tation were the Spotted Owl and Pileated Wood-
pecker, whereas the Sharp-shinned Hawk (Ac-
cipiter striatus) and Blue Grouse (Dendragapus
obscurus) showed less population declines in
fragmented areas.
LOCAL AND STAND-LEVEL EFFECTS
Washington riparian zones
In an attempt to determine the response of
birds to harvest with two different riparian zone
buffer widths, eighteen riparian areas within co-
niferous forests in the western Washington Cas-
cades were studied in 1993, 1995, and 1996
(Pearson and Manuwal 2001). The clear-cuts
created adjacent to the sampled riparian zones
caused forest fragmentation and created large
amounts of edge along the streams. Ten point
count stations were visited where birds were
counted for 6 min to determine avian relative
abundance. Each study site was visited 5-6
times during the nesting season. All sites were
studied for one year before harvest and sampled
for two years after harvest to evaluate bird re-
sponse to the buffer widths.
Species richness was higher after harvest in
the uplands compared with unharvested con-
trols. Wider buffer widths had higher species
richness than did unharvested sites. Predictably,
species considered to be edge species, for ex-
ample Dark-eyed Junco, Song Sparrow (Melos-
piza melodia), and Warbling Vireo (Vireo gil-
vus), increased after harvest. Some species,
tably the Golden-crowned Kinglet, decreased
significantly after harvest.
Washington and Oregon green tree retention
An experimental on-going study initiated in
1992 in the Pacific Northwest, called Demon-
stration of Ecosystem Management Options
(DEMO), is designed to examine the effects of
stand-level green tree retention on ecological at-
tributes of the forest. This was a daunting task
because of the scale of the study and public con-
cern over continued cutting on National Forest
lands. Details of the study design are given by
Aubry et al. (1999). In general, it consists of a
randomized block design of six treatments rep-
resenting varying levels of green-tree retention.
Each treatment unit is 13 ha in size and leave-
trees (trees remaining after harvest) were either
clumped (aggregated) or dispersed through the
harvested area. Study sites were only in upland
areas.
There are four blocks in Oregon and four in
Washington. There is substantial variation in el-
evation between blocks (210-1,710 m), but usu-
ally only about 200-300 m variation within a
block (Aubry et al. 1999). Birds were surveyed
for two years before experimental retention har-
vests were made and only two blocks in Wash-
ington were surveyed after harvest since the oth-
er two blocks had not yet been harvested. An
overview of this project and preliminary results
of pre-treatment sampling is in Lehmkuhl et al.
(1999). We report here some preliminary and
geographically limited results of the responses
of the following groups of birds: cavity-nesters,
forest floor-dwellers, and canopy-dwellers (Ta-
ble 4). Birds were surveyed by both point counts
(4 points, 160 m apart, 6 visits) and territory-
mapping (11 species only).
Among the three groups of species, forest
floor-dwellers appeared to be less impacted by
green-tree removal than the other two groups.
Bird populations declined in virtually all con-
ditions after harvest, even the control (100% re-
tention) sites. The spring of 1998 was cold and
wet in the Washington Cascades and several spe-
cies of birds either failed in their first nesting
attempt or nested late in the season (D. Manu-
wal, pers. obs.; M. Leu, pers. obs.). This may
account for the lower than expected numbers of
birds in control sites. Forest floor birds appar-
ently recognize 75% retention sites as little dif-
ferent from untreated (100%) retention sites
since there was no change in populations (Table
110 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 4. PERCENT CHANGE IN NUMBER OF BIRO TERRITORIES TO GREEN-TREE RETENTION LEVELS AFFER HAR-
VEST IN WASHINGTON IN 1998
Cavity nesters a Canopy-dwellers a Forest floor-dwellers a
Level of retention Butte Paradise Hills Butte Paradise Hillq Butte Paradise Hills
100% Retention (--0%) b -67 47 -30 -48 -48 23
75% Aggregated (25%) -73 -73 -76 -73 +29 -29
40% Dispersed (-60%) -64 91 -66 -95 -26 47
40% Aggregated (-60%) -48 54 -79 -53 -24 61
15% Dispersed (-85%) 80 -82 -93 -89 48 - 18
15% Aggregated( 85%) -79 -85 -87 91 -51 -50
a Cavity-nesters included: Brown Creeper, Chestnut backed Chickadee and Red-breasted Nuthatch; canopy-dwellers included: Chestnut backed Chick-
adee, Hermit Warbler, and Pacific-slope Flycatcher; forest floor-dwellers were: Dark eyed Junco, Winter Wren, Varied Thrush.
Amount of canopy reduction.
4). It seems clear that both dispersed and aggre-
gated 15% retention offers little habitat for cav-
ity-nesters and canopy-dwellers. The declines in
number were close to the decline in green-tree
canopy levels. These results and interpretations
are preliminary and additional post-treatment
sampling may show more definitive trends in
bird community and individual species respons-
es.
The adjustment of bird territory placement
relative to retention level and dispersion is an
especially interesting aspect of the study. Two
examples of how birds adjusted their territories
are the Dark-eyed Junco and the Hermit Warbler.
The junco was a common bird on the study site,
having 3 whole territories and 5 partial territo-
ries on a single 40% aggregated retention treat-
ment site (Butte) before harvest. After harvest,
there were 3 whole territories and 3 partial ter-
ritories. Each junco territory contained portions
of the retention circles as well as cleared area.
This fits with the anticipated response of an edge
species. Before harvest, the Hermit Warbler was
the most abundant species on the study site;
there were 12 complete territories and 5 partial
territories on the site. After harvest all but 5 ter-
ritories disappeared and each of those were lo-
cated such that there was one territory per cir-
cular retention patch. Apparently, the patch con-
tained a sufficient amount of canopy and asso-
ciated insect prey to allow nesting to occur. We
have no data on breeding success but all five
males were paired. With additional post-harvest
sampling in both Oregon and Washington, stron-
ger conclusions can be drawn from this inves-
tigation on the response of birds to fragmenta-
tion at the stand level.
OTHER INDIVIDUAL SPECIES STUDIES
There are some studies of the effects of frag-
mentation on species of conservation concern in
the Pacific Northwest such as the Spotted Owl
(Meyer et al. 1998, Franklin and Gutierrez this
volume), which is strongly positively associated
with several landscape attributes of late succes-
sional forests. There are on-going studies of
fragmentation effects on the Marbled Murrelet
(Brachyramphus marmoratus; Raphael et al. this
volume). As with studies of eastern bird com-
munities, some species such as the Gray Jay,
Brown Creeper, Winter Wren, Varied Thrush,
and Chestnut-backed Chickadee tend to decrease
with fragmentation and are often associated with
late successional forests (Rosenberg and Rapha-
el 1986, Manuwal 1991).
A long-term study of Northern Goshawk (Ac-
cipiter gentilis) demography, breeding behavior,
and habitat selection for foraging and nesting on
Washington's Olympic Peninsula was initiated in
1995 by Dan Varland and John Marzluff. To-
gether with graduate students Sean Finn and
Tom Bloxton, they are investigating the effects
of the local- (forest stand) and landscape-level
structure, composition, and spatial arrangement
of forests on goshawks. The emphasis of the
study is to understand how goshawks respond to
habitat loss and fragmentation resulting from
timber harvest. The first three years of study
concentrated on surveying all known occupied
nest areas on the Olympic Peninsula (N = 30)
to determine if past habitat modification was
correlated with current occupancy. Occupied
stands differed from unoccupied ones primarily
in having greater canopy closure, although the
percentage of the surrounding landscape cur-
rently comprised of regenerating forest also was
negatively correlated with occupancy. There-
fore, fragmentation of the mature forest land-
scape may reduce occupancy of historical nest
sites. However, their current research on the for-
aging and ranging habits of goshawks in frag-
mented forests suggest that individual pairs are
extremely resilient to forest loss and fragmen-
tation. Goshawks forage primarily in mature for-
ests, but make use of regenerating forests and
riparian gaps. They are notably unaffected by
habitat loss and fragmentation that occurs while
they are occupying an area. The working hy-
FRAGMENTATION AND BIRDS IN COASTAL FORESTS--Manuwal and Manuwal 111
TABLE 5. ABUND^NCE OF BROWN-HEADED COWBIRDS IN LOWLAND HABITAT OF WESTERN WASHINGTON FROM
BREEDING BJRD SURVEYS (BBS)
Population
BBS route Name Years Mean/year trend a
Sea level
89907 Vashon Island 2
89905 Deception Pass 5
89072 Mukilteo 4
89034 Everett 15
Mean
Lowlands, Cascade Foothills
89111 Carnation 9
89066 Bayview 4
89133 Montesano 11
89078 Pe Ell 3
89059 Raymond 2
Mean
Cascades-Low Elevation
89904 Verlot 6
89902 Cascade River 9
89043 Packwood 19
Mean
13.0 ?
22.6 -
20.5 0
10.5
16.7
19.3
15.8 -
0.4 0
13.7 0
7.5 ?
11.3
0.8
1.2
3.0
1.7
a ? indicates insufficient data; 0 no trend, decreasing.
pothesis that links these apparently contradictory
observations is that specific pairs acclimate and
adjust to forest fragmentation in and around
their breeding territories, but when these accli-
mated pairs die, new pairs are less likely to se-
lect the formerly occupied habitat for breeding.
Lack of continued selection of fragmented hab-
itat by goshawks produces the negative corre-
lation between occupancy and fragmentation,
while acclimation to fragmentation allows cur-
rent territory owners to be unaffected by frag-
mentation.
BROWN-HEADED COWBIRD PARASITISM
The Brown-headed Cowbird is a relatively re-
cent immigrant to the coastal regions of the Pa-
cific States. It became established in portions of
this region only since the 1950s (Rothstein 1994,
Morrison and Caldwell this volume). In western
Washington it may not have become established
until a little later since Jewett et al. (1953:592)
reported that the cowbird was (referring to the
1940s and 1950s) a "rare migrant and casual
winter visitant in western Washington." Since
the 1950s, the cowbird has become established
as a breeding bird in western Washington but its
distribution is clearly restricted to the Puget
Trough lowlands. A review of 12 Breeding Bird
Survey (BBS) routes in the Puget Sound area
indicates that this species is relatively common
in the highly fragmented open habitats from sea
level up to the foothills of the Cascade Moun-
tains (Table 5). Cowbird abundance decreases
with elevation, or at least with a landscape in-
creasingly dominated by coniferous forests.
Point count bird surveys in coniferous forests
conducted from 1983 to 1998 in the Cascade
Mountains at elevations ranging from 300 to
1500 m show that the Brown-headed Cowbird
is virtually absent (7 detections out of a total
56,290 bird detections; Table 6) in this land-
scape even though it is fragmented (Figs. 1 and
2). The cowbirds we detected were in recent
clearcuts adjacent to Douglas-fir forests. Factors
preventing cowbird colonization of the frag-
mented coniferous forests in the Washington
Cascades are unknown, but it is apparent that
cowbird parasitism is not currently impacting
potential hosts in the fragmented landscape of
the Washington Cascades. Cowbirds are very
rare there now but they could become a problem
in the future. Cowbirds are relatively common
in the Puget Sound Lowlands so parasitism is
undoubtedly occurring there, but its extent has
not been investigated. The proximity of the pres-
ently occupied areas to mountain habitat makes
it possible that cowbirds may eventually occupy
some of the Cascade and Coast Range montane
forests. The effects of predation on songbird
communities of the Pacific Northwest is poorly
known. A current study by R. Sallabanks is ex-
ploring this aspect in managed forests of the
Washington Cascades.
CONCLUSIONS
Fragmentation in the mountains of the Pacific
Northwest consists of open areas created by
clearcut or seed-tree logging in a matrix of for-
112 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 6. NUMBERS OF BROWN-HEADED COWBIRDS DETECTED IN CONIFEROUS FORESTS OF THE CASCADE MOUN-
TAINS OF WASHINGTON AND OREGON
Data source a N Years Cowbirds detected Total bird detections
OGWHP 46 2 0 21,962
TFW-RMZ 18 3 0 6,032
TFW-Landscape 24 3 7 20,373
USFS-DEMO-WA 24 2 0 4,446
USFS-DEMO-OR 24 2 0 3,477
Total 7 56,290
aData from point counts within 50 m of points except TFW-RMZ (within 15 m of points). Abbreviations: OGWHP (Manuwal 1991): 12 points, 6
visits, 8 min count duration; 1984, 1985. TFW-RMZ (S. Pearson and D.A. Manuwal, unpubl. data): 10 points, 6 visits, 6 min count duration; 1993,
1995, 1996. TFW-Landscape (Aubry et al. 1997): 12 Points, 6 visits, 8 min count duration, 1993, 1994, 1995. USFS-DEMO-WA (D.A. Manuwal
unpubh data): 4 stations, 6 visits, 8 min count duration; 1995, 1996. USFS-DEMO-OR (D.A. Manuwal unpubl. data): 4 stations, 6 visits, 8 min count
duration; 1995, 1996.
ests of various ages. This pattern differs from
many areas of eastern North America where for-
ests are located near or adjacent to agricultural
lands or human settlements. In the Pacific North-
west, fragmentation appears to be most exten-
sive on private commercial timberlands com-
pared with national forests. The Puget Sound
Lowlands have some areas of agriculture, mixed
with patches of forests, but this region has not
been adequately studied.
The effects of forest fragmentation are not
well documented in the Pacific Northwest com-
pared with the many studies in eastern North
America [e.g., those cited in Hagan and John-
ston (1992) and Martin and Finch (1995)]. Nev-
ertheless, some patterns seem to be emerging
from recent studies. Species richness seems to
increase in highly fragmented landscapes, chief-
ly because of the colonization of edge species,
which often nest or forage in open, shrubby hab-
itats. However, interior forest birds may be de-
clining under these conditions. The identification
of specific landscape variables responsible for
this has been difficult to determine, perhaps be-
cause birds such as the Winter Wren and Hermit
Warbler, which have small territories, respond to
stand-level factors rather than large scale ones.
There are no long term studies in the Pacific
Northwest so we have no information on how
fragmentation affects bird abundance. Short-
term investigations indicate that some species
increase while others decrease with fragmenta-
tion, a pattern also observed in the eastern Unit-
ed States.
Brood parasitism and predation have been
shown to be a major concern in the fragmented
environments of eastern North America (e.g.,
Robinson et al. 1995b), but there is no evidence
that parasitism is an important factor in the
coastal mountains of the Pacific Northwest.
However, this could become a problem as more
forested land is cleared and converted to more
open habitat.
Coniferous forests in the Pacific Northwest
are naturally heterogeneous because of the ef-
fects of fire, wind-throw, floods, and volcanic
eruptions. Compared with habitat fragmentation
in much of eastern North America, fragmenta-
tion in the mountains of the Pacific Northwest
is fundamentally different in that forest patches
are not surrounded by agricultural land or areas
dominated by human development. Instead, for-
est patches are surrounded by other forest patch-
es of different ages. Late successional forest
patches remaining after timber harvesting have
become smaller in recent decades and are less
suitable for area-sensitive bird species than larg-
er patches. Cowbird brood parasitism is not
common in the mountains but does occur in low-
land habitats. It is clear that much more research
is needed in the Pacific Northwest to determine
relationships between birds and forest fragmen-
tation.
ACKNOWLEDGMENTS
We thank S. Garman, T Spies, and J. Franklin for
sharing their information on Pacific Northwest vege-
tation. C. Grue and K. Dvornich, Washington Coop-
erative Fish and Wildlife Research Unit, Washington
Gap Analysis, provided us with digital maps. S Reu-
tebush provided the aerial photograph of Willamette
National Forest. We are grateful to the Washington De-
partment of Natural Resources (Timber, Fish and Wild-
life Agreement) for funding the riparian management
zone and landscape studies in Washington, and the
U.S. Forest Service, Pacific Northwest Forest Experi-
ment Station, Portland, OR, for funding the DEMO
project. The efforts of many field ornithologists asso-
ciated with these projects are gratefully acknowledged.
Studies in Avian Biology No. 25:113-129, 2002.
BIRDS AND CHANGING LANDSCAPE PATTERNS IN CONIFER
FORESTS OF THE NORTH-CENTRAL ROCKY MOUNTAINS
SALLIE J. HEJL, DIANE EVANS MACK, JOCK S. YOUNG, JAMES C. BEDNARZ, AND
RICHARD L. HUTTO
Abstract. We describe historical and current landscape patterns for the north-central Rocky Moun-
tains, speculate on the expected consequences of human-induced changes in coniferous forest patterns
for birds, and examine the evidence related to the expected consequences. The Rocky Mountain region
has one of the most heterogeneous landscapes in North America, combining high complexity in abiotic
gradients with fire as a major disturbance factor. In recent decades fire suppression has limited this
disturbance, resulting in altered stand structures and relatively homogeneous expanses of mid-succes-
sional forest where there were once mosaics of different-aged post-fire stands. Elsewhere, historically
homogeneous landscapes that rarely burned have become more heterogeneous due to logging. Many
torest types are less common than they were historically due to current management. Land conversion
to agriculture and development has primarily occurred in low elevations. We speculate that the con-
sequences of these changes include: (1) bird species adapted to historically homogeneous forest land-
scapes would be negatively affected by landscape heterogeneity created by timber harvest openings;
(2) bird species specialized for forest types that were once prevalent but are now uncommon may be
negatively affected by decreasing patch size and increasing isolation; and (3) birds that breed in close
proximity to human-added landscape features may be negatively affected by brood parasites or nest
predators. Brown Creeper (Certhia americana) and Golden-crowned Kinglet (Regulus satrapa) had
the strongest trends of species sensitive to fragmentation indices. Pine Siskin (Carduelis pinus), Chip-
ping Sparrow (Spizella passerina) and Dark-eyed Junco (Junco hyemalis) were positively associated
with fragmentation across most studies. Nesting success varied among landscape configurations, and
some trends paralleled abundance patterns. Brown-headed Cowbird (Molothrus ater) parasitism rates
were extremely low (0-3%) where nest success has been studied in coniferous forests of the north-
central Rockies. Across extensive and intensive studies, distance to agricultural lands was the strongest
predictor of cowbird presence. Therefore, we found evidence for the ideas that birds adapted to
homogeneous forest landscapes have been negatively affected by heterogeneity caused by timber
harvesting, that patch size is important for some birds in one vanishing habitat (old-growth ponderosa
pine, Pinus ponderosa), and that cowbirds are more abundant in conifer forests near human-added
landscape features. The effects of changes in landscape patterns on birds in the north-central Rockies
seem to be less dramatic than in eastern and midwestern North America, and different landscape
measures are more relevant to western conifer forests. We need additional research on most aspects
of breeding, nonbreeding, and dispersal ecology in relation to landscape patterns and within-stand
changes. We offer our proposed consequences as hypotheses upon which to base future tests.
Key Words: birds; fire; fire regimes; fire suppression; forest fragmentation; north-central Rockies;
landscape; landscape patterns; wildfire.
Forest fragmentation has clearly afl,ected birds
in some landscape configurations in the East and
Midwest (Porneluzi et al. 1993, Donovan et al.
1995a, Robinson et al. 1995a). In landscapes
where forests are fragmented by agriculture and
urbanization, resulting in discrete measurable
patches, species richness has been shown to in-
crease with patch area and decrease as patches
become more isolated (Whitcomb et al. 1981,
Ambuel and Temple 1983, Freemark and Mer-
riam 1986, Blake and Karr 1987). The presence
or absence of a species across patches of differ-
ent sizes suggested minimum area requirements
(Temple 1986, Askins et al. 1987, Robbins et al.
1989a). Nesting success declined (Villard et al.
1993, Donovan et al. 1995b), and edge effects
(as indicated by nest predation and parasitism)
were particularly strong where the landscape
matrix had been highly modified (Robinson
1992). These studies identified long-distance mi-
grants as particularly sensitive to area efl,ects.
The effects of landscape changes on bird pop-
ulations in conifer forests in the West seem to
be less dramatic (Rosenberg and Raphael 1986,
McGarigal and McComb 1995). Historical and
current landscape patterns are quite difl,erent in
the West than in the East and the Midwest, es-
pecially in the mountainous and sparsely popu-
lated north-central Rocky Mountains. Conifer
forests dominate the mountain slopes of this re-
gion, and conversion of lands to agriculture and
urban development generally has been restricted
to valley bottoms. While the natural heteroge-
neity of these conifer forests was variable, fire
suppression and timber harvest have created
landscape patterns with different kinds and lev-
els of heterogeneity. Nonetheless, they remain
forested ecosystems that may not present barri-
113
114 STUDIES IN AVIAN BIOLOGY NO. 25
ers to many native species (Mcintyre and Barrett
1992). The response of avian species to this dy-
namic mosaic may be species-specific and pro-
cess-specific (Haila 1999). Edge effects may
also be substantially different in forest-dominat-
ed landscapes than in agricultural ones (Hanski
et al. 1996, Bayne and Hobson 1997).
Different measures of landscape patterns are
more relevant to landscapes in western conifer
forests than those used in the East and Midwest.
For example, size and isolation of an individual
forest patch is almost impossible to measure in
conifer forests of the north-central Rockies be-
cause the forest is the matrix rather than the
patch, with most stands connected in some way
to other conifer forests that may or may not be
similar in age, species composition, and struc-
ture. The exceptions include rarer forest types,
such as old-growth ponderosa pine (Pinus pon-
derosa) or patches of recent fire disturbance.
Measures of fragmentation in western conifer
forests are thus better achieved by characterizing
patterns within a defined landscape, based on
relative amounts of forest and amounts and
types of edges. More complex variables may be
necessary, such as measures of connectivity
(Taylor et al. 1993). When patch size is used,
patch boundaries often are created somewhat ar-
tificially when a user-defined landscape outline
is imposed onto the forest matrix for analysis.
Because of these constraints, studies in western
coniferous forests usually describe the structure
of the landscape mosaic in which the forest is
embedded (see Wiens 1989) and then relate that
structure to avian populations (Rosenberg and
Raphael 1986, van Dorp and Opdam 1987,
McGarigal and McComb 1995, Schieck et al.
1995).
We investigated whether bird populations are
related to landscape changes in north-central
Rocky Mountain conifer forests and whether
these relationships are similar to what has been
reported for other regions. We define the north-
central Rockies as that area from eastern Oregon
and Washington east through Idaho and western
Montana to Wyoming (Fig. 1). We include aspen
(Populus spp.) in our discussion of conifer for-
ests because it is an integral part of many conifer
landscapes. To look at the relationships between
birds and landscape patterns, we (1) describe
historical landscape patterns and the processes
responsible for them; (2) describe current land-
scape patterns and their causes; (3) discuss im-
plications and potential consequences of human-
induced changes between historical and current
patterns for coniferous forest birds; (4) examine
the current evidence surrounding the expected
consequences; and (5) compare our findings for
the north-central Rockies to other regions.
/
FIGURE 1. The north-central Rocky Mountain geo-
graphic area. Rocky Mountain forest type boundaries
from Bailey's (1995) ecoregions of the United States,
including portions of northern, middle, and southern
Rocky Mountain steppe provinces.
HISTORICAL LANDSCAPE PATTERNS
Natural landscape heterogeneity results from
the superposition of a disturbance regime onto
vegetation patterns created by abiotic gradients
(Turner and Romme 1994). Historically, the
north-central Rocky Mountain region had one of
the most heterogeneous landscapes of any area
in North America due to a dry climate and fre-
quent lightning-caused fires, and this disturbance
regime was superimposed on complex vegeta-
tion patterns resulting from moisture gradients
and finely dissected topography.
Characterizing natural or presettlement land-
scapes can be a very difficult task (Noss 1985,
Sprugel 1991). The evidence is scattered and
subject to many potential biases (Noss 1985). In
the recent bioregional assessment of the interior
Columbia River Basin, Hann et al. (1997) used
scattered evidence, expert opinion, and simula-
tion models to estimate broad-scale landscape
patterns across the region for the 1850-1900
time period. The mid-scale assessment associ-
ated with that project (Hessburg et al. 1999)
used historical aerial photographs to characterize
landscape conditions in sampled watersheds, but
historical photos could be found for only the
"recent historical" period of the 1930s to 1960s.
Even if accurate historical data could be re-
covered for one point in time, the dynamic na-
ture of the disturbance regimes diminishes the
usefulness of that information. Fire size and se-
verity depend on previous disturbance history
(e.g., fuel buildup) as well as cyclic weather pat-
terns (Bessie and Johnson 1995). There is grow-
ing evidence that fire disturbance was extremely
variable historically and probably not in equilib-
rium across the landscape (Sprugel 1991, Turner
and Romme 1994, Brown et al. 1999). In addi-
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTS--Heft et al. 115
tion, native Americans altered fire regimes for
hundreds of years before Euro-American settle-
ment (Barrett and Arno 1982). Therefore, any
characterizations of historical landscape patterns
must be considered generalizations and take into
account the highly variable nature of the land-
scape.
ABIOTIC FACTORS
The north-central Rockies are composed of
many mountain ranges of varying raggedness
and orientation. Moisture varies with elevation
and topography, and there is also a regional gra-
dient in rainfall due to continental climate pat-
terns (Habeck and Mutch 1973, Peet 1988).
Finely dissected topography interweaves land
units of very different slopes, soils, moisture re-
tention properties, and exposures, and these pat-
terns occur at several spatial scales. Local land-
scape vegetation patterns are strongly influenced
by these abiotic gradients.
Higher elevations have lower temperatures
and receive more precipitation. Annual precipi-
tation in the north-central Rockies ranges from
less than 380 mm in intermontane valleys to
more than 1500 mm at higher elevations (Ha-
beck and Mutch 1973). These local temperature
and moisture patterns create zones of forest hab-
itat types based on the physiological require-
ments and competitive abilities of the various
tree species (Daubenmire 1956). For example, in
much of the north-central Rockies, the driest and
lowest-elevation forests historically were domi-
nated by ponderosa pine, which remains an im-
portant early-seral species up into the mid-ele-
vation zone, where Douglas-fir (Pseudotsuga
menziesii) was typically the major tree species
in climax vegetation. The less drought-resistant
Engelmann spruce (Picea engelmanni) and sub-
alpine fir (Abies lasiocarpa) compete for climax
status only in the more moist, upper-elevation
zones. Each of these zones had different fire re-
gimes (Arno 1980). Fire in many of these re-
gimes maintained large areas dominated by
shade-intolerant (early-seral) tree species, in-
cluding ponderosa pine, lodgepole pine (Pinus
contorta), western larch (Larix occidentalis),
sometimes grand fir (Abies grandis) and Doug-
las-fir, and, historically, western white pine (Pi-
nus rnonticola).
Local topography and soils can drastically al-
ter available nutrients, solar radiation, tempera-
ture, and water retention (Peet 1988, Swanson
et al. 1988). South-facing slopes and ridge tops
are much warmer and drier and may support
vegetation typical of lower elevations, if soils
allow. Sheltered valley bottoms have lower solar
radiation and may collect water and cold-air
pockets that support vegetation more character-
istic of that nearly 500 m higher on open slopes
(Peet 1988). Naturally treeless areas occur wher-
ever slopes are too steep or rocky, or where
there is prolonged summer soil drought (Dau-
benmire 1968). Areas on the east side of the
Continental Divide especially have widespread
occurrence of forest-grassland-sagebrush mosa-
ics, probably regulated by the availability of
moisture (Patten 1963) and the frequency of fire
(Arno and Gruell 1983).
In contrast, moist Pacific air reaches a limited
area in southeastern British Columbia, north-
eastern Washington, northern Idaho, and north-
western Montana. The resulting luxuriant forests
in this region appear similar to forests in the
Cascade Mountains (Peet 1988), with tree spe-
cies including western hemlock (Tsuga hetero-
phylla), western redcedar (Thuja plicata), and
grand fir (Habeck 1987). The combination of
greater precipitation and gentler topography re-
sults in relatively continuous forests in this re-
gion, including the valley bottoms where there
is often no well-defined lower timberline.
DISTURBANCE
Disturbance imposes further heterogeneity on
the landscape, at several spatial scales, by pro-
ducing a mosaic of age classes and successional
communities. Fire was historically the most
prevalent natural disturbance in the northern
Rocky Mountains (Gruell 1983).
The extent and severity of fires in the north-
central Rockies depended on the moisture gra-
dient, which varied temporally as well as spa-
tially (Arno 1980). Forests in more mesic areas
burned less often (every 50-300 years; Table 1),
so they were more likely to reach later succes-
sional stages and to accumulate larger amounts
of woody fuels, not burning until sufficient fuels
and weather conditions produced a stand-replac-
ing crown fire. Forests in drier areas would burn
more often (every 5-50 years; Table 1), before
sufficient fuels could accumulate to result in a
crown fire. These frequent underburns destroyed
seedlings of shade-tolerant tree species while
causing minimal harm to fire-resistant early-ser-
al trees, thus maintaining non-climax stands of
old-growth ponderosa pine and western larch
(Arno et al. 1997).
Historically, old-growth ponderosa pine and
western latch dominated millions of acres on
drier valley bottoms and south facing slopes
throughout much of the north-central Rockies
(Arno et al. 1997). Although these "fire-depen-
dent" (Habeck 1988) forests could be extensive,
complex topography and moisture gradients usu-
ally made these forests less homogeneous than
in the Southwest (Arno 2000). Heterogeneity
could occur at several scales, with grassland-for-
116 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 1 . REPORTED MEAN AND RANGE OF HISTORICAL FIRE INTERVALS IN GENERAL CONIFEROUS FOREST CLASSES
Mean fire
General habitat intervals b Fire interval Predominant
class a Description (yrs) range b (yrs) fire regime c
Limber pine Mostly small stands mixed with grass and 74 variable Nonlethal?
shrubs on dry or rocky sites
Warm, dry ponderosa Open stands, with grass understory main- 5-30 2-55 Nonlethal
pine or Douglas-fir tained by frequent fire
Warm, moist ponderosa Typically ponderosa pine dominant with 10 49 3-97 Nonlethal
pine an understory of Douglas-fir in the ab-
sence of fire
Cool, dry Douglas-fir Generally open stands of Douglas-fir with 35-40 variable? Nonlethal
sparse understory
Moist Douglas-fir Douglas-fir often dominates; closed-cano- 25-30 8-66 Mixed
py ponderosa pine, larch, and lodgepole
pine common in seral stages
Grand tir/mixed conifer Diverse closed-canopy forest; often devel- 13 120 5 150
ops into mixed species stand
Cool lodgepole pine Pure stands of lodgepole pine or mixed 24-50 1-88
with grand fir and whitebark pine
Subalpine fir and codomi- Spruce and other firs common in seral 57-153 50-300
nant species stages; stand-replacement fires common
Moist redcedar and west- Closed-canopy stands of redcedar and 70-120 25-200
ern hemlock western hemlock
Mixed-Lethal
Lethal-Mixed
Lethal
Lethal
a General classes of forest habitat types employed by U.S. Forest Service (Steele et al. 1981), arranged approximately on a dry to moist gradient.
b Fire-interval estimates from Arno 1980, Arno and Gruell 1983; Arno et aL 1995, 1997: Crane and Fischer 1986, Gruell et aL 1982, Gruell 1983.
c Historical fire regime thought to occur over most acreage; all habitat types could have all fire types.
est mosaics at the drier extremes and with denser
forests created by stand-replacing fires at the
wetter extremes. East of the Continental Divide,
where it is too dry for larch and too cold for
ponderosa pine, Douglas-fir forests often had
similar fire regimes (Arno and Gruell 1983). In
very dry years, stand-replacement fires may
have occurred in any of these areas (Bessie and
Johnson 1995, Brown et al. 1999).
In the more roesic areas of the north-central
Rockies (maritime-influenced forests, north-fac-
ing slopes, and mid- to high-elevation forest
types), the predominant fire regime was one of
infrequent, stand-replacement fires (Arno and
Davis 1980, Romme 1982, Fischer and Bradley
1987, Barrett et al. 1991). In fact, the origin of
most Rocky Mountain forest stands can be
traced to stand-replacement fires (Arno 1980).
Historically, most individual fires were small
(<1 ha; Strauss et al. 1989), because fuels were
too moist or sparse to spread the fire. However,
most of the area burned by stand-replacement
fires was due to a few large fires in dry years
(Strauss et al. 1989, Bessie and Johnson 1995),
so it was the large fires that created the vegeta-
tion mosaic that dominated the landscape until
the next extensive fire (Turner and Romme
1994). Large crown fires rarely consumed an en-
tire forest because of local variations in wind,
topography, vegetation type, natural fire breaks,
and fuel loads (Turner et al. 1994). These factors
produced a heterogeneous pattern of burn sever-
ities, as well as islands of unburned vegetation
(Eberhart and Woodard 1987, DeLong and Tan-
ner 1996). The degree of patchiness depended
on the dryness of fuels in the year of the fire
(Turner et al. 1994, Turner and Romme 1994).
Data on natural fire intervals in different for-
est cover types suggest that fire severity and fre-
quency were highly variable prior to current fire
suppression activities (Table 1). Frequent non-
lethal fires and infrequent stand-replacement
fires could occur in the same region depending
on weather and fuel accumulations, or individual
fires may have been of "mixed severity," with
many trees dying and many surviving (Brown
1995, Arno 2000). Mixed-severity fire regimes
occurred especially in mid-elevation, mixed-co-
nifer forests, where moisture regimes and topog-
raphy were variable, and fire-resistant tree spe-
cies (especially larch and ponderosa pine) oc-
curred. Mixed-severity fires produced heteroge-
neity at several scales, killing variable amounts
of trees within a forest stand and affecting var-
iable numbers of stands within a landscape. The
moisture regime influenced this variability in
size, with drier areas tending to have smaller
patches of lethal burns because fires burned of-
ten enough to prevent sufficient fuel accumula-
tion for extensive crown fires (Barrett et al.
1991). This typically left a patchy, erratic pattern
on the landscape that fostered development of
highly diverse communities (Barrett et al. 1991,
Arno 2000, Lyon et al. 2000).
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTS--Heft et al. 117
CURRENT TRENDS
In the north-central Rockies, most changes in
landscape patterns from historical to current are
the result of changes in the disturbance regimes
due to fire suppression and timber harvesting.
The resulting forests may differ in age, structure,
species composition, or landscape pattern, but
they remain conifer forests. The little land con-
version that has occurred is focused within the
lower elevations where forest or grassland has
been converted to agricultural land, rural resi-
dences, or urban areas.
FIRE SUPPRESSION
Fire suppression has become increasingly ef-
fective since the 1930s (Arno 1980, Barrett et
al. 1991). Through much of the low and mid-
elevation landscapes, fire suppression has altered
stand structures and landscape patterns through-
out the north-central Rockies (Tande 1979, Arno
1980, Barrett et al. 1991). Because dry, lowland
areas had fire-return intervals of 5-50 years, the
suppression of low-intensity fires for up to 70
yrs has resulted in abnormal fuel accumulations
that make the historically resistant old-growth
pine and latch more susceptible to stand-replace-
ment fire.
Harm et al. (1997) estimated that 19% of the
interior Columbia River Basin has changed to a
lethal fire regime from mixed or non-lethal over
the last century. Complex, uneven-aged stands
containing fire-resistant trees are being replaced
by even-aged post-fire stands that cover large
areas of the landscape (Hann et al. 1997). Future
fires that burn in this simplified landscape may
be larger and more homogeneous, so the ho-
mogeneity may be self-perpetuating (Arno 1980,
2000; Barrett et al. 1991).
Many areas naturally had heterogeneous land-
scapes due to a mosaic of successional stages
following stand-replacement fires. Here, fire
suppression is converting this mosaic of forest
stands from a variety of age classes into a more
homogeneous expanse of mid-successional ma-
ture forest (Hann et al. 1997). Because succes-
sion changes forest structure most rapidly in the
earliest age classes, it has taken only a few de-
cades for fire suppression to allow large expans-
es of closed-canopy, continuous forest to form
on the landscape (Tande 1979). However, in ar-
eas with stand-replacement fire regimes, the time
period of successful fire suppression may not yet
be long enough to greatly affect the historical
fire-return intervals of 140 to 400 years (Romme
1982, Barrett et al. 1991).
Fire suppression also reduces many unique
post-fire habitats on the landscape. Early post-
fire patches of standing dead trees are much re-
duced throughout the region. There also has
been a loss of shade-intolerant tree species, such
as ponderosa pine, larch, and aspen, as succes-
sion advances in the absence of fires (Hann et
al. 1997). Fire-maintained old-growth ponderosa
pine stands are an obvious example, but western
larch also formed large, open stands of fire-
maintained old growth (Arno et al. 1997). Larch
is restricted to relatively more mesic areas than
ponderosa pine, but it is the most shade-intol-
erant and fire-resistant conifer species in the
north-central Rockies (Arno and Fischer 1995),
so it is an important early-seral species as well
as being an important older-aged component of
forests in mixed-severity fire regimes. Aspen is
another early-seral tree species that regenerates
following fire. In the Centennial Mountains of
Idaho, aspen cover has been reduced 80% since
1850, while mature conifer forest increased in
area, patch size, and connectivity (Hansen and
Rotella 2000). Increasing isolation may be an-
other landscape factor affecting stands of these
tree species.
TIMBER HARVEST
With the suppression of fires, timber harvest-
ing is now the most important disturbance re-
turning conifer forests to early successional stag-
es. It is unclear whether the total area involved
is similar, however. Hann et al. (1997) estimated
that the current areal extent of early-successional
stands in moist forests (20%) is at the low end
of the historical (pre-1900) range (19-29%), is
about the same (18%) as historical in low-ele-
vation dry forests (8-20%), and higher (33%)
than historical (23-25%) in upper-elevation cold
forests. There are great differences, however, in
the landscape patterns and stand structures pro-
duced by timber harvest compared with fire
(Hann et al. 1997). Whether timber harvest in-
creases or decreases landscape heterogeneity de-
pends on the natural heterogeneity of the area
(i.e., fire regime and topography), the harvest
methods used, and the spatial scale at which
analyses are done.
Timber harvest has greatly reduced the acces-
sible, low-elevation dry forests that historically
had non-lethal fire regimes and were dominated
by old-growth ponderosa pine or western larch.
Accessible forests were preferentially logged
first, with more distant ones harvested as tech-
nology improved and road systems were created
(Hejl 1994). Few old-growth stands remain. In
the national forests of eastern Oregon and Wash-
ington, where the original low- and mid-eleva-
tion ponderosa pine forests may have been about
90% old growth, nearly three-quarters of this old
growth had been logged by 1970 (Henjum et al.
1994). In addition, 82% of the remaining old-
118 STUDIES IN AVIAN BIOLOGY NO. 25
growth patches are smaller than 100 acres, with
only 7 patches over 5,000 acres (Henjum et al.
1994). Fire suppression has resulted in further
danger to these patches by allowing the buildup
of fuels and converting patches to denser forests
with more shade-tolerant tree species. Hann et
al. (1997) estimated that the ponderosa pine cov-
er type decreased by 26% throughout the interior
Columbia River Basin since 1900. Open-canopy
old growth has diminished even more (Henjum
et al. 1994). Timber harvesting in combination
with fire suppression has also reduced old-
growth larch on the landscape. Hann et al.
(1997) estimated that the western larch cover
type (all ages) has decreased by 36% throughout
the interior Columbia River Basin since 1900.
Mid-elevation forest with mixed-severity fire
regimes historically had a diversity of stand
structures and landscape patterns. Timber har-
vesting returns some patch heterogeneity to
these forests, but generally on a coarser-grained
scale than produced by natural fires, with a more
regular pattern (Reed et al. 1996a). Clearcuts do
not retain the remnant trees or snag structure
typical of post-fire forests, nor do they create an
environment that could maintain the historical
complexity of community composition and
structure. Consequently, most of the early-seral
forest stands within this type are very different
in composition and structure relative to the na-
tive conditions (Hann et al. 1997). Harvest
methods that retain green trees (e.g., Lehmkuhl
et al. 1999) may better mimic some mixed-se-
verity fires, but still lack the snag structure or
large, downed woody debris. If the same pre-
scription is always used for this type of cutting,
it will produce a relatively simplified and ho-
mogeneous landscape.
The most productive forests in this region
were the "Cascadian" forests around northern
Idaho, where fires were rare and, therefore, large
blocks of old growth likely developed. Once
fairly homogeneous landscapes have been rid-
dled with clearcuts and other logged conditions.
In these and other forests with stand-replace-
ment fire regimes, (e.g., high-elevation lodge-
pole pine), the creation of many small clearcuts
is a departure from the pattern of disturbance
created by the natural fire regime (Brown 1995).
Similarly, in boreal forests in Canada, DeLong
and Tanner (1996) found that wildfires created a
more complex landscape pattern than clearcut
harvesting practices do, with a greater diversity
of patch sizes, more irregular shapes and bound-
aries, and more patches of mature forest inter-
mixed. These patches may be critical for bird
species that require heterogeneity in patch struc-
ture. They also provide sources of large trees
and snags (legacies) within the young post-dis-
turbance forest (DeLong and Tanner 1996). No
cutting method can create the dense snag struc-
ture that is produced by a stand-replacement fire.
It is unclear if timber harvest has created
more fragmentation than natural disturbance re-
gimes. Reed et al. (1996a) found a substantial
increase in patchiness created by clearcutting
and roads from 1950 to 1993 in high elevation
forests in the Medicine Bow Mountains of
southern Wyoming. Quantitative landscape in-
dices suggested a level of fragmentation greater
than that found in the Oregon Cascades. How-
ever, the disturbance patterns in Wyoming were
superimposed on a landscape of natural hetero-
geneity, and it is unknown what the landscape
in either 1950 or 1993 would have been like
under a natural fire regime. Tinker et al. (1998)
found similar results in the Bighorn Mountains
of north-central Wyoming. Old-growth forest
patches produced by natural disturbances in
western coniferous forests were typically much
larger and more continuous than are the remnant
patches created by timber harvesting and road
building (Tinker et al. 1998). However, they
found that roads contributed more to this change
in landscape indices than did clearcuts. It is not
known if roads are wide enough to cause harm-
ful fragmentation effects for most Rocky Moun-
tain bird species, especially in open forests, but
roads are certainly a more permanent distur-
bance than clearcuts (Reed et al. 1996b).
However atypical the landscape pattern pro-
duced by timber harvesting may be, it still leads
to forest succession and the retention of natural
vegetation. A potentially more serious impact on
the forested landscape is the permanent conver-
sion of native habitat to agriculture or residential
and urban development (including roads). In the
north-central Rockies, this conversion has been
concentrated in the valley bottoms. While this
limits the amount of fragmentation in the overall
landscape, these low elevation areas are also the
most productive ecosystems for birds (Hansen
and Rotella 1999). As rural development accel-
erates in the inland west (Knight 1997), we may
see much more serious fragmentation and edge
effects on birds due to added human features on
the landscape (e.g., Friesen et al. 1995).
PROPOSED CONSEQUENCES OF
LANDSCAPE CHANGES ON BIRDS
Based on our knowledge of the historical
landscape patterns of the region and the changes
that have occurred, we speculate about which
birds we would expect to be most affected by
landscape changes in the past 100 years in north-
central Rockies conifer forests. We offer these
speculations as a framework from which to ex-
amine the data that exist on bird trends and bird
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTS--Heft et al. 119
relationships with landscape patterns. The pro-
posed consequences of landscape changes on
birds are: (1) species that are adapted to moist
forest types that historically formed the most ho-
mogeneous landscapes (e.g., old-growth cedar/
hemlock) would be negatively affected by in-
creased landscape heterogeneity created by tim-
ber harvest openings; (2) species specialized for
forest types that were once prevalent but are
now uncommon or rare (i.e., vanishing habitats:
aspen, early post-fire forests, old-growth pon-
derosa pine, and old-growth larch) may be neg-
atively affected by decreasing patch size and in-
creasing isolation over and above the general
loss of habitat; and (3) birds that breed in close
proximity to human-added landscape features
(such as cows, horses, bird feeders, agricultural
land, or residential development) may be nega-
tively affected by brood parasites or nest pred-
ators that are attracted to these features. More
than one of these consequences could be occur-
ring in any one particular landscape.
HAS FOREST FRAGMENTATION
AFFECTED BIRDS OF THE
NORTH-CENTRAL ROCKIES?
To evaluate whether and how coniferous for-
est birds are affected by changes in landscape
patterns, we looked for evidence from each of
three sources: (1) regional population trends
based on the North American Breeding Bird
Survey; (2) studies concerning relationships be-
tween bird abundance and specific landscape
characteristics, including the effects of logging;
and (3) studies concerning relationships between
nesting success and human-caused landscape
modification.
BBS TRENDS
We assumed that if populations of some bird
species are declining as the result of changing
conditions brought on by fire suppression and
intense timber harvesting activities, then the re-
cent 33 years of Breeding Bird Survey (BBS)
data (1966-1998) collected from within the re-
gion should reflect that fact, although there may
be other reasons for any observed declines.
Thus, we determined how many conifer forest
bird species breed in the north-central Rocky
Mountains, which ones are adequately covered
by the BBS, and what the BBS data indicated
about their recent population trends. We focused
our analysis on the Central Rockies region, as
defined by Robbins et al. (1986), and the conifer
forest habitats within that region. By our own
estimate, there are 87 bird species that breed in
conifer forest habitats within the region (Table
2), and 39 of those (45%) were abundant enough
(>1.0 bird per route) and detected frequently
enough (on more than 14 routes within the re-
gion) to obtain reasonably reliable models of
their population trends (Sauer et al. 1999). The
bird species for which data are too few, and for
which we cannot expect the BBS to provide
meaningful results in the future, include those
that are rarely detected (e.g., diurnal raptors,
grouse), those that occur in habitats that are un-
common and poorly sampled by the BBS (e.g.,
burned forests), and those that are primarily noc-
turnal (owls).
Only one of the 39 forest bird species for
which the BBS provides adequate coverage ap-
pears to be declining significantly in the Central
Rockies Region--the Olive-sided Flycatcher
(Table 2; see table for scientific names of bird
species mentioned throughout text). This species
is associated with forest openings (natural and
human-created) and edges (Altman and Salla-
banks 2000), and was most common in harvest-
ed and recently burned conifer forest at sites
across northern Idaho and western Montana
(Hutto and Young 1999). Of these forest types,
burned forests have become rarer within the past
century. Because several of the species that were
not covered well by the BBS are also relatively
common in burned forests (woodpeckers), there
is even more reason to focus management atten-
tion toward the effects of fire suppression and
post-fire salvage logging, both of which have
undoubtedly affected the more fire-dependent
species negatively (Hutto 1995, Kotliar et al. this
volume).
BIRD ABUNDANCE AND LANDSCAPE FEATURES
Very few studies have been conducted that
look specifically at the relationships between
changing landscape patterns and birds in forests
of the north-central Rockies. We identified five
data sets that addressed the relationships be-
tween the abundances of bird species and some
aspect of landscape configuration. These studies
were conducted in different forest types, eleva-
tion, and climatic regimes as follows: (1) a re-
gion-wide correlational analysis based on 312-
ha landscapes centered on bird count points
across western Montana and northern Idaho,
where conifer forest was defined as one category
that included all major conifer types and a wide
range of canopy closures within those types (i.e.,
closed canopy, seed tree, shelterwood, and
group selection harvested sites; R. Hutto and J.
Young, unpubl. report); (2) a correlational anal-
ysis of spatial patterns within 300-ha landscapes
in mid-elevation closed-canopy mixed-conifer
forest, dominated by grand fir/Douglas-fir/pon-
derosa pine in west-central Idaho (Evans 1995);
(3) a comparison of a continuous 240-ha old-
growth landscape with two similar-sized old-
120 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 2. RECENT POPULATION TRENDS OF CONIFER FOREST BIRD SPECIES IN THE CENTRAL ROCKIES REGION AS
DETERMINED FROM BREEDING BIRD SURVEY DATA, 1966--1998
Species No. routes BBS trend
Turkey Vulture, Cathartes aura
Sharp-shinned Hawk, Accipiter striatus
Cooper's Hawk, Accipiter cooperii
Northern Goshawk, Accipiter gentilis
Swainson's Hawk, Buteo swainsoni
Red-tailed Hawk, Buteo jamaicensis
American Kestrel, Falco sparverius
Ruffed Grouse, Bonasa umbellus
Spruce Grouse, Falcipennis canadensis
Blue Grouse, Dendragapus obscurus
Wild Turkey, Meleagris gallopavo
Flammulated Owl, Otus fiammeolus
Great Horned Owl, Bubo virginianus
Northern Pygmy-Owl, Glaucidium gnoma
Barred Owl, Strix varia
Great Gray Owl, Strix nebulosa
Boreal Owl, Aegolius funereus
Northern Saw-whet Owl, Aegolius acadicus
Vaux's Swift, Chaetura vauxi
White-throated Swift, Aeronautes saxatalis
Black-chinned Hummingbird, Archilochus alexandri
Calliope Hummingbird, Stellula calliope
Broad-tailed Hummingbird, Selasphorus platycercus
Rufous Hummingbird, Selasphorus rufus
Lewis' Woodpecker, Melanerpes lewis
Williamson's Sapsucker, Sphyrapicus thyroideus
Red-naped Sapsucker, Sphyrapicus nuchalis
Hairy Woodpecker, Picoides villosus
White-headed Woodpecker, Picoides albolarvatus
Three-Toed Woodpecker, Picoides tridactylus
Black-backed Woodpecker, Picoides arcticus
Northern (Red-shafted) Flicker, Colaptes aurams
Pileated Woodpecker, Dryocopus pileatus
Olive-sided Flycatcher, Contopus cooperi
Western Wood-Pewee, Contopus sordidulus
Hammond's Flycatcher, Empidonax hammondii
Dusky Flycatcher, Empidonax oberholseri
Cordilleran Flycatcher, Empidonax occidentalis
Plumbeous Vireo, Vireo plumbeus
Cassin's Vireo, Vireo cassinii
Warbling Vireo, Vireo gilvus
Gray Jay, Perisoreus canadensis
Steller's Jay, Cyanocitta stelleri
Clark's Nutcracker, Nucifraga columbiana
Common Raven, Corvus corax
Tree Swallow, Tachycineta bicolor
Violet-green Swallow, Tachycineta thalassina
Northern Rough-winged Swallow, Stelgidopte¸,x serripennis
Black-capped Chickadee, Poecile atricapillus
Mountain Chickadee, Poecile gambeli
Chestnut-backed Chickadee, Poecile rufescens
Red-breasted Nuthatch, Sitta canadensis
White-breasted Nuthatch, Sitta carolinensis
Pygmy Nuthatch, Sitta pygmaea
Brown Creeper, Certhia americana
Rock Wren, Salpinctes obsoletus
House Wren, Troglodytes aedon
Winter Wren, Troglodytes troglodytes
Golden-crowned Kinglet, Regulus satrapa
Ruby-crowned Kinglet, Regulus calendula
Mountain Bluebird, Sialia currucoides
81 3.4*
58 -0.7
48 -5.4*
13 -10.2'
39 0.2
57 2.0
11 0.8
84 1.0
74 2.3
106 0.0
57 5.4*
81 -4.0*
90 -0.3
81 1.7
91 -2.0
57 2.1
9 -9.9*
72 1.5'
103 2.2*
67 -0.3
59 5.4*
63 4.6*
105 2.0
79 1.7
84 4.0
64 1.3
94 0.7
91 0.1
25 2.4
104 3.1'
32 1.1
15 1.0
62 3.7
63 3.0*
87 0.8
92 -1.2
64 1.6
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTS--Heft et al.
TABLE 2. CONTINUED.
121
Species No. routes BBS trend
Townsend's Solitaire, Myadestes townsendi
Swainson's Thrush, Catharus ustulatus
Hermit Thrush, Catharus guttams
American Robin, Turdus migratorius
Varied Thrush, Ixoreus naevius
Orange-crowned Warbler, Vermivora celata
Nashville Warbler, Vermivora ruficapilla
Yellow-rumped (Audubon's) Warbler, Dendroica coronata
Townsend's Warbler, Dendroica townsendi
MacGillivray's Warbler, Oporornis tolmiei
Wilson's Warbler, Wilsonia pusilla
Western Tanager, Piranga ludoviciana
Green-tailed Towhee, Pipilo chlorurus
Spotted Towhee, Pipilo maculatus
Chipping Sparrow, Spizella passerina
Fox Sparrow, Passerella iliaca
Lincoln's Sparrow, Melospiza lincolnii
Dark-eyed (Oregon) Junco, Junco hyemalis
Black-headed Grosbeak, Pheucticus melanocephalus
Lazuli Bunting, Passerina amoena
Brown-headed Cowbird, Molothrus ater
Pine Grosbeak, Pinicola enucleator
Cassin's Finch, Carpodacus cassinii
Red Crossbill, Loxia curvirostra
Pine Siskin, Carduelis pinus
Evening Grosbeak, Coccothraustes vespertinus
80 - 0.5
103 0.8
72 1.2
111 0.5
68 1.4
83 1.0
109 -0.5
70 1.2
96 0.9
77 - 1.0
97 0.8
13 -2.9
55 4.5*
111 0.1
65 6.8*
111 -0.4
59 8.9*
61 3.4*
86 - 1.1
72 - 0.2
79 0.7
109 0.3
62 2.2*
Note: Species without trend information were either too rare (<0.1 bird per route) or detected too infi'equently (on fewer than 5 routes) to provide
estimates; those without bolded data have either deficient regional abundance (< 1.0 birds per route) or route sample size (fewer than 14 routes).
Species showing significant declines or increases (P < 0.05) are noted with an asterisk next to the trend value.
growth and selectively-harvested landscapes,
each with embedded clearcuts in western red-
cedar/western hemlock forests in northern Idaho
(Hejl and Paige 1994); (4) a comparison of har-
vested and unharvested 20-100 ha stands of
spruce/fir in southeastern Wyoming (Keller and
Anderson 1992); and (5) a patch-based study of
old-growth ponderosa pine/Douglas-fir/western
larch in western Montana (Aney 1984). Not all
of the landscape metrics were evaluated in all
studies, and two studies (Keller and Anderson
1992, Hejl and Paige 1994) focused more on the
overall comparison of landscapes modified by
timber harvesting to unmodified areas (see Ef-
fects of logging patterns). Bird abundances were
based on point counts; point locations usually
were within conifer forest and encompassed the
natural variability in forest cover around points,
and analyses generally included only the most
common bird species detected. Thus, informa-
tion is primarily limited to passerines, because
other species are not well-sampled by point
counts.
Amount of forest
The amount of forest covering a landscape is
a frequently-reported measure of the degree of
fragmentation of that landscape (e.g., Robinson
et al. 1995a). It is one metric that can be mea-
sured easily in forested landscapes where the
forest remains highly interconnected and occurs
as the matrix, not as a patch, although it gives
no information on the spatial configuration of
the remaining habitat. It also is a measure that
can be used over large regions when the reso-
lution of the map used to measure forest cover
is too coarse to adequately capture other spatial
parameters such as patch shape and edge. In the
three landscape studies we considered, forest
cover was measured at similar extents (within
200-312 ha areas) and at similar resolutions (at
the scale of an aerial photograph or 30 m X 30
m pixel). The forest cover of interest ranged
from 3-100% across all sampled landscapes, al-
though these measures are not entirely compa-
rable among studies due to different definitions
of "forest."
A total of 10 species (five residents, three
long-distance migrants, and two short-distance
migrants) were consistently positively associated
with the amount of forest cover in at least one
study (Table 3). The probability of occurrence
of seven species increased with increasing
amounts of conifer forest in the study in which
forest was defined most broadly ("all conifer;"
R. Hutto and J. Young, unpubl. report). In
122 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 3. RELATIONSHIPS BETWEEN CONIFEROUS FOREST BIRD SPECIES AND LANDSCAPE METRICS IN THE NORTH-
CENTRAL ROCKY MOUNTAINS
Proximity
Amount of forest Patch size Edge density to edge
All Mixed Cedar/ All Mixed Ponderosa All Spruce Mixed
conifer a conifer b hemlock c conifer conifer pine d conifer rit e conifer
Positively associated with elements of continuous landscapes
Vaux's Swift (LDM, CN f) +
Gray Jay (R, OCN) (+)
Chestnut-backed Chickadee (R, CN) +
Red-breasted Nuthatch (R, CN) + + +
Brown Creeper (SDM, EN) + + +
Winter Wren (R, EN) + + +
Golden-crowned Kinglet (R, OCN) + + + + +
Swainson's Thrash (LDM, OCN) + (+)
Hermit Thrash (SDM, OCN) (+)
Varied Thrush (R, OCN) + +
Yellow-rumped Warbler (SDM, OCN) + +
Townsend's Warbler (LDM, OCN) + + +
Black-headed Grosbeak (LDM, OCN)g +
Pine Grosbeak (R, OCN) +
Mixed associations with fragmentation
Cassin's Vireo (LDM, OCN) -
Clark's Nutcracker (R, OCN) -
Western Tanager (LDM, OCN) - + -
Negatively associated with elements of continuous landscapes
Hammond's Flycatcher (LDM, OCN) -
Dusky Flycatcher (LDM, OCN)g -
Common Raven (R, OCN) - (-)
Mountain Chickadee (R, CN) - -
Ruby-crowned Kinglet (SDM, OCN) -
Townsend's Solitaire (SDM, OCN)
MacGillivray's Warbler (LDM, OCN)g -
Chipping Sparrow (LDM, OCN) - -
Dark-eyed Junco (SDM, OCN) - -
Cassin's Finch (R, OCN) - -
Red Crossbill (R, OCN) -
Pine Siskin (R, OCN) -
+
+
(+)
+
+
(+)
+ +
+
+
+
+ +
Notex: Forest types described in text. Not all landscape metrics evaluated in all five forest types. Positive association (increased abundance) denoted
by +; negative association by . Responses in parentheses significant at 0.05 < P < 0.10. All others significant at P < 0.05.
a R. Hutto and J. Young, unpubl. report. "All Conifer" forest includes seedtree, shelterwood, and group selection harvested sites.
b Evans 1995. Mixed conifer is closed canopy mature mixed conifen
"Hejl and Paige 1994.
cl Aney 1984.
e Keller and Anderson 1992.
tLDM long distance migrant, SDM - short distance migrant, R - resident (as defined by Partners in Flight); EN - enclosed nest, OCN open
cup nest, CN - cavity nest.
g Black-headed Grosbeak and Dusky Flycatcher classified as riparian by Hutto and Young 1999; MacGillivray's Warbler excluded from "All Conifer"
analyses--not restricted to conifen
closed-canopy mixed conifer forest, five species
increased in relative abundance as amount of
forest increased (Evans 1995). Three species
were more abundant in unharvested cedar/hem-
lock landscapes than in harvested landscapes,
and were less abundant than expected in har-
vested areas based on the amount of forest re-
maining (Hejl and Paige 1994). Across these
studies, Golden-crowned Kinglet was most fre-
quently associated with forest cover; Brown
Creeper and Winter Wren associations appeared
in two studies. The relationship between abun-
dance and amount of forest was not tested di-
rectly in spruce/fir (Keller and Anderson 1992),
but five species were more abundant in contin-
uous forest than in areas interspersed with clear-
cuts (see Effects of logging patterns).
A similar number (9) of species had the op-
posite association, decreasing in abundance with
increasing amounts of forest, suggesting that
they would have a positive response to fragmen-
tation. However, this negative association with
forest area was examined directly in only two
studies, and there was less correspondence be-
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTSHejl et al. 123
tween these studies. Dark-eyed Junco was the
only species that was negatively associated with
forest cover in both studies; Western Tanager
had opposing associations. More resident spe-
cies (five) were negatively associated with in-
creased amount of forest than long- (two) or
short-distance (two) migrants.
Patch size
Relationships of abundance with patch size
(the area of a continuous block of similar habi-
tat) were tested directly in three studies (Table
3). Most of the species positively associated
with larger patch size in the two landscape stud-
ies (Evans 1995; R. Hutto and J. Young, unpubl.
report) also were associated with amount of for-
est. The two variables were strongly correlated
(r = 0.69) in Hutto and Young's study, as they
probably are in many western studies. However,
Vaux's Swift, Gray Jay, Hermit Thrush, and Pine
Grosbeak were associated with patch size but
not to amount of forest in these studies (Evans
1995; R. Hutto and J. Young, unpubl. report).
Red-breasted Nuthatch, Golden-crowned King-
let, and Townsend's Warbler had the most con-
sistent positive associations with patch size be-
tween the two studies.
Interpreting Aney's (1984) study in old
growth ponderosa pine, we identified two spe-
cies (Solitary Vireo [now Cassin's Vireo] and
Brown Creeper) with possible minimum patch
size requirements. These species were absent
from stands below a certain size, even though
those stands might have been large enough to
accommodate at least one territory. Cassin's Vir-
eo (reported territory size of 0.5 ha/pair; Aney
1984) was not detected in stands less than 5 ha
(9 of 19 stands examined), but was consistently
detected in larger stands. Brown Creeper (terri-
tory size ranges from < 1 to 6.4 ha/pair; Hejl et
al. 2002) was absent from stands less than 4.5
ha (8 of 19 stands). Many species in this study
were not detected frequently enough for a pat-
tern of area sensitivity to emerge. In addition,
Aney (1984) did not consider annual turnover in
assessing presence or absence within patches
(Freemark et al. 1995).
Most species (7 of 9) negatively associated
with amount of "all conifer" forest across west-
ern Montana and northern Idaho (R. Hutto and
J. Young, unpubl. report) also were negatively
associated with increasing patch size, with the
exception of Clark's Nutcracker and Dark-eyed
Junco (Table 3). Hammond's Flycatcher and Red
Crossbill also were negatively associated with
patch size in this study. Only three species de-
creased in abundance as patch size increased in
west-central Idaho (Evans 1995).
Edge
Relationships between birds and edge density
or distance I¾om edge were evaluated in three
studies. In "all conifer" forests (R. Hutto and J.
Young, unpubl. report), all seven of the species
that were positively associated with the amount
of forest were also negatively associated with
edge density (see Table 3; r = -0.048 between
these two predictor variables, demonstrating low
correlation, and thus reasonable independence,
between them). In this instance, edge was defined
as the boundary between patches of dissimilar
cover, with 15 possible cover classifications (5
forest types, 4 open land types, 3 riparian types,
and 3 other classes) within 312-ha landscapes.
Two species (Brown Creeper and Hermit Thrash)
had a negative association with edge density in
spruce/fir (Keller and Anderson 1992). Evans
(1995) measured sensitivity to edge directly by
comparing abundance across three distances to
edge (<50 m, 50-100 m, >100 m). Edges were
defined by openings in closed-canopy forest and
the juxtaposition of forests of different ages and
canopy closure. Red-breasted Nuthatch, Golden-
crowned Kinglet, and Townsend's Warbler were
significantly more abundant as distance from
edge increased (Table 3).
Across studies, 10 species increased in abun-
dance as edge density increased or distance from
edge decreased (Table 3). Chipping Sparrow and
Pine Siskin were most frequently positively as-
sociated with edge across studies.
Effects of logging patterns
Two studies in the north-central Rockies (Kel-
ler and Anderson 1992, Hejl and Paige 1994)
compared the numbers of birds in landscapes
modified by timber harvesting to unmodified ar-
eas. In both studies, the modified areas were cre-
ated by logging (stripcuts, spot cuts, and clear-
cuts) interspersed within previously unlogged or
partially-logged forest. (Partially-logged forest
remained as continuous forest, but some trees
had been selectively removed previously.) The
two studies differed in habitat and methodology.
In the high elevation Engelmann spruce/subal-
pine fir study, Keller and Anderson did not sam-
ple clearcut areas because they did not want
stand comparisons to reflect avian use of unfor-
ested areas compared to forested areas. In the
low elevation western redcedar/western hemlock
study, Hejl and Paige sampled the complete
landscapes, allowing points to fall in clearcuts,
on edges, or in forest interior, to see how birds
responded to clearcut/forest landscapes as a
whole.
Of 16 species detected in spruce/fir and 38
species in cedar/hemlock, 9 species were com-
124 STUDIES IN AVIAN BIOLOGY NO. 25
mon to both studies. Of these nine species, three
had the same results: Brown Creepers were more
abundant in unlogged landscapes, Red-breasted
Nuthatches were similarly abundant in logged
and unlogged landscapes, and Pine Siskins were
more abundant in logged landscapes. Hermit
Thrush, American Robin, and Yellow-rumped
Warbler had opposite trends in the two studies.
Of those species found only in one study but
with significant associations, three species were
more abundant in unlogged landscapes (Moun-
tain Chickadee, Winter Wren, Swainson's
Thrush) and nine in logged landscapes (Northern
Flicker, Olive-sided Flycatcher, Townsend's Sol-
itaire, Cassin's Vireo, Warbling Vireo, Orange-
crowned Warbler, MacGillivray's Warbler, West-
ern Tanager, and Chipping Sparrow).
In both of these studies, it was difficult to as-
certain whether the associations with logged or
unlogged landscapes were caused by a simple
decrease or increase in suitable habitat caused
by logging or by the changes in landscape con-
ditions (i.e., decreased patch size, increased
edge). The fact that three species (Brown Creep-
er, Winter Wren, and Golden-crowned Kinglet)
were less abundant in harvested cedar/hemlock
landscapes than would be expected based on the
amount of forest remaining (see above under
Amount of forest) suggested that landscape
changes could at least be a partial cause of lower
numbers in those landscapes. In addition, while
most of the species identified in the two studies
have similar trends to those resulting from log-
ging in stand-level studies throughout the West
(as summarized by Hejl et al. 1995), Gray Jay,
Red-breasted Nuthatch, and Pine Siskin do not,
indicating potential landscape effects.
Synopsis
Given that there was virtually no replication
of any of the conditions among the studies that
we summarized, we suggest that the species
most or least sensitive to fragmentation, based
on their patterns of abundance, are those that
show a consistent response in several forest
types and geographic regions. Based on this as-
sumption, Brown Creeper clearly had the stron-
gest trend of species sensitive to changes in
landscape patterns, as it was associated with at
least one variable indicating landscape change
(and usually more than one) in four of the five
studies examined (Table 3). Golden-crowned
Kinglet, Red-breasted Nuthatch, Winter Wren,
Hermit Thrush, and Townsend's Warbler also
showed consistent results across studies. These
species appear as sensitive to disruptions in the
pattern of forest cover on the landscape else-
where in the West. Brown Creeper, Winter Wren,
and Red-breasted Nuthatch were correlated with
the amount of forest and/or patch size in coastal
Douglas-fir or cedar/hemlock forests (Rosenberg
and Raphael 1986, McGarigal and McComb
1995, Schieck et al. 1995), and Red-breasted
Nuthatches and Townsend's Warblers avoided
edges (Rosenberg and Raphael 1986).
Fewer species had consistent positive associ-
ations with elements of more fragmented land-
scapes in the north-central Rockies. Several spe-
cies had consistent associations with more than
one landscape element within a study, but only
three species (Pine Siskin, Chipping Sparrow
and Dark-eyed Junco) were consistent across
studies. These three species were also more
abundant in logged landscapes (Keller and An-
derson 1992, Hejl and Paige 1994). Our results
were somewhat inconsistent with other western
studies. Chipping Sparrow was associated with
edges in Douglas-fir forests in California (Ro-
senberg and Raphael 1986), but Pine Siskin and
Dark-eyed Junco were positively associated with
larger patches of old-growth Douglas-fir and
hemlock forests on Vancouver Island (Schieck
et al. 1995).
While the five studies we reviewed differed
in methods, particularly in how forest cover was
defined, none attempted to define "fragmented"
based on a minimum patch size. Thus, inconsis-
tent results among these studies are not attribut-
ed to one study considering a 200-ha patch to
be a fragment and another considering it contin-
uous forest. Two studies (Evans 1995; R. Hutto
and J. Young, unpubl. report) measured frag-
mentation indices as continuous variables across
300-ha landscapes and related bird abundances
in correlation or regression tests. One logging
study also based landscape descriptions on 240-
ha landscapes (Hejl and Paige 1994). The other
logging study used some small (20-40 ha)
patches as unmanaged controls (Keller and An-
derson 1992), but we used only an edge measure
from this study. The old-growth ponderosa pine
patch-based study included very small patches
(<4 ha) but the only variable discussed from
that study was patch size; we used a species'
presence or absence across the range of patches
as an indication of sensitivity to patch size.
DEMOGRAPHIC RELATIONSHIPS WITH LANDSCAPE
FEATURES
Several studies have suggested that the num-
ber of individual birds can temporarily increase
in areas adjacent to recent cuts due to displace-
ment of birds into the nearest suitable habitat
(Schmeigelow et al. 1997, Walters 1998). Over
the long term, high abundances can be main-
tained from source habitats and a population
trend would not be apparent (Van Horne 1983,
Vickery et al. 1992). Increased densities could
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTS--Heft et al. 125
have a negative impact on reproductive rates
through reduced pairing success, competition for
resources, and reproductive failure (Hagen et al.
1996), issues for which demographic studies are
needed. Data on the effects of landscape patterns
on bird demography are seriously lacking from
conifer forest habitats in the north-central Rock-
ies. Several recent studies are beginning to pro-
vide information to address this gap.
S. Hejl (unpubl. data) studied nesting success
of cavity-nesting and enclosed-nesting species in
a continuous old-growth (>170 yr) cedar/hem-
lock forest landscape (240 ha) and compared re-
sults to nesting success from a landscape com-
posed of recent clearcuts in a matrix of old-
growth cedar/hemlock in northern Idaho. Nest-
ing success did not differ between landscapes
for any of the five focal species (Red-naped Sap-
sucker, Chestnut-backed Chickadee, Red-breast-
ed Nuthatch, Brown Creeper, and Winter Wren)
in 1992-1994, but four species (all but Winter
Wren) had trends of lower nesting success in the
logged landscape. The sample of nests was lim-
ited, and the numbers for some species-land-
scape combinations may be too low to compute
reliable Mayfield estimates (Hensler and Nichols
1981).
D. Evans and colleagues (unpubl. report)
studied nesting success of Swainson's Thrushes
and Western Tanagers in mixed-conifer forests
in west-central Idaho. Data were obtained from
10 separate study plots, four of which were clas-
sified as located within relatively continuous for-
est areas and six of which were classified as rel-
atively fragmented. Stands were classified based
on a multivariate analysis of landscape cover
within 1 km of the avian demography study
plots. Nesting success of neither Swainson's
Thrush nor Western Tanager differed between
landscape classes, although there was a trend for
lower success of Swainson's Thrushes, and high-
er success of Western Tanagers, in fragmented
landscapes. However, overall nest success esti-
mates for both species in either landscape class
were substantially below the minimum nest suc-
cess thresholds suggested as needed to support
self-sustaining populations (Martin et al. 1996).
Evans et al. (unpubl. report) also found no re-
lationship between nest success and distance to
edge for either species. Using survival (recap-
ture and resighting of color-marked individuals)
and productivity data collected from mixed-co-
nifer habitats in Idaho, they modeled continu-
ous-landscape and fragmented-landscape popu-
lations of Swainson's Thrushes and Western
Tanagers. Population trajectories did not differ
between continuous and fragmented landscapes
for either species, and all populations declined
rapidly. Because overall estimates of annual sur-
vivorship were relatively high (0.67-0.68 annual
survivorship), the authors concluded that the de-
clines in simulated populations were mostly tied
to relatively low nesting success.
Sallabanks et al. (1999) initiated a regional
study examining the effects of landscape com-
position on avian nesting success. They moni-
tored replicate plots in managed forest land-
scapes with both silviculture and agriculture,
managed forest landscapes with active silvicul-
ture only, and unmanaged forest landscapes with
neither agriculture nor silviculture. Although
statistical analyses have yet to be conducted, a
preliminary examination of the data (2,847 nests
of 66 bird species) suggests a mix of results:
several species tend to have increasing rates of
nest success along a spectrum from managed
landscapes with both silviculture and agriculture
to unmanaged landscapes (e.g., Warbling Vireo),
others appear to be unaffected by landscape
composition (e.g., Dusky Flycatcher), and still
others have their highest success in the most
heavily managed landscapes (e.g., Mac-
Gillivray's Warbler; R. Sallabanks, pers.
comm.).
The primary cause of landbird nest failures
within the north-central Rockies region is pre-
dation, as reported elsewhere (Martin 1993). In
Idaho, predators destroyed 31-35% of all nests
monitored, depending on species and landscape
classification (D. Evans et al., unpubl. report).
Based on opportunistic observations, these au-
thors recorded evidence of red squirrel (Tamias-
ciurus hudsonicus) predation and speculated that
avian predators, such as jays, accounted for
some losses. In addition, only one of 202 nests
had evidence of cowbird parasitism. Based on
one year of data, R. Sallabanks et al. (unpubl.
report) reported that 43% of total nests (76% of
failures) were destroyed by predators in three
regions in Idaho and Montana. In a companion
study in west-central Idaho using artificial nests
baited with clay eggs, Warner (2000) identified
deer mouse (Peromyscus maniculatus), yellow-
pine chipmunk (Tamias amoenus), red squirrel,
and northern flying squirrel (Glaucomys sabri-
nus) as the primary predators of nests placed on
the ground and in shrubs. Predator assemblages
were similar between managed (i.e., with agri-
culture and/or silviculture) and unmanaged (i.e.,
without agriculture or silviculture) forest land-
scapes. Warner (2000) also documented attempt-
ed predation on clay eggs by deer, sheep, do-
mestic cattle, coyotes, ground squirrels, beaver,
and other songbirds.
Demography data show some consistency
with results based on abundance. Abundance
data indicated that 14 species are potentially
negatively affected by landscape changes caused
126 STUDIES IN AVIAN BIOLOGY NO. 25
by timber harvesting (i.e., numbers for these 14
species are either positively correlated with
more of larger forests or negatively correlated
with edge density or distance to edge; Table 3).
For the four of these 14 species for which we
have preliminary nesting success data, three
(Brown Creeper, Red-breasted Nuthatch, Swain-
son's Thrush) had lower nesting success trends
in logged landscapes. The other species (Winter
Wren) had inconsistent nesting success trends.
One of the species with a mixed association with
landscape changes according to abundance data
(Western Tanager) had a trend of greater nesting
success in fragmented landscapes. This latter re-
sult was consistent with findings by Davis
(1999) that Western Tanagers in Idaho were
most closely affiliated with relatively open
stands of primarily Douglas-fir trees.
Brown-headed Cowbird occurrence
Given that nest parasitism has been shown to
be a problem in some fragmented landscapes,
we summarized the response of Brown-headed
Cowbirds to landscape changes. Studies in the
north-central Rockies that have examined cow-
bird abundance within a landscape context con-
sistently show that proximity to agricultural ar-
eas is a strong, if not the strongest, predictor of
cowbird occurrence (Hejl and Young 1999,
Young and Hutto 1999, Tewksbury et al. 1999).
Within conifer forest sites across western Mon-
tana and northern Idaho, cowbirds were more
likely to be found in xeric forests (especially
ponderosa pine), in areas with an abundance of
cowbird hosts, close to developed, agricultural,
and riparian areas, and less likely to be found in
subalpine forests (Young and Hutto 1999). In the
Bitterroot Valley, Montana, Brown-headed Cow-
bird abundances were greatest in riparian areas,
less in xeric conifer forest, and least in riparian
conifer Ibrests (Tewksbury et al. 1999). Within
518-ha landscapes in xeric ponderosa pine/
Douglas-fir forests, landscape context was more
important than stand attributes in determining
cowbird numbers (Hejl and Young 1999). Cow-
birds were more abundant in landscapes with
more open land (agricultural land and grass-
land), deciduous riparian habitat, mature forest
(70-120 yr), and less old growth. Forest cover,
logged openings, human residences, and eleva-
tion were not important predictors of cowbird
numbers in these xeric forests. All of these stud-
ies suggest that cowbird distribution is limited
by the presence and distribution of largely sup-
plemental food supplied by human activities. In
addition, cowbirds may be more abundant in co-
nifer stands near riparian areas (but not in can-
yons or riparian conifer forests) because they are
attracted to riparian habitats that are dense with
potential hosts, and venture into adjacent conifer
forests secondarily.
Fewer data are available to assess the impact
of cowbirds on nest success. From BBIRD sites
across the West, forest coverage correlated in-
versely with nest parasitism within 10-kin radius
areas, with lower parasitization rates where for-
est coverage was greater (Hochachka et al.
1999). However, the opposite trend was seen at
the 50-km scale. Hochachka et al. (1999) hy-
pothesized that this contrary result suggests that
traits other than forest cover, such as human-
induced land-use practices that are related to for-
est cover (see Tewksbury et al. 1998). may be
responsible for these results.
Where reproductive success has been studied
in coniferous forests of the north-central Rock-
ies, cowbird parasitism rates were extremely low
(e.g., 0-3% in varied locations in west-central
Idaho, northern Idaho, and western Montana; D.
Evans et al., unpubl. data; S. Hejl, unpubl. data;
R. Sallabanks, unpubl. data). Parasitism rates are
likely to be much higher where cowbirds are
more abundant, such as in ponderosa pine for-
ests near residential development and agricultur-
al areas. Overall, however, locations supporting
higher parasitism rates currently are relatively
rare in the coniferous forest landscape of the
north-central Rockies.
DISCUSSION
We found scattered evidence in the few land-
scape studies from the north-central Rockies
supporting our expectations of the birds most af-
fected by landscape changes. We believe that the
"Cascadian" forests of northern Idaho histori-
cally were continuous, and extensive logging
and consequent fragmentation would result in
landscape conditions for which species found
there are not well adapted. In fact, the two spe-
cies (Brown Creeper, Golden-crowned Kinglet)
that were negatively associated with fragmenta-
tion indices in at least three studies in the north-
central Rockies were most commonly affiliated
with moist, continuous habitats. Additionally,
the trend for nesting success of Brown Creepers
in a fragmented landscape was half that of con-
tinuous forest (although based on a small sample
size; S. Hejl, unpubl. data). Other species asso-
ciated with moist, once-continuous forests (and
therefore ones that we would expect to be af-
fected similarly by landscape changes) are:
Chestnut-backed Chickadee, Winter Wren, Var-
ied Thrush, and Townsend's Warbler in cedar-
hemlock forests. Much of the high-elevation
spruce-fir zone also produced large expanses of
continuous forest, where the topography permit-
ted, because of the long period between fires (of-
ten 300 yr; Romme 1982). For this reason, bird
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTS--Heft et al. 127
species associated with spruce-fir forests, such
as Boreal Owl, Hermit Thrush, and Pine Gros-
beak, might be sensitive to fragmentation. Sev-
eral of the above species had our expected as-
sociations with fragmentation indices, but in
other forest types. Boreal Owl was not reported
in the studies summarized.
Whereas the "Cascadian" forests described
here are similar to Pacific Northwest forests in
structure, landscape, tree species, and bird com-
munities, these moist forests make up a relative-
ly small proportion of the north-central Rockies
as a region. Given the greater natural heteroge-
neity in the north-central Rockies, it follows that
overall, fewer species may exhibit a negative as-
sociation with fragmentation here than in the Pa-
cific Northwest.
Mid-elevation forests, primarily mixed-coni-
fer types in the Douglas-fir and grand fir zones,
had substantial natural heterogeneity historical-
ly. Although these landscapes have received
considerable logging pressure, the change from
historical patterns caused by timber harvest may
not be as pronounced as in very moist forests.
We are not certain how birds most adapted to
using these heterogeneous habitats have been af-
fected by the current level of fragmentation of
these landscapes caused thus far by timber har-
vesting, or if timber harvesting would compen-
sate for changes from fire suppression, either in
structure or extent. Most bird species that use
Douglas-fir or mixed-conifer forest also use oth-
er forest types (Hutto and Young 1999). From
the one study conducted in this forest type ex-
clusively, three species (Red-breasted Nuthatch,
Golden-crowned Kinglet, and Townsend's War-
bler) were negatively associated with more than
one fragmentation index (Table 3), but we had
classified two of these species as more associ-
ated with moist, continuous forests.
Similarly hard to interpret are the consequenc-
es of landscape changes in low-elevation dry
forests. These forests are likely to have been the
most affected by timber harvest, fire exclusion,
and proximity to agricultural land and human
development, but so many different changes
have occurred on each piece of ground that there
is no general landscape pattern that has been cre-
ated. We speculate that low-elevation, dry sa-
vannah-like lk)rests with many natural openings
(e.g., ponderosa pine) that often are intermixed
with grasslands would favor birds that exploit
relatively open habitats, and that these birds are
less likely to be negatively affected by the intru-
sion of openings caused by timber harvesting,
as long as sufficient amounts of their required
habitat elements are available (i.e., above a
"habitat loss" threshold; Andr6n 1994, Fahrig
1999). Birds associated with ponderosa pine and
many Douglas-fir cover types include Flammu-
lated Owl, Lewis' Woodpecker, White-headed
Woodpecker, White-breasted Nuthatch, Cassin's
Vireo, and Chipping Sparrow. Chipping Spar-
row had a positive association with fragmenta-
tion indices in two studies, but Cassin's Vireo
had mixed associations. In addition, it recently
has been shown that Flammulated Owls are as-
sociated with open, edge habitats (Goggans
1986) and with old-growth ponderosa pine in-
terspersed with grasslands at the large landscape
scale (Wright 1996). However, in the current era
of fire suppression, many low elevation dry for-
ests now support increased tree density and can-
opy cover (Arno et al. 1997). The consequences
of these changes in structure have not been ad-
equately explored, nor have the consequences of
human encroachment near these forests.
Patch size was important for some species in
remnant patches of old-growth ponderosa pine
(Aney 1984). This study, however, is the only
one that has examined patch size for the vanish-
ing habitats for which we are concerned, and no
one has examined whether patch isolation influ-
ences early post-fire, aspen, old-growth ponde-
rosa pine, or old-growth larch patch occupancy
by birds. We believe that these issues are espe-
cially critical for birds that specialize on these
habitats, given the trend of increasingly smaller
and more isolated patches.
Three demographic studies (D. Evans et al.,
unpubl. report; S. Hejl, unpubl. data; R. Salla-
banks, unpubl. report) found little to no cowbird
parasitism in areas fragmented by logging or in
continuous forests. Most of these specific land-
scapes were far from human-added features with
which cowbirds may be associated, but this
needs further investigation. Overall, the impact
of cowbirds on conifer forest birds in the north-
central Rockies currently appears small relative
to other factors. Parasitism rates, however, are
likely to be high in those conifer forests near
agricultural areas or residential development
(not well studied), and if human-added features
spread throughout conifer forests in the north-
central Rockies, then we would expect Brown-
headed Cowbird parasitism to increase as well.
There is fairly convincing evidence that as-
sessing the effects of changes in forest land-
scapes for birds in the north-central Rockies, as
elsewhere in the West, requires a different ap-
proach from the model developed from more
static, fragmented landscapes in the East and
Midwest in North America. More extensive for-
ested areas in the East and Midwest may indeed
have similar landscape conditions to those most
prevalent in north-central Rockies forests, but
most fragmentation studies in those regions have
dealt with "remnant patches" (sensu Forman
128 STUDIES IN AVIAN BIOLOGY NO. 25
and Godron 1986) in the middle of disturbed
habitat. In contrast, the natural situation in the
north-central Rockies is one of "disturbance
patches" (sensu Forman and Godton 1986),
such as early post-fire forests or timber harvest
openings, in the middle of a less disturbed land-
scape matrix (Faaborg et al. 1995).
These differences in patterns and processes
between regions within North America, and their
concomitant differences in avian response, have
been reviewed elsewhere. The relationships of
increased abundance and species richness with
forest fragment size were more pronounced for
long-distance migrants and open-cup nesters in
eastern and midwestern studies compared with
residents or short-distance migrants (Faaborg et
al. 1995). In northeastern and central hardwood
forests, 72% of species showing area sensitivity
in at least some studies were long-distance mi-
grants, compared with 29% in western forests
(Freemark et al. 1995). Studies in the north-cen-
tral Rockies support the conclusion that resident
species are equally or perhaps more likely to be
negatively affected by fragmentation than mi-
grants. The effect of increasing edge in eastern
North America results in greater access of some
nest predators into forests (e.g., Brittingham and
Temple 1983, Robinson 1992), but this pattern
does not necessarily hold in the landscapes of
the north-central Rockies. Timber management
(e.g., clearcuts) in western coniferous forests in-
troduces few new predators to the biotic com-
munity (Marzluff and Restani 1999). In some
landscapes of the north-central Rockies, red
squirrels and some corvids are at least as abun-
dant in uncut forest as in disturbed areas (Evans
and Finch 1994). Thus, we would expect that
predator response to changes in western conif-
erous forest landscapes, and the subsequent ef-
fects on nest success, may be better explained
by something other than "edge effects." Pred-
ator dynamics within these forests have yet to
be explored adequately.
Because habitat loss and habitat fragmenta-
tion are interdependent (Faaborg et al. 1995,
Fahrig 1999), it is difficult to separate the pos-
sible consequences of habitat configuration from
loss of habitat per se. In modeling thresholds of
fragmentation effects, Andrfin (1994) proposed
that in landscapes with >30% suitable habitat,
the amount of habitat was more important than
its configuration. Only when suitable habitat was
reduced to <30% did patch size and isolation
begin to influence bird populations. Most of the
studies in the north-central Rockies (and most
throughout the West) generally occurred in land-
scapes with >30% forest cover. Ten landscapes
in which nest success was studied by D. Evans
et al. (unpubl. report) varied from 32-78% forest
cover, and the authors believed that they may
have detected some fragmentation effects in
stands at the low end of this range. Given the
regional differences in areal extent of forest cov-
er across North America and the types of chang-
es to forests of the north-central Rockies that we
describe, it is not surprising that forest size was
a dominant influence in midwestern and eastern
studies, whereas change of within-stand struc-
ture and loss of nest and foraging substrates may
predominate in the north-central Rockies.
There are, however, instances when the model
of patch size and isolation may be applicable to
coniferous forests of the north-central Rockies--
specifically for habitats that have become scarc-
er on the landscape. This includes lower eleva-
tion old-growth habitats, which have been heavi-
ly harvested and are now disjunct, although per-
haps not surrounded by completely dissimilar
habitat. Fire disturbance patches, which current-
ly are in decline due to fire suppression, proba-
bly represent another example. From a land-
scape perspective, fire suppression and logging
not only decrease potential habitat for old-
growth specialists (e.g., Pileated Woodpecker)
and post-fire specialists (e.g., Black-backed
Woodpecker; Hutto 1995), but also further iso-
late those habitats, potentially decreasing the vi-
ability of populations of such species in the
north-central Rockies. What is most important
for these birds today is to restore the historical
patterns and the processes that created the land-
scapes for which the birds evolved (Hejl et al.
1995, Hejl 2000).
When not suppressed, stand-replacement fires
create well-defined fragments of early succes-
sional forest dominated by standing dead trees
(Hutto 1995). This is the earliest and most
ephemeral condition in post-fire succession.
These sites provide nesting opportunities for
many primary and secondary cavity nesters, and
timber drillers are attracted by the abundant bee-
tle larvae (Hutto 1995). In a literature review,
Hutto (1995) noted 15 bird species found equal-
ly or more consistently in recently burned for-
ests than in any other vegetation cover type in
the northern Rocky Mountains, and some spe-
cies were nearly restricted to such conditions
(Hutto 1995, Hutto and Young 1999). The
Black-backed Woodpecker, for example, has
been designated a "sensitive species" in several
regions by the U.S. Forest Service for precisely
that reason. Other species that were most com-
monly found in burned forests include Three-
toed Woodpecker, Hairy Woodpecker, Olive-sid-
ed Flycatcher, Mountain Bluebird, American
Robin, and Cassin's Finch (Hutto 1995). Early
post-fire patches are a naturally fragmented sys-
tem, but decades of fire suppression have de-
FRAGMENTATION IN ROCKY MOUNTAIN CONIFER FORESTSHejl et al. 129
creased the total area involved and increased the
isolation of each burn (Baker 1994). Bird spe-
cies restricted to such ephemeral, early post-fire
patches would have to be adapted to quickly col-
onize new patches, but increasing isolation may
place a strain on individuals finding new patch-
es. In addition, post-fire salvage logging may di-
minish the suitability of some patches by reduc-
ing nest sites and food resources (Caton 1996,
Hitchcox 1996, Saab and Dudley 1998).
Finally, BBS data may not be a useful tool for
evaluating the effects of landscape changes on
birds in these forests. We used BBS to examine
regional trends, because we assumed that if
landscape changes had greatly affected a spe-
cies, we would see that reflected in regional
trend information. We recognize that our inter-
pretations of these data may be limited because
BBS surveys take place on roads and therefore
do not sample all landscape situations equally,
may sample edge habitat although classified as
"forest," do not sample many conifer forest
birds well [55% of conifer birds in the north-
central Rockies (noted here) and 50% in western
North America (Hejl 1994) did not have reliable
population trends], and are limited to the most
recent 33 years. Indeed, of the 14 species most
likely to be negatively affected by fragmentation
according to community abundance studies (Ta-
ble 3), BBS has significant positive trends for
two species, indicating either that these species
have not been negatively (or may even have
been positively) affected by landscape changes
in the past 33 years, or that BBS does not sam-
ple these birds or issues very well. Alternatively,
BBS might be adequate for some of these spe-
cies or issues, and the general lack of negative
trends could indicate that many of these species
have not been negatively affected by landscape
changes during the past 33 years. We are con-
cerned, however, about the 55% of the species
that are not sampled well by BBS. Many of
these species are among those most likely to be
negatively affected by landscape changes asso-
ciated with timber harvest and fire exclusion. In
general, these species are difficult to study and
would benefit from species-specific investiga-
tions.
CONCLUSIONS
Overall, our understanding of the relation-
ships between landscape changes and conifer-
ous-forest birds in the north-central Rockies is
rudimentary. We have a growing understanding
of the landscape issues (current vs. historical
patterns and processes), but only scattered in-
formation concerning how changes in these
landscape patterns may have influenced bird
populations, and then only during the breeding
season. However, preliminary work suggests
that fragmentation is not clearly affecting as
many species as in other parts of North America.
Differences from fragmentation issues in other
regions are due to the kind and degree of frag-
mentation. In most north-central Rockies conifer
forest landscapes, forests are interconnected and
far from cowbird feeding sources or predators
associated with human residences. Since the ef-
fects of some landscape changes in the north-
central Rockies are likely to be less dramatic
than those that have been documented in the
East and Midwest, population responses of spe-
cies may be subtle and difficult to measure.
Large sample sizes are needed to determine if
subtle effects are real and biologically signifi-
cant enough to result in declining populations.
In the future, we need more studies on nesting
success, survivorship, dispersal, predator ecolo-
gy, and parasitism rates in relation to landscape
patterns as well as within-stand changes. Re-
search during the nonbreeding season also is
needed. We offer our proposed consequences as
hypotheses upon which to base future tests. Our
greatest concerns are for those species that are
associated with habitats that have changed the
most, are vanishing, or are near added landscape
features that cowbirds use. The loss of fires may
be the single greatest continuing threat to birds
in these landscapes, via the loss and isolation of
critical habitat components (such as snags).
ACKNOWLEDGMENTS
We thank the many committed field assistants who
collected bird data for the studies in Idaho and Mon-
tana. B. Beringer, C. Clark, C. Davis, J. Holmes, I.
Hovis, M. McFadzen, C. Paige, T. Thompson, W. Wil-
liams, and the University of Montana Wildlife Spatial
Analysis Laboratory were major contributors to the
field effort or data analysis. Data, suggestions, encour-
agement, and other information incorporated into this
paper were contributed by T. L. George, C. Hescock,
B. Laudenslayer, T Martin, M. Raphael, R. Sallabanks,
F. Samson, M. Slimack, D. Smith, and J. Verner. The
field research in Idaho and Montana summarized in
this review was supported by the U.S. Forest Service
(Regions I and 4, Payette and ldaho Panhandle Na-
tional Forests, Pacific Southwest Research Station,
Rocky Mountain Research Station, Pacific Northwest
Research Station, and Research Natural Areas Pro-
gram), U.S. Environmental Protection Agency, Boise
Cascade Corporation, Partnerships for Wildlife, Idaho
Department of Fish and Game, U.S. Fish and Wildlife
Service, Potlatch Corporation, and Arkansas State Uni-
versity. W. Block, D. Dobkin, and an anonymous re-
viewer provided helpful comments on an earlier ver-
sion of the manuscript.
Studies in Avian Biology No. 25:130-140, 2002.
EFFECTS OF HABITAT FRAGMENTATION ON PASSERINE BIRDS
BREEDING IN INTERMOUNTAIN SHRUBSTEPPE
STEVEN T KNICK AND JOHN T ROTENBERRY
Abstract. Habitat fragmentation and loss strongly influence the distribution and abundance of pas-
serine birds breeding in Intermountain shrubsteppe. Wildfires, human activities, and change in vege-
tation communities often are synergistic in these systems and can result in radical conversion from
shrubland to grasslands dominated by exotic annuals at large temporal and spatial scales from which
recovery to native conditions is unlikely. As a result, populations of 5 of the 12 species in our review
of Intermountain shrubsteppe birds are undergoing significant declines; 5 species are listed as at-risk
or as candidates for protection in at least one state. The process by which fragmentation affects bird
distributions in these habitats remains unknown because most research has emphasized the detection
of population trends and patterns of habitat associations at relatively large spatial scales. Our research
indicates that the distribution of shrubland-obligate species, such as Brewer's Sparrows (Spizella brew-
eri), Sage Sparrows (Amphispiza belli), and Sage Thrashers (Oreoscoptes montanus), was highly sen-
sitive to fragmentation of shrublands at spatial scales larger than individual home ranges. In contrast,
the underlying mechanisms for both habitat change and bird population dynamics may operate inde-
pendently of habitat boundaries. We propose alternative, but not necessarily exclusive, mechanisms to
explain the relationship between habitat fragmentation and bird distribution and abundance. Fragmen-
tation might influence productivity through differences in breeding density, nesting success, or pre-
dation. However, local and landscape variables were not significant determinants either of success,
number fledged, or probability of predation or parasitism (although our tests had relatively low statis-
tical power). Alternatively, relative absence of natal philopatry and redistribution by individuals among
habitats lollowing fledging or post-migration could account for the pattern of distribution and abun-
dance. Thus, boundary dynamics may be important in determining the distribution of shrubland-
obligate species but insignificant relative to the mechanisms causing the pattern of habitat and bird
distribution. Because of the dichotomy in responses, Intermountain shrubsteppe systems present a
unique challenge in understanding how landscape composition, configuration, and change influence
bird population dynamics.
Key Words: Amphispiza belli; Eremophilus alpestris; habitat fragmentation; landscape ecology; Or-
eoscoptes montanus; shrubsteppe; Spizella breweri; Sturnella neglecta.
The present rate of fragmentation in Intermoun-
tain shrubsteppe landscapes mid subsequent con-
version to unsuitable habitats is a critical man-
agement concern because of its effect on the as-
sociated avifauna (Braun et al. 1976, Knopf
1988, Saab and Rich 1997, Rotenberry 1998,
Paige and Ritter 1999, Wisdom et al. 2000).
Shrubsteppe regions in the Intermountain West,
and particularly those at lower elevations in the
Snake River Plain and interior Columbia River
Basin, represent some of the most endangered
ecosystems in North America (Noss and Peters
1995). Similarly, populations of bird species in
grassland and shrubland groups have declined
more than those in other bird groups during the
last 30 years (Knopf 1994, Paige and Ritter
1999, Peterjohn and Sauer 1999). Despite sig-
nificant habitat losses and declines in bird pop-
ulations, we still do not adequately understand
the mechanisms of bird responses to habitat
fragmentation in Intermountain shrubsteppe or,
more critically, how to reverse the loss of shrub-
steppe habitats (Rotenberry 1998).
Intermountain shrubsteppe historically con-
sisted of large expmlses of sagebrush (Artemisia
spp.), salt desert shrubs (primarily Atriplex spp.),
and an understory of bunchgrasses interspersed
with grassland patches (Hull and Hull 1974,
Vale 1975; West 1979, 1983; Wright and Bailey
1982, Billings 1994, Young 1994, West and
Young 2000). Shrubsteppe regions contained
relatively little natural vegetative heterogeneity
compared to other ecosystems in the Intermoun-
tain West (Kitchen et al. 1999) because of less
pronounced gradients in elevation, moisture, and
soil, and were highly susceptible to disturbmice
(Young and Sparks 1985). Similarly, avian di-
versity in shrubsteppe communities is low rela-
tive to other systems (Wiens and Rotenberry
1981, Wiens 1985a, Dobkin 1994, Rotenberry
1998).
Shrubsteppe birds live in habitats that now
have a vastly different disturbance regime from
that to which they were adapted. Wildfires, the
primary disturbance that destroyed shrubs, his-
torically were frequent but at small-scale, or
large but relatively infrequent. Early explorers
frequently reported fires in higher elevation, for-
ested regions of the Intermountain West but few
fires in the sparsely vegetated sagebrush valleys
(Gruell 1985). Aboriginal burning, although
common in higher elevation regions, was rare in
130
SHRUBSTEPPE FRAGMENTATION--Knick and Rotenberry 131
plains habitats because of scarcity of wild game
(Shinn 1980). Estimates of historical fire return
intervals range from 20 to > 100 years (Houston
1973, Young and Evans 1981, Wright and Bailey
1982). Sparse and patchily distributed fuels cre-
ated incomplete burns. Thus, the disturbance re-
gime was not severe enough to cause changes in
vegetation composition at large scales (Wright
1985). Shrub renewal in disturbed areas was ei-
ther by dispersal from remaining seed sources
within the disturbed area or by regrowth from
root crowns (Young and Evans 1978, 1989). The
principal heterogeneity consisted of a mosaic of
grasslands and different-aged patches of shrub-
land embedded within a larger shrub-dominated
landscape (Young et al. 1979, West and Young
2OOO).
Exotic annuals, primarily cheatgrass (Bromus
tectorum), Russian thistle (Salsola kali), and
tumble mustards (Descurainia spp., Sisymbrium
spp.), became established in the understory
around the turn of the 20th century after ground
surface disturbance caused by excessive grazing,
failed agriculture, and intentional eradication of
sagebrush (Vale 1974, Braun et al. 1976, Mack
1981, Yensen 1981). The synergistic pattern of
ground disturbance, fire recurrence, and in-
creased dominance by exotic vegetation have
caused extensive fragmentation over large spa-
tial scales and converted shrublands that once
appeared endless to early settlers in the 1800s
(Fr6mont 1845, Yensen 1982) into vast expanses
of exotic annual grasslands (D'Antonio and Vi-
tousek 1992, Young and Longland 1996, Hann
et al. 1997, Knick and Rotenberry 1997). Parts
of the Snake River Plain now burn every 3-5
years (Whisenant 1990). Using reported ex-
tremes for fire return intervals, fires that once
impacted <1-5% of the historical landscape
now burn 20-33% within some regions in an
average year. In shrubland habitats within the
Interior Columbia Basin ecosystem (eastern
Oregon, eastern Washington, Idaho, northwest-
ern Montana, and northeastern Nevada), the ra-
tio of lethal to nonlethal fires in the current fire
regime has increased greatly compared to the
historical fire regime (Hann et al. 1997). Con-
sequently, bird species that once experienced lit-
tle if any habitat change within their home range
and life span now live in a system that is un-
dergoing rapid habitat fragmentation and loss
(Knick and Rotenberry 2000). The large scale
conversion of native shrubsteppe into grasslands
dominated by exotic annual species may repre-
sent a degradation below a threshold from which
recovery to native shrublands is unlikely (West
and Young 2000).
In this paper, we discuss the effects of habitat
fragmentation on birds living in shrubsteppe sys-
tems in the Intermountain West. The pattern of
distribution and abundance of these birds is
highly correlated at multiple scales with nonspa-
tial measures of vegetative structure and florist-
ics, and with spatial measures such as shrubland
patch size, spatial texture, and shrubland-grass-
land perimeter (Rotenberry and Wiens 1980a,
Wiens and Rotenberry 1981, Rotenberry 1985;
Wiens 1985a,b; Wiens et al. 1987; Knick and
Rotenberry 1995a, 1999, 2000). However, many
of the underlying mechanisms of bird behavior
and population dynamics that create the pattern
of distribution remain unknown (Wiens et al.
1986a; Wiens 1989a,b; Rotenberry 1998, Roten-
berry and Knick 1999).
Shrubsteppe systems present a unique chal-
lenge to understanding bird population respons-
es to fragmentation. The pattern of distribution
and abundance of shrubsteppe birds is highly re-
lated to the shmbland-grassland configuration of
a region (Knick and Rotenberry 1995a, Vander
Haegen et al. 2000). In contrast, mechanisms of
disturbance that change habitat composition and
configuration, such as fire or livestock grazing,
readily cross shrubland-grassland boundaries.
Similarly, the relatively slight structural differ-
ences between a shrubland patch and an adjacent
grassland may have little influence on mecha-
nisms that affect bird population dynamics, such
as nest predation or parasitism, compared to
boundaries between forest and nonforested hab-
itats (Rotenberry 1998). Thus, fragmentation in
shrubsteppe presents a dichotomy in response to
habitat boundaries between bird distribution and
the mechanisms that create the patterns in hab-
itats and birds. In this review, we first describe
the patterns of distribution and abundance of
passerine birds in shrubsteppe regions of the In-
termountain West. We then examine potential
mechanisms by which fragmentation influences
population change to produce those patterns.
We make two important assumptions in our
review. First, and perhaps too pessimistically,
we assume that shrubland fragmentation and
loss in low elevation shrubsteppe, unlike other
ecosystems in the Intermountain West, may re-
sult in degradation below a threshold to a per-
manent state of exotic annual grasslands from
which recovery to a shrubland is not possible
without extensive efforts for restoration (Wes-
toby 1981, West and Young 2000). Second, we
make untested assumptions about scaling up;
that processes and patterns observed at the small
spatial and temporal extent of individual studies
are present at larger scales throughout the region
(Wiens and Rotenberry 1981, Allen and Starr
1982, O'Neill 1989, Wiens 1989c, Levin 1992,
Goodwin and Fahrig 1998, Rotenberry and
Knick 1999).
132 STUDIES IN AVIAN BIOLOGY NO. 25
L ß Big Sagebrush
t. Low Sagebrush
.... I.' '--.', N
FIOURE 1. Distributio of ]termoutai sagebrush
steppe regions.
STUDY REGION AND SPECIES
We conducted our review for shrubsteppe re-
gions of Idaho, Oregon, Nevada, Utah, and
Washington and including portions of Wyoming
and northeastern California (Fig. 1). The areal
extent of potential natural vegetation in shrub-
steppe habitats in this region, using Kfichler's
(1964) vegetation classes, is approximately
559,000 km 2 (Table 1). Within that region, long-
term studies of shrubsteppe birds have been con-
ducted in Oregon, Washington, and Idaho. We
base much of our discussion on bird and frag-
mentation dynamics for shrubsteppe systems in
the Snake River Plain of southern Idaho and the
Interior Columbia Basin, Washington, because
they contain studies that specifically addressed
habitat fragmentation, and because habitat frag-
mentation and loss in these areas is most pro-
nounced and may be a harbinger for other shrub-
steppe regions of the Intermountain West. We
recognize that some regions of the Great Basin,
such as eastern Oregon, have the opposite prob-
lem of loss of fire, which has led to extensive
stands of high density sagebrush. However, our
emphasis was on the effects of fragmentation,
which are most prevalent in regions currently
undergoing high rates of severe disturbance.
The primary species in this review include
Horned Larks (Eremophilus alpestris), Sage
Thrashers ( Oreoscoptes rnontanus), Brewer's
Sparrows (Spizella breweri), Sage Sparrows
(Arnphispiza belli), and Western Meadowlarks
(Sturnella neglecta). Where available, we also
TABLE 1. TOTAL AREA (KM 2) IN POTENTIAL NATURAL
VEGETATION FOR SHRUBSTEPPE CLASSES IN THE INTER-
MOUNTAIN WEST (K)CHLER 1964)
KQchler's (1964)
potential natural vegetation Area (kin 2)
38. Great Basin Sagebrush
(Artemisia ) 128,236
40. Saltbush-greasewood
(Atriplex-Sarcobatus) 115,630
50. Fescue-wheatgrass
( Festuca-A g rop yron ) 20,918
51. Wheatgrass-bluegrass
(Agropyron-Poa) 36,377
55. Sagebrush steppe
(Artemisia-Agropyron) 257,610
Total 558,771
Notes: Shrub dominated lands comprise 28-40% of the area within the
conterminous western United States (McAnher and Ott 1996). We
summed estimates within vegetation classes (McArthur and Ott 1996) for
Idaho, Utah, Oregon, Nevada, and Washington.
include information on Rock Wrens (Saipinctes
obsoletus), Loggerhead Shrikes (Lanius ludovi-
cianus), Green-tailed Towhees (Pipilo chloru-
rus), Vesper Sparrows (Pooecetes grarnineus),
Grasshopper Sparrows (Ammodrarnus savanna-
rum), Black-throated Sparrows (Arnphispiza bil-
ineata), and Lark Sparrows (ChoRdestes gram-
macus). Of these 12 species, 5 are classed by
the Partners in Flight Western Working Group
as requiring immediate conservation action in at
least 1 state or province (Table 2). In addition,
5 of these species exhibit significant population
declines in Breeding Bird Surveys conducted
throughout the western region (Sauer et al. 1997;
Table 2).
SHRUB STEPPE HABITAT DYNAMICS
HABITAT FRAGMENTATION AND LOss
Fragmentation and loss of shrubsteppe habi-
tats has been widespread and relatively rapid
throughout the Intermountain region largely be-
cause of human disturbance (Braun et al. 1976,
D'Antonio and Vitousek 1992, Billings 1994,
Young 1994, Hann et al. 1997, Mac 1998). More
than 10% of the sagebrush steppe in the Inter-
mountain region and 99% of the Palouse Prairie
grasslands in eastern Washington, Oregon, and
Idaho have been converted to agriculture (Noss
et al. 1995). Livestock grazing is pervasive
throughout the Intermountain West (Bock et al.
1993), and has influenced >99% of the shrub-
lands and severely altered >30% (West 1996).
The change in disturbance regime has facilitated
the spread of invasive plants such as cheatgrass,
and has altered both the form and function of
shrubsteppe regions throughout the Intermoun-
tain West (Young 1994). Exotic annual vegeta-
tion may indirectly influence bird productivity,
SHRUBSTEPPE FRAGMENTATION--Knick and Rotenberry 133
TABLE 2. STATES AND PROVINCES IN WHICH CONSERVATION ACTION IS RECOMMENDED BY THE PARTNERS IN
FLIGHT WESTERN WORKING GROUP AND WESTERN REGIONAL POPULATION TRENDS (% CHANGE/YEAR) IN BREEDING
Brad SURVEYS (SAUER ET AL. 1997) OF PASSERINE BIRDS BREEDING IN INTERMOUNTAIN SHRUBSTEPPE
Population change
Conservation
Species action 1966-1996 1966-1979 1980-1996
Horned Lark -2.1' - 1.7* -2.6*
Rock Wren -0.9 1.8 - 1.2
Sage Thrasher BC, ID 0.6 2.7 0.1
Loggerhead Shrike WA, BC, OR, ID -4.1' - 8. I * - 1.6
Green-tailed Towhee -0.1 - 1.6 0.7
Brewer's Sparrow BC, ID, LIT -3.5* -1.8 -3.0*
Vesper Sparrow 0.0 -0.6 0.7
Lark Sparrow WA - 1.1 0.9 -0.1
Black-throated Sparrow -0.8 2.3 - 1.2
Sage Sparrow WA, OR, ID, UT 0.5 -4.9 1.9
Grasshopper Sparrow 0.5 - 1.2 3.7
Western Meadowlark - 1.2* - 1.3 - 1.5*
* Population trend is significant (c = 0.05).
mortality, and population trends by increasing
the severity of disturbance on the habitat and
accelerating the rate of fragmentation and shrub-
land loss.
Fragmentation and loss of shrublands has
been particularly pronounced in the Snake River
Plain and Columbia River Basin (Whisenant
1990, Dobler et al. 1996). More than 99% of the
Salt Desert Shrub L 7
Grassland I -
GURE 2. Shbland loss om l 9 to 1994 in the
Snake River Birds of Prey National Conservon
Area, southwestern Idaho. The 19 vegetation map
w delineated fm fial photography. The 14
vegetation map w classified from Landsat satellite
imagery (Knick et . 1997).
basin big sagebrush (Artemisia tridentata ssp.
tridentata) communities in southern Idaho have
been converted to agriculture (Noss et al. 1995).
Within the 200,000-ha region of the Snake River
Birds of Prey National Conservation Area in
southwestern Idaho, over 50% of the existing
shrublands were destroyed by wildfires between
1979 and 1996 (Fig. 2). During that time, the
total area in grasslands, primarily cheatgrass, in-
creased from 17% to 53% (U.S. Dept. Interior
1996). Fire was the primary cause of shrubland
loss, exacerbated by disturbance caused by live-
stock grazing and military training (U.S. Dept.
Interior 1996, Knick and RotenbelTy 1997). The
average fire return interval in the National Con-
servation Area decreased from 80.5 yr between
1950 (the first year of fire records) to 1979, to
27.5 yr between 1980 to 1994. The fire return
interval is as short as 3-5 years in other parts
of the Snake River Plain (Whisenant 1990). By
comparison, the fire return intervals in the his-
torical disturbance regime, although difficult to
reconstruct, were estimated at 60-125 years for
nearby sagebrush systems at higher elevation
(Wright and Bailey 1982).
Approximately 59% of the historical distri-
bution of shrubsteppe landscapes and 35% of the
sagebrush in Washington still exists (Dobler
1994, Dobler et al. 1996, MacDonald and Reese
1998), but more land continues to be converted
each year (M. Vander Haegen, pers. comm.).
With the exception of three large areas of shrub-
steppe remaining in federal management (Yaki-
ma Training Center, Hanford Nuclear Site, Yak-
ima Indian Nation), remaining shrubsteppe hab-
itats are largely fragmented within a mosaic
dominated by agriculture (Dobler et al. 1996).
The primary cause of shrubland loss in the Co-
lumbia River Basin, Washington has been large-
134 STUDIES IN AVIAN BIOLOGY NO. 25
scale conversion of shrublands to agriculture, al-
though fires also can be significant locally in de-
stroying shrublands (Rickard and Vaughan 1988,
Cadwell et al. 1996). Landscapes converted to
agriculture are unlikely to be returned to shrub-
lands in the foreseeable future (Dobler et al.
1996, Vander Haegen et al. 2000).
Current distribution compared to historical
extent of habitats within the Interior Columbia
Basin ecosystem had decreased 33% for big
sagebrush, 34% for mountain big sagebrush, and
34% for salt desert shrubs, mostly due to agri-
culture (Harm et al. 1997). Similarly, areal extent
of habitats used by Grasshopper Sparrows had
decreased 15%, 19% for Vesper Sparrows, 20%
for Western Meadowlarks, 19% for Lark Spar-
rows, 17% for Sage Thrashers, 15% for Brew-
er's Sparrows, 21% for Sage Sparrows, 15% for
Black-throated Sparrows, and 9% for Logger-
head Shrikes (Wisdom et al. 2000).
HABITAT FRAGMENTATION AND
SHRUBSTEPPE BIRDS
FRAGMENTATION AND DISTRIBUTION OF
SHRUBSTEPPE BIRDS
Shrubsteppe birds in the Intermountain West
are distributed along major gradients between
extremes dominated by grassland and shrubland
habitats (Rotenberry and Wiens 1980a,b; Wiens
and Rotenberry 1981, Wiens et al. 1987, Wiens
1989a). Large scale conversion of shrublands to
grassland habitats dominated by exotic annuals
likely will result in loss of bird species richness,
increased numbers of Horned Larks and Western
Meadowlarks, and decreased numbers of shrub-
land-obligate species (Klebenow and Beall
1977, Rotenberry and Wiens 1978, Castrale
1982, Bock and Bock 1987, McAdoo et al.
1989, Shuler et al. 1993, Dobler 1994, Roten-
berry et al. 1995, Bradford et al. 1998).
Few studies have related distribution and
abundance of shrubland birds to the composition
and configuration of large landscapes (kin2;
Knick and Rotenberry 1995a, Vander Haegen et
al. 2000). Alternatively, measures of spatial het-
erogeneity taken at small study sites (ha) have
not correlated with species abundance or pres-
ence and may not reflect the scale at which birds
respond to their environment (Wiens 1974a). In
southwestern Idaho, we determined the distri-
bution of species in a bird community in the
Snake River Birds of Prey National Conserva-
tion Area relative to a gradient between shrub
and grassland habitats. We used a canonical cor-
respondence analysis (CANOCO; ter Braak
1986, 1988) of species abundances at 134 sites
at which we measured local vegetation charac-
teristics and landscape variables (Knick and Ro-
o J.0
_ 0.0
1.5
100
60
40
20 . G oq
x'/O ^ 0.0'g
0.0
&hrob t>øtch &ize (/Og[ro]
FIGURE 3. Relationship between local and land-
scape variables and probability of occurrence by Sage
Thrashers (A) and Sage Sparrows (B) in southwestern
Idaho (Knick and Rotenberry 1995a).
tenberry 1995b). Canonical correspondence
analysis is a multivariate direct gradient ordi-
nation of species variation relative to environ-
mental variables. The ordination axes of bird
species data are constrained to be linear com-
binations of the environmental variables, but the
species are assumed to have a unimodal re-
sponse to the environmental gradients (ter Braak
and Prentice 1988). Shrubland-obligate species,
such as Sage and Brewer's sparrows and Sage
Thrashers, were associated with Wyoming big
sagebrush (Artemisia tridentata ssp. wyomingen-
sis) communities and landscape variables of in-
creasing shrub patch size and number of shrub
cells in the 1-km radius surrounding the sample
point (Fig. 3). In contrast, Horned Larks and
Western Meadowlarks were associated with dis-
turbed vegetation communities. Predictive maps
of Sage Sparrow and Brewer's Sparrow pres-
ence, using a resource selection function based
on landscape variables and the Mahalanobis dis-
tance statistic, again demonstrated the direct re-
SHRUB STEPPE FRAGMENTATION--Knick and Rotenberry 135
Habitat Complexity
Fragmentation Index
Low
Ndium
ß High
Sage Sparrow
Presence
N
t __ Low
Medium
" ß High
10 0 10 I1ometers
FIGURE 4. Habitat fragmentation within a 5-km radius (average perimeter/area of shrub patches) (top) and
probability of Sage Sparrow presence (bottom) in a 200,000-ha shrubsteppe region in southwestern Idaho.
lationship between species presence and large
shrubland patches (Fig. 4; Knick and Rotenberry
1999).
The interaction between local vegetation char-
acteristics and landscape measures of fragmen-
tation that determine the probability of bird oc-
cupancy carries important implications for our
understanding of habitat selection and manage-
ment. Equal probabilities of occupancy were
possible with different combinations of ground
cover of sagebrush and patch size (Fig. 3).
Moreover, the shape of the selection function
changed relative to differences in value of a hab-
itat variable (Rotenberry and Knick 1999). Thus,
management questions of minimum areas re-
quired by a species may be best answered by a
probability of occupancy produced by multiple
patch sizes and characteristics. The low proba-
bility of occupancy also implies that only a por-
tion of available patches may be occupied, even
though the patch may be of sufficient size to
encompass multiple territories of individuals
(Robbins et al. 1989a).
MECHANISMS UNDERLYING THE DISTRIBUTION
PATTERNS
Landscapes generate patterns of species dis-
tribution by influencing productivity, mortality,
or movements among habitats (Wiens 1976,
1994; Urban and Shugart 1986, Danielson 1992,
Pulliam et al. 1992). Many species of birds ex-
hibit a meta-population structure composed of
source or sink populations within a region (Pul-
liam 1988, Hanski 1991, Opdam 1991, Pulliam
and Danielson 1991, McCullough 1996). We ex-
pected that fragmentation of shrublands facili-
tated mechanisms that would decrease produc-
tivity or increase mortality and thus lower the
number and individual contribution of source
populations by decreasing and isolating the area
of suitable resources, and increasing the amount
of edge (Fahrig and Merriam 1994, Wiens
1996). We reviewed studies for evidence that
fragmentation resulted in lower nest success or
productivity, increased mortality due to preda-
tion or parasitism, or influenced movements
among habitats.
Productivity
Productivity might be related to fragmentation
of shrublands and landscape configuration by
differences in breeding density, nest success, or
number of young produced. Measures of pro-
ductivity, as well as microhabitat characteristics
of nest placement have been reported for nu-
merous shrubsteppe species (Rich 1980a, b;
Reynolds 1981; Petersen and Best 1985a, b;
Winter and Best 1985; Rotenberry and Wiens
1980b, 1991). However, few studies have related
productivity to large scale measures of spatial
characteristics in Intermountain shrubsteppe sys-
tems (Knick and Rotenberry 1995b, 1996; Van-
der Haegen et al. 2000). Of these, only nest suc-
cess relative to landscape configuration has been
measured.
Young were successfully fledged at 11 of 13
Sage Sparrow nests, 27 of 36 Brewer's Sparrow
nests, and 8 of 37 Sage Thrasher nests during
1994 and 1995 in southwestern Idaho (Knick
and Rotenberry 1996). Local or landscape vari-
ables were not associated (P > 0.05) with nest-
ing success of Sage Sparrows. For Brewer's
Sparrows, increased nest success was marginally
related to increasing landscape heterogeneity (P
= 0.098), a trend that was contrary to expecta-
tion. Sage Thrasher nests were more successful
136 STUDIES IN AVIAN BIOLOGY NO. 25
40
Horned Lark
Western Meadowlark
' parrow
20
0 ........ White-crowrl Sparrow
Environmental is 1
Increasing Grassrand and Disturbance Increasing Shrub Cover
Increasing Patch Size
]OUR 5. aussJan sonse curves o bJd secJs
along the Qst nvJonmntal xJs of a coica] cor-
respondence analysis of bJd secJs d nvkonmn-
atal variables. he species sos½ curve was a func-
tion of the maximum numbe o observe[ions
site For the s½c1½s in the smp], the mod] sco½
[he environmental axis (), nd the dJssJon
along the xJs J units o stndd dvJtJon.
ectd vlu ) then is: - o' x [ [- (]/2). (x - )2]/
nd ooman 1986). nvkonmentl vJbles were r-
thickness of shrub ptch½s within I km of the sampling
oJnt.
at small spatial or temporal scales. Densities of
Sage and Brewer's sparrows did not differ con-
sistently between plots in controlled fire and un-
burned areas in eastern Idaho and densities of
Sage Thrashers did not change (Petersen and
Best 1987, 1999). In Montana, a 50% reduction
of sagebrush cover by herbicidal spraying did
not affect numbers of breeding pairs of Brewer's
Sparrows or Vesper Sparrows the following year,
but Brewer's Sparrows declined in the total-kill
sagebrush plot (Best 1972). Similarly, prediction
of densities of Sage Sparrows and Brewer's
Sparrows did not track local habitat changes in
eastern Oregon (Wiens and Rotenberry 1985,
Wiens et al. 1986b, Rotenberry 1986, Rotenber-
ry and Knick 1999).
Food resources may not limit productivity in
shrubsteppe regions except during "ecological
crunch" periods (Wiens 1974b, 1989a,b). How-
ever, no studies have related food resources in
fragmented and unfragmented habitats to differ-
ences in nesting success or clutch size. Reduc-
tion of arthropod abundance and biomass did not
adversely affect productivity of Brewer's Spar-
rows or Sage Thrashers in Idaho (Howe et al.
1996). Similarly, available biomass of arthro-
pods was >2 orders of magnitude greater than
required for bioenergetic demands of a com-
munity of shrubsteppe birds breeding in Oregon
(Rotenberry 1980).
with increasing shrub patch size (P = 0.064). In
Washington, Sage Thrashers, Brewers Sparrows,
and Lark Sparrows had lower nest success in
fragmented compared to unfragmented regions
(M. Vander Haegen, unpubl. data). In eastern
Idaho, clutch size and nest success did not differ
between an experimentally burned area that re-
duced sagebrush cover by 50% and control
plots, but no spatial characteristics of the land-
scape were measured (Petersen and Best 1987).
The pattern of species presence along a hab-
itat gradient of decreasing grassland cover and
disturbance to increased shrub cover and patch
size of shrublands changed from grassland spe-
cies, such as Grasshopper Sparrows and Horned
Larks to shrubland obligates, such as Brewer's
and Sage sparrows (Fig. 5). The density of sing-
ing males was greatest in unfragmented shrub-
land habitats for Sage Thrashers, and Brewer's
and Sage sparrows (Knick and Rotenberry 1995,
1999). Large-scale habitat changes in south-
western Idaho that increased fragmentation and
habitat richness in the landscape were associated
with lower densities of Horned Larks, Western
Meadowlarks, and Brewer's Sparrows (Knick
and Rotenberry 2000). However, bird response
was not strongly associated with habitat changes
Predation and parasitism
Edge-related processes that increase predation
or parasitism associated with increased fragmen-
tation and decreased patch size can reduce pro-
ductivity in fragmented habitats relative to larger
patches (Urban and Shugart 1986, Wiens et al.
1986a, Temple and Cary 1988, Porneluzi et al.
1993, Paton 1994). Nest predation ranged from
11-100% of the causes of nest failure in Brew-
er's Sparrows (Reynolds 1979, 1981; Petersen
and Best 1987, Rotenberry and Wiens 1989, Ro-
tenberry et al. 1999). Predators included Com-
mon Ravens (Corvus corax), Black-billed Mag-
pies (Pica pica), Loggerhead Shrikes, snakes,
long-tailed weasels (Mustela frenata), chip-
munks (Tamias spp.), and ground squirrels
(Spermophilus spp.). However, no studies have
related predation rates to fragmentation in shrub-
steppe habitats.
Brown-headed Cowbirds (Molothrus ater)
parasitize nests of Brewer's and Sage sparrows
(Rich 1978, Reynolds 1981, Biermann et al.
1987), but few data exist on the probability of
parasitism by cowbirds relative to degree of
fragmentation in shrublands. The extent to
which cowbirds also may attempt to parasitize
Sage Thrasher nests is unknown because Sage
SHRUBSTEPPE FRAGMENTATION Knick and Rotenberry 137
Thrashers reject cowbird eggs (Rich and Roth-
stein 1985, Reynolds et al. 1999).
The overall parasitism rate on Brewer's and
Sage sparrows in the Columbia River Basin,
Washington, was <10% (Vander Haegen and
Walker 1999), because most nesting attempts by
host species were started before cowbirds ar-
rived on the study areas. In addition, the rela-
tively long distance from agriculture develop-
ments and cattle feedlots, which provide feeding
areas for cowbirds, to shrubsteppe areas in
Washington may have accounted for the low
parasitism rates (Vander Haegen and Walker
1999). The rate of parasitism in Idaho and
Oregon also was low (0-13%) and may reflect
the relatively low presence of cowbirds (Rich
1978, Rotenberry and Wiens 1989, Rotenberry
et al. 1999). In contrast, cowbirds parasitized
52% of Brewer's sparrow nests in southeastern
Alberta (Biermann et al. 1987). Therefore, par-
asitism by cowbirds increases when shrublands
are converted to agriculture or cattle feedlots,
providing feeding sites for Brown-Headed Cow-
birds from which they can travel into surround-
ing areas to parasitize nests.
The structural diflrence between shrubland
and grassland to predators or cowbirds may be
less significant in producing an edge effect than
boundaries between forest and nonforested hab-
itats (Rotenberry 1998). As such, the function of
fragmentation may be indirect, by providing
homesites, feeding or watering sites, or diflrent
plant assemblages in unsuitable fragments that
increase the presence or proximity of potential
predators or cowbirds (Coker and Capen 1995,
Robinson et al. 1995a, Knight et al. 1998).
Redistribution and individual movements
In the absence of habitat-specific differences
in productivity or survival to create differences
in species abundance relative to habitat frag-
mentation, the pattern of a species distribution
also could result from individuals moving
among habitats (Dunning et al. 1992). We expect
that adults might exhibit strong site tenacity
(Wiens 1985a, Wiens and Rotenberry 1985,
Knick and Rotenberry 2000) and return after mi-
gration to the same breeding territory as the pre-
vious year regardless of any habitat alternation
(Rotenberry and Knick 1999; M. Vander Hae-
gen, pers. comm.). In contrast, young birds that
previously have not established successful ter-
ritories may seek new areas either following
fledging or upon returning from migration. We
do not know if dispersal and migration charac-
teristics, or habitats selected by juveniles differ
between those hatched in fragmented or unfrag-
mented shrublands.
Redistribution by individuals following mi-
gration and return to the breeding grounds also
could account for the pattern of distribution and
abundance relative to fragmentation. Many spe-
cies of shrubsteppe birds migrate seasonally,
breeding in the northern Great Basin, and win-
tering in the southwestern U.S. or northern Mex-
ico. Unfortunately, the considerable majority of
detailed research occurs only during the breed-
ing season. There are ample theoretical reasons
to expect that events that occur in migration or
during winter may play an equal or even greater
role in determining population dynamics on the
breeding grounds (Dunning and Brown 1982,
Knopf 1994, Sherry and Holmes 1995, Herkert
and Knopf 1998). Most importantly, the linkage
between any specific breeding area and any spe-
cific wintering area is unknown for virtually all
populations. In essence, then, the breeding
grounds of these species represent "open" sys-
tems, systems whose properties are affected by
events that lie outside the domain of study and,
hence, cannot be completely understood without
expanding the scale of study.
Linkages within a meta-population are driven
by the movements of individual animals, partic-
ularly those movements associated with natal
dispersal (although post-breeding dispersal may
also play a role in some species). Unfortunately,
empirical data relating to dispersal are usually
lacking, which severely constrains our ability to
understand and to adequately model population
dynamics in most species. Because many spe-
cies in fragmented landscapes are potentially
threatened, conservation efforts are hampered by
the lack of reliable information on dispersal. Pat-
terns of natal dispersal also are relevant to issues
of genetic structure and differentiation in popu-
lations, which also may have conservation-re-
lated consequences. Furthermore, most meta-
population models deal only with resident spe-
cies; little is known about linkages of migrant
populations breeding in a fragmented landscape,
or whether they even show meta-population
structure.
DISCUSSION
The effect of habitat fragmentation and the
increased intensity of land use on the biota and
its diversity are important considerations in the
conservation of the earth's resources (Wilson
1988, Saunders et al. 1991). Increasingly, birds
and other animals are forced to live in habitats
that have become fragmented in space by the
direct or indirect actions of humans. Our under-
standing of habitat fragmentation and its con-
sequences for bird populations have primarily
been developed from forested (Robbins et al.
1989a, Rolstad 1991, Freemark and Collins
1992, Robinson 1992, Robinson et al. 1995a) or
138 STUDIES IN AVIAN BIOLOGY NO. 25
grassland regions (Johnson and Temple 1986,
Herkert 1994). Yet, fragmentation of shrub-
steppe from disturbances such as wildfires, ag-
riculture, or other human-caused land use is
equally dynamic and has significant consequenc-
es for shrubsteppe birds as well as other taxa
(Braun et al. 1976, Knick 1999). Unlike other
ecosystems, loss of shrubsteppe may be irre-
versible once cheatgrass dominates the system
because of loss of seed sources, changes in soils,
and the increased fire frequency (Westoby 1981,
D'Antonio and Vitousek 1992, West and Young
2000).
Populations of shrubsteppe birds are of con-
servation concern in Intermountain states be-
cause of declines over part or most of the Great
Basin and Intermountain shrubsteppe regions. In
addition to passerines, population declines of
Sage Grouse (Centrocercus urophasianus) and
Columbian Sharp-tailed Grouse (Tympanuchus
phasianellus ssp. columbianus) are linked di-
rectly to fragmentation and habitat loss (Swen-
sen et al. 1987, Dobkin 1995, Connelly and
Braun 1997, MacDonald and Reese 1998; M.
Schroeder et al., unpubl. manuscript). Sage
Grouse have recently been petitioned for listing
under the Endangered Species Act because of
concerns over rangewide declines in numbers,
and Columbian Sharp-tailed grouse currently are
under status review.
Landscape analyses in shrubsteppe and other
arid ecosystems have not been as prevalent as in
other major ecosystems largely because map-
ping and describing habitats over large extents,
particularly from satellite imagery, pose difficult
technological challenges (Knick et al. 1997).
Mapping habitat change by standard remote
sensing techniques (Singh 1989, Dunn et al.
1991) also is problematic because of inability of
satellite sensors to detect vegetation in sparsely
covered shrublands. Appropriate measurement
metrics to quantify fragmentation in shrublands
are more difficult compared to agricultural and
forested systems because of the complex pat-
terns produced by fires (Knick and Rotenberry
1997). Thus, few studies have quantified spatial
attributes of composition and configuration of
landscapes relative to bird population dynamics
in shrubsteppe compared to forested systems.
The process of fragmentation operates at mul-
tiple scales of space and time. At large spatial
scales in shrublands, fragmentation was associ-
ated with distribution and abundance of popu-
lations of shrubland species. Declines in popu-
lations of Brewer's Sparrows, Western Mead-
owlarks, and Horned Larks also may be directly
related to large-scale fragmentation in Inter-
mountain shrubsteppe. Large-scale fragmenta-
tion may influence nesting success or facilitate
cowbird movements into previously unsuitable
habitats. At smaller scales, we expected that
fragmentation would affect individuals within
the population to produce the larger pattern.
Presence of shrubland birds was influenced by
local vegetation characteristics in combination
with landscape measures at spatial extents much
larger than individual home ranges. However,
we did not find convincing evidence that indi-
vidual productivity or probability of predation
was directly related to fragmentation. Thus, the
larger regional context in which shrubsteppe
birds establish their territories may be more im-
portant in determining range-wide patterns than
dynamics within that territory once established
(Rotenberry and Knick 1999). Cross-scale re-
search is needed to determine appropriate scales
at which birds respond to the system (Wiens
1974a, Wiens and Rotenberry 1980, Holling
1992).
Interaction of local and landscape variables in
predicting species presence emphasized the dif-
ficulty in defining habitat fragmentation in
shrubsteppe systems. If fragmentation is defined
relative to a species-specific probability of pres-
ence, then multiple combinations of local and
landscape variables might yield similar proba-
bilities of occupancy by individuals. Similar to
defining minimum patch requirements, our un-
derstanding of fragmentation must be done in
the context of multiple gradients of patch size,
perimeter, and the degree of isolation of the
patch (Fahrig and Merriam 1994; Wiens 1994,
1996).
The declining populations of Horned Larks
and Western Meadowlarks, determined from the
North American Breeding Bird Surveys (Sauer
et al. 1997), are contrary to our expectations
from habitat changes throughout the Intermoun-
tain shrubsteppe region. Horned Larks and West-
ern Meadowlarks are grassland species that are
common after disturbance and we would predict
increases in populations of these two species.
However, the exotic-dominated grasslands that
result from loss of shrublands throughout much
of the Intermountain region are very different
from the native grasslands to which Horned
Larks and Western Meadowlarks are adapted.
Declines in populations of Horned Lark and
Western Meadowlark populations indicate that
exotic annual grasslands are not ecologically
equivalent to native grasslands. Numbers of
Western Meadowlarks were lower but those of
Horned Larks were higher on transects in cheat-
grass compared to sagebrush communities in
southcentral Washington (Rogers et al. 1988).
In another apparent discrepancy between spe-
cies population and habitat trends, numbers of
Sage Sparrows observed on Breeding Bird Sur-
SHRUBSTEPPE FRAGMENTATION--Knick and Rotenberry 139
veys were increasing, although the trend was
statistically insignificant. Possibly, the Breeding
Bird Surveys may not be sampling the available
habitats, or tracking the habitat changes. We also
suggest that for all of these species, dynamics
on the wintering grounds may be equally, or
even more important in driving population
trends than habitat changes on the breeding
grounds.
COMPARISON TO MIDWESTERN
SHRUBLAND AND GRASSLAND
SYSTEMS
Birds living in grassland systems are experi-
encing a more extreme scenario of habitat frag-
mentation and loss than birds in shrubland sys-
tems. Conversion to agricultural cropland, live-
stock grazing, and urbanization have altered
most of the grassland ecosystems in North
America (Knopf 1994, Herkert 1995, Noss et al.
1995, Vickery and Herkert 1999). Habitat loss
exceeds 80% of the original distribution of prai-
rie grasslands and is almost complete in areas
suitable for agricultural croplands (Samson and
Knopf 1994). Other more subtle changes in
grassland habitats have resulted from differences
in the grazing regime by large herbivores and
alteration of historical fire frequencies (Saab et
al. 1995). In grasslands, as well as shrublands,
restoration of native species and processes re-
mains a significant challenge (Bock et al. 1993,
Rotenberry 1998, Vickery et al. 1999).
Fire, grazing, and climate were significant in-
fluences in native grasslands but varied in their
impact on system processes relative to geo-
graphic location. In Great Plains and eastern tall-
grass prairies, natural and aboriginal-caused fires
were large scale, intense, and frequent (5-30
year return interval), and combined with peri-
odic drought to maintain grasslands and prevent
shrub or tree growth (Wright and Bailey 1982,
Sims and Risser 2000). Grazing by large herds
of bison (Bison bison) was locally intensive but
highly variable in space and time. In contrast,
fire was the dominant disturbance in western
grasslands and shrublands because large grazers
have been absent since approximately 12,000
years presettlement (Mack and Thompson 1982,
West and Young 2000). In all grassland and
shrubland systems, fire suppression and control,
either by direct intervention or indirectly by hu-
man-created fire-breaks, have disrupted succes-
sional and cyclic pathways. Similarly, effects of
grazing have changed significantly because of
reduced native ungulate herds and increased do-
mestic livestock use, often resulting in a more
intensive disturbance that is spatially and tem-
porally uniform in the landscape (Bock et al.
1993).
Population trends of grassland birds, as a
group, decreased throughout North America
from 1966-1996; 13 of 25 species had signifi-
cant declines and 3 had significant increases dur-
ing this period (Peterjohn and Sauer 1999). Pop-
ulations of grassland species also have declined
over the past 100 years corresponding to the
long-term loss of grasslands (DeSante and
George 1994). However, as in shrubland sys-
tems, range-wide population changes detected in
Breeding Bird Surveys were not well supported
by studies at local scales (Herkert and Knopf
1998). In addition, the pattern of distribution and
abundance of grassland birds was sensitive to
landscape measures, but the mechanisms pro-
ducing those patterns remain unclear (Herkert
and Knopf 1998).
The winter ecology of grassland and shrub-
land birds is largely unknown, despite potential-
ly having a large influence on sizes of breeding
populations (Dunning and Brown 1982). Most
western grassland and shrubland bird species are
short-distance migrants to southern and south-
western United States and northern Mexico
(DeSante and George 1994, Rotenberry 1998,
Vickery et al. 1999). Therefore, influences on
populations of these species are largely North
American processes (Knopf 1994, Herkert 1995,
Rotenberry 1998).
The effects of fragmentation in shrubland or
grassland systems may be most pronounced
when the severity of disturbance results in a
highly contrasting mosaic of suitable and un-
suitable habitats derived from a previously ho-
mogeneous landscape. The structural difference
between shrublands and grasslands, or between
grasslands and agriculture or urban areas, al-
though slight relative to forest and nonforest
boundaries, nonetheless is a significant compo-
nent to bird distribution and abundance. Where
shrublands or grasslands have been fragmented
into unsuitable areas, numbers of area-sensitive
bird species decline (Johnson and Temple 1986,
Herkert 1994, Vickery et al. 1994, Bock et al.
1999, O'Connor et al. 1999, Walk and Warner
1999). Conversely, habitat fragmentation may
not be a significant factor in bird dynamics in
areas in which habitats remain largely un-
changed because the relative severity of distur-
bance is minimal or infrequent, or in landscapes
in which natural heterogeneity of habitats is
high. In Colorado foothills containing a high de-
gree of natural heterogeneity, shrubland birds
were not sensitive to landscape characteristics
(Berry and Bock 1998).
The answer may lie in behavioral mechanisms
of habitat selection, particularly the recognition
of a suitable place in which to settle for the first
time. Prior to the onset of anthropogenically-in-
140 STUDIES IN AVIAN BIOLOGY NO. 25
duced fragmentation, most of the species in this
review occurred in (and presumably were adapt-
ed to) landscapes dominated by shrublands that
were homogeneous over large spatial scales.
Perhaps reduction of these vast tracts of shrub-
lands below some minimum, but currently un-
known, size to current fragmented landscapes
simply represents a poor fit to the habitat tem-
plate of these birds.
CONCLUSIONS
The distribution of shrubsteppe birds was sig-
nificantly related to large-scale habitat fragmen-
tation. However, differences in productivity, pre-
dation, or parasitism associated with fragmen-
tation of shrublands were either unreported or
largely lacking. We suggest that individuals se-
lect location of home ranges within a hierarchy
of landscape and local vegetation characteristics
to produce the range-wide patterns of distribu-
tion. However, habitat structure may not be im-
portant in influencing mechanisms that affect
productivity and mortality among individuals.
Thus, patterns of species distribution are the re-
sult of individual movements among habitats el-
ther post dispersal or after migration. A lag ef-
fect due to site tenacity is evident in bird pop-
ulation responses to habitats (Wiens and Roten-
berry 1985; Peterson and Best 1987, 1999;
Rotenberry and Knick 1999, Knick and Roten-
berry 2000). Ultimately, populations of shrub-
land obligates may not persist in landscapes of
increasingly fragmented patches after distur-
bance (Braun et al. 1976, Rotenberry and Wiens
1980a).
ACKNOWLEDGMENTS
The USGS Forest and Rangeland Ecosystem Sci-
ence Center, Snake River Field Station, US Depart-
ment of Interior Global Climate Change Program, Uni-
versity of California, Riverside, and the Bureau of
Land Management Challenge Cost Share Program
have supported our work on shrubsteppe habitats and
passefine birds. We thank F. Howe (Utah Dept. of
Wildlife), M. Vander Haegen (Washington Dept. of
Fish and Wildlife), and T. Rich (US Bureau of Land
Management) for their discussions on shrubsteppe
birds, and R. Rosentreter (US Bureau of Land Man-
agement), N. West (Utah State University), and J.
Young (USDA Agricultural Research Services) for in-
sights into presettlement conditions of shrubsteppe re-
gions. We appreciate reviews of the manuscript by D.
Dobkin, T Rich, and P. Vickery.
Studies in Avian Biology No. 25:141-157, 2002.
HABITAT FRAGMENTATION EFFECTS ON BIRDS IN SOUTHERN
CALIFORNIA: CONTRAST TO THE "TOP-DOWN" PARADIGM
DOUGLAS T. BOLGER
Abstract. I review the existing literature on habitat fragmentation and its effects on avian populations
in coastal sage scrub and chaparral habitat in coastal southern California. Included in this review is a
consideration of the effect of fragmentation on nest predators, brood parasites, food availability, and
habitat structure and quality. Fragmentation and the creation of edge are extensive in this region. The
primary contemporary fragmenting land-use is residential development. In comparison to forested
landscapes in the East and Midwest, fragmentation in this region seems to cause more isolation in
bird populations. Local extinctions in isolated habitat fragments are common among some species of
the shrub habitat avifauna and colonizations are relatively rare. This difference may be due to more
limited dispersal ability in the year-round residents that are characteristic of this region as compared
to the long-distance migrants in the East and Midwest. Perhaps due to the semi-arid nature of the
region, fragmentation may be accompanied by more habitat degradation than in mesic regions, which
could contribute to the lack of successful colonization. In contrast to studies in the East and Midwest,
the only demographic study of avian edge effects in this system indicates that nest predation and
brood parasitism do not increase near anthropogenically-induced edges. In isolated habitat fragments
mammalian mesopredators appear to undergo "mesopredator release" in the absence of coyotes (Canis
latrans). In habitat fragments the availability of potential arthropod prey is positively related to frag-
ment size and negatively related to fragment age, but does not appear to be a function of distance to
edge. In large habitat blocks, however, the abundance of a number of arthropod taxa is lower near
edges. A particularly striking edge effect is the invasion of non-native Argentine ants along urban
edges. The effect of Argentine ants on native ants is severe but their effect on arthropods that are
more important as avian prey is less clear.
Key Words: Aimophila ruficeps; Argentine ants; bottom-up; edge effects; habitat fragmentation; Li-
nepithema humile; mesopredator release; nest predation; Rufous-crowned Sparrow; southern Califor-
nia; top-down.
Birds display varying degrees of edge and frag-
ment area sensitivity, with abundance of some
species declining sharply with fragment area or
proximity to fragment edge (Blake and Karr
1987, Sould et al. 1988, Robbins et al. 1989a,
Herkert 1994). The mechanisms generating
these sensitivities are often obscure. Since the
principal determinant of avian reproductive suc-
cess is the rate of nest predation (Ricklefs 1969),
most mechanistic studies of the effect of frag-
mentation and edge on birds have focused on
the "top-down" effects of nest predation and
brood parasitism. In fragmented forests in the
East and Midwest of North America nest pre-
dation and brood parasitism on neotropical mi-
grant forest birds has been shown to increase
with proximity to forest edge and with the de-
gree of fragmentation in the landscape (Paton
1994, Robinson et al. 1995a, Donovan et al.
1997, Hartley and Hunter 1998). Avian and
mammalian predators may increase along eco-
tones in response to increased density of nesting
birds attracted to changes in habitat structure
(Gates and Gysel 1978), or to resource subsidies
provided by human land-use (Wilcove 1985,
Andrdn 1992). Because of this, highly frag-
mented landscapes in the Midwest are apparent-
ly population sinks (Pulliam 1988) for some
neotropical migrant bird species. Their persis-
tence in those landscapes appears dependent
upon immigration from large, unfragmented
source areas (Robinson et al. 1995a).
These striking findings have led to the current
"top-down" paradigm in temperate zone frag-
mentation studies. However, generalizations de-
rived from these studies may not apply to other
species, ecosystems, and land-use types (Wiens
1997, Tewksbury et al. 1998). One land-use that
has become increasingly common is urban de-
velopment (Berry 1990, Roodman 1996). As the
world becomes increasingly urban, edge be-
tween urban development and natural habitat in-
creases as does the importance of understanding
the ecological changes that occur at these inter-
faces (Babbitt 1999). Urban/natural edges may
be especially ecologically active due to high in-
puts of materials, water, energy, nutrients, hu-
man commensal species, and high human pop-
ulation density (McDonnell et al. 1993). Only
recently have "bottom-up" effects of habitat
fragmentation on avian food availability re-
ceived attention (Burke and Nol 1998, Zanette
et al. 2000).
In coastal southern California, urban residen-
tial development is currently the principal land-
use that fragments the native shrub habitats,
coastal sage scrub and chaparral. Historically,
agriculture and grazing also contributed to the
141
142 STUDIES IN AVIAN BIOLOGY NO. 25
pattern of fragmentation. There is a conservation
planning effort ongoing for this region (Atwood
and Noss 1994) and the reserve system that re-
suits from this effort will by necessity be set
within an urban matrix. So understanding urban
edge and fragmentation effects will be vital to
the success of this conservation effort.
In this paper I summarize research on the pat-
terns of distribution and abundance of breeding
bird species in these fragmented landscapes and
the ecological mechanisms that shape these dis-
tributions. I first suggest a conceptual framework
describing fragmentation effects and the ecolog-
ical mechanisms that generate these effects.
Original data on bird abundance in the edge and
interior of large habitat blocks in San Diego
County are also presented. Finally, I review the
available literature on fragmentation effects in
this region and assess the evidence for a number
of ecological mechanisms that might generate
the effects. This review is limited to a consid-
eration of species, predominantly passefines,
that have coastal sage scrub and/or chaparral as
one of their principal breeding habitats or occur
in mosaic landscapes with these shrub habitats
and non-native grassland.
METHODS
EDGE AND INTERIOR BIRD SURVEYS
To examine the edge sensitivity of the coastal sage
scrub avifanna, variable distance point counts (Ralph
et al. 1993) were conducted in the spring of 1997,
1998, and 1999 in edge and interior locations of three
large coastal sage scrub habitat blocks in San Diego
County, CA. Details of the sites are available in Mor-
rison and Bolger (2002). For the analyses below, only
detections within 70m of the point count station were
used. Most detections of Common Ravens (see Ap-
pendix for scientific names of vertebrate species) were
beyond 70m so detections up to 150m were allowed
for this species. For most species fly-overs were not
included in the analyses. However, for species for
which most detections were by fly-over, fly-over data
were included if the path of flight intercepted a 70-m
circle around the point count station. These included
Common Raven, Anna's Hummingbird, Costa's Hum-
mingbird, and Western Scrub-Jay.
Point count locations were a minimum of 150m
apart and edge locations were at least 70m from the
urban edge. A total of 24 locations were surveyed in
1997, 15 in 1998, and 31 in 1999. Three eight-minute
counts were conducted per point per year between
March 29 and June 13. To achieve statistical indepen-
dence, locations that were sampled in more than one
year were only used in one year in the analyses, pro-
ducing the final number of locations in Table 1. The
choice of locations included in each yeaifs dataset was
made to maximize sample sizes.
For common species, the mean number of detec-
tions/station]visit was analyzed with two-way ANOVA
with year and treatment (edge vs. interior) as the fac-
tors. For uncommon species, parametric methods were
not appropriate. Instead, the frequency of presence/ab-
sence was analyzed with three-way contingency tables:
present]absent x year x treatment. If a species was
detected at least once at a location in a given year it
was designated present and absent otherwise. The sig-
nificance of the treatment effect (edge vs. interior) was
tested by comparing the chi-square value from the log-
linear model that contained all pair-wise interactions
to a model that did not contain the treatment X present]
absent term. The significance of the treatment pre-
sent]absent term was tested by the difference in chi-
square value between the models using one degree of
freedom.
RESULTS AND DISCUSSION
SOUTHERN CALIFORNIA LANDSCAPES AND
AVIFAUNA
There are five primary terrestrial habitats
within the coastal zone of southern California:
coastal sage scrub, chaparral (mixed and cham-
ise), riparian woodland/scrub, oak woodland,
and non-native grassland (Beauchamp 1986).
The two shrub habitat types, coastal sage scrub
(henceforth CSS) and chaparral, predominate
and most research on habitat fragmentation in
this region has been conducted in those habitats.
The fragmentation studies reviewed below have
been conducted in coastal San Diego County
(predominantly in CSS habitat), the Palos Ver-
des Peninsula in Orange County (CSS), and the
Santa Monica Mountains in Los Angeles County
(chaparral). Most studies cited here were con-
ducted within 20km of the coast, so for the pur-
pose of this review I will define that 20 km band
within these three counties as the coastal south-
ern California region.
Coastal sage scrub is a small-statured com-
munity of subshrubs and shrubs with average
shrub height of 1 m (Mooney 1977) that occurs
below 600m elevation in parts of seven southern
California counties: San Diego, Riverside,
Orange, San Bernardino, Los Angeles, Ventura
and Santa Barbara counties (Davis et al. 1995).
CSS shrubs are thin-leaved and drought-decid-
uous. In contrast, chaparral is composed of
large, woody sclerophyllous, evergreen shrubs
and is geographically more widespread than
CSS. It occurs from the coast to the interior Pen-
insular and Transverse Ranges up to 1500 m el-
evation.
Coastal sage scrub stands show considerable
local (DeSireone and Burk 1992) and regional
(Axelrod 1978, Westman 1981) variation in
structure and fioristics. The most characteristic
elements are Artemisia californica, Eriogonum
fasiculatum, and several Salvia species. Region-
ally, there are at least three recognized subas-
sociations, the southern coastal variety predom-
inantly in San Diego County, the northern coast-
al variety, and the inland variety primarily in
SOUTHERN CALIFORNIA FRAGMENTATION--Bolger 143
Riverside County (Axelrod 1978). Local struc-
tural variation is due to slope, aspect, substrate,
disturbance history, and the influence of non-
native grasses.
Undeveloped landscapes in this region are
mosaics of patches of the native woody com-
munities and non-native grasslands (Mooney
1977, DeSimone and Buck 1992). Near the coast
CSS tends to occur on slopes and generally drier
sites, mixed chaparral on steep north-facing
slopes, and chamise chaparral on mesa-tops.
Disturbance (fire, grazing, and mechanical) con-
tributes to the mosaic because coastal sage scrub
is often a successional community following dis-
turbance to chaparral stands. The arrival of
widespread non-native grasses and herbs may
have exacerbated this patchiness, although there
is disagreement over the pre-European extent of
native grass and herbaceous stands (Minnich and
Dezzani 1998). Frequent or intense fires can
type convert CSS and chaparral to non-native
grassland (Zedler et al. 1983). CSS in particular
is vulnerable to conversion to non-native grass-
land (Minnich and Dezzani 1998).
There are two gradients of note in this region.
First, development, and thus fragmentation, has
been most extensive nearest the coast. Conse-
quently, there is an east-west gradient in habitat
availability and fragment size in the region (see
Figure 2 for an example). There also is a habitat
gradient; coastal sage scrub predominates near
the coast, and chaparral becomes more common
inland and with increasing elevation.
Of the two shrub habitat types, CSS is of
greater conservation concern and has been more
extensively studied for fragmentation effects.
CSS is notable for its restricted range within the
U.S. and high diversity of endemic plants and
animals (Atwood 1993, Atwood and Noss
1994). CSS is widely reported to have declined
to 10-15% of its former range; however, this
percentage is based on a disputed assumption of
the pre-European cover of coastal sage scrub
(Minnich and Dezzani 1998).
There is considerable overlap in the chaparral
and coastal sage scrub avifauna (Miller 1951).
A number of bird species occur in relatively
equal numbers in CSS and chaparral, including
Wrentit, Spotted Towhee, California Towhee,
Sage Sparrow, Bewick's Wren, California
Thrasher, Western Scrub-Jay, Common Bushtit,
Lazuli Bunting, and Anna's and Costa's hum-
mingbirds. Several species usually associated
with chaparral do breed in CSS, particularly
when it is occurs in a mosaic with chaparral,
especially Blue-gray Gnatcatcher and Black-
chinned Sparrow. Only a few species are re-
stricted to coastal sage scrub. The California
Gnatcatcher and Rufous-crowned Sparrow pre-
dominantly breed in CSS, occurring only in
chaparral that is relatively open or disturbed.
Several grassland species occur in open CSS.'
Western Meadowlark, Grasshopper Sparrow,
and Lark Sparrow.
The landscape of coastal southern California
consists of four general elements. (1) The urban
matrix. This land-use is the predominant land-
cover in the region and is characterized by high
density single-family residential development.
Ornamental vegetation ranges from sparse in the
higher density neighborhoods to lush in some of
the older or more affluent neighborhoods. (2)
Isolated habitat fragments (ranging from 1 to
1000ha). Fragments occur throughout most of
the highly developed portion of the landscape.
(3) The edge of large habitat blocks; habitat
within 250m of the urban edge. (4) The interior
of large habitat blocks; habitat greater than
250m from the urban edge. These large habitat
blocks are either embedded in the urban matrix
or are contiguous with the mountainous areas to
the east.
CONSERVATION PLANNING IN THE REGION
Partly in response to petitions at the state and
federal levels to list the California Gnatcatcher
as an endangered species, the state of California
initiated the Natural Communities Conservation
Planning Program (NCCP; Atwood and Noss
1994). The state coordinates subregional plan-
ning processes that prioritize lands based on
conservation value. Private landowners volun-
tarily participate in the planning process. Puta-
tive reserves are identified and funding sought
for acquisition of lands not currently publicly
owned. The eventual listing of the gnatcatcher
as a federally threatened species in 1993 gave
further impetus to the program as participation
in the program gave landowners an avenue to
pursue incidental take permits. Planning occurs
in 11 subregions with the purpose of designating
an interconnected system of reserves, which
should result in no reduction in the ability of the
region to maintain viable populations of target
species (Atwood and Noss 1994). A Central-
Coastal Orange County subregional plan has
been approved, including 37,000 acres of re-
serve, and an MSCP subregional plan in San Di-
ego has been approved that includes 170,000
acres of reserves (see http://ceres.ca.gov/CRA/
NCCP/updates.htm).
CONCEPTUAL FRAMEWORK
Landscape patterns that suggest fragmentation
effects
Conservation biologists often use phrases
such as "the effect of habitat fragmentation on
birds"; however, exactly what these effects of
144 STUDIES IN AVIAN BIOLOGY NO. 25
fragmentation are has been hard to define. Some
of the confusion results from confounding the
patterns of abundance that result from fragmen-
tation with the ecological processes that generate
these patterns. Patterns of abundance or demo-
graphic rates in the landscape are often present-
ed as evidence of the effects of fragmentation.
These patterns fall into the following categories.
(1) Area sensitivity--density, probability of oc-
currence, survival, or reproductive success
change with fragment size, or there is a signifi-
cant difference between those rates in isolated
fragments and in large, unfragmented habitat ar-
eas. (2) Age sensitivity--density, probability of
occurrence, survival, or reproductive success
changes with fragment age (time elapsed since
insularization). (3) Edge sensitivity--density,
probability of occurrence, survival, or reproduc-
tive success changes with proximity to the frag-
ment edge. (4) Distance sensitivity--density or
probability of occurrence changes in habitat
fragments with proximity to other fragments or
large habitat blocks.
No directionality of change is implied in these
definitions to acknowledge that fragmentation
can have positive or negative effects on bird spe-
cies. These are patterns of abundance or demo-
graphic rates in space and time that suggest
these parameters change as a consequence of
fragmentation. Demonstrating a causal relation-
ship between fragmentation and these patterns
requires a consideration of the ecological mech-
anisms that proximally affect rates of birth,
death, immigration, and emigration.
Ecological mechanisms that cause
.fragmentation effects
How are the patterns of fragmentation sensi-
tivity, as defined above, produced in the land-
scape? The ecological consequences of habitat
fragmentation are complex, diverse, and perva-
sive because fragmentation affects animal and
plant populations via a number of interacting
pathways (Wilcove et al. 1986, Robinson et al.
1992, Didham 1997). For example, area effects
are manifest through the initial sampling effect
that determines the initial avian community
(Bolger et al. 1991), and through the effect of
area on population sizes and rates of extinction.
Isolation effects occur when the intervening hu-
man-modified matrix is relatively impermeable
to successful dispersal to isolated patches. This
may result in faunal relaxation in fragments, or
faunal collapse in the extreme of zero recoloni-
zation (Brown 1971, Soul6 et al. 1979). Edge
effects are biotic and abiotic effects derived from
the adjacent human-modified matrix that cause
gradients in light, moisture, and wind velocity,
increased exposure to invasive human commen-
sal species, and increased density of "edge spe-
cies" (Murcia 1995). Island biogeographic treat-
ments of habitat fragmentation focus on the re-
lationship between stochastic extinction and re-
colonization (MacArthur and Wilson 1967,
Brown 1971). However, when fragmentation is
due to the intervention of intense human land
uses, such as urbanization, habitat degradation
due to edge effects and other anthropogenic dis-
turbance are likely to be significant influences
on abundance and extinction rates. The intensity
of edge effects may also depend on the relative
amount of the developed matrix present in the
landscape (Donovan et al. 1997). The direct ef-
fects of area reduction, isolation, and edge can
lead to secondary effects (also called cascading,
community, or trophic effects), whereby the di-
rect effects of fragmentation on predators, par-
asites, competitors, resource species, or mutu-
alists in turn affect species with which these in-
teract. Changes in the abundance of the re-
source, predator, and parasite species that birds
interact with can change bird abundance through
their effect on birth and death rates. Local hab-
itat selection by birds can affect abundance
through changes in immigration and emigration
rates. Birds may avoid habitat in small frag-
ments or adjacent to edges due to structural and
floristic changes in the vegetation and altered
food availability and predator and parasite abun-
dance (Kristan et al. in press). Landscape-scale
habitat selection occurs when birds choose hab-
itat not only on the basis of local habitat con-
ditions but also on the basis of landscape-scale
factors such as patch area, isolation, and edge
proximity. As with local habitat selection this
mechanism would aftct abundance through its
effect on relative immigration and emigration
rates.
Understanding the consequences of fragmen-
tation has been hampered by our inability to iso-
late the effects of these different phenomena on
the biota. These different effects can act in op-
position or in concert. For instance, area and
edge effects can be difficult to separate because
the percentage of edge-affected habitat increases
as fragment area decreases.
FRAGMENTATION PATTERNS IN SOUTHERN
CALIFORNIA
Area and age sensitivity
The resident breeding birds of coastal south-
ern California display varying degrees of sen-
sitivity to fragment size and age. Soul6 et al.
(1988) found that the species richness of a group
of eight shrub habitat bird species (Bewick's
Wren, Spotted Towhee, California Thrasher,
Wrentit, California Quail, Greater Roadrunner,
SOUTHERN CALIFORNIA FRAGMENTATION--Bolger 145
Cactus Wren, and California Gnatcatcher)
showed both area and age effects; richness in-
creased with fragment area (range 0.4-103 ha)
and declined with fragment age (range 2-86
years). Quite small fragments (1-5 ha), if they
were relatively young (<10 years), supported
many species from this group. Species not as
restricted to shrub habitat did not show similar
sensitivity. These fragments range from I km to
15 km from the coast and most were predomi-
nated by coastal sage scrub. Some of the frag-
ments also contained stands of mixed or chamise
chaparral. Although the fragments are predomi-
nantly CSS, Sould et al. (1988) referred to these
generically as "chaparral" habitat fragments fol-
lowing the then popular terms of "soft chapar-
ral" for coastal sage scrub and "hard chaparral"
for mixed and chamise chaparral.
The observed decline in species richness with
fragment age observed by Sould et al. (1988)
implies relaxation or faunal collapse: non-equi-
librium dynamics with local extinctions in ex-
cess of infrequent recolonizations across the ur-
ban matrix (Brown 1971, Sould et al. 1979). The
existence of this extinction-recolonization im-
balance is supported by the observation that spe-
cies richness in the fragments was significantly
lower than that in similar-sized plots in contin-
uous blocks of habitat (Bolger et al. 1991). The
species richness in unfragmented plots is an es-
timate of the species richness initially present in
fragments of a similar size. In a recent resurvey
of the same fragments ten years later, Crooks et
al. (2001) tested the inferences drawn from the
static patterns. Consistent with the relaxation
conclusion, there were approximately twice as
many extinctions (30) as colonizations (12) be-
tween 1987 and 1997 among the original group
of species considered by Sould et al. (1988).
Bolger et al. (1991) demonstrated that the dis-
tribution patterns in these fragments of the five
most common of these species (Bewick's Wren,
Spotted Towhee, California Thrasher, Wrentit,
California Quail) were nested; species in spe-
cies-poor fragments were a non-random subset
of those in species-rich fragments. They con-
cluded that this pattern was generated by a gra-
dient in extinction vulnerability among the spe-
cies. Nested occurrence patterns are common in
real and virtual islands and can be produced by
among-species differences in extinction vulner-
ability (Patterson and Atmar 1986). This pattern
suggested that Wrentit was the most resistant of
the five to extinction, Bewick's Wren and Spot-
ted Towhee were intermediate, and California
Thrasher and California Quail went extinct most
quickly. Consistent with this, Crooks et al.
(2001) found that populations of the Wrentit
were only now going extinct in the smallest/old-
est fragments (5 extinctions, no colonizations).
California Quail, the most sensitive species (9
extinctions, no colonizations), underwent addi-
tional extinctions in several larger fragments
(15-64 ha) as well as a number of small/young
fragments (having apparently already gone ex-
tinct in the smaller/older fragments). California
Thrasher exhibited a similar pattern, going ex-
tinct in four small/young fragments and coloniz-
ing one. The distribution of the Spotted Towhee
changed very little in the intervening years (2
colonizations, no extinctions) and appeared to be
in quasi-equilibrium. Sould et al. (1988) had ap-
parently reached the wrong conclusions about
Bewick's Wren, which appears able to recolo-
nize across the urban matrix, experiencing 6 col-
onizations and only I extinction between 1987
and 1997. In this group of five easily surveyed
species, extinctions outnumbered colonizations
19 to 9. The results of Crooks et al. (2001) also
point out that in this system area-sensitivity can-
not be defined independently of fragment age;
both variables are important predictors of spe-
cies distributions in this fragmented landscape
(Fig. 1).
Lovio (1996) studied fragments in another
part of San Diego and found generally higher
diversity in the same species group considered
by Sould et al. (1988) in similar-sized fragments.
The differing results are probably the result of
differing levels of isolation in the two study ar-
eas. The Sould et al. (1988) and Crooks et al.
(2001) study area was in the western part of the
county and the fragments were generally isolat-
ed canyon fragments embedded in highly devel-
oped coastal mesas. Lovio's study area was
slightly east and south in the Rancho San Diego
area and many of the fragments were portions
of slopes and ridgetops that formed a fairly
dense network of patches (Lovio 1996). The
mean interpatch distances were smaller in Lo-
vio's study area (476 vs. 674 m), and the inter-
vening urban matrix was characterized by a
higher cover of mature ornamental vegetation
(Weser 1996; D. Bolger, pers. obs.). A number
of the fragments were connected to other frag-
ments by narrow habitat strips or areas of dis-
turbed and non-native vegetation (Lovio 1996)
and the set of fragments was immediately adja-
cent to a large unfragmented habitat block. So
the difference between Lovio's results and those
of Sould et al. (1988) may be indicative of the
importance of the degree of fragment isolation
and the permeability of the urban matrix. How-
ever, Lovio did not ascertain the age of frag-
ments, so differing fragment ages could also be
responsible for the differences between the stud-
ies.
146 STUDIES IN AVIAN BIOLOGY NO. 25
A Wrentit B Spotted Towbee
C California Thrasher
FIGURE 1. Graphical results of multiple logistic regression of the presence/absence of (A) Wrentit, (B) Spotted
Towhee, and (C) California Thrasher on fragment area and age. Area sensitivity is a function of fragment age.
Larger fragment area is required for persistence in older fragments. From Crooks et al. (2001).
Edge sensitivity
Bolger et al. (1997) analyzed the patterns of
abundance of the 20 most common breeding
bird species in a 260 sq. km landscape in coastal
San Diego County (Fig. 2). This landscape en-
compassed a land-use gradient that included the
interior of a large unfragmented habitat block,
its edge, and isolated fragments in the adjacent
urban matrix. For 14 of the 20 species, the fit of
logistic regression models to bird abundance
was improved by the addition of landscape met-
rics to models containing variables describing
local habitat conditions. These landscape metrics
described the percentage of CSS and chaparral
habitat versus developed land and the amount of
urban area and the amount of urban edge in the
larger landscape (250 m to 3 km) around each
sample point. Based on these analyses and a ca-
nonical correspondence analysis, the 20 species
were characterized as edge/fragmentation-insen-
sitive (10 species), edge/fragmentation-reduced
(6 species) or edge/fragmentation-enhanced (4
species). The finding that half of the common
species appear to respond to larger-scale patterns
of edge and fragmentation suggests that land-
scape structure is a significant determinant of
bird abundance in this region.
One surprising result of this study was the el-
evated abundance of urban-exploiting birds
some distance into the non-fragmented habitat
block. The abundances of House Finch, Anna's
Hummingbird (Fig. 2b), Northern Mockingbird,
and Lesser Goldfinch, species common in the
urban matrix, were higher in habitat adjacent to
the urban edge than further into the patch inte-
rion The region of higher density extended as
far as a kilometer in Anna's Hummingbird and
House Finch. These results suggest that the ur-
ban matrix could be a net source of these spe-
cies, elevating densities in natural habitat adja-
cent to the matrix.
In chaparral habitat in the Santa Monica
Mountains, Sauvajot et al. (1998) found no cor-
relation between bird abundance and proximity
to the urban edge. They also found that bird
abundance did not respond to disturbance-in-
duced changes in vegetation structure. In con-
trast, in inland CSS Kristan et al. (in press) ob-
served strong correlations between bird abun-
dance and edge-proximity that was specifically
SOUTHERN CALIFORNIA FRAGMENTATION--Bolger 147
FIGURE 2. The landscape distribution patterns of
(A) Rufous-crowned Spaow and (B) Anna's Hum-
mingbird within a 260 2 study area in coastal San
Diego County. Presence/absence denotes either detec-
tion or non-detection in a single 8-min point count at
each of 202 random locations during the spring of
1993. White eas e the undeveloped habitat mosaic
of coastal sage scrub and chapal. Stippling repre-
sents residential and coercial development. From
Bolger et al. 1997.
associated with edge-related changes in habitat
quality based on known, independent relation-
ships to vegetation composition and structure.
The lack of a correlation of disturbance to edge
proximity in chaparral may have to do with the
differing physical structure of chaparral and CSS
vegetation. Dense and robust, chaparral proba-
bly rebuffs direct human disturbance along edg-
es better than the smaller statured coastal sage
scrub.
In the only demographic study of edge sen-
sitivity in this region I am aware of (Morrison
and Bolger 2002), no difference was found in
breeding success of Rufous-crowned Sparrows,
a ground-nesting year-round resident species,
between edge and interior plots. Total reproduc-
tive output and daily nest predation rate did not
differ between pairs in habitat adjacent to urban
development (<200 m from the urban edge) as
compared to those a minimum of 500 m from
urban edge during the 1997-1999 breeding sea-
sons. P. Mock (peTs. comm.) reported similar re-
sults with California Gnatcatchers at one site in
San Diego.
EDGE SENSITIVITY
Of 21 species common enough for analysis,
11 differed significantly in abundance between
edge and interior plots in CSS in 1997-1999
(Table 1). Anna's Hummingbird, House Finch,
Northern Mockingbird, and Western Scrub-Jay
were significantly more abundant in edge loca-
tions. Common Raven showed a trend of higher
abundance in edges, but its abundance was high-
ly variable and the treatment effect was non-sig-
nificant. Black-chinned Sparrow, California To-
whee, Common Bushtit, Lazuli Bunting, Ru-
fous-crowned Sparrow, Spotted Towhee, and
Wrentit were significantly less abundant along
edges. California Thrasher showed a consistent,
but non-significant, trend of lower abundance
along edges. In a similar study, Kristan et al. (in
press) noted significant negative edge relation-
ships for California Towhee, California Thrash-
er, and Sage Sparrow, and significant positive
effects for Northern Mockingbird and European
Starling.
PATTERNS OF LANDSCAPE SENSITIVITY IN THE
COASTAL SOUTHERN CALIFORNIA AVIFAUNA
I categorized patterns of landscape sensitivity
in the CSS avifauna through a consideration of
three factors: (1) area sensitivity, (2) edge sen-
sitivity, and (3) ability to exploit the urban ma-
trix (Table 2). The area sensitivity designations
are approximate and not quantitative estimates.
Area sensitivity in this system certainly depends
on fragment age (Crooks et al. 2001) and pos-
sibly on isolation (Lovio 1996), so a simple cat-
egorization is not possible. The two categories
(10-20 ha and 100-200 ha) represent a quali-
tative contrast of area sensitivity for patches of
CSS between 20 and 60 years old and isolated
by at least 500 m of residential development.
Species categorized as sensitive to fragmentation
at the scale of 10-20 ha are often found in frag-
ments of this size but have been shown to ex-
perience local extinction (Sou16 et al. 1988, Bol-
get et al. 1991, Crooks et al. 2001). Species cat-
egorized as having 100-200 ha area sensitivity
are generally absent or rare in fragments smaller
than that size range (Lovio 1996, Bolger et al.
1997; D. Bolger et al., unpubl. data; K. Crooks
et al., unpubl. data). Edge sensitivity was de-
rived from a consideration of the relative abun-
dance of species in the interior and near the edge
(<250m from urban edge) of large habitat
blocks (Fig. 2, Table 1; Bolger et al. 1997). The
148 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 1. MEAN NUMBER OF DETECTIONS (STANDARD ERROR) WITHIN 70 M OF POINT COUNT STATIONS IN EDGE
AND INTERIOR LOCATIONS 1N 1997--1999
1997 1998 1999
F or
Edge Interior Edge Interior Edge Interior Chi-squar½ P
N 10 9 7 7 11 7
California Quail 0.20 0.11 0.29 0.30 0.48 0.43 0.57 0.45
(0.11) (0.11) (0.17) (0.14) (0.15) (0.25)
Mourning Dove 0.00 0.00 0.10 0.22 0.15 0.12 2.22 0.15
(0.00) (0.00) (0.10) (0.08) (0.09) (0.08)
Costa's Hummingbird 0.42 0.17 0.05 0.36 0.61 0.57 0.06 0.82
(0.13) (0.09) (0.03) (0.11) (0.18) (0.26)
Anna's Hummingbird a 1.48 1.00 0.97 0.72 1.52 1.01 5.69 0.021
(0.17) (0.17) (0.28) (0.24) (0.17) (0.15)
Western Scrub-Jay 0.10 0.09 0.24 0.00 1.00 0.05 4.79 0.03
(0.07) (0.06) (0.17) (0.00) (0.32) (0.05)
Common Raven 0.48 0.20 0.72 0.25 1.00 0.13 0.93 0.37
(0.14) (0.17) (0.29) (0.14) (1.00) (0.10)
Common Bushtit a 1.20 1.28 0.74 1.34 0.88 0.86 0.99 0.033
(0.28) (0.29) (0.34) (0.36) (0.22) (0.28)
Bewick's Wren 0.28 0.33 0.07 0.04 0.75 0.42 1.83 0.16
(0.09) (0.15) (0.05) (0.04) (0.15) (0.14)
Northern Mockingbird 1.00 0.19 0.61 0.03 0.26 0.05 6.82 0.009
(0.29) (0.08) (0.22) (0.03) (0.10) (0.05)
California Thrasher 0.15 0.24 0.22 0.45 0.08 0.27 1.23 0.30
(0.06) (0.11) (0.09) (0.14) (0.04) (0.17)
Wrentit a 0.55 1.28 0.65 1.40 0.51 0.85 13.23 <0.001
(0.18) (0.17) (0.18) (0.24) (0.18) (0.31)
California Gnatcatcher 0.08 0.17 0.11 0.08 0.03 0.05 0.36 0.60
(0.06) (0.07) (0.07) (0.08) (0.03) (0.05)
Lesser Goldfinch 0.30 0.52 1.42 0.77 0.76 1.13 0.84 0.37
(0.16) (0.20) (0.59) (0.25) (0.26) (0.28)
House Finch 1.90 0.22 1.36 0.14 1.64 0.10 20.91 <0.001
(0.50) (0.15) (0.66) (0.14) (0.29) (0.06)
Lazuli Bunting 0.00 0.15 0.06 0.92 0.00 0.29 14.36 <0.001
(0.00) (0.11) (0.04) (0.36) (0.00) (0.11)
Spotted Towhee a 0.80 0.74 0.42 0.98 0.36 1.01 6.25 0.016
(0.20) (0.20) (0.13) (0.24) (0.12) (0.21)
California Towhee a 2.32 2.81 2.11 2.32 1.64 1.64 0.65 0.042
(0.37) (0.41) (0.36) (0.24) (0.32) (0.38)
Rufous-crowned Sparrow a 0.78 1.17 1.80 3.08 0.23 1.14 15.86 <0.001
(0.14) (0.17) (0.23) (0.49) (0.08) (0.38)
Black-chinned Sparrow 0.03 0.15 0.00 0.12 0.00 0.17 7.36 0.008
(0.03) (0.08) (0.00) (0.07) (0.00) (0.11)
Lark Sparrow 0.00 0.17 0.00 0.08 0.00 0.00
(0.00) (0.09) (0.00) (0.06) (0.00) (0.00)
Grasshopper Sparrow 0.10 0.06 0.11 0.03 0.00 0.05 0.46 0.50
(0.10) (0.06) (0.11) (0.03) (0.00) (0.05)
a Data from these species were analyzed with 2-way ANOVA; all others were analyzed wi0 three-way contingency tables (see METHODS).
urban-exploiter category includes species that
occur in the urban matrix during the breeding
season as determined by Lovio (1996) and K.
Crooks et al. (unpubl. data). This list includes
the species likely to be found in areas of rela-
tively dense, single-family dwellings that sup-
port moderate densities of ornamental vegeta-
tion. The list of urban-exploiters would probably
differ if higher- or lower-density development
were considered (Blair 1996). Based on a con-
sideration of these three factors I placed species
into three categories: (1) species that appear
strongly negatively affected by fragmentation in
the landscape, (2) species that appear moderate-
ly negatively affected by fragmentation, and (3)
species that appear positively affected or neutral
(Table 2).
Species in the first category, strongly nega-
tively affected, are generally found only in the
largest habitat blocks remaining in the region.
These species do not occur in the urban matrix,
generally have reduced abundance near urban
edges (Table 1; Bolger et al. 1997), and are ex-
tremely rare in smaller fragments (K. Crooks et
SOUTHERN CALIFORNIA FRAGMENTATION--Bolger 149
¸ ¸
ZZZZZZZZ
150 STUDIES IN AVIAN BIOLOGY NO. 25
al., unpubl. data). They are a mixture of resident
and migrant species. This is the most problem-
atic category because the fewest data are avail-
able and alternative explanations for the land-
scape patterns of these species need further in-
vestigation. Many of these species are primarily
grassland or chaparral species that often occur
within the coastal habitat mosaic in open CSS
habitat and grassland/CSS ecotones or CSS/
chaparral ecotones. Their patterns of abundance
could reflect the distribution of these less com-
mon habitat elements that may be distributed
non-randomly with respect to fragment size or
edge proximity.
Lark Sparrows, Grasshopper Sparrows, and
Western Meadowlarks are primarily associated
with grassland but reliably occur in open coastal
sage scrub habitat in large habitat blocks. CSS
in habitat fragments is generally open, often
with a continuous understory of non-native
grasses. But these species are rarely present in
fragments. Lesser Nighthawks occur in both
chaparral and CSS, but require bare ground on
mesa tops for breeding and are rare in fragments
(Lovio 1996).
Interpretation of the distribution of some of
these species, particularly those primarily asso-
ciated with chaparral, is complicated by histor-
ical distribution patterns. The Blue-gray Gnat-
catcher and the Black-chinned Sparrow were
historically rare in the immediate vicinity of the
coast (Unitt 1984), possibly due to an east-west
gradient in the cover of chaparral habitat. So
their rarity in fragments closest to the coast may
not be due to fragmentation sensitivity. Of
course, it is possible that those historical patterns
already reflected the effects of earlier, agricul-
turally-induced habitat fragmentation. Lovio
(1996) found the Blue-gray Gnatcatcher in his
unfragmented control area, but it was absent
from all but the largest fragments in the imme-
diately adjacent landscape. The Black-chinned
Sparrow does show edge- (Table 2; Bolger et al.
1997) and area-sensitivity (Lovio 1996) within
its historical range.
Bolger et al. (1997) found that as a group the
Rufous-crowned Sparrow, Lark Sparrow, Black-
chinned Sparrow, Sage Sparrow, Western Mead-
owlark and Costa's Hummingbird displayed an
edge-sensitive abundance pattern even when the
three habitat types they examined (chamise
chaparral, CSS, and mixed chaparral) were con-
sidered separately. However, when analyzed in-
dividually with regard to habitat, the distribution
of Sage Sparrows and Western Meadowlarks
suggested their pattern may be driven by the
spatial distribution of habitat types. The other
four species did display reduced abundance in
appropriate habitat near edges. Bolger et al.
(1997) found Sage Sparrows to be associated
with chamise chaparral in their study area, but
they also occur in CSS (Unitt 1984, Lovio
1996). Lovio (1996) found Sage Sparrows only
in the two largest CSS fragments (>150 ha) in
his study area.
The species in this group whose pattern most
compellingly suggests fragmentation-sensitivity
is the Rufous-crowned Sparrow. It is abundant
and ubiquitous in unfragmented habitat, but less
abundant near edges (Table 1) and rare in iso-
lated habitat fragments (Fig. 2; Bolger et al.
1997; K. Crooks et al., unpubl. data).
I suspect that the distribution of most of the
species in this category are determined at least
in part by patterns of fragmentation and edge.
Yet because of their idiosyncratic distributions
and habitat affinities it will be difficult to dem-
onstrate this conclusively. Kristan et al. (in
press) constructed interior-based habitat associ-
ation models for a suite of CSS species using
data collected from >200 points throughout
southern California. They then applied each
model to a new set of points surveyed along an
explicit edge-to-interior gradient. Habitat quality
(as indexed by predicted probability of a species
occurrence at a point) varied significantly for the
eight species analyzed (Cactus Wren, California
Towhee, California Gnatcatcher, California
Thrasher, Sage Sparrow, Western Scrub-Jay,
Northern Mockingbird, European Starling). In-
terestingly, Sage Sparrows and California
Thrashers were significantly reduced at edges
despite the presence of suitable habitat. Clearly
the distribution of these species requires closer
examination for evidence of processes produc-
ing fragmentation sensitivity. Despite the uncer-
tainties, it is prudent at this time to consider
these species very sensitive to fragmentation.
The second category is comprised of species
that show area sensitivity in the range of 10-20
ha. A number of these species have been shown
to undergo local extinction in habitat fragments
(Soulfi et al. 1988, Bolger et al. 1991, Crooks et
al. 2001). They generally occur at lower abun-
dance in habitat fragments than in unfragmented
habitat (K. Crooks et al., unpubl. data). Some of
the species show edge sensitivity, others are
neutral with regard to edge (Table 1; Bolger et
al. 1997). These are generally resident species
and are among the common and distinctive spe-
cies of these habitats. They appear to be shrub
habitat generalists occurring abundantly in both
CSS and chaparral (Bolger et al. 1997). Most of
these species are rarely observed in the urban
matrix; however, K. Crooks et al. (unpubl. data)
found Costa's Hummingbird to be reasonably
abundant in the urban matrix and detected Spot-
SOUTHERN CALIFORNIA FRAGMENTATION--Bolger 151
ted Towhee and Bewick's Wren there at very
low abundance.
The species categorized as neutrally or posi-
tively affected by fragmentation are all urban
exploiters. They reside and breed within devel-
oped habitats in San Diego as well as other dis-
turbed habitats (Unitt 1984; D. Bolger, pers.
obs.). All display positive or neutral edge re-
sponses (Table 1; Bolger et al. 1997). They vary
in abundance in unfragmented habitat and none
display obvious area sensitivity; in fact most are
more abundant in fragments than in unfrag-
mented habitat (K. Crooks et al., unpubl. data).
MECHANISMS CAUSING FRAGMENTATION EFFECTS
IN SOUTHERN CALIFORNIA
Isolation and dispersal limitation
There is currently no direct measure of the
ability of most of the species listed in Table 2
to disperse through the urban matrix. However,
there is a good deal of correlative evidence for
some of the fragmentation-sensitive species that
suggests their ability to disperse across the urban
matrix is constrained relative to fragmentation-
tolerant species.
The relative inability of these species to col-
onize across the urban landscape is supported by
the lack of a relationship between degree of
fragment isolation and the distribution of these
species. Soul6 et al. (1988) found no relationship
between fragment isolation and species richness.
Crooks et al. (2001) analyzed single species dis-
tributions and found only Bewick's Wren's oc-
currence to be significantly positively correlated
with proximity to other fragments. This is con-
sistent with its ability to recolonize fragments,
and its occasional detection in the urban matrix
(Crooks et al. 2001). Lovio (1996) did find an
effect of isolation on species richness; this dif-
ference is likely due to the factors mentioned
earlier, smaller interpatch distances and a more
permeable matrix in his study area. Taken to-
gether the results of Lovio (1996) and Soul6 et
al. (1988) suggest a threshold of isolation and
matrix permeability below which dispersal is an
important influence on distributions. Bolger et
al. (2001) demonstrated that a group of frag-
mentation-sensitive species (category 2 species)
occurred much less frequently in narrow, linear
habitat features (ca. 60 m wide and 250 m long)
than a group of fragmentation-tolerant species
(category 3 species), suggesting the sensitive
species have more stringent corridor require-
ments and that their movements through the ur-
ban matrix are more constrained.
One of the striking features of Table 2 is the
ahnost complete correlation of fragmentation-
sensitivity with the inability to exploit the urban
matrix. This is consistent with the urban matrix
as a dispersal barrier for the fragmentation-sen-
sitive species. Clearly, the urban matrix does not
provide a barrier to the species that are able to
reside there, and in general these species do not
show fragmentation sensitivity.
The available evidence suggests that at least
in part, fragmentation-sensitive patterns of mem-
bers of the shrub avifauna are due to the isolat-
ing effects of the urban matrix. The matrix is
not necessarily a complete barrier to dispersal
but it appears to reduce colonization rates below
extinction rates for a number of species (Crooks
et al. 2001). More direct tests of this hypothesis
in the form of dispersal studies or experimental
introductions to unoccupied patches are needed.
Two studies have documented dispersal of
banded California Gnatcatchers through frag-
mented landscapes. A banded juvenile was de-
tected 1.3 km from its natal patch, having had
to cross a lightly developed landscape of large
wooded house lots and parkland (Atwood et al.
1995 cited in Bailey and Mock 1998). Bailey
and Mock (1998) also document a number of
dispersal events in a heterogeneous landscape in
San Diego. A number of these apparently oc-
curred from a large block of habitat through an
archipelago of fragments separated by blocks of
development up to 1 km wide. This study was
conducted in the same landscape as Lovio
(1996) with dense ornamental vegetation and
sufficient relief to often provide line-of-sight be-
tween patches of habitat. This probably facili-
tates inter-patch movement. So although the Cal-
ifornia gnatcatcher does show area sensitivity,
this may be more related to its large territory
requirements (Preston et al. 1998) rather than a
strict inability to recolonize isolated fragments.
However, even though dispersal through the ur-
ban matrix is possible, colonization rates could
still be in excess of extinction rates for this spe-
cies.
Edge effects: habitat degradation/local habitat
selection
Fragmentation and the creation of urban edge
exposes CSS and chaparral habitat to increased
levels of human-induced disturbance. The effect
of increasing disturbance in the form of me-
chanical damage, fire, and exotic plant invasion
on vegetation and birds in habitat fragments has
not been thoroughly described. Alberts et al.
(1993) found that fragments lose native shrub
cover through time and native plant diversity de-
clines while exotic plant diversity increases. Dis-
turbance opens up the vegetation in fragments
by causing internal fragmentation with stands of
shrubs becoming separated by non-native grass-
es and forbs.
152 STUDIES IN AVIAN BIOLOGY NO. 25
The effect of disturbance-induced changes in
vegetation structure on bird communities has not
been well-studied in this region. Sauvajot et al.
(1998) found that chaparral bird species abun-
dance did not respond to disturbance-induced
changes in vegetation structure in chaparral,
whereas Kristan et al. (in press) observed sig-
nificant changes in vegetation, as well as "hab-
itat," in CSS. Bird species clearly assort along
a gradient of shrub density from grassland to
open CSS to dense CSS and chaparral (Cody
1975, Bolger et al. 1997). By decreasing shrub
cover, disturbance should move the bird com-
munity along this gradient. However, the rela-
tionship of this avifauna to disturbance-induced
changes in shrub vegetation structure needs fur-
ther quantification.
The effect of invasive non-native annual
plants has been severe on coastal sage scrub and
may be exacerbated by fragmentation. Coastal
sage scrub has been exposed to several waves
of grass and herbaceous invaders from the Med-
iterranean and Middle East beginning with spe-
cies introduced by missionaries in the mid to late
1700s (Mooney et al. 1986, Minnich and Dez-
zani 1998). Most prominent among these invad-
ers are grasses in the genera Avena and Bromus,
and the annual forb Brassica nigra. These plants
may invade as a consequence of soil disturbance
and intense or frequent fires, and can invade un-
disturbed CSS from nearby disturbed areas
(Zink et al. 1996). Once established these an-
nuals resist native shrub recruitment (Eliason
and Allen 1997). The increase in annual biomass
increases rates of nutrient cycling (Jackson et al.
1988) and these annuals may decrease fire in-
tervals by increasing fine fuel availability (Zed-
ler et al. 1983).
Coastal sage scrub and chaparral are stable
with fire intervals of ten years or more, but de-
grade to non-native grassland under more fre-
quent fires or particular intense fires (Zedler et
al. 1983). Both chaparral and CSS shrubs re-
sprout after fire although resprouting is more
complete in chaparral species. Germination from
seed caches (Salvia spp.) or germination of
small wind-dispersed seeds (Eriogonum fasci-
culatum, Artemisia californica) is a more im-
portant source of recovery in CSS shrubs than
in chaparral species. Frequent fires can deplete
the seed bank and stored carbohydrates of root-
sprouting species and cause a vegetation type-
conversion to non-native grassland.
Non-native invasion is among the most seri-
ous threats to the conservation of native plant
and animal communities in this region. For ex-
ample, Minnich and Dezzani (1998) compared
historical vegetation data (1929-1934) to recent
survey data and concluded that loss of shrub
cover of coastal sage scrub shrubs has been ex-
tensive in the Perris Plain of Riverside County.
Modal shrub cover loss at 78 sites was 40%.
This was particularly true on north-facing
slopes, which supported high densities of non-
native grasses (Bromus spp.). Loss of shrub cov-
er occurred even in the absence of fire and graz-
ing, suggesting a competitive exclusion by the
non-native grasses, perhaps through competition
for moisture (Minnich and Dezzani 1998).
A landscape analysis of the effect of frag-
mentation and edge on disturbance regimes in
this region has not been attempted. Fragmenta-
tion and the creation of edge should increase the
exposure of native plant communities to hu-
mans, exotic invaders, fire, and mechanical dis-
turbance. It seems likely that habitat fragmen-
tation has enhanced plant invasions by disturb-
ing the native shrub vegetation and providing
colonization sources of the exotic species. For
example, Zink et al. (1996) documented the in-
vasion of undisturbed coastal sage scrub by non-
native annuals from a disturbed pipeline right-
of-way. Although the effects of non-native an-
nual plant invasion on native grasses, shrubs,
and nutrient cycling have been examined, their
effects on higher trophic levels has received lit-
tle attention. The alteration of the physical struc-
ture of CSS and chaparral habitat, and changes
in seed and arthropod food resources, could af-
fect higher trophic levels including birds.
Landscape-scale habitat selection--patch size
and isolation
Feasible observations and experiments to test
this hypothesis are elusive, so the only support
for this mechanism would be lack of evidence
for other mechanisms. This mechanism is per-
haps most feasible for the migrant species that
would not be expected to have difficulty dis-
persing across the urban matrix (e.g., Lazuli
Bunting). However, this hypothesized mecha-
nism remains speculative.
Secondary effects: top-down--predation and
brood parasitism
Morrison and Bolger (2002) found no evi-
dence to suggest that the landscape pattern of
the Rufous-crowned Sparrow results from top-
down effects near edges. Nest predation rates
and breeding productivity did not differ between
edge and interior areas. The predation result is
surprising considering that some putative nest
predators (e.g., Western Scrub-Jays and Com-
mon Ravens, Table 1; California ground squir-
rels, D. Bolger, pers. obs.) are more abundant
along edges. Video surveillance and direct ob-
servation documented ten predation events, nine
of which were by snakes (seven by California
SOUTHERN CALIFORNIA FRAGMENTATION--Bolger 153
kingsnakes, two by gopher snakes), suggesting
that snakes are the principal predator on Rufous-
crowned Sparrow nests. The rate at which
snakes were encountered by field workers was
equivalent in edge and interior areas (Morrison
and Bolger 2002).
Top-down changes may be important in iso-
lated habitat fragments. Crooks and Sould
(1999) found evidence for mesopredator release
in fragments lacking coyotes. They report that
the abundance of mesopredators (gray fox, opos-
sum, striped skunk, and domestic cat), as re-
vealed by track stations and scat transects, is
negatively correlated with coyote abundance (af-
ter accounting for the potential confounding ef-
fects of area, age, and isolation). Moreover, me-
sopredator activity is also higher at times when
coyote activity is lower. They found a significant
positive correlation between the species richness
of shrub-specialist birds and coyote presence
and conclude that the presence of coyotes en-
hances survival and reproduction of these birds
through the suppression of mesopredators. Bird
species richness showed a non-significant nega-
tive trend with increasing mesopredator abun-
dance.
Crooks and Soulfi (1999) also presented evi-
dence that the effect of coyotes on domestic cats
is particularly marked. Their radio-collared cats
often were killed by coyotes, 21% of coyote scat
examined contained cat remains, and 46% of cat
owners surveyed said they restricted their cats'
activities when coyotes were present. The effects
of cats can be severe. Based on owner surveys
they estimate that a 20-ha fragment would be
subject to predation by 35 outdoor cats that to-
gether would bring a total of 525 bird prey items
to their owners each year. The authors do not
report whether the prey items are predominantly
common urban species or species residing pre-
dominantly in natural habitat.
Brown-headed Cowbirds have been shown to
be another important top-down influence in frag-
mented forest habitat. However, they do not
seem to be as significant an influence in frag-
mented coastal sage scrub vegetation (Ellison
1999). In four years (342 nests, Riverside and
San Diego counties) in edge and interior habitat,
S. Morrison and D. Bolger (2002; unpubl. data)
found no brood parasitism by Brown-headed
Cowbirds on Rufous-crowned Sparrows. In two
years (same Riverside County site as Morrison
and Bolger) Ellison (1999) observed cowbird
parasitism in only 3 of 217 nests of Spotted and
California towhees and Sage and Rufous-
crowned sparrows collectively. Cowbirds were
detected in my edge point counts in San Diego,
but only infrequently.
In this region, the habitat in which cowbirds
are consistently a significant problem is riparian
woodland. The endangered Least Bell's Vireo is
significantly affected by cowbirds (Kus 1999) as
have been other riparian breeding birds. This
habitat is naturally patchy, but habitat loss due
to development has increased the patchiness as
well as patch isolation, and has exposed the hab-
itat to a variety of disturbances. Because breed-
ing habitat for riparian species occurs in rela-
tively small, discrete patches, it has been pos-
sible to reduce the local density of cowbirds
through trapping programs and reduce parasit-
ism on the Least Bell's Vireo (Kus 1999).
Braden et al. (1997) reported that 32% of Cal-
ifornia Gnatcatcher nests suffered cowbird par-
asitism in coastal sage scrub habitat in south-
western Riverside County. Parasitism rates were
not analyzed with respect to patch size or dis-
tance to edge so it is not possible to interpret
these data with regard to fragmentation. How-
ever, at least two of Braden's study areas were
adjacent to lakes that are fringed by riparian
vegetation, which may have attracted the cow-
birds (see below). Grishaver et al. (1998) found
much lower rates (2%) of parasitism on gnat-
catchers at a site in San Diego.
Cowbirds are noted for their large home rang-
es and the extensive distances they will fly be-
tween feeding, roosting, and host nesting areas
(Thompson 1994, Robinson et al. 1995a). It is
likely then that their abundance in southern Cal-
ifornia is related to factors distributed at a land-
scape or regional scale. The effect of urban frag-
mentation on cowbird abundance is unknown. If
cowbirds can exploit resources in the urban ma-
trix, such as seed from feeders, the urban land-
scape may be highly permeable to them and may
enhance cowbird abundance in riparian areas
that abut residential development. Further re-
search on the landscape correlates and determi-
nants of cowbird abundance in this region is
needed.
Secondary effects: bottom-up
The effect of habitat fragmentation on bird
food resources has been relatively understudied
(Burke and Nol 1998, Robinson 1998). Bolger
et al. (2000) found complex relationships be-
tween arthropods and fragment size, age, and
edge proximity. Arthropods dwelling on Cali-
fornia buckwheat (Eriogonum fasiculatum) gen-
erally decline in abundance and point diversity
with decreasing fragment size and increasing
fragment age. Thus food availability for foliage
gleaners foraging on buckwheat is potentially
lower in smaller and older fragments.
Reponses of the ground-dwelling arthropods
are more varied, but are generally similar to the
shrub insects. Interestingly, ground spiders in-
154 STUDIES IN AVIAN BIOLOGY NO. 25
crease in abundance and point diversity with de-
creasing area and increasing age (Bolger et al.
2000). The most abundant ground arthropods in
habitat fragments are common non-native spe-
cies: sowbug (Armadillidium vulgare), European
earwig (Forficula auriculatum), and oriental
cockroach (Blatta orientalis). There did not
seem to be large differences between the edge
and interior in the abundance and diversity of
ground or shrub arthropods.
In contrast, ground arthropods are generally
less abundant in the edge than the interior of
large habitat blocks in San Diego (D. Bolger,
unpubl. data). Grasshoppers, mites, spiders,
jumping bristletails, and native ants were signif-
icantly less abundant in edge plots than in inte-
rior plots. Beetles, bees and wasps, and flies did
not differ between edge and interior plots. No
arthropod order was significantly more abundant
in edge plots than in interior plots.
The arthropod taxa most vulnerable to frag-
mentation and edge are the native ants. In San
Diego, the non-native Argentine ant (Linepithe-
ma humile) invades coastal sage scrub habitat
from urban edges (Suarez et al. 1998). In iso-
lated habitat fragments (Suarez et al. 1998) and
in edge areas of large habitat blocks (D. Bolger,
unpubl. data), the abundance and diversity of na-
tive ants is strongly negatively correlated with
the abundance of the Argentine ant. Argentine
ants are invasive human commensals and have
become established in Mediterranean climates
worldwide (Majer 1994). They have been im-
plicated in the decline of native ants in a number
of locations (Erickson 1971, Ward 1987, Majer
1994, Holway 1995, Cammell et al. 1996, Hu-
man and Gordon 1996). Argentine ants possess
interference and exploitative competitive advan-
tages over native California ants (Human and
Gordon 1996, Holway et al. 1998, Holway
1999) and have higher worker densities possibly
due to reduced intraspecific competition (Hol-
way et al. 1998).
Several lines of evidence suggest that the
availability of water from irrigation and runoff
may allow the Argentine ants to invade along
edges, and moisture limitation may prevent their
invasion of undisturbed interior areas. Tremper
(1976) found Argentine ants more vulnerable to
desiccation than most native California ants.
Also, Argentine ants are able to invade riparian
habitat, but only if water flows year-round (Hol-
way 1998a).
Argentine ants are generally smaller than the
native ant species they replace, suggesting that
they may not be adequate replacements in the
diet of ant-eating birds and lizards. Suarez et al.
(2000) demonstrated that the ant-specialist
coastal horned lizard showed a strong prey pref-
erence for native ants over the Argentine ant.
Ants frequently appear in lists of prey consumed
by ground-foraging birds, but their relative die-
tary importance is unclear. Several studies have
reported negative correlations of Argentine ants,
or other exotic ants, with non-ant arthropods
(Porter and Savigno 1990, Cole et al. 1992, Hu-
man and Gordon 1997, Bolger et al. 2000),
while others have found no relationship (Holway
1998 b). Bolger et al. (2000) found significant
partial negative correlations between the abun-
dances of Argentine ants and several non-ant ar-
thropod taxa. The magnitude of the correlations,
however, were generally small suggesting the ef-
fect of Argentine ants on non-ant arthropods is
less severe than their effect on native ants.
Taken together these studies demonstrate that
arthropod communities change greatly with
fragmentation and edge. In general arthropod
abundance and diversity declines in isolated
fragments and near the edge of large habitat
blocks. Unfortunately, at this time we do not
know how these changes in arthropod commu-
nities affect bird foraging, reproductive success,
and habitat selection.
CONCLUSIONS
The studies reviewed indicate that a signifi-
cant portion of the avifauna of coastal sage scrub
and chaparral habitats in coastal southern Cali-
fornia display patterns of abundance that suggest
sensitivity to edge and fragmentation caused by
urban development. Area, age, and edge sensi-
tivity in bird abundance and presence/absence
have been demonstrated in a broad spectrum of
the avifauna (Table 1; Soul et al. 1988, Lovio
1996, Bolger et al. 1997, Crooks et al. 2001).
However, so little research has been conducted
on mechanisms that it is difficult at this time to
generalize about the forces shaping these distri-
butions. Area exerts an influence through an ini-
tial sampling effect (Bolger et al. 1991). It may
also affect extinction rates through its effect on
population size; extinction rates are higher in
smaller fragments (Crooks et al. 2001). The
available evidence suggests that elevated pre-
dation and parasitism along edges are not in-
volved (Morrison and Bolger 2002; P. Mock,
pers. comm.). Correlational evidence suggests
mesopredator release affects bird species persis-
tence in isolated habitat fragments. However, an
effect of mesopredator abundance on nest pre-
dation rate or adult or juvenile survival has yet
to be demonstrated. Arthropod community com-
position and abundance varies strongly with
fragmentation and edge suggesting that food
availability could play a role in shaping these
abundance patterns (Suarez et al. 1998, Bolger
et al. 2000; D. Bolger, unpubl. data).
SOUTHERN CALIFORNIA FRAGMENTATION Bolger 155
The characteristics of the urban matrix and
bird species responses to it may be very impor-
tant. Dispersal limitation imposed by the urban
matrix may explain area sensitivity in many
fragmentation-sensitive species. Extinction rates
of fragmentation-sensitive species exceeded col-
onization rates in fragments (Crooks et al.
2001). These species generally are not observed
to occur in the urban matrix (Table 2). Species
that are able to exploit the urban matrix do not
show fragment area sensitivity or edge sensitiv-
ity (Table 2). Clearly, as shown by the California
Gnatcatcher's ability to disperse through devel-
oped landscapes, this is not the case for all frag-
mentation-sensitive species.
The relationship between habitat degradation
and extinction and colonization rates in habitat
fragments needs clarification. Is fragmented hab-
itat sufficiently degraded to lead to local extinc-
tion or cause dispersing birds to pass up frag-
ments? Many fragments lacking particular bird
species do not differ in gross habitat character-
istics from those that do support them (D. Bol-
ger, pers. obs.). Crooks et al. (2001) found no
relationship between extinction rates and percent
native shrub cover, an index of habitat degra-
dation. I suspect that, except for the most de-
graded patches, the absence of species in the
"moderately sensitive" category (Table 2) from
fragments is due in large part to the inability of
these species to successfully disperse through
the urban matrix and colonize patches frequently
enough to counteract extinction processes. How-
ever, studies of dispersal in a variety of species
are needed, as are demographic studies in habitat
fragments and reintroduction experiments to test
the suitability of unoccupied fragmented habitat.
CONTRASTS WITH FRAGMENTATION STUDIES IN
THE EAST AND MIDWEST
Several features of the research reviewed here
appear in contrast to the work done in the East
and Midwest where top-down effects appear to
be the most important consequences of fragmen-
tation. Studies in those regions have often doc-
umented strong effects of nest predation and
brood parasitism near edges or in more frag-
mented landscapes (Robinson et al. 1995a, Don-
ovan et al. 1997). The evidence for top-down
effects in southern California is mixed. Morrison
and Bolger (2002) found that rates of nest pre-
dation or parasitism were not elevated along de-
veloped edges in the Rufous-crowned Sparrow,
although Crooks and Sould (1999) find evidence
for mesopredator release in isolated fragments.
Fragment isolation appears to be a more im-
portant influence in southern California. In the
Midwest, regional-scale dispersal appears to
maintain populations of neotropical migrants in
extensive landscape sink areas (Robinson et al.
1995a). In contrast in San Diego, isolation on
the scale of 100's of meters appears to prevent
rescue of populations of some species in frag-
ments. Either the fragmentation-sensitive species
in southern California are poorer dispersers, or
they are much better at recognizing and avoiding
sink habitat than the neotropical migrants of the
Midwest. Of course, it has not been demonstrat-
ed that fragments are demographic sinks in
southern California as they are for a number of
species in the Midwest.
The avifauna in southern California is pre-
dominantly composed of year-round resident
species as opposed to the neotropical migrant
species that dominate the eastern and midwest-
ern avifauna. The generally shorter dispersal dis-
tances of residents compared to migrants (Par-
adis et al. 1998) may help explain the relative
importance of isolation. The nature of the inter-
vening urban matrix may also play a role. The
urban matrix could be more hostile to dispersal
than the agricultural matrix of the Midwest.
Habitat degradation may be a more powerful
consequence of fragmentation and edge in the
arid West than in the Midwest and East. This
degradation may be reflected in changes in phys-
ical habitat structure or food availability in hab-
itat fragments. The effect of fragmentation on
woody vegetation structure has not been the fo-
cus of studies of fragmentation in the East and
Midwest, but one study has demonstrated lower
food availability in fragments (Burke and Nol
1998).
INFORMATION NEEDS
In addition to those already mentioned there
are a number of gaps in our knowledge that limit
our ability to understand, predict, and manage
the effects of fragmentation on birds in this re-
gion. Our understanding of the trophic effects of
fragmentation is hindered by the lack of basic
autecological data on bird foraging and diet, in-
cluding adult and nestling food. Nest predation
must be investigated on a range of bird species
to discover whether the results on the Rufous-
crowned Sparrow are generalizable to other spe-
cies nesting in different strata and with differing
landscape sensitivities. We know little about the
non-mammalian predator community in frag-
ments. Snakes appear to be quite rare in habitat
fragments (D. Bolger, unpubl. data). If this is
true what effect does this have on species that
are vulnerable to snake predation? Are predation
rates lower in fragments or does the effect of
increased mammalian mesopredators or other
predators compensate for reduced snake preda-
tion?
We also need to understand how edge effects
156 STUDIES IN AVIAN BIOLOGY NO. 25
scale with the percentage of the local landscape
that is developed (Donovan et al. 1997). Do iso-
lated habitat fragments experience more intense
edge effects than larger habitat blocks? Similar-
ly, how does the predation regime in isolated
fragments compare with predation in the edge
and interior of large habitat blocks? A virtually
untouched question is the source status of the
urban matrix for bird species that occur in both
the urban matrix and natural habitat. Bolger et
al. (1997) found elevated densities of some na-
tive urban-exploiting birds up to lkm into hab-
itat blocks. The consequences of this density
augmentation on avian communities deserves
further study.
A landscape perspective on disturbance re-
gimes is urgently needed. How do fragmentation
and edge affect non-native plant invasion, fire,
and other disturbance regimes. These are among
the most severe threats to conservation in this
semi-arid region as demonstrated by Minnich
and Dezzani's (1998) work. Physical gradients
(soil moisture, air temperature, etc.) along edges
have not been investigated in this system and
may be important. Also the effect of ENSO (El
Nifio-Southern Oscillation) driven variation in
rainfall is essential to understanding avian pop-
ulation fluctuations (Morrison and Bolger in
press) that may have important implications for
extinction rates in fragments.
CONSERVATION IMPLICATIONS
There is an extensive conservation planning
effort ongoing for coastal southern California
under the state's Natural Communities Conser-
vation Planning program (NCCP). The reserve
system that ultimately results from this effort
will by necessity be set within a predominantly
urban matrix. A species-by-species evaluation of
the conservation implications of the findings re-
viewed here is beyond the scope of this paper
and would require a region-wide evaluation of
the abundance and distribution of these species
on protected lands (J. Rotenberry et al., unpubl.
data). There are, however, a number of general
conclusions that can be drawn that are relevant
to the management of reserves in these land-
scapes.
The studies reviewed here suggest that highly
isolated shrub habitat patches less than 100 ha
provided little conservation value for fragmen-
tation-sensitive species over the long term.
However, they do support other members of the
regional fauna in abundance (Soul et al. 1988,
Crooks et al. 2001). The limitations of frag-
mented habitat for conservation are acknowl-
edged in the NCCP reserve selection guidelines
that emphasize large, contiguous blocks of hab-
itat (Atwood and Noss 1994). Denser archipel-
agos of fragments probably would support more
interpatch movement and higher abundance of
these species as suggested by a comparison of
Soul et al. (1988) and Lovio (1996). However,
since we' do not know whether fragments are
sink or source habitat for most species it seems
unwise to design landscape to encourage dis-
persal to fragments from source habitat.
Edge effects on bird abundance (Table 2; Bol-
ger et al. 1997) and the penetration of Argentine
ants along edges (Suarez et al. 1998; D. Bolger,
unpubl. data) are of concern even in large re-
serves. We still do not have an adequate under-
standing of the variety of ecological mechanisms
generating edge effects, the extent of their spa-
tial penetration into blocks of habitat or the time
course of these effects. Edge effects such as re-
duced or enhanced abundance of bird species,
Argentine ant invasion, and changes in arthro-
pod communities appear to penetrate reserves on
the scale of hundreds of meters. Thus these ef-
fects can significantly reduce the effective area
of even large reserves.
To effectively conserve the coastal southern
California biota, it will be necessary to identify
the effects of urban fragmentation and under-
stand their ecological mechanisms. There is an
understandable desire among land managers and
conservation planners for simple geographic an-
swers from ecologists: prescriptions for mini-
mum area requirements, buffer and edge effect
distances. However, easy answers are mislead-
ing, for although fragmentation and edge effects
have a geographic dimension, that is they can be
mapped to some degree of resolution, they are
primarily community ecological and population
ecological phenomena. As such, they are dy-
namic processes and their spatial dimension is
dependent upon the makeup of the local com-
munity as well as time. For example, Crooks et
al. (200l) demonstrated that area sensitivity is
not static but is a function of time. It is likely
that the spatial penetration of edge effects is also
not static.
Ecologists will only be able to make robust
management prescriptions about fragmentation
and edge effects when we have more fully ex-
amined the range of ecological mechanisms gen-
erating these effects. Even then, they will not be
simple answers expressed in meters and hect-
ares, but will be time-dependent and conditional
on the composition of the local community. So,
minimum area requirements will be expressed in
general terms for a given range of fragment age
and will depend on the condition of the vege-
tation in the fragment and the composition of the
predator community. These answers will not be
easy to map, or to explain to policy-makers, but
they will be ecologically valid. Of course geo-
SOUTHERN CALIFORNIA FRAGMENTATIONBolger 157
graphic tools such as buffer distances will con-
tinue to be important conservation planning
tools. But we cannot allow that fact to convince
policy-makers, the public, and ourselves, that
conserving the native biota of coastal southern
California in the face of a large and growing
human population will be as simple as creating
buffers of a fixed distance around reserves. In-
stead, it we will require understanding and ac-
tively managing populations and processes, and
we are a long way from possessing the neces-
sary knowledge and management capabilities to
accomplish that.
ACKNOWLEDGMENTS
The ideas presented here grew out of discussions
and collaborations with T. Case, K. Crooks, B. Kus, S.
Morrison, J. Rotenberry, T. Scott, M. Soul& and A.
Suarez. I thank D. Dobkin, P. Doran, L. George, P.
Mock, and S. Morrison, for helpful feedback on the
manuscript. I also acknowledge financial support from
the National Science Foundation and the Metropolitan
Water District of Southern California.
APPENDIX. SCIENTIFIC NAME OF ALL VERTEBRATE SPECIES MENTIONED IN TEXT OR TABLES
Birds
California Quail
Mourning Dove
Lesser Nighthawk
Costa's Hummingbird
Anna's Hummingbird
Bell's Vireo
Western Scrub-jay
Common Raven
American Crow
Common Bushtit
Bewick's Wren
Wrentit
Blue-gray Gnatcatcher
California Gnatcatcher
Northern Mockingbird
California Thrasher
European Starling
Lazuli Bunting
Spotted Towhee
California Towhee
Rufous-crowned Sparrow
Sage Sparrow
Black-chinned Sparrow
Grasshopper Sparrow
Lark Sparrow
Brown-headed Cowbird
Western Meadowlark
House Finch
Lesser Goldfinch
Reptiles
coastal horned lizard
California kingsnake
gopher snake
Mammals
Virginia oppossum
California ground squirrel
striped skunk
coyote
grey fox
domestic cat
Callipepla californica
Zenaida macroura
Chordeiles acutipennis
Calypte costae
Calypte anna
Vireo bellii
Aphelocoma coerulescens
Corvus corax
Corvus brachyrhynchos
Psaltriparus minimus
Thryomanes bewickii
Chamaea fasciata
Polioptila caerulea
Polioptila californica
Mimus polyglottos
Toxostoma redivivum
Sturnus vulgaris
Passerina amoena
Pipilo maculatus
Pipilo crissalis
Aimophila ruficeps
Amphispiza belli
Spizella atrogularis
Ammodramus savannarum
Chondestes grammacus
Molothrus ater
Sturnella neglecta
Carpodacus mexicanus
Carduelis psaltria
Phrynosoma coronaturn
Lampropeltis getula
Pituophis melanoleucus
Didelphis virginiana
Spermophilus beechyi
Mephitis mephitis
Canis latrans
Urocyon cinereoargenteux
Felis catus
Studies in Avian Biology No. 25:158-202, 2002.
EFFECTS OF ANTHROPOGENIC FRAGMENTATION AND
LIVESTOCK GRAZING ON WESTERN RIPARIAN
BIRD COMMUNITIES
JOSHUA J. TEWKSBURY, ANNE E. BLACK, NADAV NUR, VICTORIA A. SAAB,
BRIAN D. LOGAN, AND DAVID S. DOBKIN
Abstract. Deciduous vegetation along streams and rivers provides breeding habitat to more bird
species than any other plant community in the West, yet many riparian areas are heavily grazed by
cattle and surrounded by increasingly developed landscapes. The combination of cattle grazing and
landscape alteration (habitat loss and fragmentation) are thought to be critical factors affecting the
richness and composition of breeding bird communities. Here, we examine the influence of land use
and cattle grazing on deciduous riparian bird communities across seven riparian systems in five western
states: Montana, Idaho, Nevada, Oregon and California. These riparian systems are embedded in
landscapes ranging from nearly pristine to almost completely agricultural. We conducted landscape
analysis at two spatial scales: local landscapes (all land within 500 m of each survey location) and
regional landscapes (all land within 5 km of each survey location). Despite the large differences among
riparian systems, we found a number of consistent effects of landscape change and grazing. Of the
87 species with at least 15 detections on two or more rivers, 44 species were less common in grazed
sites, in heavily settled or agricultural landscapes, or in areas with little deciduous riparian habitat.
The Veery (Catharus fuscescens), Song Sparrow (Melospiza melodia), Red-naped Sapsucker (Sphyr-
apicus nuchalis), Fox Sparrow (Passerella iliaca), and American Redstart (Setophaga ruticilla) were
all less common under at least three of these conditions. In contrast, 33 species were significantly
more common in one or more of these conditions. Sites surrounded by greater deciduous habitat had
higher overall avian abundance and 22 species had significantly higher individual abundances in areas
with more deciduous habitat. Yet, areas with more agriculture at the regional scale also had higher
total avian abundance, due in large part to greater abundance of European Starling (Sturnus vulgaris),
American Robin (Turdus migratorius), Brown-headed Cowbird (Molothrus ater), and Black-billed
Magpie (Pica pica), all species that use both agricultural and riparian areas. Grazing effects varied
considerably among riparian systems, but avian abundance and richness were significantly lower at
grazed survey locations. Fifteen species were significantly less abundant in grazed sites while only
five species were more abundant therein. Management should focus on (1) preserving and enlarging
deciduous habitats, (2) reducing cattle grazing in deciduous habitats, and (3) protecting the few rela-
tively pristine landscapes surrounding large deciduous riparian areas in the West.
Key Words: agriculture; avian abundance and richness; cattle grazing; landscape fragmentation; mul-
ti-scale; riparian habitat.
Deciduous riparian areas bordering rivers and
streams in the western United States support a
higher density of breeding birds than any other
habitat type (Carothers and Johnson 1975, Rice
et al. 1983, Ohmart and Anderson 1986), and
studies explicitly comparing deciduous riparian
areas with surrounding upland communities re-
peatedly have found diversity and density of
breeding birds to be greater in riparian com-
munities (Carothers et al. 1974, Johnson et al.
1977, Stamp 1978, Conine et al. 1979, Hehnke
and Stone 1979, Knopf 1985; Anderson et al.
1985a,b; Strong and Bock 1990, Cubbedge
1994). The importance of these habitats to the
maintenance of avian communities cannot be
overemphasized. Deciduous riparian habitat
makes up less than 1% of the western land area
(Knopf et al. 1988), yet over 50% of western
bird species breed primarily or exclusively in
deciduous riparian communities (Johnson et al.
1977, Mosconi and Hutto 1982, Johnson 1989,
Saab and Groves 1992, Dobkin 1994). Due to
the proliferation of dams, intensive water man-
agement practices, and the effects of domestic
livestock, riparian areas are considered the most
heavily degraded ecosystems in the West (Ro-
senberg et al. 199l, Dobkin 1994, Ohmart 1994,
Saab et al. 1995); some western states have al-
ready lost as much as 95% of their historic ri-
pman habitat (Rosenberg et al. 1991, Ohmart
1994). The importance of remaining riparian ar-
eas for avian and other wildlife populations is
thus greatly magnified.
Two of the primary threats to the quality of
remaining deciduous riparian habitats are the
conversion of land near riparian areas into ag-
ricultural and urban land (Tewksbury et al. 1998,
Saab 1999), and cattle grazing within riparian
areas (Carothers 1977, Crumpacker 1984, Cha-
ney et al. 1990, Saab et al. 1995, Saab 1998).
The effects of these activities on individual riv-
ers have often been studied using different met-
rics, focusing on different groups of birds, and
there have been few attempts to combine data
158
FRAGMENTATION AND GRAZING--Tewksbury et al. 159
across riparian systems to look for common pat-
terns (Hochachka et al. 1999).
Although it is widely recognized that the rich-
ness and composition of breeding bird assem-
blages are at least partially dependent on the
landscape within which they are embedded
(Robinson et al. 1995a; Donovan et al. 1995b,
1997; Freemark et al. 1995, Faaborg et al. 1995,
Saab 1999), it is not clear what scale or scales
are appropriate to use when considering the ef-
fects of landscapes on bird populations (Free-
mark et al. 1995, Donovan et al. 2000). Indeed,
given the many factors that can affect the struc-
ture of bird communities (nest predation, brood
parasitism, competition for food and nesting
sites, habitat area limitations), landscapes likely
affect bird communities at multiple scales
(Wiens 1989, 1995; Urban et al. 1987, Turner
1989, Kareiva 1990, Kotliar and Wiens 1990,
Barrett 1992, Andrn 1995, Freemark et al.
1995, Hansson et al. 1995). To date, however,
few empirical studies have considered the rela-
tive importance of multiple landscape scales (but
see Tewksbury et al. 1998, Hochochka et al.
1999, Saab 1999, Donovan et al. 2000), and
there has been no attempt to examine the relative
effects of multiple land-uses across scales when
studying the composition of riparian bird com-
munities.
A focal concern in the western United States
is cattle grazing. Domestic cattle graze 70% of
the land area in the 11 western states (Crum-
packer 1984) causing extensive modifications to
vegetation (Holechek et al. 1989). These effects
are particularly apparent in deciduous riparian
areas (Carothers 1977, Crumpacker 1984, Platts
and Nelson 1985, Fleischner 1994, Saab et al.
1995). However, it is not clear which grazing
effects are dependent on local factors and levels
of grazing intensity, and to what extent grazing
effects can be generalized across a broad array
of riparian systems and grazing regimes.
Here we examine the influence of regional
(within 5 km of each study site) and local (with-
in 500 m of each study site) landscapes and the
influence of cattle grazing on the richness and
relative abundance of bird communities in seven
riparian systems dominated by deciduous trees
and shrubs. This work is the result of collabo-
ration by five independent research teams work-
ing in five western states over the past decade.
By combining efforts, we provide the first meta-
analysis of human-induced landscape change
and cattle grazing on the avian communities
breeding in these critical western habitats in the
hope of detecting consistent patterns across the
West.
METHODS
RIPARIAN SYSTEMS, SURVEY LOCATIONS, AND
LANDSCAPE CHARACTERIZATION
The seven riparian systems included in this work
vary considerably in size, physical character, local and
regional vegetation patterns, and land use (Fig. 1; Ap-
pendix 1), but all possess streamside vegetation dom-
inated by woody deciduous species (see Appendix 1
for detailed descriptions of each riparian system).
We analyzed bird species-abundance data from a to-
tal of 437 survey locations (Fig. 1; Table 1). Survey
locations were separated by at least 150 m and located
in vegetation dominated by cottonwood (Populus
spp.), aspen (Populus tremuloides), or a mixture of
species including willow (Salix spp.), valley oak
(Quercus lobam), dogwood (Comus spp.), hawthorn
(Crataegus spp.), cherry (Prunus spp.), alder (Alnus
spp.), and birch (Betula spp.). At each survey location,
relative abundance was calculated as the total number
of each species detected per visit. Surveys were either
fixed-radius point counts (five of the seven systems)
or 150-m fixed-width line transects (Table 1). We de-
fined a survey as a single visit to a point or transect
location. All studies conducted three Surveys per year.
The radius of point counts was either 40 m or 50 m,
and point duration was either five or 10 min (Table 1).
We defined two spatial scales at each study location:
regional landscapes (all land within 5 km of each sur-
vey location - 7,854 ha) and local landscapes (all land
<500 m of each survey location = 78 ha). Regional
landscape character was quantified using state GAP
databases (Scott et al. 1993) derived from satellite im-
ages (Table 1). Local landscape data were gathered
from low elevation aerial photography, ortho-photo
quadrangle maps, and high resolution digital data, de-
pending on the riparian system. Using a different data
set for local analyses allowed us to include smaller
features in analyses, such as linear riparian compo-
nents and individual buildings that could not be de-
tected at the regional scale. Metrics such as average
patch size and edge-to-interior ratios depend on map-
ping resolution, and our data resolution varied consid-
erably among sources (Table 1). Thus we confined our
analyses to the percent cover of four landscape com-
ponents: forest cover, agriculture, human habitation,
and deciduous riparian cover. The first three have been
used previously to index landscape fragmentation and
habitat conversion (Donovan et al. 1995b, 1997; Rob-
inson et al. 1995a, Young and Hutto 1999). Deciduous
riparian cover also has been used in landscape studies.
Percent cover blends aspects of patch size and isola-
tion, both of which have been found to affect riparian
bird communities (Brown and Dinsmore 1986, Gibbs
et al. 1991, Craig and Beal 1992, Saab 1999).
Our decision to compare high-resolution local data
with low-resolution regional data also reflects the
choice available to land managers, where detailed
land-use data are available only at local scales. This
approach, however, confounds differences in resolution
with differences in scale. Therefore, on three riparian
systems (Sacramento, San Joaquin, and Bitterroot riv-
ers), we compared GAP data (used for the regional
scale) with aerial photography data (used at the local
scale) on the same 500 m local landscapes to examine
correlations between estimates derived from different
160 STUDIES IN AVIAN BIOLOGY NO. 25
Local
Barren]
Lacustq|
ConiferJJ
Decil','
Shrub
Local
Barren rHurn Hab.
WateL: -A'.
. ''-Grass
[ -dShrub
Confer ,¾.i;. I Decid.
Reflional [ LOCawater.l.,
Barren3FAg,
Barren Hum. Hab. Lacurass
Water., Ag.
&,=!i-Grass Shrub
Conifer Shrub
-Decid. Dec'l?-
Relional
Water -I _
Conifer ._ss
,.... Shrub
Reflional
?-, .... Barrenq
... -,t ' ' .... Lacust. ¾Ag.
Local
Barren]
Local Lacust.' Barren¾-
Barren-ii-Hum. Hab. Water- Lacust..urn. Hah.
Lacust. .Ag. Coni,fer' Hum Hab Water \
Water Orchard Deci ' Conifer-Ag-
Decidl.'X'- /'- G rase Decid. hrub
Shrub
Barrenn IHum- Hab.
wLa;½ . t' '-A%rchard
Decid 'ass
Reflional
Lacus.t.. Ag.
Grass ' . o Orchard
Reflional
Lacust.- Hab.
Orchard
Regional
Regional
rHum. Hab.
FIGURE 1. River system locations and general landscape character of each river system. Pie charts are mean
percent cover for each landscape component averaged across all survey locations, at both local and regional
scales. Hum. Hab. = all human habitations, including houses, farms, commercial developments, and industrial
areas. Ag. = all agriculture, including row crops and land used for pasture and row crop, but excluding vineyards
and orchards. Orchard = all orchards, primarily fruit and nut trees, and vineyards. Grass = all grasslands. Shrub
= all shrublands and juniper woodlands, as bird communities were similar. Decid. = all deciduous habitats.
Conifer = Conifer forests. Water = all large bodies of wate including river channels. Lacust. = Lacustrine,
partially submerged and wet meadow habitat. Barren = permanent snow, ice, rock, or talus.
data types. For the Bitterroot Rive; the resolution of
GAP data is quite high (Table 1), so we expected some
concordance between the two techniques. For the Sac-
ramento and San Joaquin Rivers, the GAP resolution
is low, and this shift in resolution could affect results
considerably. Because the regional scale contains 100
times the area of the local scale, however; lower res-
olution at the regional landscape scale should have less
effect than lower resolution at the local scale.
LIVESTOCK GRAZING
In five of the seven riparian systems studied, grazing
occurred on some but not all of the study sites. Within
these five systems, the intensity and timing of grazing
differed considerably, from the Missouri River with
long term high-intensity grazing on grazed sites and
no cattle on rested ("ungrazed") sites for the past 30
years, to the Snake River where grazing intensity dif-
FRAGMENTATION AND GRAZING--Tewksbury et al. 161
<
<
<
>
<
040 .
162 STUDIES IN AVIAN BIOLOGY NO. 25
fered considerably among sites and was often moder-
ate or light (Appendix 1). The methods of comparison
differ as well; in the Hart Mountain and Sheldon sys-
tems, the same sites were surveyed in 1991 and 1993,
the first and third growing seasons following cessation
of long term livestock grazing. We considered the
1991 surveys "grazed" and the 1993 surveys rested.
In all other riparian systems, bird abundance was com-
pared in the same years among different locations,
rather than in the same locations among different
years. Given all these differences, we expected to find
great variation among riparian systems in the effects
of grazing, and any consistent effects should represent
general effects applicable to a wide variety of riparian
ecosystems in the West.
ANALYSIS
Relative abundance data were available for each
point count or transect survey except on the Snake
River, where data were averaged to the study site level.
To accommodate this, we performed analyses at the
site level for all riparian systems, and at the survey
location level for all areas except the Snake. Both
methods gave similar results. However, combining
data to the site level resulted in a considerable loss of
statistical power, so we present analysis of the survey
location data for all rivers except the Snake, which is
analyzed at the study site level. Our analysis of species
richness includes all areas except the Snake because
average richness per survey location could not be cal-
culated from the data available.
All variables were initially screened for deviations
from normality using one-sample Kolmogorov-Smir-
nov tests (Sokal and Rohlf 1995), and transformed
where necessary. We used square-root transformations
for count data (bird variables), and arcsine square-root
transformations for percent data (landscape compo-
nents). We examined four landscape components--hu-
man habitation, agriculture, deciduous forest, and co-
niferous forest---each at local and regional landscape
scales.
within each riparian system, we examined the ef-
fects of landscape differences on the relative abun-
dance of all individual species detected an average of
15 or more times per year on that riparian system.
Because we were primarily interested in effects that
can be generalized throughout western riparian areas,
we limited our analysis to species meeting this crite-
rion on at least two riparian systems (102 species in
total). In addition, we examined community level ef-
fects by grouping species into different guilds: primary
hosts of Brown-headed Cowbirds (see Appendix 2 for
scientific names of all species) vs. non-hosts; and long-
distance migrants vs. short-distance migrants vs. per-
manent residents. In examining the effects of grazing,
we also divided species into open nesting species vs.
primary and secondary cavity nesting species, and low
vs. high nesting species. Relative abundance of each
species is defined as the average number of individuals
detected per survey calculated by averaging values for
separate visits within a year and then averaging across
years. We also examined overall richness, calculated
as the cumulative number of species detected at each
location over the three surveys within a single year,
averaged across years.
Migratory status followed Sauer et al. (2000). Pri-
mary hosts included all species listed as common or
frequent cowbird hosts in The Birder's Handbook
(Ehrlich et al. 1988); species listed as uncommon or
rare cowbird hosts were termed secondary hosts (not
analyzed in this manuscript). For nest height, we used
the mean nest height from nesting studies on the ri-
parian systems in this study, and examined the effect
of grazing on the abundance of birds nesting below
2.5 m and above 5 m (Appendix 2).
To control for the large differences in methods
among riparian systems, we first tested the effects of
each landscape component within each riparian system
to maintain consistency in sampling. To assess land-
scape effects on the avian community, we regressed
total relative abundance, richness, and the relative
abundance of each avian guild against each of the
landscape components at both local and regional
scales, using all survey locations within each riparian
system for each river-specific analysis. To test for graz-
ing effects we used t-tests within each riparian system,
comparing community metrics and individual species
between grazed and ungrazed sites. We assumed equal
variance among population means unless P < 0.1 in
Levene tests for equality of variance. Because these
analyses are based on overall relative abundance of all
species in a guild, the results are heavily influenced by
the most common species. To examine landscape and
grazing effects on community metrics with all species
receiving equal weight, as well as to determine the
response of individual species to differences in land-
scapes, we designated each survey location as low
(lower 25%), middle (25 to 75%) or high (upper 25%)
with respect to each landscape component within each
riparian system. For tests of landscape effects on over-
all abundance, and the effects of landscapes and graz-
ing on each guild, we coded each species as either
more or less abundant in the low sites when compared
to the high sites, then used binomial tests to determine
if a significant majority of species within each guild
were significantly more abundant in the high or low
sites. For analysis of individual species, we used
Mann-Whitney U-tests to compare the abundance of
species in low and high sites for each landscape com-
ponent within each riparian system and to compare
abundance in grazed vs. ungrazed sites. We tested all
species on a given riparian system with an average of
15 or greater detections per year. As our purpose was
to evaluate the consistency of landscapes and grazing
effects across rivers, we limit our results to species
tested in at least two riparian systems. This analysis
controls for landscape differences among different ri-
parian systems because it compares abundances of
birds across the landscape extremes within each ripar-
ian system.
To examine landscape and grazing effects across ri-
parian systems, we used Fisher's combined probabili-
ties test (Fisher 1954, Sokal and Rohlf 1995). This test
evaluates the P-values from each riparian system
against the null hypothesis that there is no general
trend of significance across tests (in this case, riparian
systems). The value -2 times the sum of the natural
logs of all the P values from a group of independent
tests of a single hypothesis falls along a cumulative
Chi-square distribution with 2k degrees of freedom,
FRAGMENTATION AND GRAZING--Tewksbury et al. 163
TABLE 2. CORRELATIONS AND MEAN DIFFERENCE (1 SE) BETWEEN LANDSCAPE COMPONENTS IDENTIFIED USING
HIGH RESOLUTION LOCAL LANDSCAPE DATA AND LOWER RESOLUTION GAP DATA (USED FOR THE REGIONAL SCALE
ANALYSIS) BOTH AT THE LOCAL SCALE
Human habitation Agriculture Deciduous riparian Coniferous forest
r Diff (%)b r Diff (%)b r Diff (%)b r Diff (%)b
Bitterroot 0.20* -5.4 (0.7) 0.78*** -9.0 (1.3) 0.76*** -6.3 (1.2) 0.97*** 11.6 (1.0)
Sacramento __a - 1.2 (0.2) -0.23 5.9 (5.4) O. 11 0.2 (5.7) -- --
San Joaquin __a -2.9 (0.3) 0.17 0.8 (3.9) -0.07 7.6 (3.6) -- --
Note: * P < 0.05, ** P < 0.01, *** P < 0.005.
a Lower resolution data-source picked up no human habitation.
b % difference - % component at regional scales (low resolution) - %
component at local scales (high resolution).
where k = the number of separate tests (riparian areas)
being compared. The combined probabilities test eval-
uates where the summed value lies along the cumu-
lative Chi-square distribution. Because we are com-
paring the significance of tests for a general trend in
one direction, but trends may be either positive or neg-
ative, we had to account for the sign associated with
each P value. To do this, we used -ln P for all results
whose significance referred to a test opposite in sign
from that being evaluated. We evaluated trends in both
directions. This procedure produced a more conser-
vative test for an overall pattern across riparian sys-
tems, as it is more difficult to reject the null hypothesis
of no general effect. Using Fisher's combined proba-
bilities tests also circumvents the problems of combin-
ing data with inherent differences in detection proba-
bilities resulting from differences in survey techniques
and observers. To determine the most abundant species
across river systems, we ranked the abundance of all
species within each river system in descending order,
and computed mean abundance ranks for all species
across rivers (a mean abundance rank of one would
mean a species had the highest detection frequency in
all rivers it occurred in).
To correct for inflation of significance due to mul-
tiple testing, we used sequential Bonferroni adjustment
of significance (Rice 1989) for all correlation, regres-
sion, and t-tests. Thus for tests of landscape effects,
we corrected for a total of 64 tests within each riparian
system (four landscape components, two scales, and
eight bird community components). We also corrected
for 64 tests when examining the significance of the
combined probabilities tests across riparian systems.
For grazing effects, we corrected for 12 tests (one for
each aspect of the bird community examined).
RESULTS
For all studies combined, 180 species were
detected across 437 survey locations. Eleven
species were detected on all seven river systems.
These species, in order of mean abundance rank
(lower ranks being more abundant) were the
Brown-headed Cowbird, with a mean abundance
rank of 7.2; American Robin, 13.7; House Wren,
14.6; Yellow Warbler, 16.1; European Starling,
17.9; Black-headed Grosbeak, 18.9; Bullock's
Oriole, 21.3; Mourning Dove, 22.1; Warbling
Vireo, 24.1; Brewer's Blackbird, 29.4; and Laz-
uli Bunting, 30.1. Of the 87 species tested in-
dividually for effects of landscape components
and grazing, 44 species were significantly less
common either in grazed areas, areas with high
human habitation or extensive agriculture, or ar-
eas with less deciduous riparian habitat; 33 spe-
cies were more common under these conditions.
CORRELATIONS AMONG LANDSCAPE COMPONENTS
AND BETWEEN DATA RESOLUTIONS
Correlations among landscape components
varied considerably among riparian systems, de-
pending on the landscape context within which
each stream or river was embedded (Fig. 1). Not
surprisingly, both within and between scales, the
strongest correlations were found where the four
components we examined--human habitation,
agriculture, deciduous area, and coniferous for-
est---dominated the landscape (e.g., Snake and
Bitterroot rivers), as opposed to landscapes
dominated by shrub or grass (Appendix 3).
Landscape components varied considerably in
their correlations across scales. Relatively ho-
mogeneous and broad land uses, such as agri-
culture, were always correlated positively across
scales, whereas clumped and small land-uses,
such as human habitation, were correlated weak-
ly across scales in most riparian systems (Ap-
pendix 3). Differences in data resolution also af-
fected correlations across scales. When we con-
trolled for scale and compared both local (high
resolution) and regional (low resolution) data at
the local scale, we found strong positive corre-
lations on the Bitterroot River (Table 2), where
regional analysis was relatively fine grained (Ta-
ble 1). Even with this higher resolution regional
data (minimum mapping unit = 2 ha), however,
smaller landscape components were underem-
phasized compared with dominant landscape
components (Table 2). Where regional data were
coarse-grained, as on the Sacramento and San
Luis rivers, correlations were not significant, and
differences had high variance because compo-
nents identified with the high-resolution local
data were either missed entirely, or overempha-
sized by the low resolution landscape data.
164 STUDIES IN AVIAN BIOLOGY NO. 25
HUMAN HABITATION
At local scales, the majority of all species
(62% _+ 5% SE, five rivers) had lower relative
abundances in areas with high human habitation
compared to areas with low human habitation.
This trend was particularly apparent in long-dis-
tance migrants (66% +_ 6% less abundant in ar-
eas with high human habitation, five rivers).
These relationships were significant for both
groups in binomial tests, but because the Brown-
headed Cowbird, Yellow Warbler, and the
Black-headed Grosbeak (all very common spe-
cies) were more abundant in areas with high hu-
man habitation, there was no relationship be-
tween the total number of detections of all spe-
cies, or detections of long-distance migrants, rs.
local human habitation (Table 3). Human habi-
tation was strongly and positively correlated
with the number of Brown-headed Cowbirds de-
tected at both scales (Table 3), and the number
of non-host species detections was higher in ar-
eas with higher regional human habitation, due
primarily to the greater abundance of European
Starlings, House Wrens, and American Robins
in more densely settled areas (Table 4). The five
species showing the greatest reduction in fre-
quency in regional landscapes with high propor-
tions of human settlement were Yellow-rumped
Warbler, MacGillivray's Warbler, Warbling Vir-
eo, Swainson's Thrush, and Dusky Flycatcher
(Table 4). Populations of each of these species
are highly vulnerable to cowbird parasitism
(Tewksbury et al. 1998).
AGRICULTURE
High abundances of abundant species such as
American Robins, Yellow Warblers, and Brown-
headed Cowbirds in areas with agriculture (Ta-
ble 4) led to highly significant positive relation-
ships between total and guild detection frequen-
cy and the amount of agriculture at both scales.
However, binomial tests for direction of change
of all species in each guild were not significant
(Table 3; 53% -+ 6% of species had higher abun-
dance in areas with more agriculture), and the
only river system to show a significant majority
of species increasing with regional agriculture
was the Bitterroot (Appendix 4). In addition, re-
gional agriculture was significantly, positively
correlated with the abundance of Brown-headed
Cowbirds, which were twice as abundant in ar-
eas with high proportions of agriculture com-
pared with areas with low proportions of agri-
culture. Primary hosts, although not related to
agriculture at the local scale, showed a strong
positive relationship with the amount of agri-
culture regionally. This positive trend was driv-
en almost entirely by Yellow Warblers, the most
abundant host. Yellow Warblers were detected
far more often in areas with greater amounts of
agriculture and human habitation. In contrast,
many less abundant cowbird host species, such
as Swainson's Thrush, Warbling Vireo, Mac-
Gillivray's Warbler, and Yellow-rumped War-
bler, were rarely detected at survey locations
with high regional agriculture (Table 4). Overall,
there was no indication that the majority of hosts
were more or less abundant in landscapes dom-
inated by agriculture (Table 3; Appendix 4).
Non-hosts showed a strong positive relation-
ship with agriculture at both scales (Table 3),
primarily due to higher abundances of American
Robins, House Wrens, European Starlings, Tree
Swallows, and Bullock's Orioles in areas with
greater proportions of agriculture (Table 4). The
effects of human habitation and agriculture ap-
pear similar; in total, 24 species were signifi-
cantly more abundant in areas with high local or
regional agriculture, and 17 of these species
were also significantly more abundant in areas
with high human habitation.
DECIDUOUS RIPARIAN
Across riparian systems, areas with more de-
ciduous riparian habitat tended to have greater
avian abundance and diversity. Fifteen species
were significantly more abundant in areas with
a high proportion of deciduous habitat at the lo-
cal scale; six of these species were present in at
least four riparian systems: Yellow Warbler,
Black-headed Grosbeak, Song Sparrow, Western
Wood Pewee, Cedar Waxwing, and Orange-
crowned Warbler. Only two species were signif-
icantly less abundant in areas with greater local
deciduous riparian habitat, MacGillivray's War-
bier and Townsend's Warbler. Effects at the re-
gional scale were similar (Tables 3 and 4),
though almost half of the individual species in-
creasing were different from those increasing at
the local scale.
The amount of local deciduous riparian hab-
itat was positively correlated with virtually all
avian guilds at both scales. Binomial tests were
less convincing of a significant overall ef/Ect,
where the only significant relationship was be-
tween all species and regional deciduous ripar-
ian habitat (Table 3; 57% of species +_ 4.3%,
five rivers). The lack of significant ef/cts in bi-
nomial tests at the local scale was caused pri-
marily by eflcts on the Sacramento River,
where greater local deciduous riparian habitat
was associated with lower detection frequencies
in 67% of all species (Appendix 4).
CONIFEROUS FOREST
At the local scale, the proportion of conifer-
ous forest was not significantly related to total
FRAGMENTATION AND GRAZINGTewksbury et al. 165
relative abundance, richness, or any guild ex-
amined, after correcting for multiple tests. How-
ever, at the regional scale, conifer cover had a
strong negative effect on cowbird abundance
(combined P < 0.001). Cowbirds were detected
only half as often at survey locations with high
conifer forest when compared to locations with
low conifer forest (Table 4). Coniferous cover
was also related negatively to the abundance of
non-hosts, driven primarily by the low abun-
dance of European Starlings, American Robins,
and House Wrens in sites with high coniferous
cover. In addition, long-distance migrant abun-
dance was associated positively with percent co-
nifer forest (Table 3), due primarily to many
more detections of Warbling Vireo, Mac-
Gillivray's Warbler, Townsend's Warbler, Violet-
green Swallow, and Fox Sparrow in areas with
more conifers (Table 4). Binomial tests agreed
in direction with regressions on total guild abun-
dance, but were non-significant across rivers,
showing considerable variation in results among
individual rivers (Appendix 4).
GRAZING
The majority of all species (63% +_ 5%) were
less abundant in grazed locations (Fig. 2A; com-
bined probabilities test X2 = 42.8, P < 0.001).
After correcting for multiple tests, six species
were significantly less abundant at grazed sur-
vey locations when all riparian systems were
considered, while no species were significantly
more abundant at grazed locations (Table 5). In
addition, total relative abundance was signifi-
cantly lower in grazed areas (Fig. 2B; combined
probabilities test X2 = 48.9, P < 0.001), and spe-
cies richness showed a non-significant trend to
be lower in grazed areas (Fig. 2C; combined
probabilities test X2 = 19.8, P = 0.01, not sig-
nificant after correction for multiple tests). The
intensity of grazing effects varied greatly among
the seven riparian systems. On the Missouri,
Sacramento, and Hart systems, 68-73% of spe-
cies were less abundant in grazed areas (Fig. 2A;
binomial tests, P's < 0.007). The Missouri
showed the most dramatic effects, with 13 spe-
cies significantly less abundant in grazed areas
and only one more abundant (Appendix 5), and
the average detections per count shifted from 36
on ungrazed survey locations to 21 on grazed
survey locations. In contrast, on the Snake and
Sheldon riparian systems, species were no more
likely to be less or more abundant in these areas
(Fig. 2A). On the Sheldon, only two species dif-
fered significantly between recently grazed and
ungrazed sites, with one species more abundant
in each condition (Appendix 5).
Cowbird abundances were not significantly
different between grazed and ungrazed locations
for any of the five large riparian systems (Fig.
3A). Total primary cowbird hosts, however,
were less abundant in grazed areas (Fig. 3B;
combined X 2 = 25.3, P = 0.005), with strong
effects on the Missouri River (t = 3.3, P =
0.003) and the Snake River (t = 3.2, P = 0.002;
Appendix 5). While the majority of host species
were less abundant on grazed sites in all river
systems except the Sheldon, the low number of
species in the guild precluded significant effects
(Fig. 3C). On the Missouri River, the effects of
grazing on hosts was driven primarily by lower
abundance of Red-eyed Vireo, American Red-
start, Lazuli Bunting, Least Flycatcher, and Yel-
low Warbler in grazed areas (Appendix 5). Laz-
uli Buntings and Yellow Warblers were also sig-
nificantly less abundant in grazed sites along the
Snake River, as were Veerys and Song Sparrows
(Appendix 5). Total non-host abundance showed
no consistent response to grazing pressure (Fig.
3D; combined probabilities test X 2 = 11.3, P =
0.33), but the proportion of species that were
more abundant in ungrazed systems was typi-
cally higher than expected by chance (Fig. 3E;
combined probabilities test X 2 = 20.0, P =
0.023).
Of the migratory guilds, long-distance mi-
grants were the only group significantly less
abundant in grazed areas (Total abundance Fig.
4A: combined probabilities test X 2 = 47.7, P <
0.001; binomial mean response Fig. 4B: com-
bined probabilities test X 2 = 26.4, P = 0.003).
Across all riparian systems, five of the ten spe-
cies with significantly lower relative abundances
in grazed areas were long-distance migrants (Ta-
ble 5). The lower relative abundance of long-
distance migrants in grazed areas was particu-
larly apparent on the Missouri River, where the
average number of long-distance migrants was
21 individuals per survey in ungrazed areas and
only 12 per survey in grazed areas (Fig. 4A),
and 84% of the species were less abundant in
grazed sites (Fig. 4B). In addition to large ef-
fects on the Missouri, long-distance migrants
were significantly less abundant in grazed sites
on the Sacramento (t = 2.1, P = 0.037), and
exhibited similar non-significant trends in both
Hart Mountain and Snake River systems (P =
0.07 and 0.18, respectively). Residents showed
no significant differences between grazed and
ungrazed sites for any of the riparian systems
(Fig. 4C and 4D). The total abundance of short-
distance migrants tended to be lower in grazed
areas (Fig. 4E; combined probabilities test X 2 =
19.3, P = 0.03, not significant after correction
for multiple tests) with large differences in de-
tection frequency only on the Missouri River (t
= 3.2, P = 0.003). Individual species in this
guild were no more likely to be less or more
166 STUDIES IN AVIAN BIOLOGY NO. 25
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m V cq A V mV *q
FRAGMENTATION AND GRAZING--Tewksbury et al. 167
zzz . zz
V
168 STUDIES IN AVIAN BIOLOGY NO. 25
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FRAGMENTATION AND GRAZING--Tewksbury et al. 169
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dddddddddddd 4dd d
VVVVVV VVVV VV
170 STUDIES IN AVIAN BIOLOGY NO. 25
VVVVVV V VV
VVV
FRAGMENTATION AND GRAZING--Tewksbury et al. 171
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172 STUDIES IN AVIAN BIOLOGY NO. 25
FRAGMENTATION AND GRAZlNG--Tewksbury et al. 173
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174 STUDIES IN AVIAN BIOLOGY NO. 25
ß o.8
,._ 0.6
o
ß - 0.4
o
o 0.2
o_
# of species = 68 55 43 72 69
# of sites = 9
20 c
, 15
., 10
c 5
0
# of sites = 9
o
(.)-
12 17
20
More abundant in grazed areas
More abundant in ungrazed areas
Grazed
Ungrazed
FIGURE 2. Total response of all species to grazing
in each riparian system. Proportion of all species more
abundant in grazed or ungrazed plots (A), average
number of birds detected per survey (B), and the av-
erage number of species detected over the course of a
single year at a given location (C) for grazed and un-
grazed plots in each river system. * P < 0.05, ** P <
0.01, *** P ( 0.005. (*) = P-value not significant after
correction for multiple tests.
abundant in grazed sites (Fig. 4F; combined
probabilities test X 2 = 7.5, P = 0.679).
Total abundance of open cup nesters was sig-
nificantly higher in ungrazed survey locations
(Fig. 5A; combined probabilities test X 2 = 46.4,
P < 0.0005) and an average of 65% (_+ 8%) of
open-cup nesting species were less abundant in
grazed areas (Fig. 5B; combined probabilities
test X 2 = 35.3 P < 0.001). Primary cavity nest-
ing species trended in the same direction (Fig.
5C; combined probabilities test X2 = 20.4, P =
0.026, not significant after correction for multi-
ple tests), and secondary cavity nesters showed
conflicting patterns on different riparian systems
with no overall effect (Fig. 5E; combined prob-
abilities test X 2 = 4.4, P = 0.92). Binomial tests
suggested no overall trend for cavity nesters
(Fig. 5D and 5F), though the number of species
in each guild was too small for rigorous analy-
sis. On the Missouri, total abundances of open
cup and primary cavity nesters were significant-
ly greater on ungrazed sites (t's > 4.2, P's <
0.001) and 22 of 25 open-cup nesting species
were more abundant in ungrazed sites. Open-cup
nesting abundance was also lower on the Hart
Mountain (total abundance; t = 2.6, P = 0.013)
and Sacramento River (t = 2.1, P = 0.04) sys-
tems, with 30 of 40 species less abundant in
grazed areas on Hart Mountain (binomial test P
= 0.003) and 27 of 40 species less abundant in
grazed locations on the Sacramento (binomial
test P = 0.04).
The overall abundance of all species nesting
below 2.5 m was significantly lower in grazed
sites compared to ungrazed sites (Fig. 6A; com-
bined probabilities test X 2 = 26.4, P = 0.003)
and 67% of species in this category (_+ 5%)
were less abundant in grazed sites (combined
probabilities test X 2 = 17, P = 0.07), with all
rivers showing the same trend (Fig. 6B). In con-
trast, the combined abundance of all species
with average nesting heights higher than 5 m
showed only a non-significant trend to be lower
in grazed areas (Fig. 6C; combined probabilities
test X2 = 18.6, P = 0.045, not significant after
correction for multiple tests), and only 58% (_+
9%) of species in this guild were less abundant
in grazed sites, with the Snake and Sheldon sys-
tems showing either opposite trends or no effect
(Fig. 6D; combined probabilities test X 2 = 5.8,
P = 0.23).
DISCUSSION
This synthesis includes seven different west-
ern riparian systems, each embedded in a dif-
ferent landscape. In each system, data were
gathered by different investigators using similar
but not identical methodologies. Despite these
differences, our results demonstrate that both
landscape character and livestock grazing have
some consistent, potentially West-wide effects
on bird communities. Although some of these
effects are similar to those found in the Midwest
(landscape effects on Brown-headed Cowbirds,
for example), others will require further study to
determine the mechanisms responsible for the
patterns (the effects of grazing and agriculture
FRAGMENTATION AND GRAZING--Tewksbury et al.
TABLE 5. SPECIES SHOWING OVERALL TREND IN RESPONSE TO GRAZING
175
Less COlillllon in grazed areas More common in grazed areas
Species Rivers P Species Rivers P
American Robin 5 0.005*
Western Wood-pewee 5 0.031
Black-headed Grosbeak 5 0.080
Song Sparrow 4 0.020
Hairy Woodpecker 4 0.031 *
Mallard 4 0.055
Red-shafted Flicker 4 0.115
MacGillivray's Warbler 4 0.129
Cedar Waxwing 3 0.073
Cordilleran Flycatcher 2 0.003*
Red-eyed Vireo 2 0.008*
Fox Sparrow 2 0.014'
Green-tailed Towhee 2 0.015*
Black-capped Chickadee 2 0.017
Gray Catbird 2 0.032
Ovenbird 2 0.177
Turkey Vulture 2 0.197
Dusky Flycatcher 4 0.040
Western Meadowlark 3 0.056
Brewer's Sparrow 2 0.110
Note: Species are ranked by the number of riparian systems included in the analysis (minimum of two) and significance (P < 0.2). * Denotes significant
after Bonferroni correction for multiple tests.
on Yellow Warblers, for example). Below, we
summarize effects of different landscape com-
ponents and provide a brief synthesis of our
findings.
SCALE AND RESOLUTION
Until recently, there has been a significant gap
between theoretical work stressing the scale-de-
pendent nature of landscape effects (Wiens
1989, 1995; Dunning et al. 1992) and empirical
studies that confine analysis to a single land-
scape scale (Donovan et al. 1995b, Robinson et
al. 1995a, Thompson et al. 2000, Hejl and
Young 1999; but see Tewksbury et al. 1998,
Young and Hutto 1999, Donovan et al. 2000).
The abundance and composition of bird com-
munities are affected by multiple processes
across different landscape scales (Dunning et al.
1992, Freemark et al. 1995); even a single pro-
cess, such as nest predation, acts across multiple
scales dependent on the range size and habitat
affinities of the primary predators (Andrdn 1995,
Tewksbury et al. 1998). This variation in the
scaling of processes suggests that conservation
planning will be best served by examination of
multiple scales. Multiple-scale landscape analy-
ses allows the discovery of relationships that are
relatively scale-insensitive, and thus more easily
applied in management contexts, and it allows
determination of appropriate scales when pro-
cesses such as brood parasitism or nest predation
are considered.
Our results show that different landscape
components influence bird abundance and di-
versity at different scales. Overall, 40% of spe-
cies significantly affected by landscape factors
at one scale were not affected by these factors
at the other scale (Table 4), suggesting that ex-
amination of landscapes at only a single spatial
scale may result in loss of considerable infor-
mation. Importantly, our examination of two
landscape scales does not allow us to determine
the point when considering more land area de-
creases rather than increases the explanatory
power of a certain landscape variable, as we can
only say that a larger landscape is better than a
smaller one, or the other way around. Analyses
comparing the effect sizes of landscape com-
ponents at multiple scales would allow estima-
tion of the relative importance of landscape fea-
tures at different distances from an area of in-
terest.
The appropriate scale is also a function of
mapping resolution. Linear landscape compo-
nents and components that typically have small
patch sizes are usually underestimated when
mapping resolution is coarse. It is not particu-
larly surprising that we found no significant cor-
relations between data gathered using the low
resolution California GAP data and the detailed
CWIS data (Table 2), as the resolution of the
California GAP data (100 ha minimum patch
size) is greater than the entire area of our local
landscapes (78 ha). This coarse resolution is in-
appropriate for local scale habitat mapping, but
it may still be appropriate for larger landscape
scales as long as the biases are recognized. At
our regional scale, where we used these data, we
mapped 8000 ha around each survey location,
which allowed for a mosaic of patches even
176 STUDIES IN AVIAN BIOLOGY NO. 25
Cowbirds
A
1.5
of sites = 9 46 2026 1217 20'21 910
Grazed
I//I Ungrazed
P½;1 More abundant in grazed sites
I I More abundant in ungrazed sites
Prime hosts
>, 16
14
0 12
: 8
6
ß 4
2
#ofsites=946 2026 1217 2021 910
Non hosts
D
4 (.)
#ofsites 946 2026 1217 2021 910
,.o
' 0.6
0.4
P 0.2
Q-
c
# of species = 13 14 14
10 13
0.8
2 0.6
o
_. 0.4.
P 0.2
Q-
E
# of species = 39 23 10 11 9
.,,9
FIGURE 3. Grazing effects on cowbirds, prime hosts, and non-hosts. Total detections per survey on grazed
and ungrazed sites (A, B, and D), and proportion of species in each guild more abundant in grazed or ungrazed
sites (C and E), for cowbirds (A), prime hosts (B and C), and non-hosts (D and E) in each river system. * P <
0.05, ** P < 0.01, *** P < 0.005. (*) = P-value not significant after COlTection for multiple tests.
when these patches were 100 ha and larger. At
this level, large differences in the regional land-
scape are fully apparent, but features such as
dispersed housing or small riparian areas are not
detected. Thus the effect of changing regional
agriculture or coniferous forest cover is well
represented in the coarse-grained data, while
changes in linear deciduous riparian areas may
go undetected. As landscape data of higher res-
olution become more broadly available, com-
parisons across regions should be possible using
the same data sources for all landscape sizes,
eliminating the confounding issues of shifting
mapping resolution and allowing explicit com-
parison of scale.
HUMAN HABITATION AND AGRICULTURE
Our finding that overall avian abundance was
positively related to regional agricultural abun-
dance runs counter to findings from the East
(Croonquist and Brooks 199l, 1993), but is not
without precedent in the western United States
(Carothers et al. 1974). These results may be
better understood by examining the individual
species with large differences in abundance,
rather than by focusing on guilds (Mannan and
Meslow 1984). The high congruence in the spe-
cies increasing due to agriculture and human
habitation is partly a function of the positive cor-
relation that typically exists between agriculture
FRAGMENTATION AND GRAZING--Tewksbury et al. 177
Long-distance migrants
15 (.)
.o_ 10
#ofsites=9'46 20'26 12'17 20'21 9'10
grazed
Residents F'-7-] ungrazed
1.8 -[C
1.6 -I T
1.44
1.0
0.6
0.6
0.4
0.2
#ofstes 946 2026 1217 2021
0.9 B ***
0.6
0.5
0.4
0.3
0.2
0.1
ofspecies = 30 24 19 26 29
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
More abundant in grazed sites
More abundant in ungrazed sites
D
# of species = 14
Shod-distance migrants
>' 14
' 12
10
8
.o_ 6
ß 4
c 2
#of sites = 9'46 20'26 12
20'2'
9'10
0.9 F
0.8
(.)
0.6
0.5
0.4
0.3
0.2
0.1
# of species 2'6 1'9 1 3'1 2'9
FIGURE 4. Grazing effects on long-distance migrants, residents, and short-distance migrants. Total detections
per survey on grazed and ungrazed sites (A, C, and E), and proportion of species within each guild more
abundant in grazed or ungrazed sites (B, D, and F), for long-distance migrants (A and B), year-round residents
(C and D), and short-distance migrants (E and F) in each river system. * P < 0.05, ** P < 0.01, *** P < 0.005.
(*) - P-value not significant after correction for multiple tests.
and houses (Appendix 3). It is likely, however,
that many species with higher relative abun-
dance in areas with more agriculture also show
similar numerical responses to high human hab-
itation. Brown-headed Cowbirds use both agri-
cultural and farm areas for foraging (Thompson
1994), and European Starlings often forage in
suburban and agricultural areas (Fischl and Cac-
camise 1985). Indeed, most of the species that
are more abundant in areas with high agriculture
or human habitation often utilize multiple habi-
tats; American Robins, Black-billed Magpies,
starlings, and cowbirds are all examples. In-
creases in starlings may have consequences for
other secondary cavity nesters, as starlings can
exclude less aggressive species from cavities
(Ingold 1989, 1994, 1998; Nilsson 1984, Kerpez
and Smith 1990, Rich et al. 1994, Dobkin et al.
1995). Indeed, densities of Violet-green Swal-
lows were significantly lower in sites with high
agriculture at either scale--the same sites in
which starlings were significantly more abun-
dant (Table 4).
Higher Brown-headed Cowbird detection fre-
quency in areas with more agriculture has been
found previously across both local and regional
scales (Conine et al. 1979, Donovan 1997,
Tewksbury et al. 1999, Hejl and Young 1999,
Hochachka et al. 1999, Young and Hutto 1999).
Our finding that the detection frequency of pri-
178 STUDIES IN AVIAN BIOLOGY NO. 25
Open nesting species
' 30 A ***
[ 20
, 15
#ofsites=946 20'26 12'17 20'21 9'10
:F'-d'7'J grazed
Primary cavity-nesting species K / J ungrazed
:,, C
2.0
1.5
-- 1.0
#ofsites=946 20'26 12'17 20'21 9'10
0.9 B ***
0.7 (*) ***
0.6
0.5
0.4
0.3
0.2
0.1
of sites = 41 36 25 40 39
Mere abundant in grazed sites
I I More abundant in ungrazed sites
0.9 D
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
of sites =
Secondary cavity-nesting species
5
c 1
#ofsites=9'46 20'26 12'17 20'21 9'10
.,,9
0.9 '
0.8
0.7
0.5
0.4
0.2
0.3
0.1
of sites 1'1 7 5
,,o
FIGURE 5. Grazing effects on open nesting species, primary cavity nesters, and secondary cavity nesting
species. Total detections per survey on grazed and ungrazed sites (A, C, and E), and proportion of species in
each guild more abundant in grazed or ungrazed sites (B, D, and F), for open-cup nesting species (A and B),
primary cavity nesting species (C and D), and secondary cavity nesting species (E and F) in each river system.
* P < 0.05, ** P < 0.01, *** P < 0.005. (*) = P-value not significant after correction for multiple tests.
mary hosts was not lower in areas where cow-
birds were common is consistent with other
comparisons of cowbird density and host density
(Donovan et al. 1997, Tewksbury et al. 1999,
Young and Hutto 1999), and does not indicate
that cowbirds have no effect on host communi-
ties (De Groot et al. 1999). The demographic
effect of brood parasitism varies greatly among
different host species (Lorenzana and Sealy
1999), and we first expect lower abundances of
species that are particularly susceptible to para-
sitism. Indeed, the Dusky Flycatcher, Swainson's
Thrush, Veery, Warbling Vireo, Orange-
crowned Warbler, MacGillivray's Warbler, and
American Redstart all suffer complete or nearly
complete brood loss when parasitized (J. J.
Tewksbury, unpubl. data) and are all less abun-
dant in areas with high human habitation or high
agriculture (Table 4), areas where cowbirds are
abundant. In contrast, Yellow Warblers are more
resistant to the demographic effect of brood par-
asitism (Clark and Robertson 1981, Sealy 1995),
and they were more abundant in areas with high
human habitation and agriculture. Importantly,
human habitation and agriculture are often con-
centrated near productive riparian habitat with
large flood-plains, areas where many long-dis-
tance migrants susceptible to parasitism are
more abundant. Thus the trend for Yellow War-
blers (more abundant in these areas) may char-
acterize the natural response of other species, as
they respond to larger riparian areas, but the ef-
FRAGMENTATION AND GRAZING--Tewksbury et al. 179
Species nesting below 2.5m
#ofsites=9.6 20'26 12'17 20'21 9'10
grazed
Species nesting above 5m I/,/I ungrazed
>, 0.9 B
0.8
0.5
0.6
0.4
0.3
0.2
C3 0.1
# of species = 3 13
11 22 3'0
More abundant in grazed sites
More abundant in ungrazed sites
C
*** 0.9 D
0.7
0.6
0.5
0.4
' 0.3
0.2
0.1
# of sites = 9 46 20'26 12 '17 20'2 # of species = 33
FIGURE 6. Effects of grazing on low and high nesting species. Total detections per survey on grazed and
ungrazed sites (A and C), and proportion of species in each guild more abundant in grazed or ungrazed sites
(B and D), for species nesting below 2.5m (A and B), and species nesting above 5 m (C and D) in each river
system. * P < 0.05, ** P < 0.01, *** P < 0.005. (*) - P-value not significant after correction for multiple tests.
fect of cowbirds may counter this trend. In ad-
dition, negative correlations between cowbird
and host detection frequencies suggest that rates
of brood parasitism are positively related to
cowbird detection frequencies. While this as-
sumption is reasonable across most levels of
cowbird detection, where cowbird numbers are
high, further increases may not change parasit-
ism rates. This may be the case along the Sac-
ramento River, where high-levels of parasitism
at all sites may have already caused large re-
gional declines in many species (Gaines 1974),
so that current variation in cowbird detection
frequency is uncorrelated with parasitism rates.
The largest limitations in understanding the
effects of changing landscapes on riparian bird
communities are the correlations among com-
ponents of the landscape. In our study, we can-
not separate unambiguously the effects of agri-
culture and human habitation because of the
high correlation between these components (Ap-
pendix 3). In some cases, however, correlations
between landscape components differ signifi-
cantly among riparian systems, allowing insights
into which relationships are causative, and
which are simply due to covariation in landscape
components. For example, local deciduous hab-
itat is correlated strongly with higher host abun-
dance (Table 3). In the Bitterroot Valley, agri-
culture is correlated positively with the amount
of local deciduous habitat (Appendix 3; r =
0.47, P < 0.001), and, as a result, we see posi-
tive associations between host abundance and
regional agriculture. Conversely, along the
Snake River, local agriculture and deciduous
habitats are negatively correlated (Appendix 3;
r = -0.55, P < 0.001), and we see a strong
negative relationship between host abundance
and agriculture at the local scale (Appendix 4).
Thus, changes in host abundance are likely
caused by differences in the amount of decidu-
ous habitat, not the amount of agriculture, but
the effects are difficult to separate where these
components are positively correlated.
DECIDUOUS RIPARIAN AREA
Deciduous riparian area at the local scale is a
function of the width of the riparian corridor;
thus the positive correlations between avian
abundance and deciduous habitat likely are con-
sequences of greater habitat availability and het-
erogeneity associated with larger riparian corri-
dors (Tyser 1983, Brown and Dinsmore 1986,
Dobkin and Wilcox 1986, Craig and Beal 1992,
Keller et al. 1993). All of the species that were
significantly more abundant at survey locations
180 STUDIES IN AVIAN BIOLOGY NO. 25
with high local deciduous habitat are species tra-
ditionally considered riparian associates. The
guild-level examination of the effects of increas-
ing local deciduous area and increasing regional
agriculture suggested similar effects (Table 3),
but the individual species responding to these
landscape components were quite different (Ta-
ble 4). Fifteen species had significantly higher
abundance in larger deciduous areas, and 17 spe-
cies were higher in abundance in areas with
more regional agriculture. However, only three
species were more abundant under both these
conditions (Table 4). Thus the bird communities
in areas with high agricultural abundance share
little in common with the communities in areas
with large amounts of deciduous habitat, and
guild-based analysis may lead to erroneous con-
clusions unless the responses of individual spe-
cies are examined.
Within riparian systems, the breeding bird
community found in smaller deciduous tracts
was most often a subset of the birds found in
larger tracts. Only three species were less abun-
dant in sites with more local deciduous forest,
and one of these, the Townsend's Warbler, is typ-
ically associated with coniferous habitats. Thus,
preserving and restoring large tracts of decidu-
ous habitat likely will do more to preserve ri-
parian-associated species than will any other ac-
tion. In addition, large deciduous patches also
may reduce parasitism in parts of the patch as
distance from the nearest cowbird feeding area
increases.
CONIFEROUS FOREST
Studies in the Midwest have found that areas
with higher conifer abundance, at scales similar
to our regional scale, have lower cowbird abun-
dance and parasitism (Donovan et al. 1995b,
1997; Robinson et al. 1995a). Recent work in
the western United States, however, has sug-
gested that the abundance of human habitation
(Tewksbury et al. 1998), agriculture (Hejl and
Young 1999, Young and Hutto 1999, Donovan
et al. 2000), and the abundance of suitable hosts
(Barber and Martin 1997; Tewksbury et al.
1998, 1999) are better predictors of parasitism
pressure than is conifer abundance. Our study
supports both bodies of work--cowbirds were
not significantly less abundant in areas with
more local coniferous forest, but they were re-
lated positively to both human habitation and
agriculture, and they were also higher in larger
riparian areas, where host abundance is also
higher. At a regional scale, cowbirds did show a
strong negative correlation with the amount of
coniferous forest on the landscape, similar to re-
sults from the Midwest and East. This relation-
ship at the regional scale is most likely due to
the strong negative correlation between regional
coniferous forest cover and agriculture on the
Snake and the Bitterroot rivers (Appendix 3), the
two rivers where cowbirds and coniferous forest
are negatively related (Appendix 4). In the Bit-
terroot River system, rates of brood parasitism
have been directly related to the amount of hu-
man habitation on the landscape, not the amount
of coniferous forest (Tewksbury et al. 1998).
The effects of coniferous forest on individual
species were very similar across scales, with
over 70% of species affected showing significant
effects at both scales.
GRAZING
Variation in the intensity, duration, and timing
of grazing has been shown to influence bird
communities (Saab et al. 1995), and its effects
are particularly apparent in deciduous systems
(Fleischner 1994). Our study includes a diversity
of grazing regimes, and the effects on bird com-
munities generally match the intensity and du-
ration of the grazing. In the Missouri River,
grazed sites have had cattle on them for over 50
years, and ungrazed sites have been free of graz-
ing for over 25 years. This is reflected in the
severe effects of grazing on the bird communi-
ties. In contrast, grazing-related differences were
few in the Sheldon system, where long-term
livestock grazing has left a highly degraded set
of riparian habitats. Ungrazed survey locations
were only in their third year of rest, and the
general lack of differences in avian community
composition reflected the very limited recovery
made by the riparian plant community (D. Dob-
kin et al., unpubl. data).
Our finding that grazing had no effect on de-
tection frequencies of Brown-headed Cowbirds
in any riparian system runs counter to most pre-
vious studies (Page et al. 1978, Mosconi and
Hutto 1982, Knopf et al. 1988, Schulz and Len-
inger 1991; but see Taylor 1986). However, we
measured grazing pressure on individual study
sites, not on the landscape as a whole; thus cow-
birds may be foraging in grazed sites but search-
ing for nests in ungrazed sites, where hosts are
generally more abundant. Thus grazed and un-
grazed sites may offer different resources for
cowbirds; previous research in the Bitterroot
River system has shown that cowbird abundance
is strongly related to host abundance, as well as
distance from agriculture (Tewksbury et al.
1999), supporting this possibility.
As cowbirds are not consistently more abun-
dant in grazed areas, the much lower primary
host abundance in grazed areas may not be sim-
ply the result of higher parasitism pressure, but
instead may be due to interactions between veg-
etation differences and predation rates (Knopf
FRAGMENTATION AND GRAZING--Tewksbury et al. 181
1985), lack of appropriate settling cues in grazed
sites, or indirect interactions between food avail-
ability, foraging behavior, and nest predation
(Martin 1992). Many primary hosts are also
long-distance migrants, and we found that this
group was lower in abundance in grazed areas
as well. Saab et al. (1995) found the same result
after reviewing the literature, and suggested that
this could be due to the high proportion of open-
cup nesters among long-distance migrants and
greater sensitivity of open-cup nesters to graz-
ing. Our data are consistent with this interpre-
tation: open-cup nesters were more heavily af-
fected by grazing than were primary or second-
ary cavity nesters. Open-cup nesters accounted
for 96% of species and 81% of detections for
long distance migrants, 82% of species and 28%
of detections for short-distance migrants, and
only 58% of species and 37% of all detections
for residents.
Along the Missouri River, differences in pri-
mary cavity nesters between grazed and ungra-
zed areas were as great as differences in open-
cup nesters, a finding that contrasts sharply with
previous work (Good and Dambush 1943, Mos-
coni and Hutto 1982, Medin and Clary 1991).
The strong community-wide effects seen on the
Missouri may be related to changes in vegeta-
tion that take place with continued grazing over
long time scales (Ohmart 1994). High-nesting
birds and primary cavity nesters may escape the
immediate effects of grazing, but as cottonwood
and aspen forests age, lack of recruitment of
new trees causes a reduction in small and even-
tually large tree classes, which will affect the
density of cavity nesters (Sedgwick and Knopf
1990, Dobkin et al. 1995) and the density of
high-nesting species in general. This process
may be well advanced in grazed locations along
the Missouri, but is unlikely where grazing has
been less continuous. Our results comparing
low-nesting species to high-nesting species fur-
ther support this possibility. Low open-cup nest-
ing species have been shown to be particularly
sensitive to grazing due to the large effects cattle
have on the lower strata of vegetation (Sedgwick
and Knopf 1987, Saab et al. 1995, Saab 1998).
We also found that while both low and high
nesting species had lower detection frequencies
in grazed areas, these differences were greater
for low nesting species. Along the Missouri,
however, equally strong differences were found
for both low- and high-nesting species, suggest-
ing that long-term grazing may have affected
canopy structure, snag retention, and recruitment
of trees into the canopy (Ohmart 1994).
COWBIRDS AND LANDSCAPES
Cowbirds could pose regional threats to ri-
parian avifaunas due to their ubiquitous nature,
their tendency to reach high densities in riparian
areas (Tewksbury et al. 1999, Ward and Smith
2000), and the effects of parasitism both on in-
dividual hosts (Pease and Grzybowski 1995,
Woodworth 1999) and on community composi-
tion (De Groot et al. 1999). Because of this,
much work has examined landscape-scale ef-
fects on cowbird abundance and parasitism pres-
sure locally (Gustarson and Crow 1994, Coker
and Capen 1995, Gates and Evans 1998, Hejl
and Young 1999; Tewksbury et al. 1998, 1999;
Young and Hutto 1999), regionally (Donovan et
al. 1995b, 1997, 2000; Robinson et al. 1995a,
Thompson et al. 2000) and nationally (Hochach-
ka et al. 1999). The majority of this work in-
vestigated only one or two factors that could
limit cowbird abundance, in contrast to our re-
sults, which suggest that multiple landscape
components may be important in the western
United States.
To date, the species that are most often af-
fected by parasitism appear to be extremely hab-
itat limited (Robinson et al. 1995b), suggesting
that the primary cause of population decline is
not parasitism but habitat loss. With the steady
increase in human encroachment upon riparian
systems, and the highly mobile nature and gen-
eralist feeding strategy of the cowbird (Thomp-
son 1994, Robinson et al. 1995b), we already
have lost most of our opportunity to set aside
large riparian areas in landscapes that are remote
enough to preclude cowbirds altogether. Thus most
communities will be affected by cowbirds, and at-
tention should shiti to strategies for minimizing the
effect of cowbirds at local and regional scales. We
suggest that preserving and enhancing the size of
deciduous areas that are surrounded by few human
habitations and little agriculture will have the
greatest benefit for host populations, as cowbirds
in these landscapes are likely limited by feeding
habitat. In largely agricultural landscapes, cow-
birds are more likely limited by availability of host
nests, not feeding areas; thus moderate reductions
in feeding areas in these areas (feedlots, bird-feed-
ers, corrals, livestock pastures) may have little ef-
fect on rates of brood parasitism.
MANAGEMENT IMPLICATIONS AND SPECIES OF
PARTICULAR CONCERN
Our data suggest that the greatest threats to
western deciduous riparian systems are (1) con-
tinued deciduous habitat loss and reduction in
riparian area, (2) continued cattle grazing in re-
maining deciduous systems, and (3) increasing
concentration of homes and farms along major
riparian systems in the western United States.
All of these factors are likely to have negative
effects on bird communities in deciduous ripar-
ian areas, but rarely is it possible to extrapolate
182 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 6. SUMMARY OF ALL SPECIES SIGNIFICANTLY LESS ABUNDANT IN AREAS WITH MORE HUMAN HABITATION,
MORE AGRICULTURE, OR LESS DECIDUOUS HABITAT AT EITHER SCALE, OR IN GRAZED HABITATS, TESTED IN AT LEAST
TWO RIPARIAN SYSTEMS
Net
negativ
More human More Less Negative positive West
Species habitation agriculture deciduous Grazing responses responses BBS a
Red-naped Sapsucker 0/- -/0 -/- 4 4
MacGillivray's Warbler -/- / +/+ 4 2
Song Sparrow +/- +/0 -/- - 4 2 **
Western Scrub-jay /0 -/- 3 3
Veery 0/- -/0 -/0 3 3
Warbling Vireo 0/- -/- 3 3
Red-eyed Vireo -/- - 3 3 **
Yellow-romped Warbler 0/- -/- 3 3
Black-capped Chickadee -0/+ -/- - 3 2 **
Townsend's Warbler /0 -/- +/+ 3 1
Ruffed Grouse 0/- /0 2 2 *
American Crow 0/- 0/ 2 2
Violet-green Swallow -/- 2 2
Swainson's Thrush 0/- 0/ 2 2
Gray Catbird -/0 - 2 2
Fox Sparrow -/0 2 2
Dusky Flycatcher 0/- /0 + 2 1 *
Orange-crowned Warbler -/0 -/+ 2 1 *
Western Wood-pewee +/+ +/+ -/0 2 -2 **
American Robin +/+ +/+ 0/- - 2 -2
Cedar Waxwing +/0 +/0 -/- 2 -2
Yellow Warbler +/+ +/+ -/- 2 -2
Nuttall's Woodpecker /0 1 1
Hairy Woodpecker 1 1
Least Flycatcher /0 1 1
Ash-throated Flycatcher -/0 1 1
Cordilleran Flycatcher - 1 1
Western Kingbird 0/- 1 1
Northern Rough-winged Swallow -/0 1 1
Bewick's Wren -/0 1 1
Amehcan Redstart -/0 I 1
Western Tanager 0/- I 1
Green-tailed towhee - 1 1
Chipping Sparrow -/0 1 1 **
White-breasted Nuthatch +/0 0/- 1 0
Ruby-crowned Kinglet /0 0/+ 1 0
Black-billed Magpie +/+ 0/ 1 - 1
Black-headed Grosbeak +/0 +/0 /0 1 - 1
Red-shafted Flicker +/0 +/0 0/- 1 -2 *
Red-winged Blackbird +/+ +/+ 0/ I -3 **
Willow Flycatcher +/+ +/+ 0/ 1 -3 **
Notes: Significantly (P - 0.05) lower detection frequency ( ), significantly higher detection frequency (+), and no significant difference in detection
frequency (0) are listed for each species in which at least 2 river systems were used in the analysis. Significant effects at local and regional scales
are listed (local/regional). Species are ranked by the number of negative responses and the net (negative - positive) responses.
Trend estimates from the Western Breeding Bird Survey region (Sauer et al. 2000). Species with a declining trend (P < 0.25) in the past 20 years,
or over the course of the entire survey period, are single starred (*) and species showing significant declines (P < 0.05) are marked with double stars
(**).
from local studies to regional population trends.
The data provided here allow us to highlight
consistent trends, and by summarizing the re-
sponses to individual land uses we can also iden-
tify those species that appear to be at particular
risk due to human landscape modification and
livestock grazing (Table 6). We ranked each spe-
cies based on the number of negative responses
(lower abundance due to grazing, higher
amounts of human habitation or agriculture, or
lower amounts of deciduous habitat) making the
assumption that species vulnerable to multiple
human land-uses should receive greater attention
than species vulnerable to only one type of land-
use. Ten species had at least three negative re-
sponses. Of these, the Veery, MacGillivray's
FRAGMENTATION AND GRAZING--Tewksbury et al. 183
Warbler, Song Sparrow, Warbling Vireo, and
Red-eyed Vireo may be the most at risk, as all
but the Warbling Vireo nest lower in dense veg-
etation (Ehrlich et al. 1988; J. J. Tewksbury un-
publ. data) and all frequently suffer brood par-
asitism (Friedmann et al. 1977; J. J. Tewksbury
unpubl. data). These species were all less abun-
dant in landscapes with high human habitation
and agriculture or low amounts of riparian hab-
itat, and three respond negatively to livestock
grazing. In addition, all of these, as well as the
Red-naped Sapsucker, are found almost exclu-
sively in deciduous vegetation. We suggest that
these species should be monitored closely in
western riparian habitats, and research should be
initiated to examine mechanisms behind these
patterns.
CONCLUSIONS
Management that focuses on enhancing the
size of remaining deciduous riparian areas and
reducing cattle grazing on these areas is likely
to produce the greatest benefits for bird species
dependent on western deciduous riparian habi-
tats. In addition, strict limitations on building in
floodplains will reduce the need fbr absolute
flood control on riparian systems, which results
in reduced riparian area. Protecting the few areas
where riparian systems run through landscapes
that are relatively free of human disturbance
should be a high conservation priority both to
protect the last unaltered pieces of one of the
most endangered and important breeding habi-
tats for western birds, and to preserve these few
natural landscapes as benchmarks to use in ex-
amining the effects of land conversion. Without
natural landscapes, we may lose sight of the
conditions we are attempting to preserve.
ACKNOWLEDGMENTS
The results summarized here were produced by five
independent field teams working over the past decade,
and our work would not have been possible without
the sharp eyes and strong ears of the many people who
conducted surveys in these riparian systems. We thank
R. Hutto, B. Kus, and L. George for their comments
on earlier drafts of this manuscript.
APPENDIX 1
DESCRIPTIONS OF INDIVIDUAL RIPARIAN SYSTEMS
Sacramento
Location: all study sites are between Red Bluff and
Colusa, California. Most sites are in remnant forest
patches in the Sacramento National Wildlife Refuge.
Vegetation: the floodplain is a complex of early- to
late-successional deciduous forests dominated suc-
cessively by willows (Salix spp.) and cottonwood
(Populus spp.), sycamore (Platanus spp.), ash
(Fraxinus spp.), and valley oak (Quercus lobata).
Adjacent upper terraces are dominated by valley
oak. See Gaines (1974) for a detailed description of
study sites.
Grazing: moderate to heavy cattle grazing for the past
15+ years on grazed sites. Ungrazed sites had been
without cattle for at least 3 years before data collec-
tion.
San Joaquin
Location: all survey locations are in the northern por-
tion of Calitbrnia's San Joaquin Valley, on levee
roads adjacent to riparian stringers, grasslands, and
recently (last decade) re-flooded grasslands in the
San Luis National Wildlife Refuge.
Vegetation: similar to Sacramento River, dominated by
willows and cottonwood, sycamore, ash, and valley
oak. Willows and marsh vegetation are more com-
mon than valley oak.
Grazing: moderate to heavy cattle grazing tbr the past
15+ years on grazed sites. Ungrazed sites have been
without cattle for at least 3 years before data collec-
tion.
Snake
Location: Sites are in an 80-km stretch just down-
stream of the Idaho/Wyoming border in eastern Ida-
ho. For a detailed description of sites see Saab
(1999).
Vegetation: Cottonwood (Populus angustifolia) for-
ests. Understory species include dogwood (Cornus
stolonifera), thin-leafed alder (Alnus incana), water
birch (Betula occidentalis), and willows.
Grazing: moderate to heavy grazing for the past 30+
years on grazed sites. Ungrazed sites have been
without cattle for at least three years before data
collection.
Bitterroot
Location: survey locations were located along a 40-km
stretch of the Bitterroot River and smaller tributaries
throughout the Bitterroot Valley between Corvallis
to the north and continuing past Darby to the south.
See Tewksbury et al. (1998, 1999) for details of
study sites.
Vegetation: cottonwood and willow dominate sites
along the Bitterroot River, with dogwood, thin-
leafed alder, and water birch in smaller quantities.
Along tributaries, cottonwood, aspen, and willow
are dominant.
Grazing: all study sites were ungrazed or rested for at
least five years; thus the Bitterroot River is not in-
cluded in our analysis of grazing effects.
Missouri
Location: ungrazed survey locations were located on
the Charles M. Russell National Wildlife Refuge,
and grazed survey locations were in a 40-km stretch
of river bordering the refuge to the west.
Vegetation: riparian stands consist of mid- to late-seral
riparian vegetation (Hansson et al. 1995) dominated
by Great Plains cottonwood (Populus deltoides),
green ash (Fraxinus pennsylvanica), and willow.
Floodplains are bounded by the steep, highly eroded
"Missouri Breaks," which rise to 300m from the
floodplain and support upland vegetation dominated
by shrubs.
184 STUDIES IN AVIAN BIOLOGY NO. 25
Grazing: moderate to heavy grazing for the past 30-
120 years on grazed sites, ungrazed sites have had
no cattle for the past 30 years.
Hart Mountain
Location: all Hart Mountain sites were located in the
northwestern Great Basin on the 115,000 ha Hart
Mountain National Antelope Refuge (42025 ' N,
119040 ' W) in southeastern Oregon. Data were used
from surveys conducted along small streams in five
separate drainages.
Vegetation: riparian woodlands occurred as narrow rib-
bons of riparian habitat, primarily aspen and wil-
lows, surrounded by sagebrush (Artemisia spp.)
steppe, or as dense stands of smaller-stature trees on
sideslopes and snowpocket areas in the higher
reaches of riparian drainages. For additional details
see Dobkin et al. (1995, 1998).
Grazing: in the autumn of 1990, livestock were re-
moved completely from the Hart Mountain refuge,
ending continuous livestock use dating back to the
1870s. For this study, we classified data from 1991
(the first growing season following livestock remov-
al) as "grazed," and data from 1993 (the third grow-
ing season following livestock removal) as "rested"
or "ungrazed." We did not use data for 1992.
Sheldon
Location: all Sheldon sites were on the Sheldon Na-
tional Wildlife Refuge located in the northwestern
corner of Nevada, approximately 55 km southeast
of Hart Mountain. Riparian areas occur mostly as
narrow valleys and canyons bordered by the steep
rimrock of tablelands.
Vegetation: riparian habitat is severely limited at Shel-
don, and nearly all riparian habitat in this study con-
sisted of degraded willow-dominated areas.
Grazing: as at Hart Mountain, livestock were removed
from the Sheldon Refuge in the autumn of 1990
following continuous livestock use dating back to
the 1870s. For this study, we classified data from
1991 (the first growing season following livestock
removal) as "grazed," and data from 1993 (the third
growing season following livestock removal) as
"rested" or "ungrazed." We did not use data for
1992.
FRAGMENTATION AND GRAZiNG--Tewksbury et al. 185
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APPENDIX 5. GRAZING EFFECTS ON INDIVIDUAL SPECIES, BY RIVER
Detection/survey Mann-Whitney U-test
River system Ungrazed Grazed U W
Sacramento
Less Abundant in Grazed Areas
Tree Swallow 0.5873 0.0597 66.5 111.5 0.001
Black-headed Grosbeak 0.6412 0.2735 95.5 140.5 0.011
Downy Woodpecker 0.0960 0.0094 105.5 150.5 0.013
American Robin 0.1555 0.0409 123.0 168.0 0.044
California Towhee 0.0406 0.0000 144.0 189.0 0.060
Mourning Dove 0.1550 0.0472 127.5 172.5 0.062
Bank Swallow 0.0821 0.0000 153.0 198.0 0.089
White-breasted Nuthatch 0.0761 0.0189 146.5 191.5 0.122
Turkey Vulture 0.1250 0.0189 155.5 200.5 0.152
European Starling 0.1061 0.0094 157.0 202.0 0. 156
Western Wood-pewee 0.5840 0.3741 148.0 193.0 0.179
More Abundant in Grazed Areas
California Quail 0.0457 0.2169 78.5 1159.5 0.001
Warbling Vireo 0.0341 0.0880 105.5 1186.5 0.004
Wilson's Warbler 0.1370 0.2578 91.0 1172.0 0.007
Bewick's Wren 0.6334 0.8708 116.5 1197.5 0.039
Lazuli Bunting 0.3520 0.4999 123.5 1204.5 0.057
Lesser Goldfinch 0.1702 0.3804 142.5 1223.5 0.130
Snake
Less Abundant in Grazed Areas
Veery 0.4791 0.1161 118.0 328.0 0.001
Song Sparrow 0.8020 0.3124 117.0 327.0 0.001
Fox Sparrow 0.1606 0.0131 134.5 344.5 0.002
Black-capped Chickadee 0.3667 0.2178 150.5 360.5 0.015
Lazuli Bunting 0.1176 0.0678 154.0 364.0 0.016
Yellow Warbler 2.7632 2.2466 152.0 362.0 0.017
Mallard 0.0474 0.0118 174.5 384.5 0.029
Black-headed Grosbeak 0.2386 0.1465 162.5 372.5 0.030
Belted Kingfisher 0.0293 0.0091 189.0 399.0 0.041
Gray Catbird 0.1490 0.0763 172.5 382.5 0.047
Cedar Waxwing 0.3268 0.1940 172.0 382.0 0.050
Ruffed Grouse 0.0321 0.0056 203.5 413.5 0.058
Violet-green Swallow 0.2309 0.0971 179.0 389.0 0.059
Broad-tailed Hummingbird 0.0118 0.0022 213.0 423.0 0.096
MacGillivray's Warbler 0.0532 0.0149 196.0 406.0 0.107
Spotted Sandpiper 0.0302 0.0158 198.0 408.0 0.118
Swainson's Thrash 0.0403 0.0068 211.0 421.0 0.147
More Abundant in Grazed Areas
House Wren 0.4621 1.1689 107.0 458.0 0.001
Mourning Dove 0.2488 0.5509 149.5 500.5 0.014
Pine Siskin 0.0044 0.0529 180.5 531.5 0.019
Black-billed Magpie 0.2475 0.4988 160.0 511.0 0.026
European Starling 0.3474 1.2135 163.5 514.5 0.032
Cassin's Finch 0.0201 0.0326 208.0 559.0 0.167
Missouri
Less Abundant in Grazed Areas
Mourning Dove 2.2941 0.7917 19.5 97.5 <0.001
American Robin 2.3824 1.0833 27.0 105.0 0.001
Red-eyed Vireo 0.7059 0.0417 45.5 123.5 0.004
Red-shafted Flicker 1.6765 0.4583 39.0 117.0 0.004
Least Flycatcher 2.1176 1.2083 43.5 121.5 0.008
Brown Thrasher 0.7059 0.1250 48.0 126.0 0.009
Western Wood-pewee 1.8824 1.0833 48.0 126.0 0.011
Lazuli Bunting 1.6765 0.9167 46.0 124.0 0.011
Ovenbird 0.4706 0.0000 60.0 138.0 0.013
House Wren 2.7647 2.0000 54.0 132.0 0.028
Black-headed Grosbeak 0.7353 0.1667 57.5 135.5 0.029
Bullock's Oriole 0.6471 0.2083 57.0 135.0 0.031
202
APPENDIX 5. CONTINUED
STUDIES IN AVIAN BIOLOGY
NO. 25
Detection/survey Mmn-Whitney U-test
River system Ungrazed Grazed U W P
American Redstart 0.4706 0.0833 63.0 141.0 0.034
Yellow Warbler 3.7941 2.5833 58.0 136.0 0.047
Yellow-breasted Chat 2.8529 2.0417 59.0 137.0 0.051
Hairy Woodpecker 0.4118 0.0833 65.0 143.0 0.052
Gray Catbird 0.6176 0.1250 70.5 148.5 0.108
Common Grackle 0.6471 0.3333 76.5 154.5 0.132
Black-capped Chickadee 0.6471 0.2083 74.5 152.5 0.161
American Goldfinch 2.3529 1.5417 72.0 150.0 0.177
More Abundant in Grazed Areas
Eastern Kingbird 0.1176 0.3333 67.0 220.0 0.048
Spotted Towhee 0.9706 1.3750 67.5 220.5 0.115
Hart
Less Abundant in Grazed Areas
Cordilleran Flycatcher 0.3333 0.0000 140.0 350.0 0.005
Hairy Woodpecker 0.4286 0.0500 130.5 340.5 0.005
Green-tailed Towhee 0.5714 0.1500 121.5 331.5 0.006
Rock Wren 0.2619 0.0000 170.0 380.0 0.043
Wilson's Warbler 0.2381 0.0500 170.5 380.5 0.092
Red-tailed Hawk 0.2857 0.1000 171.0 381.0 0.138
More Abundant in Grazed Areas
Swainson's Thrush 0.1905 0.4000 160.0 391.0 0.091
Black-headed Grosbeak 0.3333 0.6500 154.0 385.0 0.094
Sheldon
Less Abundant in Grazed Areas
Western Wood-pewee 0.6000 0.0000 22.5 67.5 0.017
More Abundant in Grazed Areas
Brewer's Sparrow 0.2000 0.7778 23.0 78.0 0.039
Yellow Warbler 0.3000 0.7778 27.0 82.0 0.096
Notes: Values are mean detections per survey, md results of Mann-Whitney U-test for differences between grazed and ungrazcd. All species detected
at least 15 times on a given river system with a P < 0.2 from a Mann-Whitney U-test are included.
Studies in Avian Biology No. 25:203-220, 2002.
SPOTTED OWLS, FOREST FRAGMENTATION, AND
FOREST HETEROGENEITY
ALAN B. FRANKLIN AND R. J. GUTIIRREZ
Abstract. The Spotted Owl (Strix occidentalis) has been a focal species in the United States in terms
of loss and fragmentation of old coniferous forests. Past research has shown a strong association
between Spotted Owls and old coniferous forests. Thus, these vegetation types are considered syn-
onymous with Spotted Owl habitat. Past fragmentation of old coniferous forests in the Pacific North-
west, the Sierra Nevada, southern California, and the Southwest has resulted from natural disturbance
(e.g., fire), edaphic conditions, and timber harvesting. These processes have occurred at different rates
and levels. We reviewed the existing literature on the effects of forest fragmentation and heterogeneity
on Spotted Owls at three different scales: a range-wide scale where once-connected populations have
been isolated from each other, a population scale where populations with different fragmentation
regimes have different demographics, and a territory scale where individuals occupying territories with
different fragmentation regimes have different fitness. Studies at the range-wide scale have concen-
trated on processes, such as juvenile dispersal. There are no published studies on the effects of frag-
mentation or heterogeneity at the population scale, although the potential exists for examining those
effects with current studies. Lack of empirical data on the effects of fragmentation on Spotted Owls
led to the development of spatially-explicit simulation models as an aid to reserve design for this
species. In addition, some populations of Spotted Owls are naturally disjunct at the range-wide scale.
Most empirical studies have concentrated on the territory scale, and most of those studies have ex-
amined the effects of fragmentation and heterogeneity on occupancy. We attempted a simple meta-
analysis using effect sizes estimated from these studies. However, this analysis was hampered by lack
of replicated studies among subspecies and among provinces within subspecies. In addition, studies
did not use similar metrics to describe fragmentation and heterogeneity. Thus, empirical studies fol-
lowing simulation models are equivocal in their conclusions. Many questions remain unanswered
concerning the effects of forest fragmentation and heterogeneity on Spotted Owls. We provide a set
of key questions that need to be addressed to better understand the effects of fragmentation and
heterogeneity on Spotted Owls. We also suggest that future research concentrate on understanding
natural disturbance regimes and the extent to which timber harvesting is compensatory or additive to
natural disturbance regimes. Research on the effects of fragmentation on Spotted Owls should also
include alternative hypotheses that some levels of fragmentation and/or heterogeneity may benefit
Spotted Owl populations.
Key Words: habitat; habitat fragmentation; meta-analysis; population dynamics; Spotted Owl.
The Spotted Owl (Strix occidentalis) occurs in
the western United States, Canada, and Mexico,
and is comprised of three subspecies' the North-
em Spotted Owl (S. o. caurina), the California
Spotted Owl (S. o. occidentalis), and the Mexi-
can Spotted Owl (S. o. lucida) (Gutierrez et al.
1995; Fig. 1). All three subspecies have similar
life-history characteristics, with high adult sur-
vival, low juvenile survival, and low reproduc-
tion (LaHaye et al. 1992, Noon et al. 1992,
White et al. 1995, Forsman et al. 1996, Seamans
et al. 1999).
Habitat associations of Spotted Owls are var-
iable across and within subspecies. However, all
three subspecies have a strong association with
older forests for nesting, roosting, and foraging
(Forsman et al. 1984, Carey et al. 1990, Solis
and Gutierrez 1990, Call et al. 1992, Gutierrez
et al. 1992; Buchanan et al. 1993, 1995; Ganey
and Balda 1994, Seamans and Gutierrez 1995,
Forsman and Giese 1997, LaHaye et al. 1997,
Steger et al. 1997, Hershey 1998, Young et al.
1998, LaHaye and Gutierrez 1999). In general,
these forests are characterized by an overstory
of large (-->52 cm dbh) conifers, with a multi-
layered understory of conifers and/or hardwood
trees and shrubs, and decadence in the form of
snags and coarse woody debris. These associa-
tion have been documented at several scales (see
reviews in Gutierrez et al. 1992, 1995; Ganey
and Dick 1995). However, there are exceptions
to the association of Spotted Owls with old co-
niferous forests. Mexican Spotted Owls are
found in both old forests and in steep, incised
canyon systems with little or no forest cover
(Rinkevich and Gutierrez 1996, Ganey and Dick
1995). Nevertheless, the majority of Mexican
Spotted Owl populations are found in areas con-
taining older coniferous forests where they
strongly associate with these forests (Ward et al.
1995, Ganey and Dick 1995). In addition, owls
frequently inhabit previously logged conifer for-
ests or oak (Quercus spp.) forests (Gutierrez et
al. 1992, Folliard 1993). In these latter two sit-
uations, residual old trees are often present, the
current forest has structural characters similar to
203
204 STUDIES IN AVIAN BIOLOGY NO. 25
West Cascades
I s. o. caurlna
I S. o. occidentalis
_ S.o. luctda
FIGURE 1. Geographic distribution of three subspe-
cies of Spotted Owl (Strix occidentalis). Regions
shown for Northern Spotted Owl are from Agee and
Edmonds (1992).
old forests, and/or microclimates are modified
by marine climates or streams.
In addition to differences between subspecies,
there are subtle differences in forests used by
Spotted Owls within subspecies. For example,
Northern Spotted Owls are found in forests com-
posed almost purely of conifers in their northern
range. However, in the southern extent of their
range many hardwood species dominate the
mid- and understories while conifers still domi-
nate the overstory. Despite these and other ex-
ceptions, it is generally believed that Spotted
Owls associate with older coniferous forests and
that these forests provide some key elements for
their survival and reproduction.
Both the Northern and Mexican subspecies
were listed as threatened under the Endangered
Species Act of the United States (U.S. Fish and
Wildlife Service 1990, 1993). One criterion that
led to listing was habitat loss and fragmentation
due to logging and forest management. Existing
scientific information at the time of the listing
of these two subspecies suggested that these
owls were dependant on interior older forest for
foraging, roosting, and nesting. Another criteri-
on was the failure of existing regulatory mech-
anisms to control loss and fragmentation of old-
er coniferous forest (U.S. Fish and Wildlife Ser-
vice 1990, 1993). For similar reasons, the Cali-
fornia subspecies was recently petitioned for
listing (Center for Biological Diversity 2000).
In this paper, we first review the concepts of
fragmentation and heterogeneity as they apply
to Spotted Owls. Then, we review simulation
models developed to facilitate conservation
strategies. Next, we review the existing evidence
on the effects of habitat fragmentation on pop-
ulation processes in the three subspecies of
Spotted Owls. In particular, we examine habitat
fragmentation at three scales: range-wide, pop-
ulation, and territory. The range-wide scale en-
compasses the geographic range of each subspe-
cies. Habitat fragmentation at this scale may af-
fect meta-population dynamics and gene flow
between sub-populations (Guti6rrez and Hard-
son 1996). The population scale is nested within
the range-wide scale. Habitat connectivity is de-
termined by the dispersal ability of young Spot-
ted Owls and local movements of individuals
between territories. Potential source-sink popu-
lation dynamics will be affected by habitat frag-
mentation and these effects are measurable by
variation in rates of population change within
populations. The final scale we consider is at the
territory level. At this scale, the ability of indi-
vidual territory holders to move across their ter-
ritories may be affected by connectivity between
blocks of habitat within individual territories.
Effects of fragmentation will be expressed in
terms of reproductive output and survival of in-
dividuals, and by inter-specific interactions such
as competition, predation, and hybridization.
Clearly, these scales overlap across the three cat-
egories (range-wide, population, and territory)
that we examined. However, most studies on
Spotted Owls encompass one or more of these
three scales.
FRAGMENTATION, HETEROGENEITY,
AND SPOTTED OWL HABITAT
Mature and old-growth forests are considered
synonymous with Spotted Owl habitat. Thus,
fragmentation of these forests is considered hab-
itat fragmentation for Spotted Owls. Using the
definition of Franklin et al. (this volume), habitat
fragmentation occurs when habitat becomes dis-
continuous such that changes occur in popula-
tion processes. For example, it is unlikely that
road cuts (small-scale fragmentation) affects
Spotted Owls to the same degree as large cata-
strophic fires or clearcuts. As Franklin et al. (this
volume) point out, habitat fragmentation is es-
sentially a binary outcome (habitat versus non-
habitat) whereas heterogeneity is a multi-state
outcome. In the context of the scales discussed
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 205
Pre-disturbance
Post-disturbance
ß Old Forest
ß ,', Young Forest
[] Non-Forest
FIGURE 2. Two hypothetical scenarios in patterns of habitat fragmentation in Spotted Owls: (a) older forest
alone is considered Spotted Owl habitat, and (b) older forest in some combination with younger forest is
considered Spotted Owl habitat.
in this paper, forest heterogeneity is the diversity
of vegetation types and seral stages within a giv-
en area.
For older forests to be synonymous with Spot-
ted Owl habitat, these forests must provide the
requisite resources and conditions that promote
occupancy and allow individuals to survive and
reproduce (see definitions in Franklin et el. this
volume). However, there is evidence that other
vegetation types may also contribute to Spotted
Owl habitat. This evidence is mostly indirect
and relates to abundances of Spotted Owl prey
in different vegetation types (Rosenberg and An-
thony 1992, Williams et el. 1992, Carey and
Peeler 1995, Ward and Block 1995, Zabel et el.
1995, Sureda and Morrison 1998, Ward et el.
1998). Thus, ecotones between older forest and
other seral stages may contribute to Spotted Owl
habitat, an idea that we will explore further (see
HABITAT FRAGMENTATION AT THE TERRITORY
SCALE below).
If other seral stages contribute to Spotted Owl
habitat as suggested above, then some conver-
sion of older forest to younger seral stages does
not necessarily represent habitat fragmentation
for Spotted Owls. For example, assume a distri-
bution of old forest shown in Figure 2 prior to
disturbance. After disturbance fragments the
older forest, a new distribution of young and old
forest results. If only old forest is Spotted Owl
habitat, then fragmentation of older forest alone,
as depicted by scenario A in Figure 2, results in
habitat fragmentation for Spotted Owls. How-
ever, if young forests in some combination with
older forest constitutes Spotted Owl habitat, as
represented by the condition in scenario B in
Figure 2, then no habitat fragmentation occurs
for Spotted Owls. In the latter scenario, forest
fragmentation is represented by beterogeneity of
seral stages. Therefore, we acknowledge that
other vegetation types may contribute to Spotted
Owl habitat (e.g., forest heterogeneity) in our
examination of the empirical studies.
MODELS SIMULATING THE EFFECTS OF HABITAT
LOSS AND FRAGMENTATION ON SPOTTED OWLS
The Spotted Owl became a conservation issue
because of losses of old coniferous forest from
logging. Several management plans were devel-
oped but empirical data were generally lacking
to test the efficacy of these plans. Therefore,
simulation models were developed to examine a
critical question for management planners--
what is the likely persistence of the owl if its
habitat continues to be removed? These simu-
lation models ranged from deterministic to sto-
chastic and were used primarily in developing
management strategies for the Northern Spotted
Owl (Lande 1988, Doak 1989, Lamberson et el.
1992, McKelvey et el. 1992).
The assumption of these models varied but all
assumed that (1) habitat in the form of old co-
niferous forest was either suitable or unsuitable,
with no definitions of habitat quality; and (2)
juvenile Spotted Owls searched the landscape
during dispersal with some specific behavior,
e.g., randomly or with some finite number of
searches. All of the models predicted that Spot-
206 STUDIES IN AVIAN BIOLOGY NO. 25
ted Owls would not persist with continued loss
of old coniferous forest. An early deterministic
model (Lande 1988) predicted a critical thresh-
old for Northern Spotted Owls when the pro-
portion of suitable habitat (old coniferous forest)
on the landscape fell below 0.21. Other simu-
lation models did not make such explicit predic-
tions because assumptions on how dispersing ju-
venile owls searched the landscape was critical
in determining model results. Nevertheless, all
the models clearly predicted the demise of
Northern Spotted Owl populations, given the
model assumptions and continued loss of old co-
niferous forest.
All of the models also assumed that habitat
fragmentation would be a consequence of loss
of old coniferous forest through logging. This
was a reasonable assumption given the knowl-
edge at that time concerning Spotted Owl dis-
persal and harvest unit strategies in western co-
niferous forests. However, there were few ex-
plicit predictions from the models regarding the
nature of fragmentation resulting from habitat
loss.
CAUSES OF FRAGMENTATION AND HETEROGENEITY
Historically, fire was the major disturbance af-
fecting forested landscapes across the range of
all three subspecies (Weatherspoon et al. 1992,
Agee 1993, Skinner and Chang 1996, Swetnam
and Baisan 1996a, Taylor and Skinner 1998).
Before organized fire suppression programs, fire
occurred throughout the range of the Spotted
Owls at fairly frequent intervals with differing
degrees of intensity (Table 1, Fig. 3). California
and Mexican Spotted Owls experienced frequent
low to moderate intensity fires, whereas North-
ern Spotted Owls experienced greater variation
in fire return intervals (Table 1; see also Skinner
and Chang 1996). Owls occurring in the West
Cascades, Coast Ranges, and Redwood provinc-
es were probably less aftcted by fire than in
other parts of their range. However, these mesic
provinces experienced higher fire intensities less
frequently than drier portions of the owl's range.
Of the 3,753 owl pairs reported within the range
of the Northern Spotted Owl (Gutierrez 1994),
37% were in the Klamath and Eastern Cascades
provinces, which experienced fire regimes char-
acterized by frequent, less-severe fires than
those in western Oregon and Washington (Taylor
and Skinner 1998).
Fire suppression by humans disrupted natural
fire cycles beginning in the 20th century (Fig. 3;
Weatherspoon et al. 1992, Agee 1993, Swetnam
and Baisan 1996a), but was not relatively eflc-
rive until the late 1940s (Wills 1991). The ef-
fects of fire suppression on landscapes occupied
by Spotted Owls have been poorly understood,
<
<
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 207
Fire Suppression
1700 170 18)0 1850 19)0 1950
Year
FIGURE 3. Fire occurrence within the range of the Mexican Spotted Owl before and after fire suppression at
63 fire history sites in Arizona and New Mexico (Swetnam and Baisan 1996a).
but several studies suggested that forests prior
to fire suppression were less dense and had more
openings. Comparing aerial photos from 1944
and 1985, Skinner (1995) found that openings
(areas -->0.1 ha occupied by vegetation less than
a third the height of surrounding stands) de-
creased 39% within unlogged watersheds of the
Klamath Province in northern California. In ad-
dition, openings became smaller and more dis-
persed across the landscape after 40 years of fire
suppression. Sierran mixed-conifer forests oc-
cupied by California Spotted Owls shifted from
frequent low- to moderate-severity fires, to long-
interval, high-severity, stand-replacing fires after
fire suppression (Weatherspoon et al. 1992).
This situation probably also applied to forests
occupied by Northern and Mexican Spotted
Owls. Weatherspoon et al. (1992) also suggested
that fire suppression on Sierran forests created
more homogeneous landscapes in terms of for-
ested stand configuration. Prior to fire suppres-
sion, forests probably were dominated by large,
old trees intermixed with a complex array of
small, even-aged stands representing a wide
range of age- and size-classes (McKelvey and
Johnston 1992, Weatherspoon et al. 1992),
whereas post-fire suppression forests have be-
come more homogeneous and even-aged. How-
ever, there has been considerable disagreement
concerning forest conditions under natural fire
regimes (Sierra Nevada Ecosystem Project 1996:
63). In either case, the composition and structure
of post-fire suppression forests were complicated
by logging activities, which have largely re-
placed fire as the most frequent disturbance to
forests occupied by all three subspecies of Spot-
ted Owl.
Coincident with fire suppression, logging be-
gan in forests across the range of the Spotted
Owl at the turn of the 20th century. However,
logging on publicly-owned forests, and subse-
quent fire suppression, did not begin until
around 1940-1950 (Harris 1984, McKelvey and
Johnston 1992). In most parts of the owl's range,
logging practices shifted from uneven-aged
management to even-aged management (Harris
1984, McKelvey and Johnston 1992, Moir et al.
1995) with clearcut logging as the predominate
method. However, in the Sierra Nevada, logging
prior to the 1980s rarely used clearcutting; se-
lective logging of the largest trees was the pre-
dominant method (McKelvey and Johnston
1992). Habitat fragmentation may have occurred
if selective logging degraded the quality of older
forests for Spotted Owls. However, the matrix
resulting from this type of logging may have dif-
ferent effects than one resulting from clearcut
logging. On the other hand, clearcutting began
earlier and increased over time within the range
of the Northern and Mexican Spotted Owls than
in the Sierra Nevada (Harris 1984, Moir et al.
1995). Clearcutting has dramatically altered at
least part of the forested landscape used by Spot-
ted Owls (Fig. 4). Ripple et al. (2000) found that
prelogging landscapes in the Coast Range of
Oregon had significantly greater amounts of old-
growth forest (63% of landscape before logging
versus 44% after logging). In addition to reduc-
ing the amounts of older forest, foresters at-
tempted to disperse 10-20 ha clearcuts, which
increased fragmentation of those forests; patch
density and edge density increased while mean
patch size, largest patch size, and amount of in-
terior forest decreased. However, Ripple et al.
(2000) also found that proportions of old-growth
forest in pre-logging landscapes were highly
variable, ranging from 16-100%, which may
have been due to past stand-replacing fires.
Thus, both fire and past logging practices al-
tered landscapes occupied by Spotted Owls.
208 STUDIES IN AVIAN BIOLOGY NO. 25
< 1940
1961 - 1970 '
FIGURE 4. Distribution of old-growth forest on the
lamette National Forest, Oregon (Harris 1984).
1951 -1960
ø.'* .e:, ,
1971 - 1981
.
Blue River and McKenzie Ranger Districts of the Wil-
While clearcut logging may have been similar
to severe stand-replacing fires in that all forest
cover is removed, logging did not attempt to
mimic natural disturbance regimes, such as fire,
under which the owl evolved (McKelvey and
Johnston 1992).
HABITAT FRAGMENTATION AT THE
RANGE-WIDE SCALE
A number of authors argued that the popula-
tion process of primary concern with respect to
habitat fragmentation across the range of sub-
species is juvenile dispersal (Guti&rez and Har-
rison 1996, Turchin 1998). This was also rec-
ognized in the simulation models discussed pre-
viously (Lande 1988, Doak 1989, Lamberson et
al. 1992).
Dispersal of juvenile Spotted Owls maintains
gene flow and potential demographic connectiv-
ity between isolated populations. The impor-
tance of juvenile dispersal depends on the dy-
namics of Spotted Owl populations, e.g., wheth-
er population dynamics follow source-sink,
meta-population, etc. Regardless of how popu-
lation dynamics in Spotted Owls are structured,
the movement of individual Spotted Owls across
the landscape is primarily though juveniles. In
general, once Spotted Owls establish a territory,
they are relatively sedentary. Movements of ter-
ritory holders to other territories is relatively
rare and encompasses only short distances; Wag-
ner et al. (1996) estimated that 1.5% of non-
juvenile Northern Spotted Owls relocated to new
territories each year while moving an average of
6.5 km. An exception was noted for the Mexican
Spotted Owl, where an adult female was recov-
ered 187 km from her original territory (Gutie-
rrez et al. 1996). In contrast to territory holders,
juvenile Spotted Owls always disperse from
their natal territories (Gutierrez et al. 1985, Mill-
er 1989, Ganey et al. 1998, Willey and van Riper
2000) and move considerably longer distances
(Table 2). In addition, the distributional proper-
ties of dispersal distances for juvenile Spotted
Owls are quite similar between the Northern and
Mexican subspecies (Table 2); no data are avail-
able for the California subspecies.
If dispersal maintained demographic continu-
ity, then the degree to which habitat fragmen-
tation affects this connectivity will determine the
influences of habitat fragmentation on popula-
tion processes at the range-wide scale. A key
question with respect to dispersal is, does habitat
fragmentation affect connectivity between pop-
ulations and subpopulations of Spotted Owls?
Effects can be viewed as either complete disrup-
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 209
TABLE 2. FINAL DISPERSAL DISTANCES REPORTED FOR RADIO-TAGGED JUVENILE NORTHERN AND MEXICAN SPOT-
TED OWLS
Final dispersal distance (km) a
Subspecies Region Mean SD Range N Source
Northern California 30.5 23.5 1.0-100.0 23 Guti6rrez et al. 1985
Oregon 28.1 17.3 3.2-75.8 25 Miller 1989
Mexican Utah 29.2 22.5 1.7-92.3 26 Willey and van Riper 2000
Arizona 26.2 22.3 0.6-72.1 17 Ganey et al. 1998
a Final dispersal distance is the straight-line distance from the nest to the location farthest from the nest (Ganey et al. 1998).
tion of the connection between populations or
reduction in flow of individuals to some thresh-
old point where the connection can be consid-
ered severed.
Much of the range of the Northern Spotted
Owl and the Sierra Nevada portion occupied by
California Spotted Owls has fairly continuous
forests considered suitable for occupancy by
owls. However, across the range of the Mexican
Spotted Owl, the distribution of suitable forests
is naturally disjunct (Fig. 5). For the geographic
range of the Mexican Spotted Owl to be consid-
ered fragmented, connectivity must be affected
to a greater degree than normally experienced in
the naturally disjunct populations across the
range of this subspecies. Although it is tempting
to view Mexican Spotted Owl populations as a
type of meta-population, there is little support
for this (Keitt et al. 1995, Gutidrrez and Harrison
1998). Based on simulation modeling, Keitt et
al. (1997) found that the degree to which the
range of the Mexican Spotted Owl in the United
FIGURE 5. Distribution of forested areas within the
range of the Mexican Spotted Owl.
States (Fig. 5) is connected could be described
in terms of dispersal distance; with a dispersal
distance of at least 40-50 km, forested patches
went from being relatively disconnected to con-
nected. Of 43 juveniles radio-marked by Ganey
et al. (1998) and Willey and van Riper (2000),
25.6% dispersed distances at least 40-50 km
(Table 3). For comparison, we examined the cu-
mulative distribution of final dispersal distances
for 48 radio-marked juvenile Northern Spotted
Owls (Gutierrez et al. 1985, Miller 1989; Table
3). If forested areas within the range of the
Northern Spotted Owl were distributed in a
manner similar to that of the Mexican Spotted
Owl, 27.1% of the dispersing juveniles would
be able to move between disjunct populations
(Table 3). This suggested that a portion of a giv-
en year's juvenile cohort would be capable of
connecting a landscape of disjunct habitat patch-
es under the conditions of these studies. How-
ever, the question still remains, is this sufficient
to maintain connectivity between populations
and subpopulations within the geographic range
to maintain both demographic processes and
gene flow?
We found few empirical data on the effects of
fragmentation on Spotted Owl population pro-
cesses at the scale of the geographic range. Only
one study (Miller et al. 1997) on juvenile North-
ern Spotted Owl dispersal provided insights on
the effect of forest fragmentation on connectiv-
ity between populations. First, Miller et al.
(1997) found that juveniles used closed-canopy
forests more often than expected during dispers-
al. Second, juveniles selected equally between
less fragmented and more fragmented older for-
ests. However, they did observe a negative re-
lationship between net dispersal distance and the
proportion of clearcuts on the landscape, sug-
gesting that juveniles encountering more clear-
cuts during dispersal may be limited in their dis-
persal distance. Finally, mortality of juveniles
appeared to increase with increased use of clear-
cuts when they temporarily colonized an area,
but mortality decreased with increased use of
open sapling stands. The openness of clearcuts
210 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 3. CUMULATIVE DISTRIBUTION OF DISPERSAL DISTANCES OF RADIO-TAGGED JUVENILE MEXICAN AND
NORTHERN SPOTTED OWLS
Simulated effect on range-wide
Final dispersal % of juveniles dispersing at lea.st x km forested landscape occupied
distance by Mexican Spotted Owls
x km, where x - Mexican Northern (Keitt et al 1997)
10 74.4 81.3
20 60.5 64.6
30 34.9 41.7
40 25.6 27.1
50 14.0 12.5
60 9.3 6.3
70 7.0 4.2
80 4.7 2.1
Highly disconnected
Several independent subdivisions
Most patches joined
Highly interconnected
Note: Data on radio-tagged owls are from the sources listed in Table 2.
may make owls more vulnerable to predation or
reduce the availability of prey because clearcuts
are often dominated by dense, small shrubs. Use
of other seral stages may be related to prey, such
as the dusky-footed woodrat (Neotomafuscipes),
which achieve high abundances in early forest
seral stages (Sakai and Noon 1993, Ward et al.
1998). Thus, some degree of fragmentation may
not be detrimental to dispersing juvenile North-
ern Spotted Owls, but the effect of fragmenta-
tion of older forest may depend on the interven-
ing matrix (i.e., clearcut versus sapling stands)
between forest fragments.
Simulation models examined the potential ef-
fects of fragmentation on juvenile dispersal
across the range, or portions of the range, of the
three subspecies (Doak 1989, McKelvey et al.
1992, Noon and McKelvey 1992, Keitt et al.
1997). However, these models incorporated as-
sumptions about juvenile dispersal behavior be-
cause little empirical data existed to parameter-
ize the models. Consequently, these studies pro-
vided little real information on how habitat frag-
mentation affects Spotted Owls. However, the
model by Keitt et al. (1997) provided valuable
insights into what dispersal capabilities Mexican
Spotted Owls require to connect populations
across their range, and the models by Lamberson
et al. (1994), McKelvey et al. (1992), and Noon
and McKelvey (1992) made quantitative predic-
tions about occupancy of habitat blocks contain-
ing different numbers of Northern Spotted Owl
territories (see also review in Noon and Mc-
Kelvey 1996). The predictions from these latter
models have never been empirically tested.
Habitat fragmentation could potentially affect
gene flow as well as population dynamics, which
is a major concern of conservation biologists
(Frankel and Soul 1981). Despite the lack of
support for a demographic meta-population,
there is evidence of past gene flow among Mex-
ican Spotted Owl populations, among Northern
Spotted Owl populations and between Northern
and California Spotted Owls (Barrowclough et
al. 1999). Further, relatively little gene flow
needs to occur to maintain genetic variability
(Lande and Barrowclough 1987). Thus, it ap-
pears that fragmentation would likely have less
effect on gene flow than demography, given
what we know of juvenile Spotted Owl dispers-
al.
HABITAT FRAGMENTATION AT THE
POPULATION SCALE
Abundance and reproductive success of
Northern Spotted Owls increase with the amount
of older forest (Bart and Forsman 1992). How-
ever, there are no studies relating metrics mea-
suring forest fragmentation or heterogeneity
with population performance. Although there are
a large number of populations studies on Spotted
Owls (see Noon et al. 1992, White et al. 1995,
Forsman et al. 1996, Franklin et al. 1999 for
reviews), none relate life-history traits and/or
rates of population change ()) to forest frag-
mentation or heterogeneity. Such studies would
have to employ the population or subpopulation
as the unit of comparison rather than the indi-
vidual or territory (see HABITAT FRAGMEN-
TATION AT THE TERRITORY SCALE be-
low). For example, estimates of ) for Northern
Spotted Owls on 15 studies ranged from 0.83
('() = 0.02) to 0.98 ('() = 0.02), indicating
that variation in rates of population change ex-
ists among subpopulations (Franklin et al. 1999).
Thus, comparisons need to be made with sub-
populations of owls inhabiting landscapes hav-
ing different degrees of habitat fragmentation
(e.g., the 15 separate demographic studies in
Franklin et al. 1999). In addition, the methods
for identifying habitats and quantifying habitat
fragmentation would have to be standardized
across study areas.
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 211
TABLE 4. META-ANALYSIS ON AMOUNTS OF MATURE AND OLD-GROWTH FOREST IN CIRCLES OCCUPIED BY SPOT-
TED OWLS VERSUS RANDOM CIRCLES ON THE SURROUNDING LANDSCAPE
Subspecies k a 3 v'7ar(3) 95% CI for 3 fly 2 ....... (95% CI) CVp
Northern 7 0.680 0.011 0.474, 0.886 0.029 (0.000, 0.313) 0.251
California I 0.352 0.085 0.218, 0.923 __b __b
Mexican I 0.466 0.053 0.016, 0.915 __b __b
All subspecies 9 0.624 0.008 0.449, 0.799 0.022 (0.000, 0.230) 0.236
a Number of studies.
b Not estimable because of insufficient number of studies.
HABITAT FRAGMENTATION AT THE
TERRITORY SCALE
Most research on effects of fragmentation and
heterogeneity on Spotted Owls has been at the
territory scale, and the majority of this work re-
lated occupancy to landscape characteristics
within territories. In general, researchers exam-
ining the effects of habitat fragmentation and
heterogeneity compared occupied sites (defined
by circles of varying radii around an owl nest
or location) with sites of equal size that were
randomly placed on the surrounding landscape.
Because of the large number of studies, we used
some simple meta-analytical techniques to sum-
marize the general findings (see Appendix 1 for
methods). In summary, we first estimated effect
sizes (d), and their sampling variance (var(d))
for each study. Here, the study was the sampling
unit, with each study including 20-100 territo-
ries (see Appendix 1). Thus, we were able to
estimate sampling variances and 95% confi-
dence intervals of metrics for each study. Effect
sizes were measures, in standard deviations, of
the difference in metrics (e.g., amount of older
forest) between occupied and random sites
(Wolf 1986:27, VanderWerf 1992). Ideally, ef-
fect sizes should be compared with a distribu-
tion of effect sizes derived from published stud-
ies (Wolf 1986:27). Because such a distribution
was unavailable, we used the rough guidelines
of = 0.2 for small effects, d = 0.5 for me-
dium effects, and = 0.8 for large effects pro-
posed by Cohen (1987). We used 95% confi-
dence intervals to assess the degree to which
effect sizes overlapped zero (no effect) for each
study. Where we had -->2 studies with the same
metric (e.g., amount of old-growth), we esti-
mated a weighted mean (d), its sampling vari-
ance (3"(//)), and an estimate of the process
variation (p2 ........ ) of d. This process variation
was an estimate of the variation in the metrics
across studies and was derived by removing the
sampling variation associated with each estimate
of d (see Appendix 1). In most cases, there were
only 2-3 studies with similar metrics. In these
cases, we still estimated the effects size param-
eters and process variation. We recognized these
estimates had limited validity for inference but
we used them to pose alternative hypotheses and
as an example of how a meta-analysis of these
parameters would be useful if sufficient studies
were available with similar metrics.
We first examined the effects of amounts of
mature and old-growth coniferous forest on oc-
cupancy. We examined seven studies on the
Northern Spotted Owl, ranging from Washing-
ton to northern California, one study on the Cal-
ifornia Spotted Owl, and one study on the Mex-
ican Spotted Owl (Appendix 1). Effect sizes
across all subspecies were positive, generally
large, and, except for the California Spotted
Owl, different from zero, indicating that sites oc-
cupied by Spotted Owls had greater amounts of
older forest than sites randomly located on the
forested landscape (Table 4). In addition, North-
ern Spotted Owls appeared to have greater effect
sizes, suggesting a larger difference between oc-
cupied and random sites, than the other two sub-
species (Appendix 1). However, the other two
subspecies were each represented by only one
study and, hence, we did not capture as much
geographic variation as for the Northern Spotted
Owl. In addition, sites occupied by Northern
Spotted Owls on private timber lands in the Red-
wood Province (Fig. 1) had higher proportions
of younger forests (41-60 years) than the other
studies (Thome et al. 1999). On these private
lands, there were few stands of older forest, but
the younger stands often approached the struc-
tural characteristics of older conifer forest in the
other studies because of higher growth rates in
redwood (Sequoia sempervirens) forests (Fol-
liard 1993).
Researchers comparing occupied and random
sites used 16 different metrics of fragmentation
and 6 different measures of heterogeneity (Ap-
pendix 1). Unfortunately, none of these metrics
were represented by more than three studies,
with most used in only a single study. In addi-
tion, the majority of the studies were on North-
em Spotted Owls. We estimated effect sizes and
process variance for six of the metrics examin-
212 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 5. META-ANALYSIS OF INDICATORS OF FRAGMENTATION AND HETEROGENEITY IN CIRCLES OCCUPIED BY
NORTHERN SPOTTED OWLS VERSUS RANDOM CIRCLES ON THE SURROUNDING LANDSCAPE
Metric a k b v'rr() 95% CI for O. 2 ........ (95% CI) CVp
Indicators of Fragmentation
Mean Patch Area 3 0.865 0.002 0.777, 0.953 0.000 (0.000, 0.341) 0.000
CV Patch Area 2 0.359 0.119 -0.317, 1.035 0.177 (0.000, 250.1) 0.953
Patch Density 2 0.563 0.163 0.230, 1.354 0.260 (0.000, 338.1) 0.906
Patch Interior 2 0.440 0.045 0.024, 0.856 0.040 (0.000, 110.5) 0.455
Perimeter Density 3 0.289 0.124 -0.401, 0.979 0.342 (0.052, 15.69) 2.024
GISfYag Index 3 0.638 0.061 -1.122, -0.154 0.141 (0.000, 8.175) 0.589
Indicators of Heterogeneity
Shannon-Wiener lndex 2 0.272 0.136 -0.451, 0.950 0.220 (0.002, 277.2) 1.676
Dominance 2 -0.307 0.169 -1.113, 0.499 0.285 (0.014, 343.9) 1.442
Contagion 2 0.642 1.147 -1.457, 2.741 0.401 (0.393, 340.3) 2.671
See Appendix 1 for definitions of metrics.
Number of studies.
ing fragmentation (represented by 2-3 studies)
and three of the metrics examining heterogeneity
(each represented by two studies; Table 5). Ef-
fects that appeared to be consistent across stud-
ies (i.e., exhibited relatively low CV in spatial
process variation) were mean patch area, the
amount of patch interior, and the GISfrag index
of Ripple et al. (1991a; Table 5). Based on the
GISfrag index, Northern Spotted Owls occupied
areas having larger patches of older forest
(which supported more interior forest) that were
more numerous and closer together than the ran-
dom sites. The effect sizes for these three met-
rics were different from zero based on 95% con-
fidence intervals (Table 5). The remaining met-
rics for fragmentation and all the metrics for het-
erogeneity in Table 5 had large coefficients of
spatial process variation, and had effect sizes
with confidence intervals including zero. How-
ever, in almost all cases the estimates of spatial
process variation had extremely large confidence
intervals, indicating poor estimation due to in-
adequate numbers of studies. More importantly,
our analysis demonstrates the lack of compara-
bility among studies of Spotted Owl habitat frag-
mentation because few studies used the same
metrics. Thus, there were insufficient samples
for most metrics to allow meaningful conclu-
sions.
We also partitioned the data by gross ecolog-
ical provinces (West Cascades versus Klamath
Provinces; Fig. 1) within the range of the North-
ern Spotted Owl to examine whether large dif-
ferences between the provinces were responsible
for the high coefficients of spatial process vari-
ation (Table 6). With the three metrics (mean
patch area, interior, and GISfrag) that we con-
sidered consistent, effect sizes were similar be-
tween the two provinces and were different from
zero for each individual study. With the other
three metrics of fragmentation (CV patch area,
patch density, and perimeter density), there ap-
peared to be provincial differences that could
have accounted for the high degree of spatial
process variation observed when provinces were
pooled in Table 5. Sites occupied by Northern
Spotted Owls in the West Cascades province had
less variable patch areas, lower patch density,
and inconclusive perimeter densities in relation
to random sites. The Klamath province, on the
other hand, had more variable patch areas, high-
er patch densities, and higher perimeter densities
than random sites. Only patch density was not
different from zero.
Thus, it appears that Northern Spotted Owls
occupy sites with greater amounts of older forest
that retain higher amounts of interior forest than
forested landscapes chosen at random across
their range. This appeared to be consistent
across provinces. However, the degree of frag-
mentation in occupied versus random sites in the
Klamath province was greater than in the West
Cascade province. This was suggested by more
variable patch sizes and greater perimeter edge.
However, this would only be considered habitat
fragmentation if habitat for Northern Spotted
Owls in the Klamath province was limited to
older forest. If ecotones (represented by the pe-
rimeter of other vegetation types with older for-
est) are also Spotted Owl habitat, then this
would not represent habitat fragmen'tation, but
merely an additional component of Spotted Owl
habitat (see Franklin et al. this volume).
In general, heterogeneity of vegetation types
and forest seral stages appears to be higher in
occupied than random sites of the Northern and
Mexican Spotted Owl, but not the California
subspecies (Table 7). For the Northern Spotted
Owl in the West Cascades and Klamath prov-
inces, Shannon-Wiener indices of vegetation
type or seral stage diversity were higher on oc-
cupied sites, Simpson's index was lower, domi-
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 213
nance was lower, and contagion was lower. The
results from the East Cascades province were
opposite in terms of the Shannon-Wiener index,
dominance, and contagion. (Morganti 1993; Ta-
ble 7). However, only contagion was different
from zero. In addition, Morganti (1993) only
used 3 vegetation types whereas the other re-
searchers used 5-7; increasing vegetation types
can affect the direction and the relative magni-
tude of all the heterogeneity metrics explored
here (Morganti 1993, Meyer et al. 1998). Thus,
while Spotted Owls may occupy sites with some
degree of forest fragmentation in some areas,
sites occupied by Northern Spotted Owls ap-
peared to be more consistent in having higher
heterogeneity throughout their range. The one
study on Mexican Spotted Owls (Peery et al.
1999) had a similar effect size for Simpson's
index as for the Northern Spotted Owl in Cali-
fornia, indicating that seral stage and vegetation
type diversity was higher in occupied than ran-
dom sites. California Spotted Owls had the op-
posite trend, with occupied sites having less het-
erogeneity than random sites.
A few researchers examined the effects of
landscape metrics on life-history traits, such as
survival and reproduction. Bart (1995) found
that survival increased with the amount of older
forest within sites occupied by Northern Spotted
Owls. However, survival in this study was mea-
sured from turnover events of unmarked birds
(U.S. Dept. Interior 1992) and may not have
been an unbiased measure of survival. Similarly,
Ripple et al. (1997) found that a reproductive
index was correlated (r = 0.64, P = 0.03) with
amounts of older forest in occupied sites. How-
ever, metrics other than the amount of older for-
est were not included in the analyses in these
two studies. In the Redwood province of north-
ern California, Thome et al. (1999) found high-
est reproductive success in Northern Spotted
Owls at sites that had high proportions of 21-
40 year old lorest stands and lower proportions
of older forest. In the Klamath Province of
Oregon, average annual reproductive output in-
creased at sites with greater fractal dimension
(indicating greater landscape complexity with
increased edge), more older forest patches, and
greater proportions of hardwood forest (Meyer
et al. 1998). Their multiple regression model ac-
counted for 56% of the variation in reproductive
output. In the West Cascades province, average
annual reproductive output was not explained by
any of the habitat and landscape variables mea-
sured, but rather by decreased density of owls
in the surrounding area, which explained 85%
of the variation in reproductive output (Meyer
et al. 1998). Finally, Franklin et al. (2000) ex-
amined reproductive output, survival, and the
214 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 7. EFFECT SIZES FOR METRICS OF HETEROGENEITY MEASURED ON SITES OCCUPIED BY SFOTTED OWLS
VERSUS RANDOM SITES
Metric a Subspecies Region b 95% CI Source
Shannon-Wiener Index Northern WCAS & KLA (OR) 0.629 0.224, 1.033 Meyer et al. 1998
Shannon-Wiener Index Northern ECAS (OR) 0.109 -0.593, 0.374 Morganti 1993
Simpson's Index Northern KLA (CA) -0.690 1.147, -0.233 Hunter et al. 1995
Dominance Northern WCAS & KLA (OR) 0.706 - 1.114, -0.298 Meyer et al. 1998
Dominance Northern ECAS (OR) 0.116 -0.374, 0.607 Morganti 1993
Contagion Northern WCAS & KLA (OR) -0.378 -0.778, 0.022 Meyer et al. 1998
Contagion Northern ECAS (OR) 1.766 1.189, 2.344 Morganti 1993
Baxter and Wolf Index California SIERRA -0.775 c -1.366, -0.184 two studies
SimpsoWs Index Mexican NM -0.791 1.251, -0.330 Peery et al. 1999
a See Appendix I for definitions of metrics.
b WCAS - West Cascades province, KLA Klamath province, ECAS East Cascades province, SIERRA - Sierra Nevada Mountains; state
acronyms are in parentheses.
c Weighted mean for two studies (Bias and Gutien-ez 1992, Moen & Gutien'ez 1997) in the same area; '57(3) = 0.091.
combination of the two in a measure of habitat-
based fitness in relation to landscape habitat var-
iables of sites occupied by Northern Spotted
Owls in the Klamath province. They found that
reproductive output increased at sites with more
edge between older forest and other vegetation
types and decreased with the amount of interior
forest. Survival, however, increased with more
interior older forest and increased edge. Thus,
sites with high fitness represented a tradeoff,
balancing the amount of interior forest with edge
to achieve optimal survival and reproduction
(Fig. 6).
DISCUSSION
The effects of habitat fragmentation on spe-
cies richness and animal population dynamics
have long been of interest to ecologists. Conse-
quently, negative impacts of forest fragmenta-
tion on Spotted Owls were assumed without crit-
ical examination because this bird's habitat has
been highly disrupted by logging over the past
century (Gutidrrez 1994). Further, the Spotted
Owl is thought to be declining across its range,
presumably in response to loss of habitat (and
by corollary to increased habitat fragmentation).
The loss of habitat, owl population declines, and
the federal listing of two subspecies have
prompted a plethora of studies on the bird which
potentially lends itself to a meta-analysis of frag-
mentation patterns.
Most of the initial simulation models on Spot-
ted Owls emphasized loss of habitat rather than
the explicit effects of habitat fragmentation. As
LOW FITNESS
HIGH FITNESS
FIGURE 6. Example of occupied Northern Spotted Owl sites exhibiting low and high fitness based on habitat
characteristics of those sites (Franklin et al. 2000).
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 215
Franklin et al. (this volume) point out, habitat
loss and habitat fragmentation can have different
effects when they are considered separately and
at different scales. For example, the model de-
veloped by Lande (1988) predicted a threshold
amount of suitable Spotted Owl habitat (older
forest) below which populations should decline
to extinction. This was partially corroborated by
empirical studies that found no or few owls in
large areas where older forests had been mostly
eliminated (Bart and Forsman 1992, Johnson
1992, U.S. Dept. Interior 1992, Guti6rrez 1994).
However, these results do not address the issue
of critical thresholds for habitat fragmentation in
Spotted Owls. Later models became more so-
phisticated but still only examined loss of suit-
able habitat (e.g., Doak 1989, Lamberson et al.
1992). The models developed by Lamberson et
al. (1994), McKelvey et al. (1992) and Noon and
McKelvey (1992) did make quantitative predic-
tions about occupancy by Northern and Califor-
nia Spotted Owls at the range-wide scale in re-
lation to forest patch sizes with different shapes,
sizes, and inter-patch distances. However, these
predictions have yet to be tested with empirical
data. There has been an unfortunate disconnect
between theoretical predictions made by simu-
lation models concerning the effects of fragmen-
tation on Spotted Owls and the testing of those
predictions with empirical studies. However, this
is not unique to Spotted Owls; Doak et al.
(1992) argue for better merging of theory and
experimentation in understanding habitat frag-
mentation in general.
At the three scales in the empirical studies
that we examined, all three subspecies of Spot-
ted Owl exhibit some degree of association with
the structural characteristics of old conifer for-
est. Even when older forest is not present (e.g.,
the Redwood Province in the range of the North-
em Spotted Owl), Spotted Owls still occupy
sites that have forests structurally similar to old-
er forest in other parts of the owl's range. How-
ever, at the territory scale there is evidence that
early forest seral stages and ecotones (i.e., the
interface between conifer forests and other veg-
etation types) may contribute to Northern Spot-
ted Owl habitat in some areas (Franklin et al.
2000). In particular, early seral stages bordering
older forest may provide both abundant and
available prey for Northern Spotted Owls in the
Klamath province where hardwood trees are im-
portant components of the forests occupied by
Northern Spotted Owls. Thus, there is some ev-
idence that Spotted Owls in some parts of their
range may benefit from forest heterogeneity.
Some of this heterogeneity may result from log-
ging or other anthropocentric disturbance. These
changes are not necessarily fragmentation (sensu
Franklin et al. this volume), but the introduction
of openings and peninsulas of different seral
stages that provide edge while maintaining in-
terior forest (see Fig. 6) and heterogeneity. The
mechanisms that produce potential benefits are
still poorly understood but may relate to prey
abundance and availability (see Thome et al.
1999, Franklin et al. 2000). This situation may
only apply to areas occupied by Northern Spot-
ted Owls (and other subspecies) where forests
are mixtures of conifers and hardwoods.
Despite the plethora of habitat-based studies
on Spotted Owls, the effects of forest fragmen-
tation and heterogeneity are still poorly under-
stood. Even at the territory scale where most of
the studies have been conducted, the many dif-
ferent measures and indices used in the various
studies reduced our ability to draw inferences.
There is no unified set of metrics for measuring
fragmentation of Spotted Owl habitats; an abun-
dance of ad hoc measures exist and often re-
searchers develop their own. However, to un-
derstand the effects of habitat fragmentation on
Spotted Owls, appropriate metrics need to be de-
veloped that can be applied across studies. In the
absence of large-scale experiments, reliable
knowledge (sensu Romesburg 1981) can only be
achieved through replication of observational
studies that use similar metrics. Such consisten-
cy does not preclude novel approaches by indi-
vidual investigators. Our attempt to synthesize
such studies for Spotted Owls failed in terms of
inferences on the effects of fragmentation be-
cause researchers did not use similar metrics to
quantify habitat fragmentation. That is, each
metric of interest was represented by 3 studies
at the most. Our sample of studies was also ham-
pered because a number of researchers did not
present the requisite information (means and/or
standard deviations) to estimate effect sizes.
However, the patterns we observed in our meta-
analysis can be considered hypotheses that can
be tested with more detailed meta-analyses or
experimentation.
To understand forest fragmentation, habitat
fragmentation, and forest heterogeneity in Spot-
ted Owls, a number of key questions need to be
addressed, such as:
1. What is Spotted Owl habitat? Older conifer-
ous forest has always been considered syn-
onymous with Spotted Owl habitat but recent
studies suggest other vegetation types and
landscape attributes may contribute to Spot-
ted Owl habitat as well. Before habitat frag-
mentation can be assessed and understood,
habitat must be properly defined (Franklin et
al. this volume). In addition, definitions of
Spotted Owl habitat can only be achieved
216 STUDIES IN AVIAN BIOLOGY NO. 25
when the mechanisms behind the importance
of various components are understood. This
probably can only be achieved through anal-
ysis of empirical data (particularly of repli-
cated studies) followed by carefully con-
trolled experiments.
2. Can Northern Spotted Owls and California
Spotted Owls maintain viable populations un-
der the same range-wide fragmentation as
Mexican Spotted Owls? While preliminary
information on juvenile dispersal, a key pro-
cess in the effects of fragmentation at the
range-wide scale, is available for Northern
and Mexican Spotted Owls, this information
is still lacking for California Spotted Owls
(Verner et al. 1992). In addition, there have
been no long-term studies of juvenile dis-
persal specifically designed to examine the
effects of heterogeneity and fragmentation.
3. Do landscape configurations within subpop-
ulations have the same effect as they do at
the territory scale? This question relates to
habitat quality at a population scale, similar
to the findings of Franklin et al. (2000) at the
territory scale; that is, whether populations
can be represented as meta-populations,
source/sink populations, etc., with respect to
fragmentation and heterogeneity. For exam-
ple, populations of Spotted Owls may be able
to maintain stationary populations in frag-
mented landscape, but are they bolstered by
outside recruitment?
4. Is timber harvesting compensatory or addi-
tive with natural disturbance regimes, such
as fire? Since fire suppression, timber har-
vesting has become the dominant disturbance
causing fragmentation and heterogeneity on
landscapes occupied by Spotted Owls. To be
completely compensatory, timber harvesting
activities would have to impact forests in the
same manner as fire, and to be completely
additive, timber harvest would have to im-
pact the landscape in a manner very different
from fire. Aside from any geochemical dif-
ferences, the effects of timber harvesting on
the landscape probably lie somewhere be-
tween these two extremes. Here, we use the
terms compensatory and additive similarly to
those used in waterfowl harvest (Nichols et
al. 1984). The degree to which timber harvest
and fire disturbance affect landscapes occu-
pied by Spotted Owls is crucial to under-
standing land management options and po-
tential strategies. For example, Weatherspoon
et al. (1992) argue that a management policy
of allowing forest succession to proceed un-
interrupted by periodic natural disturbance
would likely lead to habitat degradation for
California Spotted Owls rather than toward
biologically healthy and diverse systems.
Rather, they argue management should use
natural processes as a guide to management.
RECOMMENDATIONS FOR FUTURE ANALYSES OF
FRAGMENTATION EFFECTS ON SPOTTED OWLS
Given the limitations with extant data on stud-
ies of fragmentation/landscape characteristics of
Spotted Owls we encountered, we recommend
the following:
1. Development of stronger theoretical/analyti-
cal basis for studies of fragmentation using
simulation to understand how fragmentation
indices relate to actual landscape configura-
tions (Li and Reynolds 1994).
2. Testing of predictions from simulation mod-
els with empirical studies and exposition of
explicit predictions from simulation models
to allow for such empirical testing.
3. Linkage of useful landscape metrics with life
history traits, particularly survival, reproduc-
tion, and juvenile dispersal.
4. Inclusion of alternative hypotheses that in-
clude a range of effects from positive to neg-
ative in terms of fragmentation and hetero-
geneity.
5. Reporting of mean and standard deviations of
landscape metrics used to characterize Spot-
ted Owl habitats.
6. Consistent reporting of useful metrics even if
other, better techniques are developed (i.e.,
researchers should continue to use a baseline
of metrics even if they use novel or addition-
al metrics). This has become standard prac-
tice with studies of Spotted Owl home range
where the Minimum Convex Polygon is con-
sistently used in addition to other estimators
even though scientists recognize that it is of-
ten biased.
7. Peer referees and editors should recognize
the utility and necessity of publishing studies
replicating earlier research on the same topic.
Clearly, higher standards can be incorporated
into replicated studies by sample size require-
ments (subsequent studies should have a larg-
er or "better" sample than earlier studies),
and geographic representation of sampling
(studies in areas where there have not been
studies previously executed).
We believe that these few recommendations will
lead to stronger inference regarding the effect of
habitat fragmentation on Spotted Owls. Further,
we think these recommendations may serve to
advance the understanding of fragmentation on
other bird species and the effects of fragmenta-
tion on species in general.
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 217
ACKNOWLEDGMENTS
We thank T L. George, D. Dobkin, and J. T. Roten-
berry for their editorial contributions. K. McKelvey
and J. B. Dunning provided thoughtful reviews. Fund-
ing was provided by the U.S. Forest Service, Region
5 (Contract FS 53-91S8-00-EC14).
APPENDIX 1
META-ANALYSIS AND HABITAT METRICS
For each metric measured in each study, we esti-
mated an effect size (d) as:
(Hunter and Schmidt 1990:271) where œ,, and œr are
the estimated mean from occupied and random sites,
respectively, and is the estimated pooled standard
deviation, calculated as:
= /(n o -- 1)(5o) 2 + (n, l)(r) 2
no + nr - 2
(Hunter and Schmidt 1990:271) where n o, nr, 'o, and
S,. are the sample sizes and standard deviations, re-
spectively, for occupied and random sites within each
study. In one case (Lemkuhl and Raphael 1993), stan-
dard deviations were not available so we estimated ef-
fect size between metrics from reported F-statistics
(Wolf 1986:35) as:
x/af ..... '
The sampling variance for was estimated (Hunter
and Schmidt 1990) as:
-(,) = (no + nr - 1 4 1 +
no + n, 3
We estimated a cumulative effect size (; sensu Ro-
senberg et al. 2000) across studies as:
where k is the number of studies, i is the effect size
^2
for the kth study, and w_ = l/[O'proces s + var(d)l and the
sampling variance for d as:
() _ 1 (2)
w
after Burnham et al. (1987:260-266). In this alysis,
we paitioned process vance 2 ß the viation
across studies) in each metric from the sampling v-
ice associated with estimating the for each study.
We estimated process viation by iteratively solving:
after Burnham et al. (1987:260 266). Equations (1)
and (2) wre solve simultaneously with equation (3)
to obtn d and v(d). These procedures were simil
to those proposed by Rosenberg et al. (2000) for r-
dom effects modeling of d. To assess the spatial v-
ability in metrics across studies, we used a coefficient
of process vahation (CV, ro.0 estimates as:
d
218 STUDIES IN AVIAN BIOLOGY NO. 25
SPOTTED OWLS AND HABITAT FRAGMENTATION--Franklin and Gutidrrez 219
dd - ' '
220 STUDIES IN AVIAN BIOLOGY NO. 25
¸
O
o
Studies in Avian Biology No. 25:221-235, 2002.
EFFECTS OF FOREST FRAGMENTATION ON POPULATIONS OF
THE MARBLED MURRELET
MARTIN G. RAPHAEL, DIANE EVANS MACK, JOHN M. MARZLUFF, AND
JOHN M. LUGINBUHL
Abstract. The Marbled Murrelet (Brachyramphus marmoratus) is a threatened seabird that nests on
branches of large trees within older coniferous forest in coastal areas of the Pacific Northwest. Surveys
suggest that murrelets often nest in continuous stands of mature, complexly structured forest but they
also nest in younger forest and in stands varying in size from several to thousands of hectares. We
examined how murrelet abundance and reproduction are related to the amount and pattern of nesting
habitat at regional, watershed, landscape, and nest site scales. At the regional scale, abundance of
murrelets, estimated from offshore surveys, was found to be correlated with amount of nesting habitat
in some areas and to a lesser extent with fragmentation of that habitat. We found a similar pattern at
the watershed scale. At the scale of nest sites and surrounding landscapes, fragmentation may have
greater effect on likelihood of nesting and nest success. Observations of active nests from other studies
indicated high failure rates (47 of 71 nests with known outcomes), mostly due to predation (33 of 47
nests). Corvids have been implicated as primary predators. Forest fragmentation can affect the abun-
dance and distribution of corvids, and thus it is possible that fragmentation might lead to higher rates
of predation on murrelet nests. Over the past 5 years we have tested this assumption in Washington
using artificial nests located in stands of varying structural complexity, levels of fragmentation, and
proximity to human activity. Results indicate, first, that a broad suite of predators, including at least
10 mammalian and avian species, prey on simulated eggs and chicks. Second, rates of predation are
higher within 50 m of forest edge, but this relationship varies with proximity to human activity and
with the structure of the adjacent regenerating forest. Predation increased with proximity to forest
edges when the matrix contained human settlements and recreation areas, but not when it was dom-
inated by regenerating forests. Abundance of some predators (e.g., Steller's Jays, Cyanocitta stelleri)
was greater in more fragmented landscapes, but abundance of other potential predators (e.g., Gray
Jays, Perisoreus canadensis) was greater in continuous forests, making generalizations about the ef-
fects of fragmentation difficult. Research is needed to understand how fragmentation affects both
murrelet nest site selection and the risk of nest predation so that managers can provide landscapes
able to support large populations of successfully breeding murrelets.
Key Words: Brachyramphus marmoratus; corvid; fragmentation; Marbled Murrelet; nesting habitat;
nest predation; nest success.
Forest fragmentation has been implicated as an
important factor affecting the status and trend of
the Marbled Murrelet (Brachyramphus marmor-
atus; U.S. Fish and Wildlife Service 1997a).
Forest fragmentation is the process of subdivid-
ing continuous forest patches into smaller piec-
es. In forests of the Pacific Northwest, timber
cutting primarily drives this process. For species
associated with older forest structures, fragmen-
tation of old-growth habitat leads to a reduction
in amount of that habitat as well as a change in
its pattern on the landscape. The Marbled Mur-
relet is unique among other species considered
in this volume, as it uses forest patches for nest-
ing but not foraging. It feeds and resides on ma-
rine waters for most of the year but nests on
large limbs primarily in older forest patches.
Therefore, the potential effects of forest frag-
mentation are limited to those that might affect
probability of nesting, nesting success, and sur-
vival of adults in transit to or attending nests.
For this species, fragmentation will not affect
foraging behavior or foraging success. In this
paper, we review the potential effects of forest
fragmentation on the murrelet and describe re-
cent experimental evidence of its effects.
BIOLOGY OF THE MARBLED MURRELET
It is important to understand the biology of
the Marbled Murrelet as a prelude to reviewing
fragmentation eflcts. The Marbled Murrelet is
a small seabird of the family Alcidae whose
summer distribution along the Pacific coast of
North America extends from the Aleutian Is-
lands of Alaska to Santa Cruz, California. It for-
ages primarily on small fish in the nearshore (0-
5 km) marine environment. Unlike other alcids,
which nest in colonies on the ground or in bur-
rows at the marine-terrestrial interface, Marbled
Murrelets nest solitarily and most often in large
trees in coniferous forests, traveling up to --100
km inland to reach suitable habitat. A small pro-
portion of the Alaska population nests on the
ground (Mendenhall 1992, Platt and Naslund
1995). Tree-nesting Marbled Murrelets do not
build a nest, but use a natural platform on which
to place their single egg. Both adults share
equally in incubation, exchanging once every 24
221
222 STUDIES IN AVIAN BIOLOGY NO. 25
hr (Nelson and Peck 1995). A few days after
hatching the chick is left alone at the nest for
the duration of the 30-40 d nestling period, with
adults making feeding visits, primarily at dawn
and dusk (Nelson and Peck 1995, Nelson 1997).
Due to population declines attributed to loss of
mature and old-growth forest from logging, low
nest success, and mortality at sea, this species
was federally listed as threatened in Washington,
Oregon, and California in 1992 (U.S. Fish and
Wildlife Service 1997a) and is listed as threat-
ened in British Columbia.
The Marbled Murrelet's unusual nesting hab-
itat and secretive behavior during the nesting
season kept it one of the least known North
American birds of the latter 20th century. The
first nest was not discovered on this continent
until 1974 (Binford et al. 1975), and many as-
pects of this species' ecology, at sea and inland,
are still unclear. However, in the last 10 years
relatively consistent information has emerged on
the association of Marbled Murrelets with older
coniferous forests and on stand attributes cor-
related with murrelet activity and nesting.
Across the range, sites with the highest likeli-
hood of nesting murrelets have larger trees,
more potential nest platforms, and/or greater
moss cover on tree limbs than other sites (Gren-
ier and Nelson 1995, Hamer 1995, Kuletz et al.
1995). Nest trees are larger on average than ad-
jacent trees (often the largest tree within a 25-
50 m radius), contain more platforms with great-
er cover than surrounding trees, and often have
moderate to heavy epiphyte cover (Jordan and
Hughes 1995, Kerns and Miller 1995, Naslund
et al. 1995, Manley 1999). Nest trees are often
near natural or human-created gaps in the can-
opy that murrelets use to access nests (Hamer
and Nelson 1995, Jordan and Hughes 1995,
Kerns and Miller 1995, Naslund et al. 1995,
Manley 1999). Large limbs (mean diameter =
32 cm), deformities from mistletoe and other
disease, damage, and moss cover create suitable
nesting platforms, and these features are most
often found in older forests. However, murrelet
sites also have been recorded in young (60-70
yr) forests with residual old-growth trees or
heavy mistletoe infestations (Nelson 1997). Suit-
able habitat generally occurs at <1,000 m ele-
vation, as floristics at higher elevations lack the
structural features that provide platforms. Man-
ley (1999), however, found nests at elevations
up to 1,260 m in the Bunster Range of British
Columbia. Older forests at lower elevations had
been heavily logged by the time of this study,
but it is unknown if nests occurred at higher el-
evations prior to logging.
Presumably, Marbled Murrelet nesting habitat
associations evolved under a regime of large ex-
panses of old-growth conifer forests on the land-
scape. Wildfire was the primary disturbance
agent prior to the 1800s (Agee 1993); extensive,
high intensity but low frequency (150-300 yr)
fires resulted in large areas of old forest (Gar-
men et al. 1999). Reduction in extent of old for-
est in the Pacific Northwest due to logging over
the past 100 yr has been implicated in the de-
cline of murrelet populations through reductions
in available nesting habitat (Ralph et al. 1995).
Loss of conifer forest within the inland limits of
the Marbled Murrelet range has been extensive,
but actual percentages based on area are difficult
to extract from the literature. An estimated 30%
of coastal forest remains in British Columbia
(Perry 1995). As a site-specific example, 15-
25% of old-growth forest in Clayoquot Sound,
British Columbia, was logged during 1954-
1993, most from low-elevation, large-volume
western hemlock forest (Kelson et al. 1995).
During the period 1982-1993, the murrelet pop-
ulation declined 40% in Clayoquot Sound, likely
as a result of loss of nesting habitat. In western
Washington and Oregon, roughly 18% of old-
growth forests that occurred before logging re-
mained by the early 1980s (Booth 1991); 5-10%
of old-growth redwood forest from the early
1800s remains in California (Carter and Erick-
son 1992, De Angelos and De Angelos 1998).
POTENTIAL EFFECTS OF HABITAT FRAGMENTATION
Loss of coniferous forests in the Pacific
Northwest may affect Marbled Murrelet nesting
habitat in multiple ways, including overall de-
crease in the amount of habitat available and
fragmentation of remaining habitat into smaller,
discontinuous patches with potentially greater
influence of edge phenomena. Edge effects in-
clude changes in microclimate at open edges
compared with interior sites (Chen et al. 1995,
1999), changes in vegetative species, and chang-
es in predator-prey dynamics (Kremsater and
Bunnell 1999). Most studies have difficulty sep-
arating the effects of habitat loss, per se, from
fragmentation, because habitat loss is a neces-
sary consequence of fragmentation (Fahrig
1999). Fragmentation will lead to reduced area
of habitat, including reduced amount of interior
habitat, increased number of patches of habitat,
reduced sizes of patches, increased amount of
edge, and increased isolation of patches. These
conditions, in turn, could affect overall popula-
tion size, likelihood of nesting, survival of
adults, and nesting success. These effects could
differ over the short run versus the long run. For
example, in the short run (say, 10 years), loss
and fragmentation of habitat could cause dis-
placed murrelets to locate in remaining patches,
nest in marginally suitable habitat, or travel
EFFECTS OF FRAGMENTATION ON MARBLED MURRELETS--Raphael et al. 223
greater distances to locate new, disjunct sites
(Divoky and Horton 1995). Although dispersal
and colonization mechanisms are unknown, we
speculate that if murrelets moved into remaining
available habitat, nesting success in marginal or
overcrowded habitat may decline over the long
run, leading to smaller populations and lower
nesting density. In the following sections, we re-
view the evidence for these potential effects
over a variety of geographic scales.
REVIEW OF FRAGMENTATION EFFECTS
AT MULTIPLE SCALES
REGIONAL SCALE
In a review of Marbled Murrelet population
changes, Ralph (1994) observed that, at a broad
scale, the species' distribution on the water gen-
erally corresponded to amounts of inland old-
growth forest. In California and Oregon, the ma-
rine distribution was thought to reflect remaining
older forests, mostly on federal lands (reviewed
by Ralph et al. 1995), with gaps in distribution
on the water where older forests no longer occur.
This relationship was less evident in Washington
and British Columbia, but a systematic compar-
ison of density of murrelets with density of ad-
jacent nesting habitat has not been reported. In
Alaska, breeding season concentrations gener-
ally coincided with the distribution of coastal
old-growth coniferous forest (Piatt and Ford
1993). One exception was Cook Inlet, where
there was an abundance of forest cover but few
murrelets. The lack of correspondence in this re-
gion was explained by poor foraging conditions
in Cook Inlet and a dominance of black spruce
in the forest cover, which lacks the structural
characteristics shared by nest trees.
To examine relationships between offshore
numbers of Marbled Murrelets and amount of
inland habitat in Washington and Oregon, we
compared available vegetation information to
published and unpublished murrelet data. As no
consistent vegetation map layer was available
for both states, we used different datasets but
selected for similar attributes as much as possi-
ble (see Appendix for details). In Washington,
we used a vegetation layer compiled from a
number of sources (U.S. Fish and Wildlife Ser-
vice 1997b). From this we selected late seral
habitat (mixed conifer and hardwood, with
>70% crown closure of conifer and >10%
crown closure from trees >53 cm dbh) to rep-
resent potential Marbled Murrelet nesting habi-
tat. At-sea data were summarized from mid-
summer nearshore (0-400 m) surveys conduct-
ed by the Washington Department of Fish and
Wildlife in 1997 (C. Thompson, unpubl. data).
For Oregon we used a Landsat-based vegetation
map produced by the Western Oregon Digital
Image Project (Nighbert et al., unpubl. data). We
selected multi-storied stands with mean dbh >48
cm and single-storied stands with mean dbh >74
cm within the Sitka spruce zone (Picea sitch-
ensis; Franklin and Dyrness 1973). At-sea data
were averaged over 2-km segments from July
1996 nearshore (0-500 m) surveys (C. Strong,
unpubl. data). North-south bands were estab-
lished along the coast based on how the at-sea
data were summarized (WA) or to represent ap-
proximately 50-km stretches of coastline (OR).
Inland boundaries followed Recovery Plan (U.S.
Fish and Wildlife Service 1997a) zones (80 km
in WA, 56 km in OR), and we established an
elevation cutoff of 1,067 m. Habitat was sum-
marized per band as total habitat within the
band; murrelet data were summarized as a rel-
ative estimate of total numbers of murrelets
counted within the band.
We found no correlation between murrelet
abundance and estimated amount of nesting hab-
itat at the broad scale over the entire two-state
region (Spearman correlation = 0.07, one-tailed
P = 0.391, N = 17 bands; Fig. 1). As summa-
rized in Figure 1, habitat seemed to be most
abundant on the Olympic Peninsula of Washing-
ton and in southern Oregon. Murrelet abundanc-
es were greater in the far northern band of Wash-
ington and the central bands of Oregon. Because
of the differences in habitat maps between the
two states and the perception that relationships
between at-sea distributions and inland habitat
are not as evident in Washington (Ralph et al.
1995), we also computed correlations for
Oregon alone. In that analysis, the correlation
was very weak (Spearman correlation = 0.37,
one-tailed P = 0.132, N = 11). Meyer (1999)
has argued that habitat closer to shore (within
about 25 km) may be more important than hab-
itat further away. In fact, the small concentra-
tions of murrelets off the coast of northern
Oregon in 1992 were associated with state parks
with old-growth stands near the coast (Strong
1995). Restricting the analysis to habitat within
25 km of shore, the correlations improved slight-
ly (for both states, Spearman correlation = 0.38,
one-tailed P = 0.066, N = 17; for Oregon alone,
correlation = 0.38, P = 0.126, N = 11). We
caution that this assessment was conducted at a
very broad scale, using indices for habitat and
at-sea abundance. Results were entirely a func-
tion of the vegetation layer used for mapping,
the specific at-sea data used (dates of surveys,
single vs. multi-year data, nearshore transects
vs. all transects), and the north-south bands we
defined. The offshore abundance of murrelets
does seem to have a consistent pattern, as the
at-sea distribution we depicted for Oregon
224 STUDIES IN AVIAN BIOLOGY NO 25
Neah Bay '
LaPush
Grays Harbo
Willapa Bay
Tillamook
I
Newport'--
Port
Distance from
shore (kin)
0-24
D>24
Coos
300 200 100 0 25 50 75 100 125 150
Ca#fornla
Nearshore abundance Nesting habitat (ha x 1000)
FIGURE 1. Relative abundance of Marbled Murrelets in nearshore waters within geographic bands of Oregon
and Washington in relation to amount of potential nesting habitat (represented as dark polygons on map). Bars
represent relative magnitudes in each zone (topmost pair of bars corresponds to northernmost habitat band).
Dark bars on the habitat histogram represent habitat within 24 km of the coast; open bars represent remaining
inland habitat. See text and Appendix for details and sources of data.
(based on our reanalysis of a subset of C.
Strong's data) was very similar to the murrelet
distribution he reported for 1992 (Strong 1995,
Strong et al. 1995). More refined estimates of
murrelet density and available habitat will be
forthcoming from various scientists as part of an
ongoing murrelet monitoring program. Specifi-
cally, it will be important to obtain consistent
estimates of murrelet numbers over the whole
region and to develop a more reliable estimate
of the amount of nesting habitat using the same
sources of data and analytical techniques across
all sites.
Meyer (1999) conducted a more quantitative
EFFECTS OF FRAGMENTATION ON MARBLED MURRELETS--Raphael et al. 225
spatial analysis for southern Oregon and north-
ern California. Within nine 212,000-650,000 ha
subregions along the coast, greatest marine den-
sities of murrelets were found offshore of large
blocks of consolidated old-growth forest within
a matrix of relatively abundant medium-sized,
second-growth coniferous or hardwood forests.
in subregions with few murrelets, patches of
nesting habitat were relatively small, simple-
shaped, and scattered. Offshore densities were
higher in subregions with more continuous old
growth or old growth combined with residual
old-growth forest. In fact, this study found that
inland habitat variables explained most of the
offshore distribution in this region, with marine
variables, such as type of shoreline, chlorophyll
counts, and sea surface temperature, accounting
for little variation (we note, however, that prey
densities were not included in her analysis).
WATERSHED SCALE
Several studies have explored relationships
between forest landscape patterns and murrelet
activity at the watershed scale. On the Olympic
Peninsula, Washington, 10 large drainages were
sampled with radar for 1-3 yr to compare the
numbers of murrelets flying into each drainage
with the amount and configuration of habitat
available (Raphael et al. 1999, 2002; see Cooper
et al. 1991, Hamer et al. 1995, and Burger 1997
for details on the use of radar to sample birds).
Mobile radar units were stationed within drain-
ages where the natural topography funneled
murrelets flying inland. Late-seral habitat (de-
fined as >70% crown closure with at least 10%
from trees >53 cm dbh) occurring below 1,067
m was considered potentially suitable habitat.
Late-seral habitat was 1 of 10 land cover types
derived from satellite imagery classification
(U.S. Fish and Wildlife Service 1997b). in 2000,
a year with the largest sample of drainages (N
= 10), the maximum number of murrelets de-
tected flying inland was highly correlated with
the amount of potentially suitable habitat after
accounting for drainage size (partial correlation
= 0.86, P = 0.003; Raphael et al. 1999, 2002).
Similar results were found in Clayoquot
Sound, Vancouver island, British Columbia,
from 18 watersheds sampled 3 yr with radar.
Dawn and dusk radar counts were positively
correlated with the size of the drainage and the
amount of mature forest, with the strongest cor-
relations between dawn counts and mature forest
below 600 m (Burger 2001). In multiple regres-
sion models, 60-73% of the variation in dawn
counts of murrelets among watersheds was ex-
plained by the area of mature forest at elevations
<600 m, with another 8% explained by the neg-
ative effect of the combined area of logged and
immature (<160 yr) forest. In a different study
on Vancouver Island, which used audio-visual
detections from human observers, there were
significantly fewer detections (mean detections
per point) in watersheds with <50% old growth
compared with those with >50% (Burger 1995).
Whereas relationships between murrelet
counts and overall amount of available habitat
were strong across studies, relationships with the
spatial configuration of habitat at this watershed
scale were less revealing. For the Olympic Pen-
insula study, we used our map of potential nest-
ing habitat and the program FRAGSTATS
(McGarigal and Marks 1995) to define patches
of potential habitat (a patch is a set of adjacent
habitat pixels). We then computed a number of
fragmentation metrics and tested whether radar
counts of murrelets were correlated with these
metrics. Radar counts were not significantly cor-
related with the density (number/100 ha) of late-
seral patches below 1,067 m, average size of
patches, or a patchiness index that described a
continuum from many small patches to few
large patches (Raphael et al. 2002). These re-
sults were preliminary and may have been bi-
ased somewhat by the artificial patch boundaries
created by the elevation cut-off, and by the lim-
itations of the base vegetation map.
NESTING NEIGHBORHOOD
Two studies have examined the spatial char-
acteristics of murrelet habitat within the neigh-
borhood of nest sites, at a landscape scale inter-
mediate between watersheds and nest sites. Both
studies found that forest-cover attributes could
be useful predictors of murrelet occupancy at the
neighborhood scale. Habitat features within 200-
ha analysis circles (N = 261) were described
around locations occupied and unoccupied by
murrelets on the Olympic Peninsula (Raphael et
al. 1995). "Occupied" locations were those
where behaviors that have been associated with
nesting were observed; "unoccupied" locations
had no murrelet detections. Locations were
screened to include only those surveyed to the
Pacific Seabird Group's (PSG) protocol (Ralph
et al. 1994). Within the 200-ha circular neigh-
borhoods centered on occupied locations, there
was significantly greater area in large sawtimber
and old-growth forest compared with neighbor-
hoods centered on locations with no detections.
Old growth (but not large sawtimber) occurred
in larger patches (mean = 18.6 ha) in "occu-
pied" relative to "no detection" (mean = 8.5
ha) neighborhoods. A landscape pattern index,
derived from a combination of variables includ-
ing number of patches, Shannon's and Simp-
son's diversity and evenness indices, contagion,
and amount of edge (computed using program
226 STUDIES IN AVIAN BIOLOGY NO. 25
FRAGSTATS; see Raphael et al. 1995), differed
significantly between occupied and unoccupied
neighborhoods. Neighborhoods surrounding oc-
cupied locations had a higher landscape pattern
index, indicating greater number of patches,
greater variety of patch types, smaller average
sizes of all patches, and greater amounts of edge.
Thus, occupied neighborhoods had more intact
patches of old forest but other forest classes
within these neighborhoods tended to be patch-
ier and more fragmented. The authors cautioned
that the sample of survey locations was some-
what biased, weighted by one intensive study
and placed at prospective timber sales.
With a similar approach in northern California
and southern Oregon, Meyer (1999) used several
map sources and four neighborhood sizes (50-
3,217 ha circles) centered on survey stations.
Stations with no detections were screened to en-
sure that they or the stand they were in met the
PSG protocol. Analysis circles encompassing
more than one station received the highest status
of all stations. In general across map layers,
there was more old growth, it occurred in larger
patches, and was less fragmented in occupied
compared with unoccupied locations. The pres-
ence of high-contrast edges (natural or clearcuts)
did not deter use of a site. In the California por-
tion of the study area, 50-ha neighborhoods were
always occupied if they contained >20% old
growth with >6% of that as core area (>100 m
from an edge), -->12% of the area in one large
patch, a mean patch size ->11 ha, and mean core
area >3 ha.
In support of the influence of habitat frag-
mentation on murrelet nesting activity, a map of
relatively unfragmented old-growth forest in
northern California and southern Oregon from
the late 1980s was predictive of the current lo-
cations of occupied sites (75% correctly pre-
dicted in the coast redwood zone of northern
California; Meyer 1999). Areas highly frag-
mented before the late 1980s generally didn't
support murrelets in the early 1990s.
NEST SITES
Murrelet nests are difficult to locate, and the
sample of active nests on which to assess effects
of forest fragmentation on nest fate is relatively
small. Early data from small samples from sev-
eral locations indicated extremely high failure
rates and high rates of predation, an interpreta-
tion that has been tempered somewhat by larger
sample sizes. For example, 100% of 7 nests with
known outcome failed in Alaska, 3-4 of which
may have been due to predation (Naslund et al.
1995). In Oregon, 6 of 9 (67%) nests failed, with
5 of the 6 failures from predation (Nelson and
Peck 1995). Based on the most comprehensive
compilation of nest results to date (9 nests from
Alaska, 31 from British Columbia, 4 from Wash-
ington, 17 from Oregon, and 10 from Califor-
nia), 66% of 71 nests with known outcome have
failed, and 70% of these failures were due to
predation (Manley and Nelson 1999). Overall
failure rates (not predation only) were similar
among the states with larger sample sizes--61%
in B.C., 63% in Oregon, and 70% in Califor-
nia-although Alaska nests had complete repro-
ductive failure. Predation rates (% of total nests
lost to predation) were more variable but in-
creased from northern to southern latitude--
33% in Alaska, 48% in B.C., 53% in Oregon,
and 60% in California.
For the subsample of nests from Oregon and
B.C., distance to edge (roads, clearcuts) was the
most important predictor of nest fate. Successful
nests were significantly further from edges (5 =
141 m) than failed nests (5 = 56 m, P = 0.02).
Nest failure, and predation, were highest within
50 m of an edge compared with >50 m. All
nests >150 m from an edge were successful or
failed from reasons other than predation.
While there was a trend (P = 0.12) for suc-
cessful nests in Oregon and British Columbia to
occur in larger stands (_= 491 ha) compared
with unsuccessful nests (X = 281 ha), the rela-
tively limited sample of murrelet nests precludes
a reliable region-wide analysis of the relation-
ship between stand size and reproductive suc-
cess. Marbled Murrelet nests and occupied sites
have been found in stands ranging in size from
2-565 ha, but stand size is constrained in some
geographic areas. For example, average nest
stand size in Prince William Sound, Alaska, was
smaller than other locations, but reflected what
was available (3-63 ha; Naslund et al. 1995).
Average stand size of nests in the Bunster Range
in British Columbia was 224 ha (Manley 1999).
Changes in habitat configuration in forest
landscapes to smaller patch sizes and more edge
have been proposed as increasing nest failure by
increasing the risk of Marbled Murrelet nests to
predation. From observations at active nests,
Common Ravens (Corvus corax) are known
predators of Marbled Murrelet eggs and adults;
Steller's Jays (Cyanocitta stelleri) are known
predators of chicks and strongly-suspected pred-
ators of eggs (Nelson and Hamer 1995, Manley
1999). Other species implicated but not docu-
mented as nest predators include Gray Jay (Per-
isoreus canadensis), American Crow (Corvus
brachyrhynchos), Great Horned Owl (Bubo vir-
ginianus), and Cooper's Hawk (Accipiter coop-
eri; Nelson 1997). Peregrine Falcon (Falco per-
egrinus), Sharp-shinned Hawk (Accipiter stria-
tus), Northern Goshawk (Accipiter gentilis), and
Red-shouldered Hawk (Buteo lineatus) have tak-
EFFECTS OF FRAGMENTATION ON MARBLED MURRELETSRaphael et al. 227
en adult murrelets in forests (Marks and Naslund
1994, Singer et al. 1995, Nelson and Hamer
1995; E. Burkett, pers. comm.). It is theorized
that adult murrelets' cryptic breeding plumage,
limited visits to nests, and timing of visits to
coincide with low light levels (dawn and dusk)
evolved to minimize predation.
How these potential predators have responded
to a changed forest landscape is the best indi-
cation of the extent to which the risk of preda-
tion at Marbled Murrelet nests has been elevated
by forest fragmentation. For increased rates of
predation to be linked to fragmentation, preda-
tors must increase in numbers or forage exten-
sively along edges or small fragments; the di-
versity of predators must be highest at forest
edges, small fragments, or in fragmented land-
scapes (Marzluff and Restani 1999); or predators
must have greater foraging success along edges
compared with interior habitats.
Corvid populations have increased in the
western U.S. with increased urbanization, agri-
cultural intensification, and human activity in
forests and woodlands (Marzluff et al. 1994). In-
creases in American Crows, Common Ravens,
and Western Scrub-Jays (Aphelocoma calforni-
ca) are especially pronounced. Human refuse,
bird feeders, lawns, and road kills appear to be
fueling the corvid increase. Recreation sites
have similar, but more local, effects in murrelet
habitat, leading to large increases in ravens (S.
Singer, pers. comm.) and crows (this study).
Several studies have demonstrated that Stell-
er's Jays can be considered an edge species, and
thus benefit from increased fragmentation of for-
est landscapes. In a study combining point
counts with telemetry data in potential Marbled
Murrelet nesting habitat on Vancouver Island,
transects were established in forests and along
three types of edges: roads, clearcuts, and rivers
(Masselink 1999). The greatest number of jays
was detected along clearcut edges, and numbers
were higher at all edges compared with interior
forest. Among sites sampled with audio-visual
surveys along the central B.C. coast, Steller's
Jays and American Crows were detected more
frequently in sites fragmented by logging com-
pared with unfragmented (unlogged) forest
stands (Rodway and Regehr 1999).
However, it should be noted that Steller's Jay
response to fragmentation is not unequivocal. In
another coastal B.C. study, this species' abun-
dance was not associated with patch size in rem-
nant (left from logging) old-growth Douglas-tiff
western hemlock forest (Schieck et al. 1995).
Similarly, there were no significant correlations
with landscape variables, including stand size,
edge, landscape composition, and patterns in the
southern Washington Cascades (Lehmkuhl et al.
1991). In Douglas-fir forest in northwestern Cal-
ifornia, only 12% of --2,500 detections were
made on edges, abundance decreased with in-
creased proximity and length of clearcut edge,
and this species was not associated with the per-
cent of clearcut or length of edge in 1,000-ha
landscape blocks (Rosenberg and Raphael
1986). These studies suggest relationships be-
tween numbers of predators and fragmentation,
but further work is needed to determine whether
foraging efficiency of predators is affected by
fragmentation.
ARTIFICIAL NEST EXPERIMENTS
METHODS
To specifically address the effects of landscape con-
figuration on the risk of Marbled Murrelet nests to pre-
dation and the behavior of potential predators, we con-
ducted an artificial nest experiment for five breeding
seasons on the western side of the Olympic Peninsula,
Washington (Marzluff et al. 1999, unpubl. data). The
study area was adjacent to a major concentration of
murrelets in Washington (Varoujean and Williams
1995), and in a landscape used substantially by nesting
murrelets (Harrison et al. 1999). Study stands were se-
lected in a randomized block design to investigate the
effect of forest structure (simple, complex, and very
complex), proximity to human activity (< 1 km and >5
km), and landscape fragmentation (stands in continu-
ous forest versus those surrounded on at least 3 sides
by 1-15 yr-old regenerating forest). Effects of frag-
mentation were indicated by the responses of predation
and corvid nest predators to: (1) the isolation of stands
by regenerating forest, (2) the distance from forest
edge, and (3) the interaction of proximity to human
activity with stand isolation and distance from forest
edge.
Artificial nests were selected for these experiments
because of the extreme difficulty in locating a suffi-
cient sample of active nests to design a rigorous ex-
perimental study. We are aware of potential biases of
using artificial nests (e.g., Major and Kendal 1996,
Storaas 1988, Willebrand and Marcstr6m 1988). How-
ever, these are minimized in our case because we (1)
accurately simulated murrelet nests, eggs, and chicks,
and (2) limited our presence around nests (see details
below). Additionally, murrelet nests are especially
easy to mimic because (1) eggs are laid in simple de-
pressions on moss-covered branches, (2) eggs are
sometimes left unattended for several hours during in-
cubation, and (3) nestlings are left alone for much of
the day after they reach three days of age (Nelson and
Peck 1995, Manley 1999). We explicitly discuss any
biases in our use of artificial nests elsewhere (Marzluff
et al. 2001, Luginbuhl et al. 2001) and show that rates
of predation at our nests are higher, but not signifi-
cantly higher than those at natural nests. Here we are
concerned with comparing rates of nest predation
among various treatments. Such comparisons are un-
biased because we used the same techniques in all tests
and developed ways to assess the importance of all
possible nest predators in each treatment (see below).
We climbed trees to place 923 nests in 49 stands of
80- to >200-yr-old forests. We simulated nests at typ-
228 STUDIES IN AVIAN BIOLOGY NO. 25
ical heights and locations for murrelets: on moss-cov-
ered branches with diameter >11 cm, within the live
crown, >15 m above the ground, well covered from
above ( % overhead cover = 84.1%, SE = 0.39, N
= 923), and close to the trunk ( distance to bole =
38.9 cm, SE = 0.84, N = 923; Hamer and Nelson 1995,
Singer et al. 1995).
To minimize disturbance that might cue predators to
the nest's location (i.e., damage to the bark from spurs
or human scent trails left from touching the bole or
limbs), we climbed trees using 11-mm static climbing
rope following Perry (1978); avoided contact with the
tree by climbing with ascenders and rappelling to the
ground; wore latex or vinyl gloves while taking mea-
surements and preparing the nest; and marked nest
trees on the ground with white plastic flagging hung
in a random direction approximately 3 m from the tree
(Luginbuhl et al. 2001). The entire process of climb-
ing, placing nests, and rappelling took approximately
90 minutes.
Nests were placed in separate trees >50 m apart and
only six nests were placed in a given stand at any one
time to reduce the effects of area-restricted searching
practiced by Common Ravens and American Crows
(Marzluff and Balda 1992), and to decrease the pos-
sibility that high nest densities may cause predators to
associate our activities with food rewards (Sieving
1992, Major et al. 1994). To increase sample size per
stand, we replicated experiments from three to five
years per stand. No nest trees were used more than one
year, but annual replication allowed us to place 18-30
nests in each stand. Each year, two artificial nests (one
with an egg and one with a nestling) were placed at
each of three distances from the forest edge (<50 m
from the edge, approximately 100 m from the edge,
and >200 m from the edge).
An important improvement we made over typical
artificial nest experiments was to simulate nest con-
tents with plastic eggs and taxidermy mounts of nest-
lings. We painted eggs to resemble Marbled Murrelet
eggs, coated them with wax (household paraffin) to aid
with predator identification (Meiller 1987, Haskell
1995a), and stored them in cedar chips for >12 hr prior
to placement to limit human scent. Plastic eggs were
slightly larger than actual Marbled Murrelet eggs (64
mm x 44 mm vs. 59.8 mm x 37.6 mm; Nelson 1997).
Nestling models were made from domestic chicken
chicks preserved with borax. They were dark-colored
(mostly black), approximately 10 cm long, and were
placed in a posture that imitated a crouched or sleeping
nestling. Although decay of mounted nestlings was
limited (they appeared visually unchanged after 30 d),
they emitted odor perceptible to humans. However,
real Marbled Murrelet nests with a well-developed fe-
cal ring also give off odor perceptible to humans from
2 m away (T. Hamer, pers. comm.). We used eggs and
chicks because (1) they represent both life history stag-
es of murrelets vulnerable to nest predation; (2) eggs
are highly attractive to corvids (Heinrich et al. 1995)
and provide visual cues to their location; and (3)
chicks offer olfactory cues as well as visual ones,
which may better mimic a real nest and attract scent-
oriented predators (Ratti and Reese 1988, Major 1991,
Whelan et al. 1994, Darveau et al. 1997). We con-
firmed the predatory ability of small mammals detect-
ed at chick mounts with two years of experimental
research (Bradley 2000; J. Bradley and J. Marzluff,
unpubl. data). Mice attacked and displaced live pigeon
chicks (including those capable of vigorous defense
and outweighing mice ten-fold) in captivity and in the
wild. Flying squirrels attacked and killed pigeon chicks
in captivity. Thus, seemingly "inappropriate" mounted
chicks actually accurately indicated the importance of
scent-oriented nest predators in our experiments.
The fate of each nest was monitored remotely to
avoid continually advertising a nest's location. A mo-
tion-sensitive radio transmitter was placed in each
model; ground crews could then determine if a nestling
or egg was disturbed by checking the transmitter pulse
rate (similar to a standard mortality switch). We mon-
itored nests every other day for 30 d, the approximate
incubation or brooding period of Marbled Murrelets
(DeSanto and Nelson 1995). Remote monitoring al-
lowed determination of predation date (as opposed to
simply noting success or failure) while limiting the
amount of human presence at the nest sites. Remote
monitoring also allowed us to reclimb simulated nests
immediately after predation, before other predators or
heat from sunlight obscured clues to predator identity
left in wax. Occasionally no evidence of predation was
found on eggs or chicks despite a change in pulse rate
(Luginbuhl et al. 2001). When this occurred, we reset
the pulse rate and continued to monitor the nest.
We used a variety of techniques to identify potential
predators. In addition to eggs, transmitters inside
chicks were coated with household paraffin to record
marks left by predators. We monitored 82 artificial
nests using 35mm cameras attached to an active infra-
red motion detection system (Trailmaster © Model TM
1500, Goodson and Assoc., Inc., Lenexa, KS) as de-
scribed by Hernandez et al. (1997). These cameras im-
print photographs with date and time, and are equipped
with auto-advance, allowing photography of subse-
quent predators without researchers re-visiting the nest.
They provide an important way to calibrate the pred-
ator identification we based on marks in wax. Nests
observed with cameras were not included in the deter-
mination of predation rate (as indicated by number of
days to predation).
We used Kaplan-Meier procedures to estimate the
survival rate of nest contents (Pollock et al. 1989).
Survival among groups was compared with the log
rank test so that all measures of survivorship were
weighted equally (Lee 1980). We assumed each nest
was independent in survivorship analyses. This al-
lowed us to include covariates accounting for differ-
ences in nest microsites and set-up times in the anal-
ysis. Inclusion of covariates may better illuminate dif-
ferences due to design factors (Schueck and Marzluff
1995), but use of nests as experimental units may ar-
tificially inflate our sample size (and significance lev-
els) due to pseudoreplication (Hurlbert 1984).
The relative abundance of potential avian nest pred-
ators (corvids) was determined from surveys in study
stands using a modified point count procedure. These
methods are detailed in Luginbuhl et al. (2001).
RESULTS
From our experiments, rates of predation in
continuous stands did not differ from rates in
EFFECTS OF FRAGMENTATION ON MARBLED MURRELETS--Raphael et al. 229
A. All Nests
o.8
0.6
0.2
o.o
I---- Forest Fragmentst
0 5 10 15 20 25 30
13. Nests Far (> 5km) From Human Activity
0.8
0.6
0.4
0.2
o.o
--- F0re!t Fragment
35
0 5 10 15 20 25 30 35
C. Nests Near (< lkm) Human Activity
- Foreit Fragment
;::" o.8
r..f)
o.6
z
' 0.4
0.2
o
o
- o.o
0 5 10 15 20 25 30 35
Days Since Nest Was Placed in Field
FIGURE 2. Survivorship of artificial Marbled Mur-
relet nests in fragmented and continuous forest, Olym-
pic Peninsula, WA. Mean survivorship (symbols) _+ 1
SE is plotted separately for (A) all forest fragments (N
= 524) relative to all continuous forest (N = 399); (B)
fragments (N - 249) and continuous forest (N = 179)
near campgrounds and small human settlements; and
(C) fragments (N = 275) and continuous forest (N =
220) far from human activity centers.
Conbnuous
Fragmented
fragmented stands. Roughly 80% of nests were
preyed on after 30 d, regardless of whether they
were placed in forest fragments or continuous
forests (Fig. 2A); the daily pattern of nest loss
over the 30-d period of exposure was nearly
identical in fragments and continuous forest
(Fig. 2A; X(l = 0.64, P = 0.42). Proximity to
0.0 0.5 1.0 1.5 2.0
Corvid Abundance
FIGURE 3. Rates of predation (mean days until a
nest was depredated) in relation to mean abundance of
corvids in fragmented and continuous stands in the
Olympic Peninsula, WA. Values are means from 3 to
5 stands _+ I SE. After Luginbuhl et al. (2001).
human activity affected the influence of forest
fragmentation on predation within a stand (in-
teraction between proximity and fragmentation;
F(hs49) = 4.7, P = 0.03). Far (>5 km) from hu-
man activity, nests in fragments had slower rates
of predation than nests in continuous forest (Fig.
2B; X2(1) = 2.45, P = 0.12). In contrast, nests in
fragments near (<1 km) human activity had
rates of predation similar to nests in continuous
forest (Fig. 2C; X2½) = 0.25, P = 0.65).
In continuous stands, predation rates (as in-
dicated by number of days to predation) in-
creased as abundance of corvids increased (r =
-0.98, N = 6, P = 0.001; Fig. 3). In fragmented
stands, we found no relationship between corvid
abundance and rate of predation (r = -0.35, N
= 6, P = 0.500; Fig. 3). The lack of a relation
in fragmented stands may be related to edge ef-
fects (see below) that may be more important in
fragmented stands, or it may reflect the narrow
range (0.8-1.4 birds; Fig. 3) of predator abun-
dance in our sample of fragmented stands.
A particular predator did not appear to ac-
count for the lack of a fragmentation effect. The
effect of fragmentation was minimal regardless
of whether we simulated eggs or chicks (inter-
action between type of mimic and fragmenta-
tion; F(1,849 ) = 0.66, P = 0.80), despite the fact
that most predation on eggs was by corvids and
most predation on chicks was by mammals (Lu-
ginbuhl et al. 2001). Total corvid abundance was
similar among stands varying in proximity to
human activity and fragmentation (all P-values
in ANOVA > 0.48, N = 113 stand years; Fig.
4). Steller's Jay abundance varied as a joint
function of proximity to human activity and
fragmentation (interaction: F(1,108 ) = 6.87, P =
0.01), but this species was most abundant in
230 STUDIES IN AVI BIOLOGY NO. 25
I American Crows
r/// Common Ravens
-- Gray Jays
, ß Steller's Jays
'0 N = 21
' - , =N=21 N=32
Far Far Nr Near
Continuous Fragmeed Coinuous Fragmted
F[6E 4. Compositio, of c cotrid community
determined by point count scys ia stands of yin[
conti[ui W d proxiMty to human activity centers,
Olympic Peninsula, WA. Sample sizes are numbers o½
stands times aurabet of ycs each stand was surcy.
fragments far from human activity, which was
the condition associated with the slowest (not
fastest) rate of predation (Figs. 2 and 4).
The distance of a nest from the edge of the
forest-matrix interface was not consistently re-
lated to the rate of nest predation. Nests within
50 m of the forest edge tended to be preyed on
faster and to a greater extent than nests further
into the stand's interior (Fig. 5A; X2(2) = 4.75, P
= 0.09). This "edge effect" was consistent and
strong near human activity where the edge of the
forested stand abutted a campground or small
settlement. There, nests within 50 m of the edge
were preyed on significantly faster than nests
>200 m from the edge (Fig. 5B; X2(2) = 3.96, P
= 0.05). However, this "edge-effect" was in-
consistent far from human activity where the
matrix only included regenerating forest. Here,
nests 100 m from the edge fared best, but rates
were similar to those 50 m and 200 m from the
edge (Fig. 5C; X2(2) = 0.25, P = 0.62).
Corvid nest predators drove the changes in
nest predation in relation to distance from the
forest fragment edge. In settings far from human
activity the relative importance of corvid nest
predation was lowest 100 m from the fragment
edge (Fig. 6A), the distance associated with the
lowest overall rate of predation (Fig. 5B). Like-
wise, fragments abutting human activity centers
had the least predation 200 m from the edge
(Fig. 5C), where the relative amount of corvid
predation was also lowest (Fig. 6B).
Stand size did not affect predation rates. In an
ongoing study in Oregon using similar methods
as we report, J. Luginbuhl (unpubl. data) found
no difference (X2½) = 0.23, P = 0.63) in preda-
tion rates between large stands (30-60 ha) and
small stands (16-28 ha). Stand shape did have
a weak affect on predation rates, with higher
A. All Nests
1.0
0.8
0.6
0.4
0.2
0.0
- * - 50m
100m
0 5 10 15 20 25 30 35
B. Human Activity Center in Matrix
1.0
0.8
0.6
0.4
0.2
0.0
- ß - 50m
0 5 10 15 20 25 30 35
Matrix of Regenerating Forest
1.0
0.8
0.6
0.4
0.2
o.o
[- ß 50m
100m
200m
0 5 10 15 20 25 30 35
Days Since Nest Was Placed In Field
FIGURE 5. Survivorship of simulated murrelet nests
at varying distances from the edge of forest fragments,
Olympic Peninsula, WA. Survivorship ( + 1 SE) at
50 m, 100 m, and 200 m is evaluated in (A) all stands
regardless of proximity to human activity; (B) only in
fragments surrounded by 1-15-yr-old clearcuts; and
(C) only in fragments adjacent to campgrounds and
small settlements. Sample sizes are 208, 204, and 206
for all fragments (A); 116, 113, and 115 for fragments
surrounded by clearcuts (B); and 92, 91, and 91 for
fragments adjacent to human activity (C) at 50 m, 100
m, and 200 m from the edge, respectively.
EFFECTS OF FRAGMENTATION ON MARBLED MURRELETS-Raphael et al. 231
7o
40.
30.
10.
c 8O
0
70
(o
$o
z 40
c 20
= 10
0
FIGURE 6.
A. Far from Human Activity (> 5 krn)
50m 100m 200m
I Corvid r
, Mammal
B. Close to Human Activity (< 1 kin) Unknown
50m 100m 200m
Distance From Forest Edge
Percentage of nests at different distances
from the forest edge preyed on by corvids (Gray Jays,
Steller's Jays, American Crows, and Common Ravens)
versus small mammals (mice, squirrels, and occasion-
ally weasels) when the matrix is (A) far from human
activity (>5 km) and (B) close to human activity (< 1
km). Sample sizes are given in Fig. 4.
rates of predation in linear versus compact
stands (Xz(,) = 3.16, P = 0.08).
DISCUSSION
It is apparent that loss of older forest in the
Pacific Northwest, primarily due to logging but
also through other disturbance processes, has re-
duced the total area of suitable murrelet nesting
habitat and caused remaining habitat to become
more fragmented. From examining the evidence
of the potential effects of habitat fragmentation
on nesting habitat and populations of the Mar-
bled Murrelet at four geographic scales, we
found that it is difficult to separate the effects of
fragmentation from the concomitant effect of
habitat loss. Murrelet response to aspects of
fragmentation generally appeared at the smaller
scales investigated, including nest stands and
nest stand neighborhoods, although at-sea abun-
dances of murrelets were correlated with spatial
configurations of habitat in specific locations of
southern Oregon and Northern California (Mey-
er 1999). Marbled Murrelet nests appear partic-
ularly vulnerable to human-induced edges (e.g.,
roads and clearcuts) such as those studied in
Oregon and British Columbia. Our work with
artificial nests supported this conclusion in part,
as we did find that rates of predation generally
were greater within 50 m of edges, especially in
stands close to human activity (recreation sites
and small settlements). However, the artificial
nest study also demonstrated that relationships
between nest success and forest habitat likely
are more complex because the composition of
the nest predator assemblage is diverse and
varies among locations.
The overall lack of an obvious fragmentation
effect on artificial nests appears to be due to the
diversity of nest predators and to our observa-
tions that other factors affecting predator abun-
dance, such as proximity to people and refuse
and forest structure, can swamp effects of frag-
mentation. Among corvids, the total number of
individuals remained relatively constant among
fragmented and continuous landscapes. This oc-
curred despite variation in the composition of
the corvid community (Fig. 4). In particular, the
two species of jays showed reciprocal responses
to fragmentation that likely equalized the total
nest predation risk with respect to fragmentation.
Steller's Jays frequented fragmented landscapes,
whereas Gray Jays were most abundant in con-
tinuous landscapes (Fig. 4). Small mammals
were abundant and diverse nest predators in our
study area as well, and they were not confined
to fragmented or continuous landscapes. This
further reduced the relationship between preda-
tion and fragmentation (Marzluff and Restani
1999).
Effects of fragmentation on nesting success
can vary depending on the forest structures sur-
rounding nesting stands. In remote locations,
where forests are fragmented by timber harvest
and the matrix surrounding fragments is com-
posed of regenerating forest, nest predation rates
from our artificial nest experiment were not el-
evated, despite increases in Steller's Jay popu-
lations in such landscapes. Ongoing research in
Oregon suggests that rates of predation are ele-
vated in remote fragments surrounded by young
clearcuts with berry-producing shrubs compared
with fragments surrounded by clearcuts without
berries or by older regenerating forest (Marzluff
and Restani 1999; J. Luginbuhl et al., unpubl.
data). In contrast, in locations near human set-
tlements and recreation areas where forest frag-
ments abut human activity centers, fragmenta-
tion is likely to increase the risk of nest preda-
tion (Fig. 5C). A diverse corvid community near
human activity (Fig. 4) that feeds on human re-
fuse, offerings at feeders, and berries in exotic
plantings and early successional landscapes like-
ly drives this effect. The relative importance of
232 STUDIES IN AVIAN BIOLOGY NO. 25
TABLE 1. POTENTIAL SHORT TERM AND LONG TERM EFFECTS OF FRAGMENTATION OF NESTING HABITAT ON LOCAL
POPULATION SIZE AND DEMOGRAPHICS OF THE MARBLED MURRELET IN THE PACIFIC NORTHWEST
Fragmentation effect Population Adult Number Nest
on nesting habitat size survival of nests success
Reduced amount of nesting habitat
Smaller patch size (reduced area of interior
habitat, increased edge)
Increased number of patches c
Increased isolation of patches
O/- a 0/0 O/- -/0
0/- 0/0 / _/_b
0/0 0/0 0/0 0/0
-/- -/- 0/- -/0
a Symbols to left of slash are short term effects (<10 years); symbols following slash are longer term effects (>10 years but more generally several
decades). Symbols are: .... (negative or deleterious), "0" (neutral). "+" (positive). A negative effect on any demographic parameter is assumed to
cause population decline in the longer term.
b Effects will vary depending on suite of predators at particular sites. This often depends on the agent of fragmentation and resulting matrix. Some
predators are more abundant in continuous forest, others respond to edge (see text).
c Effects given for number of patches per se, all else relatively equal. (In larger context of fragmentation, we assume these patches would be smaller,
in addition to being more numerous.)
corvids as nest predators declined at nests great-
er than 200 m from edges abutting human activ-
ity (Fig. 6B).
An especially intriguing result (with manage-
ment implications) is our observation that for-
ests of simple structure are associated with the
smallest corvid populations (Marzluff et al.
1999). Maintaining even-aged forests in places
of human settlement should therefore be an ef-
fective management strategy to reduce regional
corvid populations. The siting of recreational de-
velopment in forested ecosystems also needs to
be rethought. Rather than place campsites in
structurally complex (aesthetically pleasing)
landscapes, placement of campsites in structur-
ally simple landscapes where predator popula-
tions are limited and where Marbled Murrelets
rarely nest would reduce risk of nest predation.
Based on our review of other studies and our
own work, we offer the following speculations
on the potential effects of fragmentation on pop-
ulations of the Marbled Murrelet. The primary
effects of fragmentation are a reduction in total
area of habitat, smaller average sizes of habitat
patches (along with reduced area in interior hab-
itat and increased amount of edge), increased
number of patches, and increased isolation of
patches. These consequences of habitat loss and
fragmentation can affect population size, likeli-
hood of nesting, survival of adults, and nesting
success. As shown in Table 1, these effects dif-
fer from the short term to long term.
Reduced amount of nesting habitat potentially
could result in short term displacement and
crowding of nesting birds into remaining patches
of habitat, although there is no direct evidence
that Marbled Murrelets would respond in this
way. Murrelets are thought to exhibit site fidelity
(Nelson 1997); if so, birds that had been nesting
in former habitat might fail to breed for several
years until they either find new habitat or die.
In that case, numbers of nests would decline im-
mediately. If displaced birds move to adjacent
nesting habitat, then crowding of nests will oc-
cur. In either case, population size would not be
affected in the short term. However, crowding
of nests could result in increased predation and
lower nesting success. Assuming short term
crowding, we speculate that nesting density in
remaining habitat would relax to pre-harvest
levels over the longer term, and population size
would decrease. Changes in distribution and
population declines observed at broad scales
along the coast where substantial habitat has
been lost (Carter and Erickson 1992, Kelson et
al. 1995) support the concept that population de-
clines are associated with loss of habitat.
Smaller patch size and its concomitant reduc-
tion in interior habitat and increased edge will
result in short term and long term increases in
rates of predation on nests (Manley and Nelson
1999; discussed above), although the strength of
this effect will vary depending on the suite of
predators occurring in the area (Andrdn 1992,
Nelson and Hamer 1995, Marzluff and Restani
1999). Our artificial nest results suggest that the
agent of fragmentation and concomitant devel-
opment of the matrix around the patches is im-
portant to the strength and significance of resul-
tant edge effects. For example, when human set-
tlement or recreational development fragments
habitat and surrounds patches, then edge effects
may be substantial. Smaller patches also may
result in fewer nesting attempts overall, as some
areas will no longer be considered suitable hab-
itat and thus not be occupied by murrelets. In
northern California, occupied locations con-
tained larger patches and lower edge/area than
unoccupied patches (Meyer 1999). Over the lon-
ger term these effects will lead to smaller pop-
ulations if fewer fledglings are recruited into the
breeding population. The effect on adult survival
is less clear, as the response to fragmentation
measures of species known to take adult Mar-
EFFECTS OF FRAGMENTATION ON MARBLED MURRELETS--Raphael et al. 233
bled Murrelets (see text) is not well documented
(but see Rosenberg and Raphael 1986; Mc-
Garigal and McComb 1995, 1999).
Increased number of patches is not likely to
affect population size or survival in the short or
long term, except as an indirect consequence of
related effects on patch size and total area of
nesting habitat. Increased isolation of patches
could lead to fewer nesting attempts, as poten-
tially suitable habitat patches >5 km from other
active nesting habitat are less likely to be oc-
cupied (Meyer 1999). Isolation also could lead
to short and long term decrease in adult survival
through increased vulnerability of murrelets to
predators. Although we know of no direct evi-
dence for this effect, we speculate that a mur-
relet flying over regenerating forest has greater
exposure to avian predators that one flying over
mature canopy, but it is also true that most
flights to attend nests take place at dusk and
dawn when diurnal predators are not active. If
this increased risk to predation does occur, the
long term result would be a reduction in number
of nests and a reduction in population size.
SUMMARY
At the regional scale, we found no correla-
tions between murrelet numbers and amount of
nesting habitat at the broad scale along the entire
Washington and Oregon coast; we found weak
correlations if we restricted our analysis to in-
land habitat within 25 km of the coast. However,
in southern Oregon and northern California,
murrelet densities offshore were higher in sub-
regions with more unfragmented and non-isolat-
ed old growth or old growth combined with re-
sidual old-growth forest.
At the watershed scale, we and other research-
ers found that numbers of murrelets flying into
delineated drainages were strongly correlated
with the amount of potential nesting habitat
within those drainages, but that indices of frag-
mentation were not correlated with murrelet
abundance.
At the neighborhood scale (--200-ha areas
surrounding stands surveyed for murrelets), po-
tential nesting habitat occurred in larger patches
and was less fragmented at neighborhoods oc-
cupied by murrelets compared with unoccupied
neighborhoods, although the entire neighbor-
hood tended to be patchier and more fragmented
due to the diversity of patches of younger forest.
The presence of high-contrast edges (natural or
clearcuts) did not seem to deter use of a site.
At the scale of individual nests, distance to
edge was an important influence on nest fate. In
Oregon and British Columbia, nest failure (pri-
marily from predation), was highest in nests
within 50 m of an edge; nests >150 m from an
edge were successful or failed from reasons oth-
er than predation. Some evidence suggested that
nests were more successful in larger stands
(-500 ha) than smaller stands (<300 ha), but
successful nests have been observed in a wide
range of stand sizes.
Our artificial nest experiments showed similar
rates of predation in fragmented and continuous
stands; the lack of an obvious fragmentation ef-
fect appeared to be due to the diversity of nest
predators, the influence of forest structures sur-
rounding nesting stands, and proximity to hu-
man activity. Total abundance of avian predators
(corvids) was similar in fragmented and contin-
uous stands; predation rates increased with
abundance of predators in continuous stands but
not in fragmented stands. In remote locations far
from human activity, predation rates were great-
er in continuous stands than in fragmented
stands; predation rates were similar in frag-
mented and continuous stands close to human
activity.
Despite the many insights that have emerged
from our review of existing studies and our new
work with artificial nests, a number of important
research questions remain. Understanding trade-
offs between predation risk and quality of nest-
ing habitat will require further investigation into
how much simple-structured forest in a land-
scape is enough to reduce predator populations
without reducing use of the remaining complex
forest for nesting by murrelets. Additional work
is certainly needed to better understand how the
variety of processes interacts to affect nest site
selection, survival, and reproductive success of
the murrelet and how these behaviors are influ-
enced by fragmentation of nesting habitat. In
particular:
ß How do the likelihood of nesting and char-
acteristics of nest sites vary in relation to
amount and type of edge?
ß How does adult survival, particularly suscep-
tibility to predation, vary with size, shape, and
isolation of nesting stands?
ß How does fragmentation of continuous nest-
ing habitat affect the behavior of resident
murrelets (that is, do displaced resident birds
nest in adjacent stands that might be of lower
quality, and can they move into stands that
are occupied by other nesting murrelets)?
ß What is the role and effect of mammalian
predators on real nests and how do mamma-
lian predators respond to fragmentation of
murrelet nesting habitat?
Although many questions remain, we are
heartened that new research is underway, much
of it stimulated by requirements for monitoring
population and habitat trends of this threatened
234 STUDIES IN AVIAN BIOLOGY NO. 25
species. Efforts to better define attributes of
nesting habitat and to relate population trends to
trends in the amount and pattern of habitat will
contribute to conservation of this unique bird.
ACKNOWLEDGMENTS
We thank C. B. Meyer, S. K. Nelson, I. C. Mmley,
C. W. Thompson, C. S. Strong, and A. Burger for al-
lowing us to use their unpublished data. Our artificial
nest experiments were supported by the Sustainable
Ecosystems Institute, Rayonier, National Council for
Air and Stream Improvement, Washington Department
of Natural Resources, Olympic Natural Resources
Center, the Pacific Northwest Research Station of the
U.S.D.A. Forest Service, U.S. Fish and Wildlife Ser-
vice, Boise Cascade Corporation, Willamette Indus-
tries, and Oregon Department of Forestry; D. E. Var-
land, L. S. Young, S. P. Horton, S. P. Courtney, J. E.
Bradley, and E. A. Neatherlin contributed to that work.
We particularly thank the many field assistants who
conducted the field experiments and gathered obser-
vations. B. Galleher prepared habitat maps and aided
with GIS analyses. This manuscript benefited from re-
views by S. K. Nelson, T. L. George, and an anony-
mous reviewer.
APPENDIX
DETAILS OF HABITAT MAPPING FOR FIGURE l
We used published reports of the characteristics of
Marbled Murrelet nest stands to identify potential nest-
ing habitat in Oregon and Washington. Given that
nests have been found in smaller-diameter trees with
epiphyte cover or deformities that create suitable plat-
forms and in younger stands with remnant old-growth
trees (Nelson 1997), but that remnant trees are not eas-
ily classified from satellite imagery, we accepted hab-
itat that met the minimum dbh of known nesting stands
rather than using dbh of nest trees. This may have
inflated our estimates of habitat in some areas. Stands
supporting tree nests in Oregon and Washington (N =
26) had a reported mem dbh of 47.7 cm (Hamer and
Nelson 1995), although we were unable to discern how
many trees were measured to arrive at stand diameter.
Five of 9 Oregon nests were located in mature/old-
growth stands, with mature trees defined as ->46 cm
dbh (Nelson md Peck 1995). In comparison, minimum
nest tree size was 76 cm (N = 45) in OR and 88.5 cm
(N = 6) in WA (Nelson 1997). Only potential nesting
habitat was extracted from the covers described below.
No spatial analyses were performed on these data.
Washington
The vegetation layer was a mosaic compiled from
approximately 20 sources that identified Northern
Spotted Owl (Strix occidentalis caurina) habitat, in-
cluding satellite imagery classifications and state, fed-
eral and private agency mapping (USFWS 1997b). It
included the Washington Department of Natural Re-
source's owl mosaic (1988-1993), the USDA Forest
Service's owl habitat data from Olympic National
Park, the WDNR/WDFW habitat map of the western
Olympic Peninsula, harvest chmge data (1989 and
1991), and several private timber industry databases.
This was the most up-to-date coverage for all land
ownerships within the study area. Late-seral habitat
was one of 10 land cover classes, and the only class
that included characteristics of suitable murrelet habi-
tat. Late seral was defined as mixed conifer/hardwood
with >70% crown closure from conifers and >10%
crown closure from trees >53 cm dbh. This class po-
tentially contained some stands that would not have
been included as habitat had we been able to specify
tree size, composition, and structure. Resolution was
100-m pixels. We further defined suitable habitat as
<1,067 m (3,500 ft) elevation. Inland extent of the
marbled murrelet zone was defined as 80 km (50 mi;
USFWS 1997a). Since the focus of this assessment
was coastal distribution of murrelets as related to hab-
itat, we included up to 80 km in from the outer coast,
not 80 km from all salt water in WA. We separated
the northern portion of the Olympic Peninsula along a
watershed boundary to correspond to at-sea data
around the tip of the Peninsula into the Strait of Juan
de Fuca.
Oregon
The Western Oregon Digital Image Project (WOD-
IP) vegetation layer was derived from Landsat TM im-
agery classification (Nighbert et al., unpubl. data) Res-
olution of the original data was 25 m, and was resam-
pied to 100-m pixel size. It was comprised of 247 com-
binations of diameter, canopy closure, number of
canopy layers, and species composition. We selected
conifer and mixed conifer/hardwood, multi-storied
stands with mean dbh >48 cm. We accepted all crown
closures, given the range of 12-99% at OR nests
(Hamer and Nelson 1995). We dropped down to the
>48 cm dbh size, as opposed to including only >74
cm (the largest size class available), to capture youn-
ger, potentially suitable habitat and to keep our criteria
for OR habitat similar to that used for WA. Given the
fire and harvest history in portions of the Sitka spruce
(Picea sitchensis) zone (Franklin and Dymess 1973,
Perry 1995), and the difficulty in capturing habitat
within this zone (S. K. Nelson, pers. comm.), we also
included single-storied stands with mean dbh >74 cm
within this narrow corridor along the OR coast. These
criteria may have overestimated suitable murrelet hab-
itat in some regions. We set the inland extent of the
murrelet zone at 56 km (35 mi), corresponding to the
Recovery Zone (USFWS 1997a). For consistency, we
applied the same elevation screen as in WA, defining
habitat as -<1,067 m, although this elevation is higher
than known nest sites in Oregon.
Murrelet zones from at-sea data
Of the at-sea survey data available, we selected
summer surveys from 1997 in Washington (C. Thomp-
son unpubl. data from 1999 report). We included only
nearshore transects (<500 m), as these were run more
consistently. These data were summarized over vari-
able-length transects (25 105 km), with some sections
surveyed multiple times. We selected transects that,
pieced together, covered the entire coastline. We used
the break points between transects to establish hori-
zontal bands along the coast. The peninsula configu-
ration of the Washington coastline presented a different
scenario than Oregon. We opted to include at-sea
counts from the north side of the peninsula (the west-
EFFECTS OF FRAGMENTATION ON MARBLED MURRELETS--Raphael et al. 235
ern Strait of Juan de Fuca), as these birds could po-
tentially be accessing some of the same habitat as birds
on the outer coast. At-sea densities were reported as
the number of murrelets by transect length X 200-m
width. For sections with multiple surveys within our
temporal and spatial criteria (summer months, near-
shore distances), we calculated an average density.
Of the Oregon data available (C. Strong, unpubl.
data), 1996 had the more complete coverage of the
coastline. For the 149 2-km stretches of shoreline sur-
veyed in both 1996 and 1997, average nearshore den-
sities did not differ between years (t = 0.216, P =
0.829), so we selected the 1996 data because of its
greater coverage. We selected July nearshore surveys
(400-600 m from shore). Densities were reported for
each 2-km section, and transects were divided into
three regions (north, central, south; Strong et al. 1995).
We maintained regional breaks, and within regions av-
eraged densities over 45-50 km sections. These section
and region breaks established our 11 horizontal bands.
Studies in Avian Biology No. 25:236-270, 2002.
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