EVOLUTION, ECOLOGY,
CONSERVATION, AND
MANAGEMENT OF
HAWAIIAN BIRDS:
A VANISHING AVIFAUNA
IRONTISPIICI: Hawai'i '0'0 (1o1< nbilis), largesl of the '0'0's and best-known by the indigenous inhab-
itants of Hawai'i. Formerly widespread and ½onon on the island of Hawai'i, it disappeared early in the 20
century, with Ihe last known specimen from Ka'0 Crater on 13 May 1902 (Kepler el ai. in press). Painting by
H. Douglas Pram Jr.
EVOLUTION, ECOLOGY,
CONSERVATION, AND
MANAGEMENT OF
HAWAIIAN BIRDS:
A VANISHING AVIFAUNA
J. Michael Scott, Sheila Conant, and Charles van Riper, III, Editors
Studies in Avian Biology No. 22
A PUBLICATION OF THE COOPER ORNITHOLOGICAL SOCIETY
Cover photograph of 'Anianiau (Hemignathus parvus) foraging on kanawao (Broussaisia arguta) by Jack Jeffrey.
STUDIES IN AVIAN BIOLOGY
Edited by
John T Rotenberry
Department of Biology
University of California
Riverside, CA 92521
Studies in Avian Biology is a series of works too long for The Condor,
published at irregular intervals by the Cooper Ornithological Society. Manu-
scripts for consideration should be submitted to the editor. Style and format
should follow those of previous issues.
Price $29.00 for softcover and $48.50 for hardcover including postage and
handling. All orders cash in advance; make checks payable to Cooper Orni-
thological Society. Send orders to Cooper Ornithological Society, % Western
Foundation of Vertebrate Zoology, 439 Calle San Pablo, Camarillo, CA
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ISBN: 1-891276-25-5 (cloth) ISBN: 1-891276-18-2 (paper)
Library of Congress Control Number: 2001 131292
Printed at Allen Press, Inc., Lawrence, Kansas 66044
Issued: 16 March 2001
Revised: 8 March 2002
Copyright ¸ by the Cooper Ornithological Society 2001
CONTENTS
DEDICATION ..................................................... viii
LIST OF AUTHORS ............................................... ix
INTRODUCTION ..................................................
........... J. Michael Scott, Sheila Conant, and Charles van Riper, III 1
HISTORICAL PERSPECTIVES
Introduction ... Charles van Riper, III, Sheila Conant, and J. Michael Scott 14
How many bird species in Hawai'i and the Central Pacific before first con-
tact? ................................ John Curnutt and Stuart Pimm 15
Patterns of success among introduced birds in the Hawaiian Islands ......
............. Michael P. Moulton, Karl E. Miller, and Eric A. Tillman 31
SYSTEMATICS
Introduction ........................................ Helen E James 48
Molecular systematics and biogeography of the Hawaiian avifauna .......
.......................... Robert C. Fleischer and Carl E. Mcintosh 51
Evolutionary relationships and conservation of the Hawaiian anatids .....
................................................ Judith M. Rhymer 61
The interplay of species concepts, taxonomy, and conservation: lessons from
the Hawaiian avifauna .......... H. Douglas Pratt and Thane K. Pratt 68
Why the Hawai'i Creeper is an Oreomystis: what phenotypic characters re-
veal about the phylogeny of Hawaiian honeycreepers H. Douglas Pratt 81
Phylogenetic placement of the Po'ouli, Melamprosops phaeosoma, based on
mitochondrial DNA sequence and osteological characters .............
................. Robert C. Fleischer, Cheryl L. Tarr, Helen E James,
Beth Slikas, and Carl E. Mcintosh 98
STATUS AND TRENDS
Introduction ............... J. Michael Scott and Charles van Riper, III 106
The status and population trends of the Newell's Shearwater on Kaua'i: insights
from modeling .... David G. Ainley, Richard Podolsky, Leah Deforest,
Gregory Spencer, and Nadav Nur 108
Migration of Northern Pintail across the Pacific with reference to the Ha-
waiian Islands ......... Miklos D. E Udvardy and Andrew Engilis, Jr. 124
The Hawai'i rare bird search 1994-1996 ..............................
..................... Michelle H. Reynolds and Thomas J. Snetsinger 133
Status and distribution of the Po'ouli in the Hanaw¾ Natural Area Reserve
between December 1995 and June 1997 .............. Paul E. Baker 144
ECOLOGY
Introduction ......................................... Sheila Conant 152
Drepanidine movements in relation to food availability in subalpine wood-
land on Mauna Kea, Hawai'i ......................................
............... Steven C. Hess, Paul C. Banko, Michelle H. Reynolds,
Gregory J. Brenner, Leona P. Laniawe, and James D. Jacobi 154
Breeding productivity and survival of the endangered Hawai'i Creeper in a
wet forest refuge on Mauna Kea, Hawai'i ...........................
............... Bethany L. Woodworth, Jay T. Nelson, Erik J. Tweed,
Steven G. Fancy, Michael P. Moore, Emily B. Cohen,
and Mark S. Collins 164
Significance of old-growth forest to the Hawai'i ',kepa ................
................................................ Leonard A. Freed 173
Demographic comparisons between high and low density populations of
Hawai'i 'kepa .................................... Patrick J. Hart 185
Breeding characteristics of the 'Akohekohe on east Maui ...............
.......................... Ellen M. VanGelder and Thomas B. Smith 194
'kohekohe response to flower availability: seasonal abundance, foraging,
breeding, and molt ...............................................
...................... Kim E. Berlin, John C. Simon, Thane K. Pratt,
James R. Kowalsky, and Jeff S. Hatfield 202
Age-related diet differences in two nectar-feeding Drepanidines: the ',kohe-
kohe and the 'Apapane ........................... John H. Carothers 213
LIMITING FACTORS
Introduction ............... J. Michael Scott and Charles van Riper, III 220
Limiting factors affecting Hawaiian native birds .......................
......................... Charles van Riper, III, and J. Michael Scott 221
Habitat use and limiting factors in a population of Hawaiian Dark-rumped
Petrels on Mauna Loa, Hawai'i ....................................
........... Darcy Hu, Catherine Glidden, Jill S. Lippert, Lena Schnell,
James S. MacIvor, and Julian Meisler 234
Interaction between the Hawaiian Dark-rumped Petrel and the Argentine ant
in Haleakalg National Park, Maui, Hawai'i ..........................
... Paul D. Krushelnycky, Cathleen S. N. Hodges, Arthur C. Medeiros,
and Lloyd L. Loope 243
Distribution and potential impacts of avian poxlike lesions in 'Elepaio at
Hakalau Forest National Wildlife Refuge ......... Eric A. VanderWerf 247
Immunogenetics and resistance to avian malaria in Hawaiian honeycreepers
(Drepanidinae) ................... Susan I. Jarvi, Carter T Atkinson,
and Robert C. Fleischer 254
Changes in native and introduced bird populations on O'ahu: infectious dis-
eases and species replacement .....................................
................ Cherie Shehata, Leonard Freed, and Rebecca L. Cann 264
What caused the population decline of the Bridled White-eye on Rota, Mar-
iana Islands? ............. Steven G. Fancy and Thomas J. Snetsinger 274
The evolution of passefine life histories on oceanic islands, and its impli-
cations for the dynamics of population decline and recovery ..........
........................................... Bertram G. Murray, Jr. 281
Newly emergent and future threats of alien species to Pacific birds and
ecosystems .... Lloyd L. Loope, Francis G. Howarth, Frederick Kraus,
and Thane K. Pratt 291
RECOVERY AND MANAGEMENT
Introduction ...................... J. Michael Scott and Sheila Conant 306
Effects of predator control on the survival and breeding success of the en-
dangered Hawaiian Dark-rumped Petrel .............................
............. Cathleen S. Natividad Hodges and Ronald J. Nagata, Sr. 308
Foraging behavior and temporal use of grasslands by NSnS: implications for
management ................. Friederike Woog and Jeffrey M. Black 319
An ecosystem-based management approach to enhancing endangered water-
bird habitat on a military base ........................ Diane Drigot 329
Why isn't the Nihoa Millerbird extinct? ...............................
................................... Sheila Conant and Marie Morin 338
Reintroduction and translocation of 'Oma'o: a comparison of methods ....
............ Steven G. Fancy, Jay T. Nelson, Peter Harrity, Jope Kuhn,
Marla Kuhn, Cyndi Kuehler, and Jon G. Giffin 347
Restoration techniques for Hawaiian forest birds: collection of eggs, artificial
incubation and hand-rearing of chicks, and release to the wild .........
.......... Cyndi Kuehler, Alan Lieberman, Peter Harrity, Marla Kuhn,
Jope Kuhn, Barbara Mcllraith, and John Turner 354
Conservation status and recovery strategies for endemic Hawaiian birds ..
................. Paul C. Banko, Reginald E. David, James D. Jacobi,
and Winston E. Banko 359
Evaluating the cost of saving native Hawaiian birds ....................
............................................ William W. M. Steiner 377
LITERATURE CITED .............................................. 384
DEDICATION
This STUDIES IN AVIAN BIOLOGY volume is dedicated to Dean Amadon, Paul H. Baldwin, and
David Woodside, colleagues and friends who laid the foundation for the recent renaissance of studies
of the endemic birds of Hawai'i and a link with ornithologists of the late 19 th century. It is because
many of the researchers in Hawai'i, and those in particular who have contributed to this book, have
anchored their scientific premises and hypotheses on the contributions of these three men, that we
dedicate this STUDIES IN AvIAN BIOLOGY to them.
Dean Amadon was stationed with the U.S. Army in Hawai'i in 1944 and 1945, spending most
of his time on the island of O'ahu, and two months on the Big Island as well. His interest in
Hawaiian honeycreepers had been aroused earlier while he was at the American Museum of Natural
History working with the ornithological collections of Lord Walter Rothschild. In Hawai'i, Amadon
worked with Bishop Museum collections and got into the field to observe birds whenever he was
free from his military duties. After the war he returned to academia to earn his doctorate at Cornell
University. His dissertation, eventually published as The Hawaiian Honeycreepers (Amadon 1950),
became a classic work on the systematics of the honeycreepers. It was the first thorough revision
of the group based on Mayifs "modem synthesis" of evolutionary theory. While working on the
Big Island, Amadon had been assisted by Paul Baldwin, whose research focused on life history
and ecology of the honeycreepers.
Paul H. Baldwin was one of the true pioneers of Hawaiian ornithology. During the 1930s while
Paul was working on his master's of science (on ocean crabs) at the University of Hawai'i, he was
selected biologist for the Civilian Conservation Corps, stationed at Hawai'i Volcanoes National
Park. It was at this position that Paul began collecting the first quantitative behavioral information
on the Hawaiian avifauna. Following World War II, he enrolled at the University of California at
Berkeley to complete his PhD. Coupling information that he had collected at Volcanoes National
Park during the 1930s with intensive fieldwork in 1948-1949, Paul completed the first intensive
behavioral work on banded Hawaiian honeycreepers. His study quantified for the first time physi-
ological cycles, population movement patterns, avian diets, and evolutionary patterns in Hawaiian
birds. He correlated these data with environmental factors (particularly climate), forest structure,
and resource availability. Paul Baldwin's 1953 paper, Annual cycle, environment and evolution in
the Hawaiian honeycreepers (Aves: Drepaniidae), still stands as a milestone in Hawaiian ornithol-
ogy. Paul's contributions to Hawai'i extend far beyond his 1953 work, with seminal papers on the
Nene, a number on introduced birds (e.g., the Red-billed Leiothrix), economic impacts of the in-
troduced mongoose, and impacts of cattle grazing on the native forests.
David Woodside was 15 years old when he began assisting George C. Munro in the field. Munro
later published Birds of Hawaii (1944), which included the first comprehensive survey of the dis-
tribution of Hawaiian forest birds since the turn of the century. Woodside has worked with virtually
every well-known ornithologist and agency that has engaged in research on Hawaiian birds, and
has probably seen more Hawaiian birds and visited more haunts of Hawaiian birds than any living
person. He was employed as a wildlife biologist for the Territory and later the State of Hawai'i for
many years. After retiring from the state wildlife agency, he began working for the refuge branch
of the U.S. Fish and Wildlife Service in 1980, where he continues to work today. Dave joined the
Hawaii Audubon Society as a charter member when he was 15, and has contributed his time and
expertise to studies and conservation of Hawaiian birds for a lifetime. Although he has witnessed
the extinction of many Hawaiian birds, he is among the fortunate few living souls who have seen
such birds as the O'ahu 'Alauahio, 'O'fi, Kama'o, and Kaua'i 'O'O.
LIST OF AUTHORS
DAVID G. AINLEY
H. T. Harvey and Associates
3150 Almaden Expressway, Suite 145
San Jose, CA 95118
CARTER T. ATKINSON
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 218
Hawaii National Park, HI 96718
PAUL E. BACER
U.S. Geological Survey
Pacific Island Ecosystems Science Center
P.O. Box 44
Hawaii National Park, HI 96718
(Present address: 8 Raglan Court, Silloth Cumbria,
CA5 4BW, UK)
PAUL C. BANKO
U.S. Geological Survey
Pacific Island Ecosystems Research Center
Kilauea Field Station, P.O. Box 44
Hawaii National Park, HI 96718
WINSTON E. BANKO
U.S. Geological Survey
Pacific Island Ecosystems Research Center
Kilauea Field Station
Hawaii National Park, HI 96718
(Present address: 332 Redwood Place,
College Place, WA 99324)
KIM E. BERLIN
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
JEFFREY M. BLACK
Department of Wildlife
Humboldt State University
Arcata, CA 95521-8299
GREGORY J. BRENNER
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
REBECCA L. CANN
Department of Genetics & Molecular Biology
John A. Bums School of Medicine
University of Hawaii at Manoa
Honolulu, HI 96822
JOHN H. CAROTHERS
Museum of Vertebrate Zoology and Department of
Zoology
University of California
Be/keley, CA 94720
EMILY B. C(HEN
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44 Building 344
Hawaii National Park, HI 96718
MARK S. COLLINS
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44, Bu.ilding 344
Hawaii National Park, HI 96718
SHEILA CONANT
Department of Zoology
University of Hawaii at Manoa
2538 McCarthy Mall
Honolulu, HI 96822
JOHN CURNUTT
Department of Ecology and Evolutionary Biology
University of Tennessee
Knoxville, TN 37919
REGINALD E. DAVID
Rang Productions
EO. Box 1371
Kailua-Kona, HI 96745
LEAH DEFOREST
EO. Box 6122
Hilo, HI 96720
DIANE DRIGOT
Environmental Department
Marine Corps Base Hawaii
MCBH Kaneohe Bay, HI 96863-3002
ANDREW ENGILIS, JR.
Ducks Unlimited, Inc.
3074 Gold Canal Drive
Rancho Cordova, CA 95670
(Present address: Department of
Wildlife, Fish, and Conservation Biology
University of California
Davis, CA 95616)
STEVEN G. FANCY
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44, Building 344
Hawaii National Park, HI 96718
ROBERT C. FLEISCHER
Molecular Genetics Laboratory
National Zoological Park
Smithsonian Institution
Washington, DC 20008
LEONARD A. FREED
Department of Zoology
University of Hawaii at Manoa
Honolulu, HI 96822
JON G. GIFFIN
Hawaii Dept. Land and Natural Resources
Division of Forestry and Wildlife
P.O. Box 4849
Hilo, HI 96720
CATHERINE GLIDDEN
Hawaii Volcanoes National Park
P.O. Box 52
Hawaii National Park, HI 96718-0052
PETER HARRITY
The Peregrine Fund
Keauhou' Bird Conservation Center
P.O. Box 39
Volcan,o, HI 96785
PATRICK J. HART .
Department of Zoology
University of Hawaii at Manoa
Honolulu, HI 96822
JEFF S. HATFIELD
U.S. Geological Survey
Patuxent Wildlife Research Center
Laurel, MD 20708-4017
STEVEN C. HESS
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
CATHLEEN S. NATIVIDAD HODGES
Haleakala National Park
Resources Management Division
P.O. Box 369
Makawao, Maui, HI 96768
FRANCIS G. HOWARTH
Department of Natural Sciences
Bernice P. Bishop Museum
P.O. Box 19000-A
Honolulu, HI 96819
DARCY HU
Hawaii Volcanoes National Park
P.O. Box 52
Hawaii National Park, HI 96718-0052
JAMES D. JACOBI
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
HELEN E JAMES
Department of Vertebrate Zoology
National Museum of Natural History
Smithsonian Institution
Washington, DC 20560
SUSAN I. JARVl
Molecular Genetics Laboratory
National Zoological Park
Smithsonian Institution
3001 Connecticut Ave. NW
Washington, DC 20008
(Present address: Department of Biology
University of Hawaii-Hilo
200 W. Kawili St.
Hilo, HI 96720)
JAMES R. KOWALSKY
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
FRED KRAUS
Department of Land and Natural Resources
Division of Forestry and Wildlife
1151 Punchbowl Street
Honolulu, HI 96813
PAUL D. KRUSHELNYCKY
U.S. Geological Survey
Haleakala National Park Field Station
Box 39
Makawao, HI 96768
CYNDI KUEHLER
The Peregrine Fund
Keauhou Bird Conservation Center
P.O. Box 39
Volcano, HI 96785
JOPE KUHN
The Peregrine Fund
Keauhou Bird Conservation Center
P.O. Box 39
Volcano, HI 96785
MARLA KUHN
The Peregrine Fund
Keauhou Bird Conservation Center
P.O. Box 39
Volcano, HI 96785
LEONA P. LANIAWE
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
ALAN LIEBERMAN
The Peregrine Fund
Keauhou Bird Conservation Center
P.O. Box 39
Volcano, HI 96785
JILL S. LIPPERT
Hawaii Volcanoes National Park
P.O. Box 52
Hawaii National Park, HI 96718-0052
LLOYD L. LOOPE
U.S. Geological Survey
Pacific Island Ecosystems Center
Haleakala Field Station
P.O. Box 369
Makawao, Maui, HI 96768
JAMES S. MACIVOR
1207 Tedford Way
Oklahoma City, OK 73116
BARBARA MCILRAITH
The Peregrine Fund
Keauhou Bird Conservation Center
P.O. Box 39
Volcano, HI 96785
CARL E. MCINTOSH
Molecular Genetics Laboratory
National Zoological Park
Smithsonian Institution
Washington, DC 20008
ARTHUR C. MEDE1ROS
U.S. Geological Survey
Haleakala National Park Field Station
Box 39
Makawao, HI 96768
JULIAN MEISLER
P.O. Box 851
Burlington, VT 05402
KARL E. MILLER
Department of Wildlife Ecology & Conservation
P.O. Box 110430
University of Florida
Gainesville, FL 32611-0430
MICHAEL P. MOORE
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44, Building 344
Hawaii National Park, HI 96718
MARIE MORIN
Department of Zoology
University of Hawaii at Manoa
2538 McCarthy Mall
Honolulu, HI 96822
MICHAEL P. MOULTON
Department of Wildlife Ecology & Conservation
P.O. Box 110430
University of Florida
Gainesville, FL 32611-0430
BERTRAM G. MURRAY, JR.
Graduate Program in Ecology and Evolution
80 Nichol Avenue
Rutgers Uniqersity
New Brunswick, NJ 08901-2882
RONALD J. NAGATA, gR.
Haleakala National Park
Resources Management Division
P.O. Box 369
Makawao, Maui, HI 96768
JAY T. NELSON
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44, Building 344
Hawaii National Park, HI 96718
NADAV NUR
Point Reyes Bird Observatory
Stinson Beach, CA 94970
STUART PIMM
Department of Ecology and Evolutionary Biology
University of Tennessee
Knoxville, TN 37919
RICHARD PODOLSKY
Avian Systems
Fort Lee, NJ 07024
H. DOUGLAS PRATT
Museum of Natural Science
Louisiana State University
Baton Rouge, LA 70893
THANE m. PRATt
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
MICHELLE H. REYNOLDS
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
JUDITH M. RHYMER
Department of Wildlife Ecology
University of Maine
Orono, ME 04469
LENA SCHNELL
US Army, CDR, USAG-HI-PTA
Attn: Evironmental Office
APO AP 96556-5703
J. MICHAEL SCOTI'
U.S. Geological Survey
IDCFWRU
College of Natural Resources
University of Idaho
Moscow, ID 83844-1141
CHERIE SHEHATA
Department of Genetics and Molecular Biology
John A. Burns School of Medicine
University of Hawaii at Manoa
Honolulu, HI 96822
JOHN C. SIMON
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 44
Hawaii National Park, HI 96718
BETH SLIKAS
Molecular Genetics Laboratory
National Zoological Park
Smithsonian Institution
Washington, DC 20008
THOMAS B. SMITH
Department of Biology
San Francisco State University
1600 Holloway Ave.
San Francisco, CA 94132
(Present address: Center for Population Biology
University of California
Davis, CA 95616)
THOMAS J. SNETSINGER
U.S. Geological Survey
Pacific Island Ecosystems Research Center
P.O. Box 1319, Kaua'i Forest Bird Project
Kekaha, HI 96752
GREGORY SPENCER
P.O. Box 6122
Hilo, HI 96720
WILLIAM W. M. STEINER
U.S. Geological Survey
Pacific Island Ecosystems Research Center
3190 Maile Way
Honolulu, HI 96822
CHERYL L. TARR
Department of Biology and Institute of Molecular
Evolutionary Genetics
208 Erwin W. Mueller Laboratory
Pennsylvania State University
University Park, PA 16802
ERIC A. TILLMAN
Department of Wildlife Ecology & Conservation
EO. Box 110430
University of Florida
Gainesville, FL 32611-0430
JOHN TURNER
The Peregrine Fund
Keauhou Bird Conservation Center
EO. Box 39
Volcano, HI 96785
Etak J. TWEED
U.S. Geological Survey
Pacific Island Ecosystems Research Center
EO. Box 44, Building 344
Hawaii National Park, HI 96718
MIKLOS D.E UDVARDY (DECEASED)
California State University, Sacramento
EPac A. VANDERWERF
University of Hawaii at Manoa
Department of Zoology
Edmonson Hall, 2538 The Mall
Honolulu, HI 96822
ELLEN M. VANGELDER
U.S. Geological Survey
Halemkala National Park
Box 369
Mmkawao, HI 96768
CHARLES VAN RIPER III
U.S. Geological Survey
Forest and Rangeland Ecosystem Science Center
Colorado Plateau Field Station
P.O. Box 5614
Northern Arizona University
Flagstaff, AZ 86011
BETHANY L. WOODWORTH
U.S. Geological Survey
Pacific Island Ecosystems Research Center
EO. Box 44, Building 344
Hawaii National Park, HI 96718
FRIEDERIKE WOOG
Libanonstr. 66
70184 Stuttgart
Germany
Studies in Avian Biology No. 22:1-12, 2001.
INTRODUCTION
J. MICHAEL SCOTT, SHEILA CONANT, AND CHARLES VAN RIPER, III
Hawai'i, a string of high and low islands
stretching 1,900 km across the Central Pacific,
has long captured the imagination of ornitholo-
gists. The Hawaiian Islands are the most isolated
archipelago in the world, and as a result, were
one of the last places on the planet to be popu-
lated (Fig. 1). The islands range from 25 million
year-old Kure, at the extreme northwest end of
the archipelago, to Hawai'i, the largest, south-
ernmost, and the youngest island at less than 1
million years old (Fig. 2; Stearns 1966, Carson
and Clague 1995). The climate varies dramati-
cally from arid, tropical seashores receiving less
than 26 cm (10 in) of precipitation on the lee-
ward slopes of the main islands, to the windward
peaks of the Alaka'i Swamp on Kaua'i, where
it is not uncommon for torrential rains to drop
52 cm (20 in) in a day, or to record 1,152 cm
(450 in) in a single year. The tropical lowland
areas contrast dramatically with the high alti-
tude, alpine ecosystems, and stone deserts,
where it freezes every night. The landscape is
as varied as it is dynamic. The tropical environ-
ments at sea level contrast dramatically with the
snow capped peaks of Mauna Loa and Mauna
Kea, which reach more than 4,000 m in height
above sea level and more than 9,000 m from
their base in the ocean from which they were
born (Stearns 1966, Carson and Clague 1995).
The Hawaiian archipelago is extremely dynam-
ic, with Loihi Seamount, an incipient island,
presently going through the birthing process at
a depth of 950 meters 30 km off the southern
coast of Hawai'i (Carson and Clague 1995).
Polynesians first reached the Hawaiian archi-
pelago about 500 AD, and Europeans not until
Captain James Cook's third voyage of discovery
in 1778. With a little imagination and use of
early voyagers' and naturalists' notes, one can
create in the mind's eye a pre-Polynesian Ha-
wai'i (Rothschild 1893-1900, Henshaw 1902a;
Kirch 1982a, 1985). In these presettlement is-
lands, millions of seabirds nested not only on
offshore islets, isolated cliff faces, and barren
subalpine areas where they are found today, but
on the beaches and in adjacent forests, bringing
tons of nitrates and phosphates from the sea. The
transport of nutrients from marine environments
by birds has significant impact on terrestrial en-
vironments, resulting in increased plant growth
and increases in those species that depend on
plants for habitat and food (Polls and Hurd
1996, Ryan and Watkins 1989; Anderson and
Polis 1998, 1999). As one moved inland, nu-
merous species of geese, including ten that we
know were flightless, grazed in the open grass-
lands. The forests must have been alive with
various species of Hawaiian honeyeaters, honey-
creepers, owls, and hawks, flightless species
(such as rail and ibis), and a variety of large-
billed finches. The dawn song chorus of this
ghost avifauna will never again be heard, but
one can dream.
Captain Cook's third voyage of discovery did
not contribute greatly to our ornithological
knowledge of the islands. Only 11 species and
subspecies were ,described based on specimens
collected during Cook's voyage, all from Kaua'i
and Hawai'i (Medway 1981). The first compre-
hensive characterizations of Hawaiian birds
were the almost simultaneous publications by
Rothschild (1893-1900) and Wilson and Evans
(1890-1899). These detailed descriptions of Ha-
waiian birds were augmented by the careful doc-
umentation of the natural history and ecology of
these birds by Henshaw (1902a,b) and Perkins
(1893, 1901, 1903). These works established a
foundation from which all current Hawaiian or-
nithology is measured. In this monograph, we
hope to provide another milestone of informa-
tion on the avifauna of the Hawaiian Islands and
the surrounding Pacific area, from which during
the next century ornithologists might measure
future changes in this avifauna. And most cer-
tainly there will be changes.
Historical changes to the Hawaiian avifauna
started early, and only 100 years after Cook's
exploration of the islands there were reports of
species that had apparently gone extinct (Perkins
1903). At the turn of the century, R. C. L. Per-
kins (as cited in Munro 1944:69) wrote:
"When I first arrived in Kona, the Great Ohia
trees, at an elevation of 2,500 feet, were a
mass of bloom and each of them was literally
alive with hordes of Crimson 'Apapane and
Scarlet 'I'iwi; while continually crossing from
the top of one great tree to another, the ''6
could be seen on the wing sometimes six or
eight at a time .... The 'Amakihi was nu-
merous in the same trees but less conspicuous
and occasionally one of the long billed Hem-
ignathus. Feeding on the fruit of the Ieie could
be seen the Hawaiian Crow commonly and the
'O'fl in great abundance. The picture of this
noisy, active, and often quarrelsome assembly
2 STUDIES IN AVIAN BIOLOGY NO. 22
FIGURE 1. The Hawaiian archipelago and other major islands in the Pacific Ocean.
Kure Atol
o .Midway Islands
Pearl and Hermes Reef
Lisianski
Island Laysan
ß Island
Maro Reef Gardner Pinnacles
Tern Island
La Perouse Pinnacle .
French Frigate Shoal.,
ß Necker Island
, Nihoa
Kaua'i
Ni'ihau
Kaula-
Lana'i '==- Maul
Kaho'olawe '-- J
Hawai'i
The
Hawaiian Islands
100 200 300
Statute Miles
FIGURE 2. The Hawaiian Islandsß Detailed maps of individual islands can be found in the chapters that follow,
INTRODUCTION--Scott et al. 3
of birds, many of them brilliant colors, was
one never to be forgotten. After the flowering
of the Ohia was over, the great gathering nat-
urally dispersed, but even then the bird pop-
ulation was very great."
By 1930 however, things had changed greatly
when Munro (1944:68) stated:
"Since civilization came to the Hawaiian Is-
lands, the experience of the native perching
birds has been tragic. My conclusions after the
survey (1936-1937) were that 25 species have
a fair chance of survival, while 30 species
were gone or likely to become extinct."
Today native birds are almost absent from the
remaining lowland forests of Kona. In their
place is an eclectic group of alien species, the
result of a large number of planned and un-
planned releases (see Moulton et al. this vol-
ume). Today, only the 'Elepaio (Chasiempis
sandwichensis), Hawai'i 'Amakihi (Hemigna-
thus virens), 'I'iwi (Vestiaria coccinea), and
'Apapane (Himatione sanguinea) can be seen re-
liably, and these not in all areas. The large-billed
finches, honeyeaters (species once ubiquitous),
'O'O (Psittirostra psittacea), and 'Oma'o
(Myadestes obscurus) are gone, while the 'ke-
pa (Loxops coccineus), 'Akiap61'au (Hemig-
nathus munroi), and Hawai'i Creeper (Oreomys-
tis bairdi) occur in vanishingly small numbers
in fewer than five isolated pockets of native for-
est. At this writing, the number of free-flying
'Alal (Corvus hawaiiensis) can be counted on
one hand.
The true magnitude of these losses would,
however, not be known until the pioneering re-
search of the husband-and-wife team of Storrs
Olson and Helen James (James and Olson 1991,
Olson and James 1991). They documented the
extinction of at least 50% of the Hawaiian avi-
fauna prior to the first use of the Linnean System
to describe a Hawaiian species. One hundred
nine endemic species are known to have oc-
curred in the Hawaiian Islands, 35 of which
(32%) are still extant. Nineteen additional taxa
were extant in the 18 th century, and 55 (50%)
are known only from the fossil and subfbssil rec-
ord (Table 1).
Reasons for losses of many Hawaiian bird
species have been well documented, including
the destruction of habitat (Cuddihy and Stone
1990) and taking of birds (van Riper and van
Riper 1982, Banko et al. this volume, Hu et al.
this volume, van Riper and Scott this volume),
predatory mammals (Tomich 1969, Kramer
1971, Atkinson 1977), introduced birds
(Schwartz and Schwartz 1949, Lewin 1971,
Lewin and Lewin 1984, Mountainspring and
TABLE 1. BIRDS KNOWN FROM FOSSIL RECORDS OR
KNOWN TO BREED IN THE HAWAIIAN ISLANDS
Group
dan- Popula-
Species known ger- tions
Spe- ed __
Histor- cies spe- 51
Fossil ic extant cies <50 500
Seabirds 1 22 22 2 2 1
Herons 0 1 0 0 0 0
Ibises 2 0 0 0 0 0
Waterfowl 10-11 3 3 3 0 0
Hawks 2 1 I 1 0 0
Rails 10 4 2 2 0 0
Stilts 0 I 1 1 0 0
Owls 4 1 1 0 0 0
Crows 3 1 1 1 1 0
Honeyeaters 0 6 1 1 1 0
Oldworld Flycatch-
ers 0 1 1 0 0 0
Oldworld Warblers 0 1 1 1 0 0
Hawaiian Thrushes 0 6 2 1 0 1
Honeycreepers 13 31 20 9 4 3
Notes: Information on fossil birds includes only those records assigned
species status (James and Olson 1991, Olson and James 1991 ). Additional
species are being described. Historical status is based on several sources
(Scott et al. 1989, Stone 1989, and Pyle 1997). In the last 11 years three
species have become extinct: Kaua'i '6'6 (Moho broccatus), Kama'o
(Myadestes myadestinus), and Oloma'o (Myadestes lanaiensis) based on
the standard of extinct until proven extant (Diamond 1987). The 'l'iwi
(Vestiaria coccinea) is declining in numbers and is disappearing froIll
areas formerly occupied. The numbers of two other species have de-
creased to less than 50 individuals. Species with less than 50 and 500
censused individuals are provided as indicators of jeopardy. The effective
population size lbr these species is unknown but likely to be one-half to
one-quarter censused population size (Primack 1993). For the 29 species
listed by the U.S. Fish and Wildlife Service as endangered, 8 continue
to decline, 6 are of unknown status, and 15 are stable in numbers
(USFWS 1996a).
Scott 1985), and diseases (Warner 1968, van
Riper et al. 1986, Atkinson et al. 1993a,b,c,
1995; Jarvi et al. this volume, Shehata et al. this
volume). The combined effect of these losses has
been summarized in papers by Scott et al.
(1986), van Riper and van Riper (1985), Ralph
and van Riper (1985), Freed et al. (1993), and
van Riper and Scott (this volume).
While many species have succumbed to ex-
tinction (Table 1), major steps have been taken
recently to save Hawai'i's endangered species.
The U.S. Fish and Wildlife Service has estab-
lished two national wildlife refuges (Hakalau
Forest and Kona Forest National Wildlife Ref-
uges) on the island of Hawai'i with a primary
objective of protecting endangered forest birds.
Combined, these preserves total nearly 16,194
ha (40,000 acres). The National Park Service has
eliminated goats (Capra hircus) and sheep (Ovis
aries) from Hawai'i Volcanoes and Haleakala
National Parks. In addition, large acreages are
now pig- (Sus scrofa) free in that park. Similar-
4 STUDIES IN AVIAN BIOLOGY
TABLE 2. CHECKLIST OF THE BIRDS OF HAWAII
NO. 22
Symbols for status
R - Resident native species; normal does not leave islands: Re - Resident, endemic species, not extinct; Rx - Resident, endemic species, presumed
extinct; Res - Resident; indigenous species, subspecies is endemic; Hawaiian; Ri - Resident; indigenous species, Hawaiian form is not endemic.
A - Alien introduced species; resident; normally does not leave the islands: Al - Alien; long established and breeding since before 1940; An -
Alien, new introduced since 1950; apparently established; Ax - Alien; formerly long established and breeding for more than 25 years, but now no
longer present in Hawaii.
E (or T) immediately preceding the genus name designates a species or subspecies currently listed as Endangered (or Threatened) on the Federal List
of Endangered species.
B - Breeding species in Hawaii, native, most individuals leave Hawaii when not breeding: Bo - Breeder, species breeds only in Hawaii; Bes -
Breeder, species also breeds elsewhere; Hawaiian subspecies breeds only in Hawaii; Bi - Breeder, Hawaiian form also breeds elsewhere.
V - Visitor species, breeds elsewhere, occurs in Hawaii when not breeding: Vc - Visitor, common migrant to Hawaii; Vr - Visitor, regular migrant
to Hawaii in small numbers; Vo - Visitor, occasional to frequent migrant to Hawaii; Vs - Visitor, accidental straggler to Hawaii; Vd = Visitor,
accidental straggler to Hawaii, recorded in Hawaii only as dead remains.
Common name Scientific name Status
GREBES PODICIPEDIDAE
Pied-billed Grebe Podilymbus podiceps Ri
Horned Grebe Podiceps auritus Vs
Red-necked Grebe Podiceps grisegena Vs
Eared Grebe Podiceps nigricollis Vs
ALBATROSSES DIOMEDEIDAE
Laysan Albatross Phoebastria immutabilis Bi
Black-footed Albatross Phoebastria nigripes Bi
Short-tailed Albatross E-Phoebastria albatrus Vo
PETRELS, SHEARWATERS PROCELLARIIDAE
Northern Fulmar Fulmarus glacialis Vo
Kermadec Petrel Pterodroma neglecta Vs
Herald Petrel Pterodroma arminjoniana Vs
Murphy's Petrel Pterodroma ultima Vs
Mottled Petrel Pterodroma inexpectata Vo
Juan Fernandez Petrel Pterodroma externa Vo
(Hawaiian Petrel)--Dark-rumped Petrel E-Pterodroma phaeopygia Res
sandwichensis
White-necked Petrel Pterodroma cervicalis Vo
Bonin Petrel Pterodroma hypoleuca Bi
Black-winged Petrel Pterodroma nigripennis Vo
Cook's Petrel Pterodroma cookii Vs
Stejneger's Petrel Pterodroma longirostris Vd
Bulwer's Petrel Bulweria bulwerii Bi
Jouanin's Petrel Bulweria fallax Vs
Streaked Shearwater Calonectris leucomelas Vs
Flesh-footed Shearwater Puffinus carneipes Vo
Wedge-tailed Shearwater Puffinus pacificus B i
chlororhynchus
(New Zealand Shearwater)Buller's Puffinus bulleri Vs
Shearwater
Sooty Shearwater
Short-tailed Shearwater
Christmas Shearwater
(Newell's Shearwater) Townsend's
Shearwater
Little Shearwater
STORM-PETRELS
Wilson's Storm-Petrel
Fork-tailed Storm-Petrel
Leach's Storm-Petrel
(Hawaiian or Harcourt's Storm-Petrel)--
Band-rumped Storm-Petrel
(Sooty Storm-Petrel)--Tristram's Storm-Pe-
trel
TROPICBIRDS
White-tailed Tropicbird
Red-billed Tropicbird
Red-tailed Tropicbird
Puffinus griseus Vr
Puffinus tenuirostris Vo
Puffinus nativitatis Bi
T-Puffinus auricularis newelli Be
Puffinus assimilis Vs
HYDROBATIDAE
Oceanires oceanicus Vs
Oceanodroma furcata Vs
Oceanodroma leucorhoa Vr '
Oceanodroma castro Bi
Oceanodroma tristrami Bi
PHAETHONTIDAE
Phaethon lepturus Ri
Phaethon aethereus Vs
Phaethon rubricauda Bi
rothschiMi
INTRODUCTION--Scott et al. 5
TABLE 2. CONTINUED
Conlmon name Scientific nanle Status
BOOBIES SULIDAE
(Blue-faced Booby)--Masked Booby Sula dactylatra personata Ri
Brown Booby Sula leucogaster plotus Ri
Red-footed Booby Sula sula rubripes Ri
CORMORANTS PHALACROCORACIDAE
Pelagic Cormorant Phalacrocorax pelagicus Vs
FRIGATEBIRDS FREGATIDA E
Great Frigatebird Fregata minor palmerstoni Ri
Lesser Frigatebird Frigata ariel Vs
HERONS, EGRETS ARDEIDAE
Great Blue Heron Ardea herodias Vs
Great Egret Ardea alba Vs
Snowy Egret Egretta thula Vs
Little Blue Heron Egretta caerulea Vo
Cattle Egret Bubulcus ibis An
(Green-backed Heron)--Green Heron Butorides virescens Vs
Black-crowned Night-Heron Nycticorax nycticorax hoactli Ri
IBISES THRESKIORNITHIDAE
White-faced Ibis Plegadis chihi Vs
GEESE, DUCKS ANATIDAE
Fulvous Whistling-Duck Dendrocygna bicolor Ri
(White-fronted Goose)--Greater White- Anser albifrons Vs
fronted Goose
Emperor Goose Chen canagica Vo
Snow Goose Chen caerulescens Vs
Canada Goose Branta canadensis Vo
(Nn)--Hawaiian Goose E-Branta sandvicensis Re
Brant Branta bernicla Vo
(Whistling Swan)--Tundra Swan Cygnus columbianus Vs
Gadwall Anas strepera Vs
(European Wigeon)--Eurasian Wigeon Anas penelope Vs
American Wigeon Anas americana Vr
Mallard Arias platyrhynchos A1, Vo
(Koloa)--Hawaiian Duck E-Arias wyvilliana Re
Laysan Duck E-Arias laysanensis Re
Blue-winged Teal Arias discors Vo
Cinnamon Teal Arias cyanoptera Vs
Northern Shoveler Arias clypeata Vc
Northern Pintail Anas acuta Vc
Garganey Arias querquedula Vo
Green-winged Teal Arias crecca Vr
Canvasback Aythya valisineria Vs
Redhead Aythya americana Vs
Common Pochard Aythya ferina Vs
Ring-necked Duck Aythya collaris Vo
Tufted Duck Aythya fuligula Vs
Greater Scaup Aythya marila Vo
Lesser Scaup Aythya affinis Vr
Harlequin Duck Histrionicus histrionicus Vs
Surf Scorer Melanitta perspicillata Vs
Black Scoter Melanitta nigra Vs
Long-tailed Duck Clangula hyemalis Vs
Bufflehead Bucephala albeola Vo
Common Goldeneye Bucephala clangula Vs
Hooded Merganser Lophodytes cucullatus Vs
Common Merganser Mergus merganser Vs
Red-breasted Merganser Mergus serratot Vs
Ruddy Duck Oxyura jamaicensis Vs
HAWKS, EAGLES ACCIPITRIDAE
Osprey Pandion haliaetus Vo
Black Kite Milvus migrans Vs
Steller's Sea-Eagle Haliaeetus pelagicus Vs
6
TABLE 2. CONTINUED
STUDIES IN AVIAN BIOLOGY
NO. 22
Common name Scientific nalne Status
Northern Harrier Circus cyaneus Vs
Gray Frog-Hawk Accipiter soloensis Vs
('Io)--Hawaiian Hawk E-Buteo solitarius Re
Rough-legged Hawk Buteo lagopus Vs
Golden Eagle Aquila chrysaetos Vs
FALCONS FALCONIDAE
Merlin Falco columbarius Vs
Peregrine Falcon E-Falco peregrinus Vo
FRANCOLINS, OLD WORLD QUAIL,
TURKEY PHASIANIDAE
Chukar Alectoris chukar A1
Gray Francolin Francolinus pondicerianus An
Black Francolin Francolinus?ancolinus An
Erckel's Francolin Francolinus erckelii An
Japanese Quail Coturnix japonica A1
Red Junglefowl Gallus gallus A1
Kalij Pheasant
(Green Pheasant, Common Pheasant)-- Lophura leucomelanos An
Ring-necked Pheasant Phasianus colchicus A1
Common Peafowl Pavo cristatus A1
Wild Turkey Meleagris gallopavo A1
NEW WORLD QUAIL ODONTOPHORIDAE
California Quail Callipepla californica A1
Gambel's Quail Callipepla gambelii A1
RAILS, GALLINULES, COOTS RALLIDAE
Laysan Rail Porzana palmeri Rx
Hawaiian Rail Porzana sandwichensis Rx
(Hawaiian Gallinule)--Common E-Gallinula chloropus Res
Moorhen sandvicensis
(American Coot)--Hawaiian Coot E-Fulica alai Res
American Coot Fulica americana Vs
CRANES GR UIDAE
Sandhill Crane Grus canadensis Vs
PLOVERS CHARADRIIDAE
(Gray Plover)--Black-bellied Plover Pluvialis squatarola Vr
(Lesser or American Golden-Plover)-- Pluvialis Mva Vc
Pacific Golden-Plover
Mongolian Plover Charadrius mongolus Vs
Common Ringed Plover Charadrius hiaticula Vs
Semipalmated Plover Charadrius semipalmatus Vo
Killdeer Charadrius vociferus Vs
Eurasian Dotterel Charadrius morinellus Vs
STILTS RECURVIROSTRIDAE
(Hawaiian Stilt)--Black-necked Stilt E-Himantopus mexicanus knud- Res
seni
SANDPIPERS, WADERS SCOLOPACIDAE
Greater Yellowlegs Tringa melanoleuca Vs
Lesser Yellowlegs Tringa flavipes Vr
Wood Sandpiper Tringa glareola Vs
Solitary Sandpiper Tringa solitaria Vs
Willet Catoptrophorus semipalmatus Vs
Wandering Tattler Heteroscelus incanus Vc
(Siberian Tattler, Polynesian Tattler)-- Heteroscelus brevipes Vs
Gray-tailed Tattler
Spotted Sandpiper Actiris macularia Vs
Whimbrel Numenius phaeopus Vs
Bristle-thighed Curlew Numenius tahitiensis Vr
Far Eastern Curlew Numenius madagascariensis Vs
Hudsonian Godwit Limosa haemastica Vs
Bar-tailed Godwit Limosa lapponica Vo
Marbled Godwit Limosa kdoa Vs
Ruddy Tumstone Arenaria interpres Vc
Red Knot Calidris canutus Vs
Sanderling Calidris alba Vo
INTRODUCTION--Scott et al. 7
TABLE 2. CONTINUED
Common name Scientific name Status
Semipalmated Sandpiper Calidris pusilla Vs
Western Sandpiper Calidris mauri Vo
Red-necked Stint Calidris ruficollis Vs
Little Stint Calidris minuta Vs
Long-toed Stint Calidris subminuta Vs
Least Sandpiper Calidris minutilla Vo
Baird's Sandpiper Calidris bairdii Vs
Pectoral Sandpiper Calidris melanotos Vr
Sharp-tailed Sandpiper Calidris acuminata Vr
Dunlin Calidris alpina Vr
Curlew Sandpiper Calidrisferruginea Vs
Buff-breasted Sandpiper Tryngites subruficollis Vs
Ruff Philomachus pugnax Vo
Short-billed Dowitcher Limnodromus griseus Vo
Long-billed Dowitcher Limnodromus scolopaceus Vr
Common Snipe Gallinago gallinago Vo
Pin-tailed Snipe Gallinago stenura Vs
Wilson's Phalarope Phalaropus tricolor Vo
Red-necked Phalarope Phalaropus lobatus Vs
Red Phalarope Phalaropus fulicaria Vs
JAEGERS, GULLS, TERNS, NODDIES LARIDAE
South Polar Skua Stercorarius maccormicki Vs
Pomarine Jaeger Stercorarius pomarinus Vr
Parasitic Jaeger Stercorarius parasiticus Vs
Long-tailed Jaeger Stercorarius longicaudus Vs
Laughing Gull Larus atricilla Vo
Franklin's Gull Larus pipixcan Vs
Black-headed Gull Larus ridibundus Vs
Bonaparte's Gull Larus philadelphia Vo
Mew Gull Larus canus Vs
Ring-billed Gull Larus delawarensis Vo
California Gull Larus califbrnicus Vs
Herring Gull Larus argentatus Vo
Slaty-backed Gull Larus schistisagus Vs
Western Gull Larus occidentalis Vs
Glaucous-winged Gull Larus glaucescens Vo
Glaucous Gull Larus hyperboreus Vs
Black-legged Kittiwake Rissa tridactyla Vs
Gull-billed Tern Sterna nilotica Vs
Caspian Tern Sterna caaTia Vs
Great Crested Tern Sterna bergii Vs
Sandwich Tern Sterna sandvicensis Vs
Common Tern Sterna hitundo Vs
Arctic Tern Sterna paradisaea Vo
Little Tern Sterna albifrons Vs
Least Tern Sterna antillarum Vo
Gray-backed Tern Sterna lunata Bi
Sooty Tern Sterna fuscata oahuensis Bi
Whiskered Tern Chlidonias hybridus Vs
Black Tern Chlidonias niger Vs
(Common Noddy)--Brown Noddy Anous stolidus pileatus Ri
(Hawaiian Noddy, White-capped Noddy)-- Anous minutus melanogenys Res
Black Noddy
Blue-gray Noddy Procelsterna cerulea saxarilis Ri
(Common Fairy-Tern, Fairy Tern)-- Gygis alba rothschildi Ri
White Tern
AUKLETS, PUFFINS ALCIDAE
Cassin's Auklet Ptychoramphus aleuticus Vs
Parakeet Auklet Aethia psittacula Vd
Horned Puffin Fratercula corniculata Vs
Tufted Puffin Fratercula cirrhata Vd
8
TABLE 2. CONTINUED
STUDIES IN AVIAN BIOLOGY
NO. 22
Common name Scientific name Status
SANDGROUSE
Chestnut-bellied Sandgrouse
DOVES
Rock Dove
(Chinese Dove, Lace-necked Dove)-
Spotted Dove
(Barred Dove)--Zebra Dove
Mourning Dove
PARAKEETS
Rose-ringed Parakeet
CUCKOOS
Common Cuckoo
Yellow-billed Cuckoo
BARN OWLS
Barn Owl
TYPICAL OWLS
(Hawaiian Owl)--Short-earned Owl
NIGHTHAWKS
Common Nighthawk
SWIFTLETS
(Uniform, Island or Gray SwiftleO--Guam
Switflet
KINGFISHERS
Belted Kingfisher
HONEYEATERS
'O'o'a'a--Kaua'i 'O 'O
O'ahu 'O'o
(Moloka'i 'O'o)--Bishop's 'O'O
Hawai'i 'O'O
Kioea
CROWS
('Alala)--Hawaiian Crow
MONARCH FLYCATCHERS
'Elepaio
{ Kaua'i 'Elepaio } --
{ O'ahu 'Elepaio }--
{ Hawai 'i 'Elepaio }-
LARKS
(Eurasian Skylark)--Sky Lark
SWALLOWS
Barn Swallow
TITS
(Japanese Tit, Yamagara)--Varied Tit
BULBULS
Red-vented Bulbul
Red-whiskered Bulbul
OLD WORLD WARBLERS
(Uguisu)--Japanese Bush-Warbler
Millerbird
{ Laysan Millerbird }--
{Nihoa Millerbird}-
THRUSHES, SOLITAIRES
(Shama Thmsh)--White-rumped Shama
(Large Kaua'i Thrush)--Kg. ma'o
(O'ahu Thrush)--'maui
Oloma'o
{(Moloka'i Thrush)Moloka'i Olo-
ma'o}--
PTEROCLIDIDAE
Pterocles exustus An
COLUMBIDAE
Columba livia A1
Streptopelia chinensis AI
Geopelia striata AI
Zenaida macroura An
PSITTA CIDAE
Psittacula krameri An
CUCULIDAE
Cuculus canorus Vs
Coccyzus americanus Vs
TYTONIDAE
Tyto alba An
STRIGIDAE
Asio fiammeus sandwichensis Res
CAPRIMULGIDAE
Chordeiles minor Vs
APODIDAE
Aerodramus bartschi An
ALCEDINIDAE
Ceryle alcyon Vs
MELIPHA GIDAE
E-Moho braccatus Re
Moho apicalis Rx
Moho bishopi Rx
Moho nobdis Rx
Chaetoptila angustipluma Rx
CORVIDAE
E-Corvus hawaiiensis Re
MONARCHIDAE
Chasiempis sandwichensis
C. s. sclateri Re
C. s. ibidis Re
C. s. sandwichensis, ridgwayi, Re
bryani
ALA UDIDAE
Alauda arvensis AI, Vs
HIRUNDINIDAE
Hirundo rustica Vs
PARIDAE
Parus varius Ax
PYCNONOTIDAE
Pycnonotus cafer An
Pycnonotus jocosus An
SYLVIIDAE
Cettia diphone A1
Acrocephalus familiaris
A. f familiaris Rx
E-A. f kingi Re
TURDIDAE
Copsychus malabaricus AI
E-Myadestes myadestinus Re
Myadestes woahensis Rx
Myadestes lanaiensis
E-M.l. rutha Re
INTRODUCTION--Scott et al. 9
TABLE 2. CONTINUED
Conmon name Scientific name Status
{ (Lgna'i Thrush)--Lgna'i Oloma'o}--
(Hawai'i Thrush)--'0ma'o
(Small Kaua'i Thrush)--Puaiohi
BABBLERS
Greater Necklaced Laughing-thrush
Gray-sided Laughing-thrush
(Melodious Laughing-thrush, Chinese
Thrush)--Hwamei
(Pekin Nightingale, Japanese Hill-robin)-
Red-billed Leiothrix
WHITE-EYES
(Mejiro)--Japanese White-eye
MOCKINGBIRDS
Northern Mockingbird
STARLINGS, MYNAS
European Starling
Common Myna
PIPITS
Olive-backed Pipit
Red-throated Pipit
American Pipit
EMBERIZIDS
Yellow-faced Grassquit
Saffron Finch
(Brazilian Cardinal)Red-crested
Cardinal
Yellow-billed Cardinal
Savannah Sparrow
Snow Bunting
CARDINALS
(American or Kentucky Cardinal)--
Northern Cardinal
MEADOWLARKS, GRACKLES
Western Meadowlark
Great-tailed Grackle
FINCHES
CARDUELINE FINCHES
(Linnet)--House Finch
Common Redpoll
(Green Singing-Finch)--Yellow- fronted
Canary
(Canary)--Common Canary
HAWAIIAN HONEYCREEPERS
FINCH-BILLED HONEYCREEPERS
Laysan Finch
Nihoa Finch
Lgna'i Hookbill
Palila
Lesser Koa-Finch
Greater Koa-Finch
(Grosbeak Finch)--Kona Grosbeak
Maui Parrotbill
SLENDERBILLED
HONEYCREEPERS
Hawai'i 'Amakihi
{ Hawai'i 'Amakihi }--
{ Maui 'Amakihi }--
O'ahu 'Amakihi
Kaua'i 'Amakihi
M. l. lanaiensis Rx
Myadestes obscurus Re
E-Myadestes palmeri Re
T1MALllDAE
Garrulax pectoralis A1
Garrulax caerulatus A1
Garrulax canorus A1
Leiothrix lutea A1
ZOSTEROP1DAE
Zosterops japonicus A1
MIMIDAE
Mimus polyglottos AI
STURN1DAE
Sturnus vulgaris Vs
Acridotheres tristis A1
MOTA C1LL1DAE
Antbus hodgsoni Vs
Antbus cervinus Vs
Antbus rubescerts Vs
EMBER1Z1DAE
Tiaris olivacea An
Sicalis fiaveola An
Paroaria coronata A1
Paroaria capitata A1
Passerculus sandwichensis Vs
Plectrophenax nivalis Vs
CARD1NAL1DAE
Cardinalis cardinalis A1
1CTER1DAE
Sturnella neglecta A1
Quiscalus mexicanus Vs
FRINGILLIDAE
CARDUELINAE (subfamily)
Carpodacus mexicanus A1
Carduelis fiammea Vs
Serinus mozambicus An
Serinus canaria A1
DREPANIDINAE (subfamily)
PS1TT1ROSTR1N1 (tribe)
E- Telespiza cantans Re
E- Telespiza ultima Re
E-Psittirostra psittacea Re
Dysmorodrepanis munroi Rx
E-Loxioides bailleui Re
Rhodacanthis fiaviceps Rx
Rhodacanthis palmeri Rx
Chloridops kona Rx
E-Pseudonestor xanthoph3;s Re
HEM1GNATH1N1 (tribe)
Hemignathus virens
H. v. virens Re
H. v. wilsoni Re
Hemignathus fiavus Re
Hemignathus kauaiensis Re
10
TABLE 2. CONTINUED
STUDIES IN AVIAN BIOLOGY
NO. 22
Common name Scientific name Status
(Lesser 'Amakihi)--'Anianiau
(Green Solitaire)--Greater 'Amakihi
Lesser 'Akialoa
Greater 'Akialoa
{ Kaua'i 'Akialoa }--
{ O 'ahu 'Akialoa }--
{Lana'i 'Akialoa}--
Nukupu'u
{Kaua'i Nukupu'u}--
{O'ahu Nukupu'u }--
{Maui Nukupu'u }--
'Akiap61g'au
(Kaua'i Creeper)--'Akikiki
(Olive Green Creeper)--Hawai'i
Creeper
(O'ahu Creeper)--O'ahu 'Alauahio
(Moloka'i Creeper)--Kgkgwahie
(Maui Creeper)--Maui 'Alauahio
{ Maui 'Alauahio }--
{ Lana'i 'Alauahio }--
(Kaua'i kepa)--'Akeke'e
'kepa
{ O'ahu ',kepa }--
{Maui ',kepa }--
{ Hawai'i 'kepa }-
RED AND BLACK
HONEYCREEPERS
Ula-'ai-hawane
'I'iwi
Hawai'i Mamo
(Perkins Mamo)--Black Mamo
(Crested Honeycreeper)--'kohekohe
'Apapane
{Laysan Honeycreeper }-
{ 'Apapane }--
Po'ouli
OLD WORLD SPARROWS
(English Sparrow)--House Sparrow
WAXBILLS, MANNIKINS
Red-cheeked Cordonbleu
Lavender Waxbill
Orange-cheeked Waxbill
(Red-eared Waxbill)--Black-rumped
Waxbill
Common Waxbill
(Strawberry Finch, Red Munia)--Red
Avadavat
African Silverbill
(Ricebird, Spotted Munia)--Nutmeg
Mannikin
Tricolored Munia
Chestnut Munia
Java Sparrow
Hemignathus parvus Re
Hemignathus sagittirostris Rx
Hemignathus obscurus Rx
Hemignathus ellisianus
H. e. procerus Rx
H. e. ellisianus Rx
H. e. lanaiensis Rx
Hemignathus lucidus
E- H. l. hanapepe Re
H. I. lucidus Rx
E-H. 1. qffinis Re
E-Hemignathus munroi Re
Oreomystis bairdi Re
E-Oreomystis maria Re
E-Paroreomyza maculata Re
Paroreomyza fiammea Rx
Paroreomyza montana
P.m. newtoni Re
P.m. montana Rx
Loxops caeruleirostris Re
Loxops coccineus
L. c. wolstenholmei Rx
E-L. c. ochraceus Re
E-L. c. coccineus Re
DREPANIDINI (tribe)
Ciridops anna Rx
Vestiaria coccinea Re
Drepanis pac(fica Rx
Drepanis funerea Rx
E-Palmeria dolei Re
Himatione sanguinea
H. s. freethii Rx
H. s. sanguinea Re
E-Melamprosops phaeosoma Re
PASSERIDAE
Passer domesticux AI
ESTRILDIDAE
Uraeginthus bengalus An
Estrilda caerulescens An
Estrilda melpoda An
Estrilda troglodytes An
Estrilda astrild An
Amandava amandava A1
Lonchura cantans An
Lonchura punctulata A1
Lonchura malacca A1
Lonchura atricapilla An
Padda oryivora An
Note,: This table is modified from Robert Pyle's 1997 checklist of the birds of Hawaii. In all cases we have deferred to the American Ornithologist
Union's 1998 Checklist of North American birds and the 42nd Supplement to the Checklist (AOU 2000) for common and scientific names and
sequence of families and species, We have added macrons. diacritical marks, and glottal stops to all common names as indicated by Pyle (1997).
Subspecies of resident species known to occur in the islands are indicated in brackets. Common names in parentheses are those commonly used in
Hawai'i but not accepted by the AOU Check-list.
INTRODUCTIONsScott et al. 11
ly, The Nature Conservancy has pursued an ag-
gressive control program for alien species that
threaten the viability of native species popula-
tions and the ecological integrity of native Ha-
waiian ecosystems and established several large
biological reserves. While the Sierra Club, Na-
tive Plant Society, Hawaii Audubon Society, and
a number of state and federal agencies have all
taken actions on behalf of Hawai'i's native flora
and fauna, despite their efforts and extensive re-
search efforts in the last 25 years (Banko et al.
this volume, Steiner this volume), populations
and species of native birds continue to be lost.
Nonnative birds species comprise a large part of
the current avifauna (Table 2).
If there is to be any hope of retaining even a
majority of the currently endangered and threat-
ened native Hawaiian species, more aggressive
efforts are needed to seriously reduce agents
known to be detrimental to native species (Smith
1985, 1989; Cuddihy and Stone 1990, Stone
1989, Banko et al. this volume, Scott and van
Riper this volume). Despite widespread docu-
mentation of the impact of feral cats (Felis ca-
tus) on birds (Eberhard 1954, van Aarde 1978,
Jehl and Parkes 1982, Tomkins 1985, Churcher
and Lawton 1987, van Reusenburg and Bester
1988, Bloomer and Besler 1992, Seto and Co-
nant 1996, Athens 1997, Radunzel et al. 1997),
there are currently no cat control programs in
place for passerine species and only limited ef-
forts on behalf of seabirds (Hodges and Nagata
this volume). Likewise, while the impact of rats
(Rattus spp.) on Hawai'i's avifauna has yet to
be fully documented, Atkinson's (1977) corre-
lational study was suggestive, as was the extinc-
tion of five populations of native birds on Big
South Cape Island in New Zealand shortly after
the arrival of the roof rat (Rattus rattus; Atkin-
son 1985). Studies in New Zealand (Atkinson
and Bell 1973) and elsewhere have shown the
strong positive response of native species when
nonnative rats are eliminated (Radunzel et al.
1997). In spite of this evidence, predator control
programs are rare and are not being implement-
ed over areas large enough to elicit a population
response by native species. The elimination of
rats from Midway Island is an exception (R.
Shallenberger, pers. comm.).
In the absence of management activities to
control or eliminate known causes of mortality
to Hawaiian avifauna over areas comparable to
the size of the distributional area of the threats,
individuals will die, populations will be lost, and
species will continue to go extinct. For some
threats (e.g., predators, ungulates), known con-
trol techniques (e.g., Taylor and Katahira 1988,
Katahira et al. 1993) only need be applied at a
scale that is meaningful (the distributional area
of a population or species). For others, such as
avian malaria and avian pox, new techniques
such as genetic engineering of disease resistant
birds and introduction of sterile male mosquitoes
must be developed and applied.
A first step to buy time and simultaneously to
restore populations of other endemic Hawaiian
species (plants and invertebrates) would be to
restore the composition and structure of higher
elevation xeric and mesic forest habitats on
Maui and Hawai'i by eliminating alien animals
and plants (e.g., rats, cats, ungulates, and foun-
tain grass) from these areas. These recovered
and restored habitats would act as refugia from
avian diseases so prevalent at lower elevations.
The idea for this book came during informal
discussions at the 67 th annual meeting of the
Cooper Ornithological Society in Hilo, Hawai'i,
in April 1997. During that meeting there were
47 presentations on natural history, ecology and
taxonomy of Hawaiian birds. We invited select-
ed authors of those presentations to submit
manuscripts for consideration in a peer reviewed
book on the birds of HawaiT To fill gaps in
topics covered we solicited eight additional
manuscripts. There was a high degree of redun-
dancy in references cited among authors. Be-
cause of this we chose to create a combined lit-
erature cited.
Common and scientific names of birds follow
the 7 th edition of the American Ornithologists
Union Check-list (AOU 1998). Quentin Tom-
ich's Mammals in Hawaii (Tomich 1986) was
our reference for mammal names. For flowering
plants we relied on Manual of the Flowering
Plants of Hawai'i (Wagner et al. 1990 a,b).
"Pronunciation of Hawaiian names is aided by
the use of a reversed apostrophe ('), to indicate
the glottal stop, a stopping of sound, as between
the vowell sounds in oh-oh in English; and by
macrons over vowels--a, , , o, fi--which de-
note long stress. An asterisk preceding a place
name indicates that pronunciation is uncertain"
(Armstrong 1983:231). The orthography follows
the revised and enlarged Hawaiian Dictionary
(Pukui and Elbert 1986). For place names we
followed the revised and enlarged Place Names
of Hawaii (Pukui et al. 1976). When names
could not be located there the spelling in the
Atlas of Hawaii (Armstrong 1983) was followed.
This monograph includes 35 papers, most of
which were presented at the 67 th meeting of the
Cooper Ornithological Society in Hilo, Hawai'i,
in April 1997. Each paper has been peer re-
viewed by the editors and at least one outside
reviewer. We have grouped the 35 chapters in
12 STUDIES IN AVIAN BIOLOGY NO. 22
this book into six sections, each introduced with
a historical review. Taken together, they report
on the state of our knowledge concerning the
Hawaiian avifauna at the end of the 20 th century.
Hopefully, this synthesis volume will assist in
some small way to help preserve the unique avi-
fauna of Hawai'i and the Pacific islands so that
future generations will be able to observe and
hear some of the incredible sights and sounds
that we have been privileged to experience dur-
ing our short 'tour of duty' researching one of
the most unique avifaunas on this planet.
ACKNOWLEDGMENTS
We thank Robert Pyle for permission to use a mod-
ified version of his Check-List of Hawaiian Birds and
for his comments on drafts of Table 2. Sue McMurray
tracked manuscripts and correspondence to author's
queries. Sue McMurray and Andrea Reese completed
the onerous task of combining references from indi-
vidual papers into a single combined Literature Cited.
Steve Mosher found a second home in the library as
he checked references against the original publications.
Lenny Freed was instrumental in launching the idea
for publishing manuscripts from the Hilo meeting of
the Cooper Ornithological Society as an integrated
monograph in STUDIES 1N AVlAN BIOLOGY and provided
valuable comments on manuscripts. Melissa Madsen
read all manuscripts for grammar and adherence to
STUDIES 1N AVlAN BIOLOGY format, consistency with
place names of Hawa'i, and correct usage of glottal
stops, macrons, and diacritical marks in the spelling of
Hawaiian words. Kathy Merk's unfailing commitment
to completing this book was a huge morale booster;
she tracked manuscripts, corresponded with authors,
and made edits on manuscripts as needed. John Roten-
berry was the epitome of what a professional editor
should be; his insightful comments, rigorous attention
to detail, and manner of conveying need for change
made him a pleasure to work with. H. Douglas Pratt
graciously provided a painting of the Hawai'i '0'8 for
the frontespiece of this book, as well as the line draw-
ings that precede each section. We thank Patrick Ching
for the numerous drawings of native Hawaiian birds
scattered throughout the text. Jack Jeffrey kindly pro-
vided the photograph of an 'Anianiau feeding on a
kanawao that graces the cover. Funds for publication
of this book and administrative support were provided
by the U.S. Geological Survey, Idaho Cooperative Fish
and Wildlife Research Unit, and the Department of
Fish and Wildlife, University of Idaho, Moscow, Ida-
ho. To all these individuals a special mahalo nui loa
(deep thanks) for all that you have done.
Historical Perspectives
Studies in Avian Biology No. 22:14, 2001.
HISTORICAL PERSPECTIVES--INTRODUCTION
CHARLES VAN RIPER, III, SHEILA CONANT, AND J. MICHAEL SCOTT
The record of Hawai'i's avifauna is one of
change; a change that is reflected in steadily di-
minishing numbers of species and abundance
(Pratt 1994). Our historical perspectives provide
insights into how many species there were and
some documentation of their distribution, but
only minor insights into their abundance, with
size, shape, and bill forms allowing vague in-
ferences concerning niches occupied and re-
sources exploited. Nothing is known of clutch
sizes, population characteristics, or ecological
interactions of extinct species. For these reasons,
more than 50% of Hawai'i's bird species will
always be a ghost avifauna.
The history of ornithological exploration in
Hawai'i is a legacy of missed opportunities, with
the first extensive surveys of the avifauna com-
ing 100 years after the discovery of the islands
by Europeans in 1778 (Olson and James 1994a).
Historically, recorded species are but a small
fraction of what occurred in the islands prior to
European colonization. Some species were sim-
ply overlooked; the Po'ouli (Melarnprosops
phaeosorna) was not discovered until 1972 (Cas-
ey and Jacobi 1974). Olson and James (1991,
James and Olson 1991) nearly doubled the
known number of endemic species based on
their descriptions of new species from fossil and
subfossil remains. New discoveries of fossil spe-
cies continue today.
In the first chapter of this volume, Curnutt and
Pimm estimate that the Pacific avifauna was
composed of nearly 1,500 species, of which ap-
proximately 240 survive. For example, they es-
timate that there were 12 species of rails endem-
ic to the Hawaiian Islands, versus the 7 currently
described (Olson and James 1991; Table 2). In
the second chapter, Michael Moulton and his co-
authors document the introduction of 140 spe-
cies in 14 different orders and ask, "Why do
some introduced species succeed and others
fail?"
14
Studies in Avian Biology No. 22:15-30, 2001.
HOW MANY BIRD SPECIES IN HAWAI'I AND THE CENTRAL
PACIFIC BEFORE FIRST CONTACT?
JOHN CURNUTT AND STUART PIMM
Abstract. Since European settlement, extinctions of Pacific island birds have been widespread and
well documented. Subfossil evidence indicates that the Polynesians caused extinctions of an even
greater magnitude. Estimating the prehuman Pacific avifauna is difficult because the existing fossil
record is inevitably incomplete. We use the theoretical framework of island biogeography to make
estimates of the numbers of endemic rails, parrots, pigeons and doves that existed in the Pacific before
human contact. We formulate two sets of estimates for each taxon by assuming that: (1) endemism is
defined as a distribution limited to a single island, and (2) endemism is a distribution limited to a
single-island group. These two assumptions lead to different results (884 compared with 242 endemic
species). We refine our predictions by applying topographical and disturbance parameters. Our best
estimate is that 332 endemic species of the three taxa once existed in the Pacific, of which 210 are
not accounted for in the paleontological and historical data. Applying this ratio of known to missing
species for all landbirds, we estimate the original Pacific avifauna to be composed of less than 1,500
species, of which approximately 230 survive. Our estimate of the original Pacific avifauna falls be-
tween two earlier conflicting predictions (800 and much greater than 2,000). Our predictions of the
number of species missing on each type of island are testable. Our results can be used to focus research
efforts on islands that are more likely to have held species of interest. Furthermore, our results can
be interpreted to predict the risk of future extinctions that may result from habitat loss or rising sea
levels.
Key Words: biogeography; doves; extinctions; Pacific Islands; parrots; pigeons; rails; sea level; tsu-
namis.
The Hawaiian Islands form one of the largest
and most diverse archipelagoes in the Pacific. As
a group, they lead the world in numbers of his-
torically extinct and currently endangered spe-
cies of birds (King 1985). This dismal legacy,
however, did not befall the Hawaiian Islands
alone. Untold bird extinctions doubtlessly oc-
curred across the Pacific over the four millennia
since humans first set sail there. What was the
magnitude of the loss of bird species in the Pa-
cific?
"The Pacific" denies an easy definition. De-
fined in the context of human settlement over
the last 4,000 years, we will consider 41 island
groups (Fig. 1). They span the Hawaiian Islands
in the northeast, west to the Marianas and Palau,
southwest through Vanuatu, south to New Zea-
land and east to Easter Island. Pratt et al.'s
(1987) field guide covers all but Vanuata (for
which see Bregulla 1992), New Zealand (see
Falla et al. 1983), and Easter (which has no ex-
tant landbirds).
There are roughly 240 extant native species
of landbirds in this region (Falla et al. 1983,
Pratt et al. 1987, Bregulla 1992). The largest
families are Pachycephalidae (whistlers; 40
spp.), Columbidae (pigeons and doves; 34 spp.),
Muscicapidae (Old World flycatchers; 28 spp.),
Rallidae (rails; 21 spp.), Psittacidae (parrots; 19
spp.), and Fringillidae (Hawaiian honeycreepers;
19 spp.).
To the above number of species we must add
those that we know once existed but are now
known only through historical records and fos-
sils. Among the islands of the Pacific, the many
vertebrate extinctions that occurred since the
sixteenth century subsequent to the arrival of
European explorers are well documented. For
example, Diamond (1984) reported that, since
1600, Micronesia and Polynesia suffered rough-
ly 100 bird species extinctions. The forces re-
sponsible for the loss of these species were the
same as those that operate today, primarily hab-
itat loss and the introduction of exotic species
(Steadman 1997a,b). A much greater extinction
event preceded the arrival of Europeans and was
concurrent with the first human contact (Stead-
man 1997a,b). Beginning about 4,000 years ago
with Melanesia and Micronesia and ending
about 1,500 years ago with Hawai'i, Easter Is-
land, and New Zealand, humanity brought the
last habitable places on Earth under its domain
(Rouse 1986).
European explorers found well-developed, ag-
ricultural-based societies on all of the larger Pa-
cific islands. It is not known how many of the
smaller, less suitable islands were visited only
temporarily by the wandering islanders (Oliver
1961). Habitat loss and exotic species (including
dogs and pigs) doubtlessly caused the extinction
of many species of endemic birds on the per-
manently settled islands. Even on smaller unin-
habited islands endemic species, many of them
flightless rails that had evolved in the absence
15
16 STUDIES IN AVIAN BIOLOGY NO. 22
14.
"24
2O
FIGURE 1.
x,6o '
The islands of the Pacific. Numbers refer to
34 ß
tie,
40'
island groups referred to in the text and listed in Table 1.
of terrestrial predators, could have been har-
vested to extinction by temporary human occu-
pants.
We have evidence of these unrecorded extinc-
tion events in the fossil record (Olson and James
1982a, 1991; Milberg and Tyrberg 1993). Ar-
cheological efforts in Hawai'i by Olson and
James (1982a, 1991; James and Olson 1991) and
throughout the rest of the Pacific (Balouet and
Olson 1987; Steadman 1991, 1992, 1993,
1997a,b; Kirch et al. 1995), have uncovered a
large number of avian fossils that were depos-
ited concurrently with early human occupation
of the islands. Not all islands have been
searched, and even if they were, it is unlikely
that all extinct species would be found. Thus,
the total number of extant and extinct species
identified to date is an underestimate of the di-
versity of the prehuman Pacific avifauna.
An exact count of the number of landbird spe-
cies known only as fossils is difficult to tally
because they are not clearly enumerated in some
published accounts. The Hawaiian Islands held
62 fossil species (James and Olson 1991, Olson
and James 1991) and New Zealand held 44 spe-
cies (Steadman 1995). The other islands of the
Pacific that have been searched held something
less than 100 additional species (Steadman
1995). Thus, roughly 200 species of Pacific
landbirds are known only from the fossil record.
Summing the number of extant, historically
extinct, and prehistorically extinct (fossil) spe-
cies, there are 540 known species of landbirds
in the Pacific. This number is too low because
the fossil record is incomplete. An accurate es-
timate of the prehuman Pacific avifauna depends
on an accurate estimate of the "missing" fossil
species.
Pimm et al. (1994) estimated the prehuman
number of Pacific island landbirds by applying
sampling analyses to fossil data. Briefly, given
the number of species known only by fossils,
those known by modern observations (i.e., those
that still survive and those extinct since Euro-
pean colonization), and those known by both
fossils and modern observations one can deduce
the number of "missing" species from an island.
Applying this method to data on the landbirds
HOW MANY BIRD SPECIES--Curnutt and Pimm 17
of the tropical Pacific (including New Caledo-
nia), Pimm et al. (1994) deduced that the num-
ber of known fossil species (ca. 200) is only half
of the actual number of species that disappeared
before European colonization. Pimm et al.
(1994) estimated the original avifauna to include
nearly 800 species of landbirds. Excluding data
from New Caledonia and including data l¾om
New Zealand, to fit the boundaries to the current
study, does not appreciably change these esti-
mates.
A much higher estimate of the original Pacific
avifauna was proposed by Steadman (1995,
1997). On finding fossil evidence of up to three
or four now extinct species of flightless rails on
islands he investigated, Steadman (1995,
1997a,b) suggested that the 800 major islands of
the Pacific held more than 2,000 species of this
taxon and lower numbers of other taxa--all
driven to extinction as a result of first human
contact. Steadman's (1995) approach set the
question of original avifauna in the context of
island biogeography.
In this paper we apply a robust theoretical
framework, island biogeography theory (Mac-
Arthur and Wilson 1967a), to the Pacific islands
to determine the number of islands that could
have held endemic species of rails (Rallidae),
pigeons and doves (Columbiformes), and parrots
(Psittaciformes). We chose these taxa because
they are well represented in the fossil record.
Thus, we do not estimate the entire prehuman
landbird fauna; instead our results can indicate
the magnitude of the loss of bird diversity that
has occurred since first human contact. We in-
clude in our analyses all named islands of New
Zealand, Micronesia, central and eastern Mela-
nesia, and Polynesia that experienced first hu-
man contact no earlier than 4,000 years before
present (Rouse 1986). Unlike Steadman (1995,
1997), we incorporate data on habitat diversity,
changing sea levels during the Holocene, and
tsunamis. Each of these factors influences the
effective size of islands for landbirds. Put sim-
ply, MacArthur and Wilson's (1967a) theory of
island biogeography predicts more species on
larger islands and those close to a source of im-
migrants, and fewer species on small or isolated
islands. We perform two distance analyses: dis-
tance-from-source, as proposed by MacArthur
and Wilson (1967a); and, distance between is-
lands--isolated islands are more likely to pro-
duce species endemic to one island than those
that have very near neighbors (Mayr 1963). By
applying reasonable assumptions to this ques-
tion, we hope to develop a more accurate esti-
mate of the prehuman Pacific avifauna than has
been produced to date.
We first identify those islands of the Pacific
that have the potential to maintain populations
of landbirds. We then extrapolate the numbers
of endemic rails, pigeons, and parrots that could
have existed on all of these islands by applying
the known maximum of each taxon recorded on
different island sizes and types. In lhct, we cal-
culate two estimates of the number of endemic
species by using two definitions of endemism.
We then refine our estimates by considering eco-
logical and environmental characteristics.
IDENTIFYING THE BIRD ISLANDS
We do not expect all islands of the Pacific to
hold birds. Some islands are too small to support
viable populations of landbirds. Some islands
may also fall outside of the known range of the
taxa we are investigating. These limitations to
bird distribution are diagrammed in Figure 2 Our
first task, then, is to estimate how many islands
there are in the Pacific, and which of these could
support a population of landbirds.
How MANY ISLANDS
No one knows how many islands there are in
the Pacific Ocean. Estimates range from 30,000
to less than half of that number (Bryan 1963).
The distribution of island sizes is fractal--that
is, as one looks at the Pacific at finer scales, one
finds more islands in a characteristic way. Thus,
most islands are very small. We limited our data
to named islands. We obtained gazetteer data
(latitude, longitude, name) from the U.S. De-
fense Mapping Agency's (DMA) database avail-
able on the internet. This search yielded 3,463
islands.
We assigned each island to an island group
according to an arbitrary grouping scheme. Ob-
vious archipelagos were identified as groups
(e.g., the Gilbert Islands), as were single islands
not obviously associated with an archipelago
(e.g., Rapa). The result was 41 island groups
(Table 1; Fig. 1). As described below, we first
grouped islands that are very close to each other.
Our primary reason for this was to add small
islets to the larger islands that they surround and
to unite many "islands" that occur as parts of
individual atolls. Second, we determined which
islands are too far from a source of immigrants
for each taxon. Finally, we determined the size
and topography of each island.
ISLANDS AND ISLETS
If two islands were near enough to each other
to allow a species to move between them, then
neither would produce an endemic species
(Ricklefs and Schluter 1993). But how close is
close enough? No data exist on this subject for
birds in the Pacific. We know that the limiting
distances between islands are surely taxon spe-
18 STUDIES IN AVIAN BIOLOGY NO. 22
Species' distribution limit
Region of possible endemism
Lack of isolation
Island size
FIGURE 2. Theoretical framework for endemism of Pacific island birds. Islands that are too small to maintain
persistent populations will not produce endemic species (lower size limit), nor will larger islands subject to
inhibitory disturbance regimes (effective lower size limit). Some islands are close enough to allow genetic
exchange between populations and will not produce endemic species (lack of isolation), while others lay outside
of the distribution of some taxa (species' distribution limit).
cific and this, in turn, is affected by the mode
and propensity of movement exhibited by each
taxon. For the three taxa we consider in this pa-
per, rails have a higher wing load (ratio of
weight to wing area) than pigeons or parrots
(Raynet 1988). Thus, it would take relatively
more energy for a rail to fly a fixed distance than
it would a pigeon. Left free to speculate, we
chose a minimum distance equivalent to 0.1 ø of
latitude or longitude ( 11 km at the equator) as
sufficient for allowing isolation of breeding pop-
ulations. We chose this distance primarily for
ease of calculation, but also we feel that such a
distance would provide an adequate barrier to
movement for rails--the most stationary taxon
because of its propensity to quickly evolve to-
ward flightlessness (Trewick 1997).
We summed the sizes of all islands that were
closer than 0.1 ø of latitude or longitude to each
other. This grouping scheme reduced our data to
788 island sets. Hereafter, we refer to island sets
as "islands."
WHICH ISLANDS ARE TOO FAR
Landbirds are not distributed evenly across is-
lands. Just as islands that are too close will pro-
hibit divergence; islands that are too distant from
a source population may not be colonized at a
rate sufficient to allow persistence (Ricklefs and
Schluter 1993).
We tested for the effect of distance-from-
source on the distribution of each of our three
taxa with multiple regressions. All of the taxa
we consider in this paper have their origins in
the Old World (rails: Ripley 1977; pigeons:
Goodwin 1983; parrots: Forshaw 1977). We
used Map © (Apple Computers, Inc.) software to
determine distances between geographic centers
of island groups and the following (geologically)
continental source areas: Australia (Brisbane),
Papau New Guinea (New Britain), Philippines
(Manila), and Taiwan (Taipei). Since island size
is the most effective predictor of species diver-
sity (MacArthur and Wilson 1967a), we per-
formed stepwise multiple linear regression of the
number of species on total area of each island
group, then added distance. We repeated this
process for each of the distances generated from
the four sources listed above.
At best, these multiple regressions only weak-
ly explained the variation in species numbers
with distance (R < 0.2) and were only signifi-
cant for parrots and pigeons (P < 0.05). For this
analysis, it is better for the data to speak for
themselves. Figure 3 shows the distribution of
rails, parrots and pigeons among the 41 island
groups of the Pacific. Rails arc found throughout
the region, reaching the most remote groups in-
cluding Hawai'i and Easter Island. Paradoxical-
ly, rails, for which even the largest ocean is not
HOW MANY BIRD SPECIES--Curnutt and Pimm 19
TABLE 1. ISLAND GROUPS OF THE PACIFIC OCEAN IN-
CLUDED IN OUR ANALYSES
No. of
Group island Topogra-
Group number sets Area (km 2) phy
Melanesia
Vanuatu 1 38 11,400 H
Fiji Islands 2 74 1,860 H
Micronesia
Palau 3 8 447 H
Yap 4 2 175 H
Chuuk 5 21 230 L
Mariana Islands 6 13 910 H
Pohnpei 7 2 360 H
Kosrae 8 1 100 H
Marshall Islands 9 28 255 L
Gilbert Islands 10 18 290 L
Nauru 11 2 36 L
Polynesia
NW Hawai'i 12 2 8 L
Hawai'i 13 9 16,700 H
Wake 14 1 230 L
Johnson Atoll 15 1 2 L
Howland 16 1 10 L
North Line Islands 17 7 745 L
Phoenix 18 5 37 L
Tuvalu 19 6 27 L
Rotuma 20 1 49 H
Wallis and Futuna 21 2 275 H
Samoa 22 8 3,500 H
Tokelau Islands 23 3 13 L
North Cook Islands 24 5 10 L
Tonga Islands 25 18 563 H
Niue 26 1 258 L
South Cook Islands 27 9 234 H
South Line Islands 28 2 8 L
Marquesas Islands 29 11 1,062 H
Society Islands 30 10 1,710 H
Tuamotu Arch. 31 11 248 L
Gambier 32 6 21 L
Pitcairn Islands 33 2 8.5 H
Rapa 34 1 40 H
Tabuai Islands 35 4 120 H
Easter Island 41 1 170 H
Kermadec Islands 36 2 34 H
Norfolk 37 1 37 H
Lord Howe 38 1 10 L
New Zealand 39 33 267,800 H
Chatham Islands 40 4 1,085 H
"Group Number" refers to numbers shown on Figure 1. Island sets are
named Islands that are within 0.1 ø latitude and longitude of each other.
We include only those sets with combined areas of >150 HA. Topogra-
phy is either high relief (H) or low-relief (L).
large enough to prohibit colonization, can quick-
ly evolve to flightlessness (Diamond 1991). The
distribution of pigeons has apparently been lim-
ited by the vast expanses of ocean that isolate
Hawai'i and Easter Island, for neither has ap-
parently held this taxon. For Easter Island, the
nearest island to have ever held a pigeon is Pit-
cairn (1,600 km), and for Hawai'i, it is the North
Cook Islands (3,500 km). Parrots have been
found on Easter but not the Hawaiian Islands
(nearest island with parrots-Marquesas, 3,800
km distant).
For our analyses, therefore, we consider all
islands of suitable size as potential sites for rail
colonization; all but the Hawaiian and North-
west Hawaiian Islands for parrots; and, all but
the Hawaiian groups and Easter Island for pi-
geons.
SIZES OF ISLANDS
The final parameters we consider in determin-
ing which island sets could maintain populations
of landbirds are size and topography. We ob-
tained data on the sizes of islands from various
sources in the literature and from direct mea-
surements from maps (ranging in scale from 1:
10,000 to 1:300,000). Some islands listed in the
DMA database were not found on maps (or re-
ferred to in any literature we searched), thus, we
have no data on their sizes. However, we are
confident that we have size estimates for all of
the major islands (i.e., > 2 km 2) and for many
lesser islands, and those with missing data are
from the smallest size classes. Our confidence
lies in the fact that island sizes fall within a class
of negative exponential distributions known as
Zipf-Mandelbrot (Fairthorne 1969). For the is-
lands for which we have data, we plotted the
size distributions on log-log axes. The Zipf-
Mandelbrot distribution predicts a straight line
for this graph (Fig. 4), and we can interpret de-
viations from the linear fit as "missing" islands.
By extending the linear fit below 1 km 2 to our
smallest recorded island size (10 ha), we predict
that about 800 islands are missing from our is-
land size data set.
While landbirds do occur on very small is-
lands in the Pacific, these are members of sat-
ellite populations of larger nearby islands. For
example, the Antipodes Island Parakeet (Cy-
anoramphus unicolor) is found in low numbers
on Archway Island (6 ha)--the smallest of the
Antipodes Islands (Taylor 1985). The species is
also found on the 54-ha Bollons Island, which
is much less than 1 km from Archway Island.
The greatest part of this species' population,
however, is on the 20 km 2 Antipodes Island--
about 1 km from Bollohs. The loss of the An-
tipodes Island population would probably lead
to the eventual extinction of this species. It
would not make ecological sense to identify
Archway Island as one suitable for sustaining a
population of parrots. Similarly, we can safely
ignore the existence of the 800 "missing" is-
lands in our data because they are too small to
hold endemic species of landbirds.
The smallest Pacific island known to hold an
endemic rail is Wake Island, 6.5 km 2 and home
20 STUDIES IN AVEAN BIOLOGY NO. 22
'R
' R,P,D ' RD'
.p
. R,P
% R,P,D
;tO'
40'
FIGURE 3. The distribution of rails (R), parrots (P), and pigeons and doves (D) among the Pacific islands.
Numbers correspond to group names in Table 1 and indicate island groups that hold none of the three taxa
mentioned above.
to Rallus wakensis. The smallest island to hold
an endemic pigeon is 28 km 2 Maketea (Tuamotu
Archipelago), home to Ptilinopus chalcurus; and
the smallest island to hold an endemic parrot is
Norfolk Island (33.7 km 2) where remains of
Nestor produetus have been recovered.
These minima may not be actual; all islands
have not been sampled. We performed a Monte
Carlo simulation (Efron and Tibshirani 1993) to
predict the minimum size of an island that
should support an endemic species from the ob-
served distribution of island sizes with endemic
species. Using data on island sizes, we randomly
selected a number of islands equivalent to the
number that we knew held endemic species of
each taxon. For example, 23 islands held at least
one endemic species of rail. We randomly se-
lected 23 islands from the entire set of 834 and
recorded the minimum size of this subset. We
then calculated the mean minimum value of 100
repetitions. By repeating this process with in-
creasing cutoff values applied to the entire data
set, we determined the lower 95% confidence
limit within which our known minimum island
size fell (Fig. 5).
Some islands have held more than one en-
demic species of a taxon. For parrots and pi-
geons there were one and two islands, respec-
tively. For these taxa we could not perform the
above described simulation to determine the
minimum island sizes for two or more species--
the sample size is too small. For rails, however,
of which 10 islands held more than one endemic
species, we could estimate the minimum island
size for two species by applying the simulation
(with a sample size of 10). To determine which
islands could have held more than two species
of rail (or more than one species of parrot or
pigeon), we assumed that the smallest island for
which we had data was the actual minimum.
TYPES OF ISLANDS
Our measure of habitat diversity was very
coarse. We described islands as "high-relief" or
HOW MANY BIRD SPECIES--Curnutt and Pimm 21
0.5-
0
i 4 5 6
Log Size (ha)
FIGURE 4. The relationship between island sizes
and their frequency. The linear fit was calculated after
excluding the two smallest size classes (open circles)
and the three largest size classes (not shown). The area
within the triangle represents islands with size data
missing from our data set, assuming island sizes ex-
hibit a Zipf-Mandelbrot distribution.
"low-relief." High-relief islands were those de-
scribed in the literature as volcanic, hilly, or
mountainous or whose representation on maps
included hachures. Low-relief islands were all of
those described as atolls or were lacking ha-
chures on maps that normally include such data.
High-relief islands are rich in habitat diversity
compared to low-relief islands (Adler 1992). We
apply the same topography to entire groups by
summing the areas of all islands within groups
and defining them as high relief if > 50% of the
total area is attributed to high-relief islands.
EXTRAPOLATING ENDEMICS
To estimate the potential number of endemic
species that each taxon held, we determined the
known maximum number of endemics (living
and fossil) on islands of different sizes and to-
pographies throughout the Pacific. After esti-
mating the size of the smallest islands which we
would expect to find endemics on, we used these
numbers to predict the maximum numbers of en-
demic species with reference to the distribution
of island sizes and topographies within each is-
land group (Fig. 6). We tallied the number of
known endemics and the number of predicted
endemics across taxa for each island group then
5000-
4500
4000
3500
3000
2500
2000
15002
1000
500.
0;
....... o Pigeons (B)
........ ,.- ........ Rails (C)
........ ........ Parrots (A)
Predicted Minimum size (ha)
FIGURE 5. Results of a simulation whereby we randomly selected a number of islands equivalent to the
number occupied by endemic species of each taxon. The x-axis represents the lowest value in the data set for
each simulation, the y-axis is the 95% lower confidence limit of the mean of 100 repetitions. A, B, and C
represent the actual minimum sizes for parrots, pigeons, and rails, respectively. The vertical lines intercept the
x-axis at the smallest island size we would expect to find endemics of the respective species.
22 STUDIES IN AVIAN BIOLOGY NO. 22
-4
ß Low-relief islands
[] High-relief islands / (12) - 3
)8) - 2
J (1) .................................. (1) J (4) (4,) 1
Log Size (ha)
FIGURE 6. The size distribution of islands of the Hawai'i group classified as high relief and low relief. The
solid line indicates the maximum number of endemic rails found on all high-relief islands in the Pacific while
the dashed line indicates maxima for low-relief islands. We multiplied the maxima for each size class by the
number of islands in each size class to predict the number of endemic rails that could have existed in each
island group. Numbers in parentheses indicate the number of rails expected for each island size X the number
of islands.
calculated the proportion of missing endemic
species.
Our use of maxima reflects the potential lack
of fossil data on some islands. For example,
well-searched Mangaia of the South Cook Is-
lands group held four endemic rails. Tofua of the
Tonga Islands, with a similar size and topogra-
phy, revealed none. For our estimates we assume
that Tofua held four endemic rails. This may be
incorrect; to paraphrase Montaigne, speciation is
not so often the result of great design as of
chance. There may never have been endemic
rails on Tofua simply because no rails have sur-
vived there long enough to speciate.
Since the true number of prehistoric endemics
cannot be known, we must be content with es-
timating this number by setting realistic limits
based on the available data. Of the four factors
we consider as aftkcting endemism, we have
data on absolute lower island size and distance
from source. Data do not exist for two other fac-
tors-eftkctive lower island size (disturbance ef-
fects) and the minimum distance between is-
lands needed to produce endemism (dispersal ef-
fects). Thus, we are left with the familiar quan-
dary of decreasing our certainty as we increase
the number of parameters. We address the prob-
lem of prehistoric disturbance on a group by
group basis later. Our approach to effective dis-
tance between islands is as follows.
As noted earlier, we grouped all islands 11 km
or closer to each other into sets. While an 11
km expanse of ocean may prohibit the move-
ment of a flightless rail, it may have less effect
on a strong-flying pigeon. We could further
group our islands by diftkrent distances for each
taxon, but this would be a series of educated
guesses at best. Instead, we approach this prob-
lem by determining the maximum number of en-
demics that we know to occur in each island
group. For example, the Red-bellied Fruit Dove
(Ptilinopus greyii) is found on 28 islands of the
Vanuatu group (total area of 11,000 km2). Thus,
it does not fit our definition of a single-island
endemic. It is, however, found only in the Va-
nuatu group, so it does exhibit a form of endem-
ism. In Vanuatu, this species is found on both
low- and high-relief islands. We conclude then
that any island group that is dominated by high-
relief islands and has a combined area the size
of the Vanuatu group would hold an endemic
pigeon.
We, therefore, produce two estimates for each
taxon--the number of endemics at single islands
and the number of endemics at island groups.
The true number of endemic rails, pigeons, and
parrots that have existed in the Pacific probably
falls somewhere between these two values.
THE BIRDS
We chose rails, parrots, and pigeons for our
analyses because they are well represented in the
fossil record. We reviewed all available litera-
ture on the distribution of extant, historically ex-
HOW MANY BIRD SPECIES--Curnutt and Pimm 23
TABLE 2. AN ESTIMATE OF THE NUMBER OF RAIL SPE-
CIES 1N THE PACIFIC BEFORE HUMAN COLONIZATION
Num- Predict-
bet of cd total
Number spe- number
of is cies/is- of spe-
Island size and topography lands land cies
<600 ha, high and low relief 578 0 0
600-1000 ha, high and low relief 44 1 44
<1000 ha, low relief 61 I 61
1000-6400 ha, high relief 86 2 172
<6400 ha, high relief 65 4 260
Total 834 537
Maximum numbers of species are gleaned from the data for each size/
topography of island. The predicted number of species is the product of
maxima and the number of islands.
tinct, and subfossil species of these taxa in the
Pacific. We assigned each species to all islands
on which it was known to occur.
RAILS
Single-island endemics
We catalogued 55 species of rails known to
have occurred in the Pacific. Of these, only five
(all extant) are not restricted to either single-is-
land sets or single-island groups. Two-thirds of
the species are known only from fossil data and
65% are endemic to one island. Endemic rails
are found on only 13 of the 41 island groups
The results of our simulation show that the
smallest island with an endemic rail (6.5 km 2)
falls within a distribution that has a lower 95%
confidence limit of 6 km 2. Both high- and low-
relief islands have held single endemic species
of rails, thus, we expect that all 256 islands that
are larger than 6 km 2 held at least one species.
Ten islands, all high relief, held more than one
endemic species. The smallest of these was Lord
Howe Island (10 km2), which held two species,
followed by Mangaia (64 kin2), which held four.
Since four species of endemic rails is the max-
imum we encountered, we apply this value to all
larger islands. Table 2 and Figure 6 illustrate our
method of prediction of the number of rail spe-
cies for the entire Pacific and specifically for the
Hawaiian Island group.
We performed the same analysis on each is-
land group and estimated that approximately 537
endemic rail species existed in the Pacific, of
which 482 are not accounted for by a living or
fossil species. Over one-third (36%) of the miss-
ing endemics are attributed to only two
groups--Vanuatu (94) and Fiji (86). Whereas 13
groups hold no endemics nor are expected to, 14
others hold none but should. Of the remaining
13 groups, 11 hold fewer endemics than ex-
pected, and two (Wake Island and Lord Howe
Island) hold the number of endemics we predict
(one and two, respectively).
Island-group endemics
Eleven of the 55 species of rails in the Pacific
are endemic to groups of islands. The occur-
rence of the Wake Island Rail (Rallus wakensis)
on Wake Island, an island group in itself, insures
the expectation of at least one endemic rail on
all low-relief groups except Johnston Atoll,
which is too small. For groups with high-relief
islands, the maximum number of endemics rang-
es from two for groups as small as 10 km 2 (Lord
Howe) to 12 for groups larger than 16,700 km 2
(Hawai'i). Summing over all groups, we expect
143 endemic rails in the Pacific based on our
island group analysis.
PARROTS
Single-island endemics
Of the 24 species of parrots we catalogued, 9
are endemic to single islands. The majority of
these (5) are found in the southwest Pacific. No
low-relief islands hold endemic parrots. Norfolk
Island (33.7 km 2) represents the smallest island
to hold an endemic parrot (Nestor produetus).
We estimated that the lower size limit of islands
that would support endemic parrots is 28.5 km 2.
Excluding the Hawaiian islands and Easter Is-
land, there are 110 high-relief islands of 28.5
km 2 or greater. The only island with more than
one species of endemic parrot is the largest in
our data set--South Island, New Zealand
(149,000 km2). Thus, we attribute three species
to this island only, for a total of 94 species ([91
islands * 1 species] + [1 island * 3 species]).
Island-group endemics
In contrast to the rails, a large proportion of
parrot species (30%) in the Pacific show endem-
ism to single groups of islands. The smallest
group to hold an endemic is Norfolk (34 km2),
home to Nestor produetus. We apply this value
of one endemic to 18 of the 22 island groups
that contain high-relief islands. We predicted
two endemic parrot species to Vanuatu and Fiji.
New Zealand held four endemics. The total
number of endemic parrots we expect from our
analyses of island groups is a mere 29 species.
PIGEONS AND DOVES
Single-island endemics
We catalogued 43 species of pigeons and
doves in the Pacific. Only nine of these are en-
demic to single islands. Of these, five are known
only from fossil remains and are identified only
to genus. Huahine of the Society Islands held
the highest number of endemics with three of
24 STUDIES IN AVIAN BIOLOGY NO. 22
the unknown species (Ducula sp., Gallicolumba
sp., and Ptilinopus sp.). Henderson Island of the
Pitcairn group held two endemics--the extant
Henderson Island Fruit Dove (Ptilinopus insu-
laris) and a fossil Gallicolumba sp. The remain-
ing four endemics were found on Rapa (Rapa
Fruit Dove, Ptilinopus huttoni), Mangaia of the
South Cook Islands (Gallicolumba sp.), Makatea
of the Tuamotu Archipelago (Makatea Fruit
Dove, Ptilinopus chalcurus), and Espiritu Santo
of the Vanuatu group (Santa Cruz Ground Dove,
Gallicolumba sanctaecrucis).
The smallest island to hold an endemic was
Makatea of the Tuamotu Archipelago. Makatea is
28 km 2 and low relieœ We estimate that the small-
est island likely to hold an endemic pigeon or dove
would be 20.7 km 2. Islands with more than one
endemic are Henderson (36 km 2) with two species
and Huahine (75.5 km 2) with three--both of these
islands are high relief. Again, excluding Easter Is-
land and the Hawaiian groups, our estimate of the
total number of enderrfics is thus: (53 islands * 1
species) + (25 islands * 2 species) + (50 islands
ß 3 species) = 253 species.
Island-group endemics
Just as we saw that a greater proportion of
parrots showed endemism to groups of islands
than the less mobile rails, a full 51% of the pi-
geons and doves are restricted to single-island
groups compared to 30% for parrots. Thus, there
appears to be a positive relationship between
flight ability and area over which endemism ex-
tends.
Vanuatu held the most species (6) of pigeons
and doves that were restricted to an island
group, and the Marianas held the next highest
number (5). These, and the other large groups
of islands (Chuuk, Fiji, New Zealand, the Soci-
ety Islands, and Tonga) account for 39 of the
total 64 species of island-group endemic pigeons
and doves. Unlike parrots, endemic pigeons and
doves are also found on large low-relief groups.
Two species are restricted to the Tuamotu Ar-
chipelago, a fact that leads us to predict the same
number of species on the Marshall Islands.
THE ESTIMATED NUMBER OF ENDEMICS
Our exercise produced two sets of estimates
of the number of endemic species in each of
three taxa. For estimates based on single-island
endemism, we predict 537 species of rails, 94
species of parrots, and 253 species of pigeons
and doves for a total of 884. We can account for
only 57 single-island endemic species of the
three taxa as either fossil, extinct or extant. Es-
timates based on island-group endemism yield
145 species of rails, 29 species of parrots, and
64 species of pigeons and doves (Fig. 7). We
can account for 40 of these as fossil, extinct, or
extant. Thus, we predict that the total number of
endemic species of these taxa that once occurred
in the Pacific falls between 242 and 884.
TESTING THE MODELS: KNOWN VERSUS
ESTIMATED ENDEMISM
We may now investigate factors that would
refine our predictions. Which estimates better re-
flect the known distribution of endemic rails,
parrots, and pigeons and doves in the Pacific--
those derived from single-island endemics or
those from island-group endemics? To answer
this question, we compare our predicted values
with the known distribution of endemic birds.
We calculated two indices of the proportion
of total missing endemics (all taxa combined)
per island group, one for each of our definitions
of endemism. We added I to all values of the
total number of endemics known to exist and to
the totals predicted from our two definitions of
endemism. We did this so that we could calcu-
late proportions (number of known endemics/
number of predicted endemics) without having
zero values in either the numerator or denomi-
nator. We arcsine transformed the proportions to
make the distribution normal and ranked the re-
sults. We then compared the ranks by perform-
ing a linear regression of single-island endemic
ranks on island-group endemic ranks (Fig. 8).
Not surprisingly, the linear fit was significant
(F = 18.37, P < 0.01). The slope was less than
unity (b = 0.56) suggesting that when the pre-
dicted number of endemics corresponds with the
actual number of island-group endemics, the sin-
gle-island prediction is low and vice versa. We
tested for the influence of the number of islands
in each group on both of our predictions. Neither
set of predictions correlates with this parameter
(r < 0.2 for both). Identifying each group as
high relief (50% of total area is high relief) or
low relief reveals the pattern responsible for the
disparity between the two sets of ranks (Fig. 9).
Predictions correspond best with known endem-
ism for low-relief groups when endemism is de-
fined as a single-island distribution. Conversely,
for high-relief groups, predictions based on
group endemism correspond best with the num-
ber of known endemics. We believe there are
ecological reasons for this.
Groups of low-relief islands tend to have
smaller islands than high-relief groups (ANO-
VA: F = 4.21, P = 0.04). For low-relief groups,
an individual island approach to endemism
would successfully identify those few large is-
lands in the group that could support a large
population of birds. In contrast, predictions
based on group endemism would lead to over-
estimates because the area across each group is
HOW MANY BIRD SPECIES--Curnutt and Pimm
1000
25
800'
600'
[] Parrots
[] Pigeons
[] Rails
ß ', 400'
E 200'
4--'
A B C D
FIGURE 7. Total predicted numbers of endemic rails, parrots, and pigeons in the prehistoric Pacific under four
sets of assumptions: (A) endemic species are those that occur on only one island; (B) endemic species are those
that occur within single-island groups; (C) low-relief island groups produce endemic species at single islands
and high-relief island groups produce endemics at island groups; and, (D) the same as (C) with modifications
driven by patterns of disturbance (sea-level change and tsunamis).
summed. Conversely, the assumption of single-
island endemism for the larger islands of high-
relief groups ignores factors that potentially lim-
it the size of bird communities. In his analysis
of the assembly of the fruit-pigeon guild in New
Ranked prop. of group endemism
FIGURE 8. Ranked proportions of predicted num-
bers of endemic birds (rails, parrots, and pigeons com-
bined) over known numbers of endemics. Values on
the y-axis were generated using the assumption of sin-
gle-island endemism while those on the x-axis were
generated with the assumption of island-group endem-
ism.
Guinea, Diamond (1975) showed that the entire
species pool is never found in one locality. Some
species never occurred together and some sets
of species excluded particular species. This ef-
fect is primarily due to competition between
species with closely related niches. Another eco-
logical factor that over inflates the estimates for
high-relief islands stems from our grouping
across taxa. Some high-relief islands may pro-
vide habitat for each of the three taxa we dis-
cuss, but it may be unreasonable to assume that
all of them do.
We can now refine our original estimates of
endemism by calculating the totals for each tax-
on separately for low- and high-relief island
groups using the appropriate assumptions of en-
demism (low-relief and single-island endemism;
high-relief and island-group endemism). This
yields 206 species of rails, 38 species of parrots,
and 101 species of pigeons and doves (Fig. 7).
These sum to 345 species across taxa.
WHERE THE ENDEMICS ARE AND
WHERE THEY ARE NOT
Five island groups (Johnson Atoll, Howland,
South Line, Gambier, and North Cook) are all
low relief. They have no endemic species, nor
are expected to under the assumption of single-
island endemism. Our interpretation of the re-
26 STUDIES IN AVIAN BIOLOGY NO. 22
10'
-10 ÷
-2O
-3O
ß
oo o o
ß
o
o ß o
o o.
o ß ß
o ß
ß ß o
ß ß ß 0 0
ß 0 ß 0 ß
ß
High-relief
Low-relief
0 10 20 30 40 50
Ranked proportion of group endemism
FIGURE 9. Residuals of the linear relationship of predicted endemic species under single-island endemism
versus island-group endemism (Fig. 8) with each island group defined as either high or low relief.
suits for the remaining 36 island groups depends
on two assumptions. First, the maximum number
of endemics recorded represents the actual max-
imum of each taxon that could occur on each
type of island and, second, the recorded maxima
on each island size/topography are applicable to
all islands in each class. There is a chance that
the first assumption is incorrect. Continued ex-
cavation of subfossil remains may well produce
more species of birds, even on islands that are
already well represented with endemics. The
second assumption ignores differences in the
history of islands across the Pacific. While there
is little we can do to refine our predictions in
light of the uncertainty of the first assumption,
we can investigate the history of the Pacific is-
lands to uncover patterns of species numbers on
island groups.
The name "Pacific" belies this ocean's vio-
lent history. Natural disturbance of the Pacific
islands can be a potentially limiting factor in
speciation among birds. Stoddard and Walsh
(1992) list five environmental factors that influ-
ence island ecosystems: vulcanicity and earth-
quakes, sea-level change, tsunamis, rainfall pat-
terns, and hurricanes. We investigate two of
these: sea-level change and tsunamis. We chose
these factors because they operate at regional
scales, their effects are unambiguous, and they
occur across a temporal scale that is consistent
with evolutionary time.
SEA-LEVEL CHANGE
A number of studies concerning sea-level
change in the Pacific over the last 10,000 years
have been reported in the literature (Ota et al.
1988, Pirazzoli and Montaggioni 1988, Yonek-
ura et al. 1988, Pirazzoli 1991). Throughout the
Pacific, sea level was much lower 10,000 years
before present (BP) than any time since. At that
time, global sea levels were rising rapidly with
the melting of the glacial ice sheets. Indeed, the
massive infusion of water into the oceans led to
regions of hydroisostasy (depression of the
ocean floor by water loading) and consequent
elevated sea levels (Pirazzoli 1991). Thus, from
6,000 BP to as late as 1,200 BP some island
groups had sea levels significantly higher than
at present.
During the last glacial maximum (18,000 BP),
when sea levels were nearly 150 m lower than
today, all islands of the Pacific were larger. For
example, the Fiji group currently has a com-
bined area of 18,600 km 2, whereas at 18,000 BP
its area was over 35,000 km 2 (Gibbons and Clu-
nie 1986). With rising sea level there would
have been a loss of area and habitat. Thus, many
island groups probably held more endemic spe-
cies in the distant past than they did even in
prehistoric times. Isostatic effects have been re-
corded for French Polynesia, the South and
North Cook Islands, and the Marquesas Islands
HOW MANY BIRD SPECIES--Curnutt and Pimm 27
(Pirazzoli and Montaggioni 1988, Yonekura et
al. 1988, Stoddard and Walsh 1992; Table 2). As
late as 1,200 BP, these groups exhibited less sur-
face area than today--with groups such as the
Tuamotu Archipelago disappearing almost com-
pletely (Gibbons and Clunie 1986).
This scenario raises two important consider-
ations for our estimates of the prehuman avifau-
na. First, the decrease in area of many large is-
lands that began at 18,000 BP would have
caused a decrease in the number of bird species.
This decrease may not have been contemporary
with the decrease in area. Diamond (1972)
showed that the reduction of one large island,
the D'Entrecasteaux Shelf, into a number of
small fragments should have led to a reduction
of the number of bird species to a new equilib-
rium. However, he suggests that the time to
reach the new equilibrium is dependent on the
size of the new island. Thus, there could be a
lag time (of several thousands of years in the
above case) before the actual species numbers
reflect the restraints of the size of the new island.
We are not aware of any studies similar to Di-
amond's (1972) that address the islands included
in our analyses. We will assume that the avifau-
na of the islands was at equilibrium at 4,000 BE
In doing so, we risk underestimating the number
of species on all islands but those affected by
the above mentioned isostatic effect; for these
islands, our estimates would be to high.
The second consideration regarding sea level
and endemism is the effect of elevated sea levels
on low-relief islands. The low-relief island
groups of Gainbier, North Cook, and the Tua-
motu Archipelago were affected by isostatic sea
levels (Table 3). Of these, only Tuamotu is ex-
pected to have single-island endemics. We pre-
dict six species of rails and six species of pi-
geons-one pigeon exists (Ptilinopus chalcu-
rus). Of this group's 60 islands, only five are
greater than 30 km 2. Apparently, this species
was able to survive the elevated sea level of
6,000-1,200 BP among these islands. The Fiji
group is dominated by large high-relief islands
but also holds a large number of surrounding
low-relief islands. This group experienced sea
levels nearly 2 m higher than present as late as
2,500 BP (Gibbons and Clunie 1986). Endem-
ism would have been improbable in these is-
lands up to that time because of the lower extent
of the area. We predict that eight species of pi-
geons and 16 species of rails could have inhab-
ited these low islands--none are known to have
existed there. We removed the low-relief islands
from the total area and calculated the number of
endemic species we would expect on Fiji based
on group endemism. This had no effect on our
predictions. The size of Fiji's high-relief islands
TABLE 3. ISLAND GROUPS FOR WHICH PUBLISHED DATA
EXIST ON MEAN SEA LEVELS (RELATIVE TO PRESENT; IN
METERS) AT THREE PERIODS OF THE HOLOCENE (FROM
PIRAZZOLI 1991); MAXIMUM SEA LEVEL AND TIME OF OC-
CURRENCE (OTA ET AL. 1988, PIRAZZOLI AND MONTAG-
GION! 1988, YONEKURA ET AL. 1988, PIRAZZOLI 1991);
AND MAXIMUM TSUNAMI RUN-UP HEIGHT (NATIONAL GEO-
LOGIC DATA CENTER)
Group
Mean relive sea level
Years before present x 10 3 Maxi-
Maximum mum
10 5 2.5 sea level run-up
Melanesia
Vanuatu
Fiji
Micronesia
Palau
Yap
Chuuk
Marianas
Pohnpei
MarshalIs
Gilbert
Polynesia
Hawai 'i
North Line
Tuvalu
Samoa
Norda Cook
Tonga
South Cook
Marquesas
Society
Tuamotu
Gainbier
Pitcairn
Rapa
Tabuai
Kermadec
Norfolk
New Zea-
land
Chatham
+ 1 0 2 (2500)
-40 -2 - 1
+4.5 +2.4
-40 -5 -2
+2.4
-3 +2.4
>-15 0 0
+0.6
5 -2
-17 -1 +1
>-20 +0.5 +1
> 20 +0.9 +0.9
0
5.9
0
1.9
1.9
0
16.8
0
1.9
1 (1500) 0
0
1.7 (3400) 0
1 (1500) 9
1 (1500) 3.4
1 (1200) 2.3
1 (1500)
0
1 (1500) 1.8
1 (1500)
0 12
0
0 5.9
0 0
are near the maximum for the Pacific, and the
removal of the low-relief islands did not lead to
a change of the maximum number of species
expected.
Johnson et al. (1996), investigating the evo-
lution of cichlid fish, reported the most rapid
vertebrate speciation known--on the order of
3,000 years. Thus, high sea levels up to 1,200
BP must have reduced bird speciation on some
Pacific islands. The eflbct of our sea-level anal-
yses on our predictions results in the removal of
five species of pigeons and six species of rails
from our total.
TSUNAMIS
Tsunamis are a series of high-energy waves
propagated by a major displacement of earth un-
28 STUDIES IN AVIAN BIOLOGY NO. 22
FIGURE 10. Areas affected by tsunamis (shaded) and the direction of tsunamis arrows) in the Pacific from
1900 to 1983 as reported in the Worldwide Tsunami Database (Lockridge and Smith 1984).
der the sea. They can have devastating effects
on islands. For example, in the early morning
hours of I April 1946 an earthquake in the Aleu-
tian Islands, Alaska, caused a tsunami. Within
minutes a manned lighthouse on Unimak Island
had been obliterated with all hands lost. Four
and a half hours later and over 3,000 km away
the same tsunami hit the Hawaiian Islands.
Reaching a maximum run-up height of nearly 17
m, it smashed into the Island of Hawai'i taking
another 241 lives. This same series of waves
caused casualties and property damage in Cali-
fornia and as far south as central Chile (Lock-
ridge and Smith 1984, Myles 1985).
Tsunamis of this magnitude are frequent with
14 occurrences in the Pacific Basin from 1900
to 1983 (Lockridge and Smith 1984). As with
sea-level change, the effect of tsunamis on is-
lands is variable. Islands without surrounding
submarine shelves are more susceptible to re-
motely generated tsunamis because there is little
to absorb the energy of the waves before they
make contact. Topography and elevation above
sea level are also obvious factors in determining
the effect of tsunamis on islands.
We accessed the Worldwide Tsunami Data-
base, compiled by the National Geologic Data
Center (http ://j ulius.ngdc.noaa.gov/seg/hazard/
tsudb.html), for recorded occurrences of tsuna-
mis within our study site. Uninhabited islands
are not well represented in the data set. For each
occurrence we noted the location of the tsunami,
its maximum run-up height, and its point of or-
igin. We then classified our island groups as ei-
ther susceptible to tsunamis or unaffected (Table
3).
The earliest recorded tsunami in our study
area occurred in 1843. Since then over 130 tsu-
namis have been recorded. The Hawaiian Is-
lands have seen the most tsunamis, a result of
their central location relative to areas of seismic
activity around the Pacific Rim and the lack of
any energy-absorbing shelves around the group.
Figure 10 shows regions affected by tsunamis
and, when known, the direction traveled by tsu-
namis from their point sources.
HOW MANY BiRD SPECIES--Curnutt and Pimm 29
We have data on tsunamis for 21 of our 41
island groups. Ten of these, however, have max-
imum recorded run-up heights of zero. That is,
tsunami events do not noticeably affect these
groups. Many of these fortunate island groups
are low relief, including the extensive Marshall
Islands. Ten of the remaining eleven groups are
high relief and have experienced run-up heights
from less than 2.0 to 16.8 m. The sole low-relief
group affected by tsunamis is the Tuamotu Ar-
chipelago with a maximum run-up of 2.3 m.
The disturbance caused by tsunamis on high-
relief islands is primarily limited to coastal ar-
eas, below the altitudinal distribution of most of
the species we are concerned with. The effect of
tsunamis on the fauna of the Tuamotu Archipel-
ago, however, could be devastating. Most of the
islands of this group are only a few meters in
elevation, and the combined effect of higher sea
level during the mid- and late-Holocene with
tsunamis helps explain why this group has fewer
endemics than we predict based on its size and
topography. Finally, the Tonga group experi-
enced a maximum run-up height of 4.0 to 6.0
m. This group is dominated by high-relief is-
lands; however, 193 kul 2 of its total 563 km 2
consists of low-relief islands. Assuming tsuna-
mis were frequent and devastating enough to
prevent endemism on these low islands, we can
calculate a refined estimate of the number of en-
demics for this group by excluding all low-relief
islands. This exercise results in the loss of one
species of rail and one species of pigeon, leaving
35 rails, 12 pigeons, and 4 parrots attributed to
the Tonga group.
Combining the effects of sea-level change and
tsunamis, we can refine our previous estimate of
predicted endemic species in the Pacific as fol-
lows: 199 endemic rails, 38 endemic parrots,
and 95 endemic pigeons and doves (Fig. 7).
PROBLEM GROUPS
Even after incorporating the above adjust-
ments to our predicted numbers of species, ac-
tual species account for less than half of the pre-
dicted numbers for 13 of the 23 high-relief
groups. Six groups (Rotuma, Tabuai, Wallis and
Futuna, Yap, Tonga, and Kermadec) have no ac-
tual island-group endemics although we predict
from two to five species for these groups. For
low-relief groups, 10 (Nauru, Northwest Ha-
wai'i, Tokelau, Tuvalu, Gilbert, Niue, Phoenix,
Chuuk, Marshall Islands, North Line Islands)
have no actual single-island endemics although
we predict from 1 to 20 species for these groups.
In all, we predicted 210 species of rails, pigeons,
and parrots that are not accounted for as either
fossil, extinct, or extant.
DISCUSSION
We estimate that there were approximately
330 species of rails, pigeons, and parrots on the
islands of the Pacific before human colonization
began 4,000 years ago. Approximately one-third
of these species are accounted for as either ex-
tant, historically extinct, or as fossils. Pimm et
al. (1994), who looked for all landbirds, pre-
dicted that the fossil record was only half com-
plete and that the original avifauna was about
800 species. In reviewing the fossil, historical,
and current data, we could account for only one-
third of the estimated number of species in the
taxa we looked at. We should therefore apply a
three-fold correction to the total number of
known landbirds (540) and conclude that the en-
tire Pacific landbird fauna was comprised of
1,620 or so species before human colonization.
This simple multiplication, however, ignores dif-
ferences in extinction rates between taxa. Stead-
man (1997a,b) suggested that flightless rails suf-
fered a greater proportion of extinctions than
any other taxon of birds. If so, an estimate of
1,500 species would be too high.
In comparing our results to Steadman's (1995)
estimates, we must limit our consideration to
rails--the only taxon that Steadman makes a
quantitative estimate of. We estimate that the
prehuman Pacific held about 200 species of rails,
of which 21 are extant. Steadman's (1995) esti-
mate (2,000+ species of rails) is an order of
magnitude greater than ours. Like Steadman, we
based our analyses on the roughly 800 larger
islands of the Pacific. However, where Steadman
simply multiplied a maximum number of rails
per island by the number of islands, we incor-
porated into our analyses statistical probabilities
and geographical, topographical and environ-
mental data. Thus, we believe that Steadman's
(1995) estimate of the prehuman avifauna is too
high.
More fieldwork will inevitably bring new data
to light. The discovery of more fossil species
will potentially alter our estimates because of the
multiplicative nature of our analyses. The dis-
covery of one new fossil rail on a small island
could conceivably add 800 to our current esti-
mate of 200. This would still be half as much
as the highest proposed number of rails (Stead-
man 1995). Currently, we suggest that the pre-
human avifauna consisted of more than 800 and
less than 1,500 species of landbirds. Further re-
search (as outlined below) is needed to refine
our estimates and to conserve the remaining spe-
cies of the Pacific islands.
CONSERVATION CONCERNS
The loss to extinction of even our lowest pre-
dicted number of endemic species is disturbing.
30 STUDIES IN AVIAN BIOLOGY NO. 22
Much more disturbing is the potential effect of
this prehistoric loss on the biodiversity of the
future. Habitat loss and the introduction of ex-
otic species have had profound negative effects
on endemic Pacific landbirds (Atkinson 1985,
Pimm 1987). For rails, some of the progenitors
of the clan of now extinct endemics may have
themselves become extinct and anthropogenic
disturbance on many islands may make recolon-
ization by extant rails impossible. Thus, even for
a rapidly speciating taxon like flightless rails, the
potential for diversity has been greatly dimin-
ished.
Another conservation concern for Pacific
landbirds is the rise of global sea levels. Al-
though predictions of the rate of sea-level rise
are rife with uncertainty, it is clear that global
warming and subsequent rises in sea level will
occur for centuries into the future (Hutter et al.
1990). Even with a moderate estimate of 4 to 6
cm per decade (Hutter et al. 1990, Wigley and
Raper 1993) many low-relief islands will be in-
undated within the next few centuries.
FUTURE RESEARCH OPPORTUNITIES
Our predictions of the prehistoric Pacific is-
land avifauna are testable. Using our results, re-
searchers can focus excavation efforts on those
islands that we predict will hold fossils of the
greatest number of extinct species. Thus, we
provide our analyses and results as a guide for
continued work in this area of biodiversity. We
conclude with the following suggestions for fur-
ther study:
Where to look for subfossil birds
We predict that the greatest number of extinct
landbirds existed on high-relief islands of at
least I km 2 in size. The greatest part of the
"missing" rails are from Fiji and Vanuatu.
These areas should be surveyed intensely for
subfossil remains. Searches should, perhaps,
also include island shelves that are currently
submerged. Gibbons and Clunie (1986) make a
strong argument for extending archeological ex-
cavations to these areas because they were ex-
posed and possibly colonized during the human
expansion into the Pacific.
Analyze the loss of potential species richness
A thorough understanding of the phylogenetic
relationship between the landbird species of the
Pacific would serve to identify the mechanisms
of speciation and the ancestral species that most
contribute to the potential diversity of each tax-
on. A molecular genetic analysis and mapping
of the relationship of these species may also un-
cover phylogenetic differences in speciation
rates, dispersal, and habitat utilization.
Predict the ef/kcts of rising sea level on
current bird diversity
We have described the effect of area and to-
pography on bird species diversity. Currently,
models are available that predict changes in sea
level both globally and regionally (Wigley and
Raper 1993). The application of sea-level
change projections to Pacific islands would re-
sult in predicted size distributions of islands, to
which our approach can be applied. This will
allow us to predict the expected loss of bird spe-
cies in the Pacific in the coming century. These
analyses, coupled with more traditional efforts
(e.g., Franklin and Steadman 1991) could also
be used to map a survival strategy for Pacific
biodiversity in light of the threat of future sea-
level rise.
ACKNOWLEDGMENTS
We thank M. Moulton, D. Steadman, K. Reese, R.
Walker, S. Conant, and one anonymous reviewer for
their comments. SLP thanks the Pew Fellowship in
Conservation and the Environment for support.
Studies in Avian Biology No. 22:31-46, 2001.
PATTERNS OF SUCCESS AMONG INTRODUCED BIRDS IN THE
HAWAIIAN ISLANDS
MICHAEL P. MOULTON, KARL E. MILLER, AND ERIC A. TILLMAN
Abstract. At least 140 species of 14 different orders of birds have been introduced to the six main
Hawaiian Islands. The introduced species came from six continents and the introductions were carried
out by a variety of agents including state and local governments, private citizens, and the acclimati-
zation society known as the Hui Manu. The introductions mostly occurred during the early to mid-
twentieth century. Most (79%) of the intentional introductions were of species from three orders:
Galliformes, Columbiformes, and Passeriformes.
Introduction success rates were significantly greater for passeriforms than for either columbiforms
or galliforms, although the reasons for this are unknown. In predicting the fate of future introductions,
only the columbiforms showed an "all-or-none" pattern of introduction history. Successful species
had larger native geographic ranges than did unsuccessful species, which supports the hypothesis that
range size is correlated with the ability to adapt to a new environment. Finally, in a partial test of the
introduction effort hypothesis we found that galliforms successfully introduced to the island of Hawai'i
were introduced in significantly larger numbers than unsuccessful species.
Key Words: doves; game birds; introduced species; introduction effort; introduction success; native
range size; perching birds; pigeons.
Numerous species of birds from six continents
have been introduced to the Hawaiian Islands
(Caum 1933, Berger 1981, Long 1981, Pratt et al.
1987). These species were introduced by a variety
of groups for a variety of reasons. As noted by
Berger (1981), the first avian introduction came
with early Polynesians who brought the Red Jun-
glefowl (Gallus gallus) for food. Since that time,
a number of private citizens have brought species
to Hawai'i (e.g., Caum 1933). Some of these in-
troductions were made inadvertently as individual
birds escaped captivity (e.g., Melodious Laughing-
thrush or Hwamei, Garrulax canorus, on O'ahu),
whereas others were intentionally released for aes-
thetic reasons or even as an attempt at biological
control (Caum 1933). There also have been inten-
sive efforts both by private citizens (e.g., Lewin
1971) as well as state and county agencies
(Schwartz and Schwartz 1949; Walker 1966, 1967)
to establish populations of various game birds for
recreational hunting. In the early to mid-twentieth
century, the acclimatization society known as the
Hui Manu actively introduced several species to
various islands (Caum 1933, Berger 1981).
Regardless of their source, a central question
in any study of introduced birds is "Why do
some species succeed and others fail?" In sev-
eral papers we and our colleagues have argued
that competition has played an influential role in
determining the outcomes of passerine species'
introductions in Hawai'i (Moulton and Pimm
1983, 1986a, 1987; Moulton 1985, 1993; Moun-
tainspring and Scott 1985; Moulton et al. 1990;
Moulton and Lockwood 1992). These arguments
are based on three main findings. First, intro-
ductions tend to be less successful when more
species of introduced birds are already present
(Moulton 1993; Moulton and Pimm 1983,
1986a). Second, there is a pattern of limiting
similarity among congeneric pairs of introduced
birds: differences in bill length are significantly
greater in pairs that coexist than in pairs of spe-
cies that were not able to coexist (Moulton
1985). And third, successful introduced passer-
ines show a pattern of morphological overdis-
persion (Moulton and Pimm 1987, Moulton and
Lockwood 1992); i.e., successful species are
morphologically more different from each other
than expected by chance.
Although these three patterns are consistent
with predictions from competition theory, other
explanations for patterns in introduction out-
comes have been advanced. These include intro-
duction history of a species (Simberloff and
Boecklen 1991) and introduction effort (e.g.,
Pimm 1991, Veltman et al. 1996).
The idea that introduction history can predict
future introduction outcomes is appealing in its
simplicity. The concept comes from Simberloff
and Boecklen (1991) who argued that whenever
and wherever a given species is introduced, it
tends to either always succeed or always fail.
This leads to an "all-or-none" pattern in the dis-
tribution of birds introduced onto a series of is-
lands: some species being successful on "all"
the islands in the series and others being suc-
cessful on "none" of the islands. If introduced
birds actually follow this pattern, then predicting
the outcome of future introductions would be
greatly simplified. Moulton (1993) and Moulton
and Sanderson (1997), however, argued that the
all-or-none pattern reported by Simberloff and
Boecklen (1991) for passerine birds was pri-
marily an artifact of sample size.
31
32 STUDIES IN AVIAN BIOLOGY NO. 22
Another factor that might influence the out-
come of introductions is the effort invested in
the introduction process. Griffith et al. (1989)
found that introduction effort along with habitat
quality were associated with introduction out-
come. Similarly, Pimm (1991 ) studied introduc-
tions of seven game bird species (all of which
had been successfully introduced somewhere in
the world) in the western United States and
found that there was a very high (360/424 =
85%) failure rate. Pimm's analysis indicated that
the failure rate was particularly high when fewer
than 75 individuals were released. More recent-
ly, studies of introduced birds in New Zealand
(Veltman et al. 1996, Duncan 1997, Green 1997)
have concluded that introduction effort is the
most influential variable in determining which
species succeed. In each of the three studies, the
authors reported that successful species were in-
troduced in larger numbers and more frequently
than were unsuccessful species.
Several authors have reported a positive re-
lationship between the size of the native geo-
graphic range of a species and its average abun-
dance (e.g., Bock and Ricklefs 1983, Brown
1984). If widespread species tend to be ecolog-
ically more generalized than species with narrow
distributions, we would predict that successful
introduced species would tend to be those that
have larger native ranges.
Many analyses of avian introduction success
in Hawai'i have focused on passerine birds (e.g.,
Moulton and Pimm 1983, 1986a,b, 1987; Wil-
liams 1987, Moulton and Lockwood 1992), yet
passerines represent fewer than half the total
number of birds that have been introduced to the
Hawaiian Islands (Berger 1981, Long 1981).
Our objectives in this paper were to examine
patterns of success for introduced species in Ha-
wai'i across three taxonomic orders of birds:
Galliformes, Columbiformes, and Passeriformes.
Specifically, are the success rates of nonpasser-
ine birds different from those of the passerines?
Second, is an all-or-none pattern evident in the
nonpasserine orders? Third, is native range size
greater for successful introduced species than for
unsuccessful introduced species in passerines
and nonpasserines? And, fourth, does introduc-
tion effort play a role in determining the success
of introduced birds in Hawai'i?
METHODS AND MATERIALS
We used Caum (1933), Schwartz and Schwartz
(1949), Munro (1960), Walker (1966, 1967), Lewin
( 1971), Berger ( 1981 ), Long ( 1981 ), Lever (1987), and
Pratt et al. (1987) to compile lists of nonindigenous
birds introduced to the Hawaiian Islands. In compiling
our lists we attempted to ascertain not only the current
status of each species but also the date of first intro-
duction. In our analyses we considered species to be
successful if they were present on an island in 1990.
We considered species to be unsuccessful if there were
no recorded observations after 1990. Scientific names
of 140 species introduced in the Hawaiian Islands are
provided in Appendix 1. Scientific names of intro-
duced species not included in our statistical analyses
are provided in Appendix 2.
In order to determine success rates for the species in
the different orders, we considered a species to be suc-
cessful if it succeeded on any island, and unsuccessful
only if it failed on every island on which it was released.
By this approach, even if a species fails on all but one
island, we believe that environmental conditions in the
archipelago overall were potentially suitable for establish-
ment and that perhaps differences in the mechanics of the
release or interactions with other species might have oc-
curred on islands where the species failed. We compared
introduction success rates across orders with a chi-square
test of equal proportions.
We used range maps in Long (1981) to estimate
native range size for all introduced species, except
Garrulax caerulatus and Callipepla douglasii, which
were not included by Long. We used a grid method
similar to the methods of Moulton and Pimm (1986b).
We placed a small acetate grid over the native range
map in Long (1981) and counted the number of
squares that were intersected. Each square represented
approximately 259,000 km 2. In earlier analyses of na-
tive range size of introduced passerines in Hawai'i
(Moulton and Pimm 1986b), Uraeginthus angolensis
and U. cyanocephala were omitted because of concern
about the potential confusion with young U. bengalus
in the field. However, we included all three Uraegin-
thus species in this analysis because Berger (1981) re-
ported each was seen and identified in the wild.
We used Mann-Whitney tests for all our range size
comparisons because data were not normally distrib-
uted. We compared native geographic range sizes of
successful versus failed introductions, both within and
across orders.
RESULTS
At least 140 species of nonindigenous birds
from 14 orders have been released in the Ha-
waiian Islands (Table 1). Our results differ from
earlier totals of 162 species (Long 1981) and
170 species (Berger 1981) for two reasons. First,
those authors followed a somewhat different tax-
onomy. For example, Berger (1981) listed the
Green Pheasant (Phasianus versicolor) as being
a distinct species, whereas we followed Sibley
and Monroe (1990) and treated it as being con-
specific with the Ring-necked Pheasant (Phasi-
anus colchicus). Second, at least among the pas-
serines, we have excluded several species in-
cluded by Long and Berger on grounds that sim-
ply too few individuals (i.e., < 5) were released.
Simberloff and Boecklen (1991) list 14 of these
species in their Appendix B, although based on
Berger (1981 ) we included the two Uraeginthus
species (U. angolensis and U. cyanocephala).
Although a great diversity of species has been
released into the Hawaiian Islands, for the most
INTRODUCED BIRDS--Moulton, Miller, and Tillman 33
TABLE 1. SPECIES OF BIRDS INTRODUCEO TO THE HA-
WAIIAN ISLANDS (CAUM 1933, BEI.GER 1981, LONG
1981)
Number of
Order species
Tinamiformes 1
Pelecanifonnes 1
Ciconiifonnes 3
Falconiformes 1
Galliformes 40
Turniformes 1
Gruifonnes 1
Charadriiformes 2
Anserifonnes 4
Columbiformes 18
Psittacifonnes 14
Strigifonnes 1
Apodifonnes 1
Pas seritbnnes 52
part three orders accounted for the bulk of the
introductions. These are the game birds (Galli-
formes), pigeons and doves (Columbiformes),
and perching birds (Passeriformes). These spe-
cies represent 110 introductions (Appendices 3-
5). Berger (1981) lists 14 species of a fourth
order, Psittaciformes. However, according to
Berger (1981), 13 of these species were acci-
dental introductions. Moreover, Pratt et al.
(1987) considered only one species of this order
(Psittacula krameri) to be successful in Hawai'i.
Thus, we restricted our tests to the three orders
for which there was evidence for intentional in-
troductions: Galliformes, Columbiformes, and
Passeriformes.
HISTORICAL PERSPECTIVE
In order to develop a historical perspective on
the phenomenon of introductions for the galli-
forms, columbiforms, and passeriforms, we cat-
egorized introductions by time period (Fig. 1).
Historical peaks in the number of introductions
were evident for each order.
For galliforms, the number of species' intro-
ductions increased steadily from 1901 until the
early 1960s and then declined to zero. There has
not been an introduction of a new species of
galliform into the Hawaiian Islands since 1965
(Francolinus adsperus). For columbiforms, the
peak occurred in the 1920s. Indeed, there have
been only two introductions (Zenaida asiatica in
1961 and Zenaida macroura in 1962) of species
from this order since 1960. The passeriforms
also appear to show a decline in the number of
introductions after the 1960s (Fig. 1). Closer in-
spection reveals an even sharper decline in the
frequency of introductions, with only one new
passerine species introduced since 1980 (Estril-
da astrild in 1981). The remaining nine species
were all present on other islands in the archi-
pelago prior to 1975 and possibly arrived onto
new islands via interisland colonization.
SUCCESS RATES
Success rates differed significantly among or-
ders (X 2 = 14.59, df = 2, P < 0.005). Among
25
pre-1876 1876-1900 1901-25 1926-50
Year
1951-75 post-1975
ß Galliformes []Columbiformes [] Passeriformes ]
FIGURE 1. Chronology of species introductions to the Hawaiian Islands.
34 STUDIES IN AVIAN BIOLOGY NO. 22
0.8
0.6
0.4
0.2
o
Hawaii Maui Lanai Molokai Oahu Kauai
Island
[] Galliformes [] Columbiformes [] Passeriformes
FIGURE 2. Success rates (number of successful introductions/total number of introductions) per order across
the six main Hawaiian Islands.
passetines, 33 of 52 (64%) species have been
successful on at least one island (Appendix 3).
The success rates for galliform and columbiform
species were not nearly so high. Only 12 of 40
(30%) introduced galliform species (Appendix
4) and 4 of 18 (22%) introduced columbiform
species (Appendix 5) have been successful on at
least one island.
Within islands the success rates also were
variable (Fig. 2). For passetines, Moloka'i and
Lana'i shared the highest rates of success at 1.00
(13/13 for Moloka'i and 11/11 for LUna'i).
Lana'i also had the highest success rate for gal-
liforms (9/15, 0.60), whereas Moloka'i had the
highest rate for columbiforms (3/4, 0.75; Fig. 2;
Table 2). Although it is tempting to compare
rates among islands across the different orders,
results of any tests would be misleading because
of the high potential for nonindependence. For
example, with respect to passetines, only seven
species were introduced to islands other than
TABLE 2. SUCCESS RATES (NUMBER OF SUCCESSFUL
INTRODUCTIONS/ToTAL NUMBER OF INTRODUCTIONS) PER
ORDER ACROSS THE SIX MAIN HAWAIIAN ISLANDS
Island Galliformes Columbiformes Passedformes
Hawai'i 0.32 0.56 0.80
Maui 0.45 0.27 0.84
Lana'i 0.53 0.43 1.00
Moloka'i 0.53 0.60 1.00
O'ahu 0.26 0.33 0.60
Kaua'i 0.40 0.375 0.75
O'ahu (five to Kaua'i and two to Hawai'i). For
galliforms, only O'ahu and Hawai'i have any
unique species.
ALL-OR-NONE PATTERNS
The hallmark of an all-or-none distributional
pattern of introduced birds on islands would be
presence of few, if any, mixed species. Mixed
species are those that are successful on some
islands and unsuccessul on others (Simberloff
and Boecklen 1991). In principle, species re-
leased onto one island could show a mixed out-
come if they spread to another island and then
fail on one of the two islands. In practice this is
very difficult to detect, because those species
with the ability to spread to other islands could
do so repeatedly giving the impression that they
were established on the second island even if
they were actually not able to survive there. This
would be an example of what Brown and Ko-
dric-Brown (1977) have termed a "rescue ef-
fect." With this in mind we believe that analyses
for all-or-none patterns should be limited to
those species that were physically introduced to
more than one island.
In their analysis of introduced Hawaiian birds,
Simberloff and Boecklen (1991) reported that
among 19 introduced columbiform species, only
one (Pterocles exustus) showed a mixed out-
come, having succeeded on Hawai'i, and failed
on Moloka'i and Kaua'i. However, Sibley and
Monroe (1990) placed this species in the order
Ciconiiformes. If this species is excluded, 18
columbiform species remain, 11 of which were
INTRODUCED BIRDS--Moulton, Miller, and Tillman 35
30
25
ß - 2O
ta 15
o
5 10
5
0
I IUnsuccessful []Successful
<10 10-20
20-30 30-40 40-50 50-75
Size of Native Range
>75
FIGURE 3. Size of native geographic range for unsuccessful versus successful introduced species. Range size
measured in number of 259,000 km 2 map blocks (see Methods and Materials).
introduced onto more than one island. The ob-
servation of no mixed species out of eleven pos-
sible is evidence for an all-or-none pattern.
Among the Galliformes, 23 species were re-
leased onto two or more islands. At least seven
of 23 (30%) have had mixed outcomes: Calli-
pepla californica, C. gambelii, Alectoris chukar,
Coturnix japonica, Gallus gallus, Pavo crista-
tus, Meleagris gallopavo (Appendix 4). Thus,
there is not an all-or-none pattern among the in-
troduced game birds.
Moulton and Sanderson (1997) and Moulton
(1993) argued that mixed species tended to be
those introduced onto more islands. With this in
mind we compared the median numbers of is-
lands of introduction for always unsuccessful,
always successful, and mixed species. Medians
differed significantly (H = 8.95, P = 0.012),
with the highest median recorded for mixed spe-
cies (6.0), and medians of 3.0 for always unsuc-
cessful species and 6.0 for always successful
species. As a further test we combined species
that were always successful with those that were
always unsuccessful and compared the com-
TABLE 3. RESULTS OF NATIVE RANGE SIZE COMPARI-
SONS BETWEEN SUCCESSFUL (S) AND UNSUCCESSFUL (F)
INTRODUCED SPECIES (MEAN NUMBER OF 259,000 KM 2
GRID SQUARES)
Order S F P
Galliformes 22.2 16.6 0.099
Columbiformes 36.1 23.3 0.123
Passeriformes 33.0 17.5 0.015
bined median with that of the mixed species.
These medians also differed significantly (H =
5.23, P = 0.022).
RANGE SIZE
We estimated native range size tbr 108 intro-
duced species. Range size was significantly larger
in successful species than in unsuccessful species
(approximate X2 = 10.95, df = 1, P < 0.001; Fig.
3; Table 3). Within orders, range size differences
were significant for passefines (P = 0.015) and
marginally significant in game birds (P = 0.099).
However median range size did not diftr signifi-
canfly between successful and unsuccessful col-
umbiforms (P = 0.123). In all three orders, the
successful species had larger median native range
sizes than did unsuccessful species.
INTRODUCTION EFFORT
Data are available for only a partial test of the
influence of introduction eftbrt on introduction
success. Lewin (1971) provided numbers of indi-
viduals released for 26 Galliformes on the island
of Hawai'i (Table 4). Most of the data were de-
rived from private releases by the owners of the
Pu'u Wa'awa'a Ranch, but in some instances data
from releases made by state agencies were includ-
ed. We excluded Coturnix japonica because it al-
ready was successful, apparently having colonized
the island froln Maui and/or Lana'i (Schwartz and
Schwartz 1949), and there were no further releases
by the state or the owners of the ranch. The me-
dian number of individuals introduced was 179 for
successful galliform species (N = 9) and 14 for
unsuccessful galliform species (N = 17). Medians
36 STUDIES IN AVIAN BIOLOGY NO. 22
TABLE 4. NUMBER OF INDIVIDUALS OF SPECIES OF
GAME BIRDS, PIGEONS, AND DOVES RELEASED ON HAWAI'I
(LEwIN 1971)
Number
Species released Status
Colinus virginianus a
Oreortyx pictus
Callipepla squamata
Callipepla californica
Callipepla gambelii
Callipepla douglasii
Ammoperdix griseogularis
Cyrtonyx montezumae
Alectoris chukar
Alectoris barbara
Francolinus francolinus
Francolinus pintadeanus
Francolinus pondicerianus
Francolinus adsperus
Francolinus icterorhynchus
Francolinus clappertoni
Francolinus erckelii
Francolinus leucoscepus
Coturnix chinensis
Bambusicola thoracica
Lophura leucomelanos
Gallus sonneratii
Phasianus colchicus
Syrmaticus reevesii
Pavo cristatus
Meleagris gallopavo
Zenaida macroura
Zenaida asiatica
Streptopelia risoria (= decaocto ?)
Streptopelia chinensis
Geopelia striata
108 F
88 F
14 F
412 S
546 F
ll3 F
20 F
8 F
110 S
104 F
226 S
10 F
214 S
4 F
9 F
10 F
179 S
27 F
8 F
12 F
67 S
14 F
244 S
180 F
2 S
ll5 S
168 S
40 F
ll F
8 S
18 S
a See Appendix 1 for common names.
were significantly different in a Kruskal-Wallis test
(H = 5.25, P = 0.02).
Data for the columbiforms appear to be equal-
ly compelling, although we have not tested this
group since there were just seven species intro-
duced and two of these already were established
on Hawai'i at the time of the introductions by
the Pu'u Wa'awa'a Ranch (Lewin 1971).
DISCUSSION
The introduction process in the Hawaiian Is-
lands has been highly nonrandom with respect to
phylogeny. Thus 10 of the 14 orders are repre-
sented by five or fewer species. The three orders
that are represented by more species are those that
have been the focus of intentional introductions.
Thus, most galliforms were likely introduced to
enhance prospects for recreational hunting, and
most columbiforms were introduced for recrea-
tional hunting or lbr aesthetic reasons. Passefines
were introduced for a variety of reasons, including
biological control and aesthetic reasons, as well as
accidental releases of cage birds.
The phenomenon of avian introductions, at least
for the three orders we have focused on here, ap-
pears to be historical, with most introduction ef-
forts having come to a close. There have been no
columbiform or galliform introductions to the Ha-
waiian Islands in more than 30 years. Moreover,
no new passefine species have been introduced to
the islands since 1981. This is not to say that there
will not be future introductions from these, or oth-
er, taxa. Indeed, there have been recent sightings
of various parrot species since 1990. For example,
Pyle (1994) reported that 10 to 15 Nanday Para-
keets (Nandayus henday) were seen on the island
of Hawai'i.
In terms of success rates, we found that pas-
serine species had a significantly higher overall
success rate than either of the nonpasserine or-
ders. The reasons for this are unclear, but the
pattern is highly significant. It is possible to ex-
plain some of this result via the propagule size
hypothesis. We found a significant relationship
between propagule size (i.e., introduction eflbrt)
and the success rates of galliforms introduced to
the island of Hawai'i. Caum (1933) also noted
that several columbiform species apparently
were introduced in very small numbers. How-
ever, it remains to be shown that passerines were
systematically released in larger numbers.
The simplest potential predictor of the out-
come of species' introductions is introduction
history (Simberloff and Boecklen 1991). If in-
troduction history alone were an adequate pre-
dictor of introduction outcomes we should have
detected clear all-or-none patterns within the or-
ders we analyzed. Moulton (1993) and Moulton
and Sanderson (1997) argued that the all-or-none
patterns reported for passerines introduced to the
Hawaiian Islands and elsewhere may be due to
sampling artifact. When we extended the anal-
ysis here to include the columbiforms and gal-
liforms, only the columbiforms show any evi-
dence for such a pattern. Thus, we found little
evidence to support the notion that introduction
history is an adequate predictor of future intro-
duction outcomes.
Our analyses suggested that one consistent
predictor of introduction success was size of na-
tive geographic range. In all three orders we ob-
served that successfully introduced species had
larger native ranges than unsuccessful species.
These results are consistent with the hypothesis
that species with larger ranges are ecologically
more generalized (Brown 1984) and hence better
able to adapt to a new environment.
In a partial test of the introduction eftbrt hy-
pothesis, we found that galliforms introduced suc-
cessfully to Hawai'i were introduced in larger
numbers than were unsuccessful species. However,
it should be noted that some species were suc-
cessful with initial releases of as few as two in-
dividuals; e.g., a single pair of Peafowl (Pavo cris-
tams) released on the Pu'u Wa'awa'a Ranch in
1909 led to the successful establishment of the
INTRODUCED BIRDS--Moulton, Miller, and Tillman 37
species on Hawai'i (Lewin 1971). Also, for 6 of
the 15 unsuccessful species, >85 individuals were
released (Colinus virginianus, Callipepla dougla-
sii, Callipepla gambelii, Syrmaticus reevesii, Or-
eotyx pictug Alectoris barbara; Table 4). We do
not know if successful game birds on islands other
than Hawai'i were introduced in higher numbers
than were unsuccessful species. Because data are
lacking for passeriform and columbiforrn species,
a thorough test of the introduction effort hypoth-
esis was not possible.
ACKNOWLEDGMENTS
We thank J. M. Scott, S. Conant, R. Walker, B. Den-
nis, and an anonymous reviewer for their comments
on earlier versions of the manuscript. Florida Agricul-
tural Experiment Station JS #R-07766. A. van Doorn
assisted with review of the literature of psittaciform
introductions. MPM wishes to thank C. J. Ralph, C. P.
Ralph, and A. C. Ziegler for their kindness and hos-
pitality during fieldwork in Hawai'i.
APPENDIX 1. SCIENTIFIC AND COMMON NAMES OF 142 SPECIES INTRODUCED TO THE HAWAIIAN ISLANDS (NOMEN-
CLATURE FOLLOWS SIBLEY AND MONROE 1990)
Scientific name Common name
Acridotheres tristis
Agapornis roseicapillis
Alauda arvensis
Alectoris barbara
Alectoris chukar
Amandava amandava
Amazona ochrocephala
Amazona viridigenalis
Ammoperdix griseogularis
Anas discors
Anas platyrhynchos
Ara macao
Bambusicola thoracica
Brotegeris jugularis
Bubulcus ibis
Cacatua galerita
Cacatua moluccensis
Callipepla californica
Callipepla douglasii
Callipepla gambelii
Callipepla squamata
Caloenas nicobarica
Cardinalis cardinalis
Carpodacus mexicanus
Cettia diphone
Chalcophaps indica
Chrysolophus amherstiae
Chrysolophus pictus
Colinus virginianus
Collocalia vanikorensis
Columba livia
Copsychus malabaricus
Copsychus saularis
Coturnix chinensis
Coturnix japonica
Coturnix pectoralis
Crax rubra
Cyanoptila cyanomelana
Cygnus olor
Cyrtonyx montezumae
Eclectus roratus
Eolophus roseicapilla
Erithacus akahige
Erithacus komadori
Estrilda astriM
Estrilda caerulescens
Estrilda melpoda
Common Myna
Rosy-faced Lovebird
Skylark
Barbary Partridge
Chukar
Red Avadavat
Yellow-crowned Parrot
Red-crowned Parrot
See-see Partridge
Blue-winged Teal
Mallard
Scarlet Macaw
Chinese Bamboo-Partridge
Orange-chinned Parakeet
Cattle Egret
Sulphur-crested Cockatoo
Salmon-crested Cockatoo
California Quail
Elegant Quail
Gambel's Quail
Scaled Quail
Nicobar Pigeon
Northern Cardinal
House Finch
Japanese Bush-Warbler
Emerald Dove
Lady Amherst Pheasant
Golden Pheasant
Northern Bobwhite
Uniform Swiftlet
Rock Pigeon
White-rumped Shama
Oriental Magpie-Robin
Blue-breasted Quail
Japanese Quail
Stubble Quail
Great Currasow
Blue-and-White Flycatcher
Mute Swan
Montezuma Quail
Eclectus Parrot
Galah
Japanese Robin
Ryukyu Robin
Common Waxbill
Lavendar Waxbill
Orange-cheeked Waxbill
38
APPENDIX 1. CONTINUED.
STUDIES IN AVIAN BIOLOGY
NO. 22
Scientific name Common name
Estrilda troglodytes
Falco (rusticolus ?)
Francolinus ada7verus
Francolinus clappertoni
Francolinus erckelii
Francolinus francolinus
Francolinus icterorhynchus
Francolinus leucosepus
Francolinus pintadeanus
Francolinus pondicerianus
Gallicolumba luzonica
Gallus gallus
Gallus sonneratii
Garrulax albogularis
Garrulax caerulatus
Garrulax canorus
Garrulax chinensis
Garrulax pectoralis
Geopelia cuneata
Geopelia humeralis
Geopelia striata
Geophaps lophotes
Geophaps plumikra
Geophaps smithii
Geotrygon montana
Gracula religiosa
Grallina cyanoleuca
Lagonosticta senegala
Larus novaehollandiae
Larus occidentalis
Leiothrix lutea
Leptotila verreauxi
Leucosarcia melanoleuca
Lonchura cantans
Lonchura malacca
Lonchura oryzivora
Lonchura punctulata
Lophura leucomelanos
Lophura nycthemera
Melanocorypha mongolica
Meleagris gallopavo
Melopsittacus undulatus
Mimus polyglottos
Myiopsitta monachus
Nandayus henday
Neochen jubata
Nothoprocta perdicaria
Numida meleagris
Oreortyx pictus
Ortalis cinereiceps
Paroaria capitata
Paroaria coronata
Paroaria dominicana
Parus varius
Passer domesticus
Passerina ciris
Passerina cyanea
Passerina leclancherii
Pavo cristatus
Penelope purpurascens
Perdix perdix
Phalacrocorax carbo
Phaps chalcoptera
Phasianus colchicus
Phoenicopterus ruber
Black-rumped Waxbill
Gyrfalcon?
Red-billed Francolin
ClappertoWs Francolin
Erckel's Francolin
Black Francolin
Heuglin's Francolin
Yellow-necked Spurfowl
Chinese Francolin
Grey Francolin
Luzon Bleeding-Heart
Red Junglefowl
Grey Junglefowl
White-throated Laughingthrush
Grey-sided Laughingthrush
Hwamei
Black-throated Laughingthrush
Greater Necklaced Laughingthrush
Diamond Dove
Bar-shouldered Dove
Zebra Dove
Crested Pigeon
Spinifex Pigeon
Partridge Pigeon
Ruddy Quail-Dove
Hill Myna
Magpie-Lark
Red-billed Firefinch
Silver Gull
Western Gull
Red-billed Leiothrix
White-tipped Dove
Wonga Pigeon
African Silverbill
Black-headed Munia
Java Sparrow
Scaly-breasted Munia
Kalij Pheasant
Silver Pheasant
Mongolian Lark
Wild Turkey
Budgerigar
Northern Mockingbird
Monk Parakeet
Nanday Parakeet
Orinoco Goose
Chilean Tinamou
Helmeted Guineafowl
Mountain Quail
Grey-headed Chachalaca
Yellow-billed Cardinal
Red-crested Cardinal
Red-cowled Cardinal
Varied Tit
House Sparrow
Painted Bunting
Indigo Bunting
Orange-breasted Bunting
Common Peafowl
Crested Guan
Grey Partridge
Great Cormorant
Common Bronzewing
Ring-necked Pheasant
Greater Flamingo
INTRODUCED BIRDS Moulton, Miller, and Tillman
APPENDIX 1. CONTINUED.
39
Scientific name Common name
Platycercus adscitus
Porphyrio porphyrio
Psittacula krameri
Pterocles exustus
Pycnonotus cafer
Pycnonotus jocosus
Rhipidura leucophrys
Rollulus rouloul
Serinus leucopygius
Serinus mozambicus
Sicalis fiaveola
Streptopelia chinensis
Streptopelia decaocto
Sturnella loyca
Sturnella neglecta
Syrmaticus reevesii
Syrmaticus soemmerringii
Tiaris olivacea
Turnix varia
Tympanuchis cupido
Tympanuchus phasianellus
Tyro alba
Uraeginthus angolensis
Uraeginthus bengalus
Uraeginthus cyanocephala
Urocissa erythrorhyncha
Vidua macroura
Zenaida asiatica
Zenaida macroura
Zosterops japonicus
Pale-headed Rosella
Purple Swamphen
Rose-ringed Parakeet
Chestnut-bellied Sandgrouse
Red-vented Bulbul
Red-whiskered Bulbul
Willie-Wagtail
Crested Partridge
White-romped Seedeater
Yellow-fronted Canary
Saffron Finch
Spotted Dove
Eurasian Collared-Dove
Long-tailed Meadowlark
Western Meadowlark
Reeve's Pheasant
Copper Pheasant
Yellow-faced Grassquit
Painted Buttonquail
Greater Prairie Chicken
Sharp-tailed Grouse
Barn Owl
Blue-breasted Cordonbleu
Red-cheeked Cordonbleu
Blue-capped Cordonbleu
Red-billed Blue Magpie
Pin-tailed Wydah
White-winged Dove
Mourning Dove
Japanese White-Eye
APPENDIX 2. LIST OF 31 SPECIES FROM I 1 ORDERS NOT INCLUDED IN STATISTICAL ANALYSES. WITHIN EACH CELL,
THE FIRST LINE INDICATES DATE OF FIRST INTRODUCTION (OR FIRST REFERENCE TO INTRODUCTION) AND STATUS (S
SUCCESSFUL; F = FAILED); THE SECOND LINE INDICATES MODE OF INTRODUCTION (1 = PRIVATE; 2 = STATE OR COUNTY
AGENCY; 3 = UNKNOWN, INCLUDES ESCAPE FROM CAPTIVITY; 4 = POLYNESIANS; 5 = HuI MANU); AND THE THIRD
LINE INDICATES REFERENCE
Species O'ahu Kaua'i Maul Hawai'i Moloka'i Lna'i
Nothoprocta perdicaria 1966 F
2
1
Phalacrocorax carbo
Phoenicopterus ruber
Bubulcus ibis
Pterocles exustus
Falco (rusticolus?) a
1929 F
1
1
1959 S 1959 S 1959 S 1959 S
1 1 1 1
7 7 7 7
1961 F 1961 S
2 2
5,11 5,11
1929 F
1
1
1959 S
1
7
1961F
2
5,11
1890s F
1
1
1959 S
1
7
40
APPENDIX 2. CONTINUED.
STUDIES IN AVIAN BIOLOGY
NO. 22
Species O'ahu Kaua'i Maul Hawai'i Moloka'i Lana'i
Turnix varia
Poyphyrio porphyrio 1933 F
3
1
Larus novaehollandiae 1924 F
3
1
Larus occidentalis 1933 F
3
1
Cygnus olor
Neochen jubata 1922 F
2
1
Anas platyrhynchos b
Anas discors c 1932 F
2
1
Tyto alba 1959 S
2
7
Collocalia vanikorensis 1962 S
2
7
Brotegeris jugularis 1933 F
3
1
Cacatua galerita 1933 F
3
1
Cacatua roseicapilla 1933 F
3
1
Cacatua moluccensis 1981 F
3
7
Ara macao 1933 F
3
1
Melopsittachus undulatus 1933 F
3
1
Psittacula krameri 1933 S
3
1,7
Nandayus nenday 1981 F
3
7
Myiopsitta monachus 1970 F
3
7
Amazona viridigenalis 1971 U
3
7
1922 F 1922 F
2 2
I I
1933 F
3
1
1928 F
2
1
1920 F
1
1
1955 S
1
6
1981S 1981S
3 3
7,10 7,10
1981U
3
13
1959 S 1959 S 1958 S 1959 S
2 2 2 2
7 7 7 7,11
INTRODUCED BIRDS--Moulton, Miller, and Tillman
APPENDIX 2. CONTINUED.
41
Species O'ahu Kaua'i Maul Hawai'i Moloka'i Lfina'i
Amazona ochrocephala 1969 F
3
7
Eclectus roratus 1981 F
3
7
Agapornis roseicapillis 1973 F
3
7
Platycercus adscitus
Urocissa erythrorhyncha 1966 F
1
7
1877 F
1
1
References: I - Caum 1933:2 Schwartz and Schwartz 1949:3 - Munro 1960; 4 Walker 1966:5 Walker 1967:6 Lewin 1971; 7 -
Berger 1981; 8 - Moulton and Pimm 1983:9 - Scott et al. 1986:10 - Pratt et al. 1987; I 1 - Simberloff and Boecklen 1991; 12 - Moulton 1993;
13 - Pyle 1994:14 - Wunz 1992.
a Caum (1933) listed F. rusticolus only as a tentative identification.
b May have interbred with natural migrants, as well as fetal individuals.
c Species identity uncertain. Caum (1933) stated the species is Querquedula discors (Blue-winged Teal, Anas discors); however, he also reported
that the individuals came from Australia where the Blue-winged Teal does not occur.
APPENDIX 3. INTRODUCED PASSERINES ON SIX MAIN HAWAIIAN ISLANDS (SEE APPENDIX 2 FOR EXPLANATION OF
TERMS)
Species O'ahu Kaua'i Maui Hawai'i Moloka'i LSna'i
Acridotheres tristis 1872 S 1883 S
1 3
12 8
Alauda arvensis 1867 S 1870 F
3 1
12 1,8
Amandava amandava 1900 S
3
12
Cardinalis cardinalis 1929 S 1929 S
3,5 1
1,8 1,8
Carpodacus mexicanus 1870 S 1886 S
3 3
12 8
Cettia diphone 1929 S 1988 S
1,2 3
1 11
Copsychus malabaricus 1939 S 1931 S
5 1
11 1
Copsychus saularis 1932 F 1922 S
5 1
1 1,12
Cyanoptila cyanomelana 1929 F
2,5
1,8
Erithacus akahige 1929 F
2
1
Erithacus komadori 1931 F
3
8
Estrilda astrild 1981 S
3
12
1883 S 1883 S
3 3
8 8
1886 S 1902 S
3 3
8 8
1987 S 1987 S
3 3
11 11
1949 S 1929 S
3 2
8 1
1886 S 1886 S
3 3
8 8
1980 S
3
11
1937 F
5
8
1883 S 1883 S
3 3
8 8
1917 S 1917 S
3 3
8 8
1951S 1957 S
3 3
8 8
1886 S 1886 S
3 3
8 8
1979 S 1980 S
3 3
11 11
42
APPENDIX 3. CONTINUED.
STUDIES IN AVIAN BIOLOGY
NO. 22
Species O'ahu Kaua'i Maui Hawai'i Moloka'i Lfina'i
Estrilda caerulescens 1965 S 1978 S
3 3
12 11
Estrilda melpoda 1965 S 1989 S
3 3
12 MPM
Estrilda troglodytes 1965 F 1975 S
3 3
12 11
Garrulax albogularis 1919 F
1
1
Garrulax caerulatus 1947 S
3
8
Garrulax canorus 1900 S 1918 S 1902 S 1909 S 1909 S
3 1 1 1 1
1,8 1,8 1,8 1,8 1,8
Garrulax chinensis 1931 F
1
1
Garrulax pectoralis 1962 S
3
11
Gracula religiosa 1960 S
3
11
Grallina cyanoleuca 1922 F 1922 F
2 2
1 1
Lagonosticta senegala 1965 F
3
11
Leiothrix lutea 1928 S 1918 S 1928 S 1928 S 1928 S
2 1 2 2 2
1 1 1 1 1
Lonchura cantans 1984 S 1984 S 1978 S 1972 S 1981 S
3 3 3 3 3
11 11 11 11 11
Lonchura malacca 1936 S 1976 S
3 3
8 11
Lonchura oryzivora 1964 S 1983 S 1986 S 1981 S
3 3 3 3
12 11 11 11
Lonchura punctulata 1883 S 1883 S 1883 S 1883 S 1883 S
3 3 3 3 3
8,12 8 8 8 8
Melanocorypha mongolica 1914 F
1
8
Mimus polyglottos 1931 S 1946 S 1933 S 1959 S 1951 S
5 3 5 3 3
1,8 8 1,8 8 8
Paroaria capitata 1973 S
3
11
Paroaria coronata 1928 S 1928 S 1960 S 1976 S 1963 S
1,5 3 3 3 3
1,11 8,11 11 11 11
1979 S
3
11
1883 S
3
8
1970 S
3
11
1976 S
3
11
INTRODUCED BIRDS--Moulton, Miller, and Tillman
APPENDIX 3. CONTINUED.
43
Species O'ahu Kaua'i Maui Hawai'i Moloka'i Lg. na'i
Paroaria dominicana 1931 F
5
1
Parus varius 1928 F 1890 F 1928 F 1928 F
2 1 2 2
1,8 1,8 1,8 1,8
Pasxer domesticus 1871 S 1917 S 1917 S 1917 S 1917 S 1917 S
3 3 3 3 3 3
1,8 8 8 8 8 8
Passerina ciris 1937 F
5
8
Passerina cyanea 1934 F 1937 F
3 5
8 8
Passerina leclancherii 1941 F 1941 F
5 5
8 8,11
Pycnonotus cafer 1966 S
3
11
Pycnonotus jocosus 1965 S
3
11
Rhipidura leucophrys 1926 F
2
1,8
Serinus leucopygius 1965 F
3
11
Serinus mozambicus 1964 S 1977 S
3 1
11 11
Sicalis fiaveola 1965 S 1966 S
3 3
11 11
Sturnella Ioyca 1931 F
1
1
Sturnella neglecta 1931 F 1931 S 1934 F
2 1 3
8 1,11 3
Tiaris olivacea 1974 S
3
11
Uraeginthus angolensis 1965 F
3
7
Uraeginthus bengalus 1965 F 1973 S
3 3
11 11
Uraeginthus cyanocephala 1969 F
3
12
Vidua macroura 1962 F
3
12
Zosteropsjaponicus 1929 S 1929 S 1938 S 1937 S 1938 S 1938 S
2,5 5 3 5 3 3
1,11 1,11 8 8 8 8
44
APPENDIX 4.
OF TERMS)
STUDIES IN AVIAN BIOLOGY NO. 22
INTRODUCED GAME BIRDS ON THE SIX MAIN HAWAIIAN ISLANDS (SEE APPENDIX 2 FOR EXPLAINATION
Species O'ahu Kaua'i Maui Hawai'i Moloka'i Lana'i
Crax rubra 1928 F
2
1
Penelope purpurascens 1928 F
2
1
Ortalis cinereiceps 1928 F
2
1
Numida meleagris 1928 F 1874 F 1928 F 1928 F 1908 F 1914 F
1 1 1 1 I 1
1,10 1,10 1,10 1,10 1,10 1,10
Colinus virginianus 1906 F 1906 F 1906 F 1906 F 1906 F 1906 F
2 2 2 I 2 2
1,4 1,4 1,4 4 1,4 1,4
Oreortyx pictus 1929 F 1929 F
2 2
1 1
Callipepla squamata 1961 F
2
6
Callipepla californica 1855 F 1855 S 1855 S 1855 S 1855 S 1855 S
3 3 3 3 3 3
1,10 1,10 1,10 1,10 1,10 1,10
Callipepla gambelii 1958 F 1958 F 1958 F 1958 S 1958 S
2 2 2 1,2 2
4,10 4,10 4,10 6,10 4,10
Callipepla douglasii 1959 F
1
6
Tympanuchus cupido 1895 a F 1933 a,b F
1 1
1 1
Tympanuchus phasianellus 1932 F
2
1
Cyrtonyx montezumae 1961 F
l
6
Ammoperdix griseogularis 1959 F
1
6
Alectoris chukar 1923 F 1957 S 1957 S 1949 S 1923 S 1923 S
2 2 2 2 3 3
1,10 4,10 4,10 5,10 4,10 4,10
Alectoris barbara 1961 F 1959 F 1961 F 1959 F
2 1,2 2 2
4,10 4,6 4,10 4,10
Francolinus francolinus 1959 S 1959 S 1959 S 1959 S
2 2 1,2 2
9 9 6 9
Francolinus pintadeanus 1962 F
1
6
Francolinus pondicerianus 1958 S 1958 S 1958 S 1959 S 1958 S 1958 S
2 2 2 I 2 2
4,5,10 4,5,10 4,5,10 6 4,5,10 5
Francolinus adsperus 1965 F
1
6
Francolinus icterorhyn- 1961 F
chus 1
6
INTRODUCED BIRDS--Moulton, Miller, and Tillman
APPENDIX 4. CONTINUED.
45
Species O'ahu Kaua'i Maui Hawai'i Moloka'i Lfina'i
Francolinus clappertoni 1961 F
1
6
Francolinus erckelii 1957 S 1957 S 1957 S 1958 S 1957 S 1957 S
2 2 2 1,2 2 2
5,10 5,10 5,10 6 5,10 5,10
Francolinus leucosepus 1959 F
2
6
Perdix perdix 1910 F 1926 F 1929 F
1 1 2
1 1 1
Coturnix chinensis 1922 F 1910 F 1922 F 1922 F 1922 F
2 1 2 2 2
1 1 1 1 1
Coturnix pectoralis 1922 F 1922 F
2 2
3 3
Coturnixjaponica 1921 F 1921 S 1921 S 1921 S 1921 S 1921 S
3 3 2 3 3 2
2,10 2,10 1,10 2,10 2,10 1,10
Rollulus rouloul 1924 F
2
1
Bambusicola thoracica 1959 F 1961 F
2 1
4,5,10 6
Lophura leucomelanos 1962 S
1
6,10
Lophura nycthemera 1932 F 1870 F
2 1
1 1
Gallus gallus PH c S PH S PH F PH F PH F PH F
4 4 4 4 4 4
2,10 2,10 2,10 2,10 2,10 2,10
Gallus sonnerati 1962 F
1
6
Phasianus colchicus 1865 S 1865 S 1865 S 1865 S 1865 S 1865 S
1 1 1 1 1 1
1,10 1,10 1,10 1,10 1,10 1,10
Syrmaticus reevesii 1960 F 1960 F 1960 F 1959 F 1960 F 1960 F
2 2 2 1 2 2
4,10 4,10 4,10 6 4,10 4,10
Syrmaticus soemmerringii 1907 F 1907 F 1907 F
2 2 2
1 I 1
Chrysolophus pictus 1932 F 1870 F
2 1
1 1
Chrysolophus amherstiae 1932 F
2
1
Pavo cristatus 1860 S 1860 F 1860 S 1928 S 1860 F 1860 F
1 1 1 1 1 1
1,10 1,10 1,10 1,10 1,10 1,10
Meleagris gallopavo 1815 F 1815 F 1815 S 1815 S 1815 S 1815 S
1 1 1 I I 1
1,10 1,10 1,10 1,10 1,14 1,10
May have been Tympanuchus phasianellus (Caum 1933).
Based on "indefinite reports" (Caum 1933).
Prehistoric introduction.
46
APPENDIX 5.
TERMS )
STUDIES IN AVIAN BIOLOGY NO. 22
INTRODUCED COLUMBIDS ON SIX MAIN HAWAIIAN ISLANDS (SEE APPENDIX 2 FOR EXPLANATION OF
Species O'ahu Kaua'i Moloka'i Hawai 'i Moloka'i LSna'i
Caloenas nicobarica 1928 F 1922 F
2 2
1 1
Chalcophaps indica 1924 F
2
1
Columba livia 1796 S 1796 S 1796 S 1796 S 1796 S 1796 S
3 3 3 3 3 3
1 1 1 1 1 1
Gallicolumba luzonica 1929 F
1
1
Geopelia cuneata 1928 F 1929 F
2 2
1 1
Geopelia humeralis 1992 F 1922 F 1928 F
2 1 2
1 1 1
Geopelia striata 1922 S 1922 S 1922 S 1922 S 1922 S 1922 S
2 2 2 2 2 2
1 1 1 1 1 1
Geophaps lophotes 1922 F 1922 F 1922 F 1922 F
2 2 2 2
1 1 1 1
Geophaps plumifera 1922 F 1922 F
2 2
1 1
Geophaps smithii 1992 F 1922 F
2 2
1 1
Geotrygon montana 1933 F
3
3
Leptotila verreauxi 1933 F
3
3
Leucosarcia melanoleuca 1922 F 1922 F
2 x, 2
1 x 1
Phaps chalcoptera 1922 F
2
1
Streptopelia chinensis 1879 S 1890 S 1890 S 1890 S 1890 S 1890 S
3 3 3 3 3 3
1 8 8 8 8 8
Streptopelia decaocto 1928 F 1920 F 1928 F
1 1 2
1 1 1
Zenaida asiatica 1961 F
2
6
Zenaida macroura 1962 S
1
9
Systematics
Studies in Avian Biology No. 22:48-50, 2001.
SYSTEMATICS--INTRODUCTION
HELEN E JAMES
Unreachable to amphibians, reptiles, and most
land mammals, the Hawaiian Archipelago has
been colonized naturally only by the most vagile
of vertebrates. The native terrestrial vertebrates
of the islands consist entirely of birds and a cou-
ple of species of bats. Indeed, the islands are so
remote from other complex terrestrial ecosys-
tems that even birds have difficulty establishing
themselves. The native birds that dwell as year-
round residents in Hawai'i's terrestrial and wet-
land habitats can be traced to as few as 20 col-
onizing species (James 1991).
These successful colonists speciated and
evolved in the islands to give rise to an avifauna
with over 100 resident species. Sadly, many ex-
traordinary species are extinct and known only
through fossil remains. The fossil species in-
clude large flightless waterfowl, flightless wood-
land ibises, many flightless rails, a variety of
raptors, three or four large crows, and diverse
species of Hawaiian honeycreepers or drepani-
dines (Olson and James 1991, James and Olson
1991). Despite these losses, a host of remarkable
endemic species survived in the islands long
enough to be studied and appreciated by orni-
thologists. Most of the survivors are passerinc
forest birds, including many species in the adap-
tive radiation of drepanidines. Besides passer-
ines, the only birds that escaped early extinction
are a hawk, an owl that is probably a recent
colonist, the Hawaiian Goose (Branta sandvi-
censis), and a variety of smaller waterbirds (in-
cluding some that had moved into terrestrial
habitats).
The Hawaiian Islands are one of the world's
hottest of hot spots for the extinction of birds.
Twenty-four endemic species of birds have be-
come extinct there since 1778, and another eight
are either recently extinct or imminently threat-
ened (these figures vary slightly according to the
taxonomy followed; Pratt 1994). In addition, the
thirty-five fossil species that have been de-
scribed and approximately twenty that are cur-
rently waiting to be described are thought to
have disappeared mainly in the prehistoric pe-
riod of human settlement (Olson and James
1991, James and Olson 1991). The causes of the
decline and extinction of so many birds include
habitat degradation and loss, introduced patho-
gens such as avian malaria and poxvirus, and
introduced predators such as the small Indian
mongoose (Herpesres auropunctatus).
Hawai'i's avifauna has garnered considerable
48
attention from ecologists and evolutionary biol-
ogists. The extreme geographic isolation of the
resident birds, the clear-cut barriers to dispersal
within the archipelago (water gaps between is-
lands), and the roughly linear progression of is-
land ages (the islands to the northwest being old-
er than those to the southeast), provide a rela-
tively simple setting where the processes that
underlie modem biogeographic patterns may be
relatively accessible to inference. Classic papers
on Hawaiian birds have addressed such topics as
the allopatric model of speciation (Amadon
1950), character displacement (Hock 1970), dy-
namic equilibrium theory in island biogeography
(Juvik and Austring 1979), and the processes un-
derlying macroevolutionary change (Amadon
1950, Hock 1970, 1979). The basic information
relied upon in these studies is the systematics
and distribution of Hawai'i's endemic birds.
Formal study of the systematics and distri-
bution of Hawai'i's birds began in the late eigh-
teenth century, when the specimens collected on
Captain James Cook's third voyage (in 1778-
1779) reached England. The century that fol-
lowed saw the steady addition of new species
from Hawai'i, as subsequent voyages returned
to western ports with specimens, and later, var-
ious foreigners took up residence in the islands
and made their own collections (Olson and
James 1991, 1994a). The lure of discovery fi-
nally inspired a period of intense exploration of
the islands aimed specifically at collecting and
describing the native birds and other endemic
organisms. Between 1887 and 1902, the islands'
birds were thoroughly sampled by Scott Wilson,
R. C. L. Perkins, and especially by Lord Walter
Rothschild's collectors Henry Palmer, G. C.
Munro, and E. Wolstenholme, followed shortly
by H. W. Henshaw (Olson and James 1994a).
These efforts lead to three comprehensive pub-
lications (Rothschild 1893-1900, Wilson and
Evans 1890-1899, Henshaw 1902a, and Perkins
1903).
Decades after this age of exploration and dis-
covery, papers on the systematics and evolution
of Hawaiian birds began to appear with regular-
ity again. Miller (1937) studied anatomical ad-
aptations for terrestriality in the Hawaiian
Goose, while most other authors focused on the
adaptive radiation of drepanidines (e.g., Amadon
(1950) on eclectic systematics and speciation,
Richards and Hock (1973) on functional anato-
my, Raikow (1977) on myology, Sibley and
SYSTEMATICS Helen F. James 49
Ahlquist (1982) on DNA-DNA hybridization,
Johnson et al. (1989) on protein electrophoresis,
Tarr and Fleischer (1993, 1995) on mitochon-
drial DNA). Also, beginning in the 1970s, fossil
birds were being found in Hawai'i with surpris-
ing frequency (e.g., Olson and Wetmore 1976,
Olson and James 1982b, 1984, James et al.
1987, Olson and James 1991, James and Olson
1991).
As the papers in this volume attest, more ef-
fort is now focused on the systematics of Ha-
waiian birds than at any time since the 1890s.
This coincides with a renaissance in phyloge-
netic research, spurred by advances in methods
of analysis and by the technological revolution
in molecular genetics. Hawaiian birds attract ex-
tra attention because of the urgency of studying
species threatened with extinction, and the need
to place the new fossil species in an evolution-
ary context.
The most active program in molecular genet-
ics of Hawaiian birds is that of Robert C.
Fleischer and his collaborators. A long-term
goal of this program is to study the evolutionary
genetics of each endemic lineage of Hawaiian
birds. Fortunately, even the extinct fossil lin-
eages can be studied, through amplification and
sequencing of DNA fragments f¾om fossil bones
(Cooper et al. 1996, Paxinos 1998, Sorenson et
al. 1999). By including appropriate outgroups
and assuming a molecular clock based in part on
earlier Hawaiian drepanidine research (Fleischer
et al. 1998), Fleischer and Mcintosh (this vol-
ume) are able to estimate the length of time that
each lineage has been present in the islands.
Their paper offers a glimpse of the types of
questions we can answer with molecular genet-
ics that we could only speculate about before,
and also hints at the large number of molecular
genetic studies of Hawaiian birds that are cur-
rently in progress.
The value of genetics and systematics to con-
servation of endangered species is exemplified
by Judith Rhymer's contribution on the endan-
gered Hawaiian Duck (Anas wyvilliana) and
Laysan Duck (Anas laysanesis). Using a battery
of molecular genetic techniques, Rhymer ad-
dresses several pressing questions that will af-
fect the management plans for these two species.
First, she shows that the Hawaiian and Laysan
Ducks have separate evolutionary histories and
certainly merit species rather than subspecies
status. She also cites anecdotal evidence that
Laysan Ducks rarely hybridize in captivity.
Combined with her previous collaborative re-
search showing that the former range of the Lay-
san Duck included the main Hawaiian islands
(Cooper et al. 1996), this lays the groundwork
for possible reintroduction of the Laysan Duck
in the main islands. Rhymer also develops mo-
lecular markers that can be used to monitor the
extent of hybridization between Hawaiian Ducks
and introduced Mallards. Such hybridization
threatens the survival of Hawaiian Ducks on
O'ahu but, so far, not on Kaua'i. The informa-
tion and genetic tools provided by Rhymer will
be indispensable in formulating management
plans for these rare species.
Phylogenetic analysis can also contribute to
conservation planning by providing a way to as-
sess the phylogenetic "distinctiveness" of
threatened species. The number of threatened
species is disproportionate to the funding that is
available to help them, forcing managers to
make hard decisions about which species to fo-
cus upon. One objective of such decisions is to
preserve evolutionary diversity. It is consequent-
ly useful to know to what degree a particular
threatened species differs from its surviving rel-
atives. The study by Fleischer et al. in this vol-
ume assesses the evolutionary relationships and
phylogenetic distinctiveness of an endangered
drepanidine, the Po'ouli (Melamprosops phaeo-
soma), using genetic and osteological data. Both
datasets place the Po'ouli within the clade of
drepanidines. However, an index of distinctive-
ness applied to both datasets also indicates that
the Po'ouli is very different from other living
drepanidines, both genetically and morphologi-
cally. Fleischer et al. conclude that saving the
Po'ouli from imminent extinction would be well
worth the effort from this perspective.
Douglas Pratt, who contributes a cladistic
analysis of the drepanidine radiation based on
eclectic phenotypic characters, recommends that
no changes be made to his taxonomy in the light
of molecular genetic data, which he regards as
preliminary, inconsistent, and in the case of mi-
tochondrial DNA sequences, perhaps giving a
false signal due to hybridization (although there
are no confirmed hybrids among the drepanidi-
nes). Where his results conflict with my disser-
tation research on drepanidine osteology (James
1998), he describes my work as perhaps based
on superficial resemblances and illustrative of
the weaknesses of "single character or single-
complex analyses." My results are remarkably
congruent with Raikow's (1977) early cladistic
analysis of myology and external anatomy, but
Pratt also considers Raikow's character analysis
to be vague where it conflicts with his own re-
sults. I can only urge readers to consult the orig-
inal sources and form their own opinions.
Two corrections should be made here, how-
ever. Pratt (p. 88, this volume) implies that my
tree topologies bring together unrelated species
with similar bill shapes in the red-and-black
plumaged group and the green plumaged group.
50 STUDIES IN AVIAN BIOLOGY NO. 22
Actually, my analysis (James 1998) recognized
the red-and-black birds as a clade, including the
full range of bill morphologies from "finch-
like" to long and sickled. None of the green
birds with parallel bill morphologies joined this
clade. Also, whereas Pratt states that James and
Olson (1991) previously suggested lumping
Loxioides and Chloridops, we actually wrote
that future research may justify merging Loxioi-
des with Telespiaa.
The contribution on species concepts by Pratt
and Pratt is very much in the tradition of Pratt's
dissertation (Pratt 1979), an eclectic assessment
of alpha taxonomy with emphasis on vocaliza-
tions, plumages, and behavior as potential iso-
lating mechanisms. Many allopatric populations
of island birds were long ago demoted to sub-
species by Ernst Mayr and others who embraced
his biological species concept. For example, in
his dissertation, which was supervised by Mayr,
Amadon (1950) applied the biological species
concept to the drepanidines and came up with
many fewer species than were recognized by the
late 19 th century authorities (see Pratt 1979).
However, Pratt and Pratt argue that Amadon and
Mayr often erred in applying their own species
concept, or simply lacked information that
would have kept them from lureping. Properly
applied, they feel that the biological species con-
cept would elevate most of Amadon's allopatric
subspecies to full species status. Although they
stress potential isolating mechanisms in their
evaluations, their way of applying the biological
and phylogenetic species concepts result in very
similar taxonomic lists. While the debate over
species concepts continues, non-taxonomists can
take comfort in knowing that, with the growth
of knowledge about Hawaiian birds, the choice
of species concept now appears to have little ef-
fect on the species-level taxa that are recog-
nized.
This is an exciting time for evolutionary and
biogeographic studies of HawaiTs avifauna.
The abundance of fossils enables us to study
morphological change through time, calculate
rates of species turnover and extinction using
data with real time depth, and gain insight into
the former ranges and habitat preferences of en-
dangered species. With ancient DNA we can
identify fossil species, place them on phyloge-
netic trees, and even study their population ge-
netics over long stretches of time. Because the
genetic divergences between isolated island pop-
ulations cannot be older than the islands them-
selves, multiple local calibrations of the mini-
mum rates of DNA sequence change are possi-
ble in Hawai'i. Putting aside differences of opin-
ion on whether genetic or phenotypic data are
best for phylogenetic analysis (see Pratt, this
volume, and Fleischer and Mcintosh, this vol-
ume), phylogenetic hypotheses can be strength-
ened and insights into character evolution can
be gained through comparison of data and re-
sults from these two types of studies. The con-
fluence of knowledge from these various sources
is leading to a much improved picture of change
in Hawai'i's avifauna through time. The growth
of information from genetics, phylogenetics, and
paleontology is contributing not only to basic
knowledge, but in important ways to conserva-
tion management as well.
Studies in Avian Biology No. 22:51-60, 2001.
MOLECULAR SYSTEMATICS AND BIOGEOGRAPHY OF THE
HAWAIIAN AVIFAUNA
ROBERT C. FLEISCHER AND CARL E. MCINTOSH
Abstract. The Hawaiian avifauna is exceptional for its high proportion of endemic taxa, its spectac-
ular adaptive radiations, and its level of human induced extinction. Little has been known about the
phylogenetic relationships, geographical origins, and timing of colonization of individual avian lin-
eages until recently. Here we review the results of molecular studies that address these topics. Mo-
lecular data (mostly mitochondrial DNA sequences) are available for 14 of the 21 or more lineages
of Hawaiian birds. We briefly review results of phylogenetic analyses of these data for lineages that
have experienced major and minor radiations, and for single differentiated species and probable recent
colonists. When possible, we determine the mainland species that are genetically most closely related.
We find evidence that roughly half of the >21 lineages colonized from North America; not even a
quarter appear to have come from South Pacific Islands. Our data also provide little evidence that
Hawaiian bird lineages predate the formation of the current set of main islands (i.e., >5 Ma), as has
been found for Hawaiian Drosophila and lobeliads.
Key Words: adaptive radiation; biogeography; Hawaiian avifauna; mitochondrial DNA; molecular
systematics.
In 1943 Ernst Mayr published a short paper in
The Condor summarizing his hypotheses about
the geographic origins and closest living rela-
tives of each known lineage in the Hawaiian avi-
fauna. Mayr (1943) concluded that half of 14
hypothesized colonizations were of American
origin and only two lineages arose from Poly-
nesia. Therefore, although Hawai'i is considered
part of the "Polynesian Region" because most
of its biota and its human inhabitants had Pol-
ynesian ancestors, in terms of its birds Hawai'i
is in the Nearctic Region. Since Mayr's paper,
other authors have posited similar systematic hy-
potheses and biogeographic scenarios based on
morphological, ecological, and distributional
data (e.g., Amadon 1950, Pratt 1979, Berger
1981). Paleontology has offered only minor res-
olution of the relationships of ancestral lineages
or the timing of speciation events; although
there is an excellent Holocene fossil record in
Hawai'i (Olson and James 1982a, 1991; James
and Olson 1991), the pre-Holocene record is ex-
tremely limited (though one excellent fauna
dates to >0.12 Ma ago; James 1987).
In recent years, molecular methods have prov-
en extremely useful for inferring evolutionary
relationships among taxa and the relative time
frames during which taxa evolved (Avise 1994,
Hillis et al. 1996). Inference from molecular data
may be the best available way to reconstruct
phylogenetic relationships and determine geo-
graphical origins and evolutionary time frames
for Hawaiian taxa. In part this is because mor-
phological or behavioral changes are often adap-
tive responses subject to natural or sexual selec-
tion (i.e., as part of the process of adaptive ra-
diation), and they do not usually show constancy
in their rates of change. Thus they can poten-
tially mislead on issues of common ancestry via
homoplasy. DNA sequences, on the other hand,
while obviously not evolving in a perfect clock-
like fashion (see below), do change over time,
and evolve more continuously than morphology.
Also, with the exception of a relatively few non-
synonymous changes within protein sequences,
they generally evolve via mutation and drift (Nei
1987, Avise 1994), and are not as subject to ho-
moplasy via convergence or stasis as are mor-
phological or other characters. Thus major adap-
tive shifts in, for example, the bills of Hawaiian
honeycreepers, may occur within some lineages
(e.g., to thin and decurved in the nectarivorous
'I'iwi, Vestiaria coccinea), while not in others
(e.g., conical and finchlike in the Laysan Finch,
Telespiza cantans), in spite of an identical
amount of time since evolving from their puta-
tively "finch-billed" common ancestor. There
are methods for detecting symplesiomorphic
versus synapomorphic characters in phylogenet-
ic analysis, but the higher variance in rates of
change of morphological characters remains a
problem for phylogenetic reconstruction (Hillis
et al. 1996).
While there have been significant molecular
investigations of particular Hawaiian plant and
invertebrate taxa (especially Drosophila; e.g.,
Hunt and Carson 1983, DeSalle and Hunt 1987,
DeSalle 1992), few molecular studies detailing
evolutionary histories of the Hawaiian avifauna
have been made until recently (e.g., Tarr and
Fleischer 1993, 1995; Feldman 1994, Cooper et
al. 1996; Fleischer et al. 1998, 2000, this vol-
ume; Paxinos 1998, Sorenson et al. 1999,
Fleischer et al. in press, Rhymer this volume; C.
Tarr, E. Paxinos, B. Slikas, H. James, S. Olson,
A. Cooper, and R. Fleischer, unpubl. data).
51
52 STUDIES IN AVIAN BIOLOGY
TABLE 1. THE ELEMENTS OF THE HAWAIIAN AVIFAUNA
NO. 22
Taxon Family No. of species a Geographic origin b Comments c
Non-passeriformes:
Ibises Plataleidae -->2 N.A. minor radiation, flight-
less, Apteribis?
Night Heron Ardeidae 1 N.A. recent colonist, Nyctico-
rax nycticorax
Moa-nalos Anatidae >4 W. Hemisphere minor radiation?, 3
flightless duck gen-
era?
True Geese Anatidae ->3 N.A. minor radiation, Bran-
ta, ?e
Moderu Ducks Anatidae 2 N.A. and Asia I _+ diftrentiated, 1 re-
cent colonist, Arias e
Porzana Rails Rallidae ->12 Pacific/unknown major radiation?, ->2
colonizations?
Large rallids Rallidae 2 N.A.? recent colonists?, coot
and moorhen
Black-necked Stilt Recurvirostridae 1 N.A. recent colonist, Himan-
topus knudseni e
Eagle Acciptridae I Asia recent colonist, Haliaee-
ms leucophrys?
Buteo Acciptridae 1 N.A. differentiated, Buteo so-
litarius e
Harder Acciptridae 1 Unknown differentiated, Circus
dossenus?
Long-legged Owls Strigidae 4 Unknown minor radiation, Grailis-
trix spp. 47
Short-eared Owl Strigidae l Unknown recent colonist, Asio
fiammeus sandwichen-
sis
Passeriformes:
Crows Corvidae ->4 Unknown minor radiation?, Corvus
spp., 3?, I e
Millerbird Sylviidae I South Pacific differentiated, Acroce-
phalus familiaris e
'Elepaio Myiagridae -> 1 Australasia differentiated, Chasiem-
pis sandwichensis
Thrushes Muscicapidae 5 W. Hemisphere minor radiation, Myad-
estes spp., 37, 1 e
Honeyeaters Meliphagidae ->6 South Pacific minor radiation, Moho
spp., Chaetoptila, all?
Honeycreepers Fringillidae >50 Asia or N.A.? major radiation, drepani-
dines, most? or e
>21 lineages 13 families ->102 species
a Number of species within each lineage/family, based on James and Olson (1991), Olson and James (1991), and H. James (pers. comm.).
b N.A. - North America; W - West.
c ? denotes at least SOllle Illembers extinct; e denotes at least some illelllbers endangered.
Components of the Hawaiian avifauna vary
greatly in the degrees to which they have spe-
ciated and become modified morphologically
and ecologically (Table 1). For example, the Ha-
waiian drepanidines (Hawaiian finches or hon-
eycreepers) have evolved incredible morpholog-
ical, ecological, and behavioral diversity across
more than 50 species and are one of the most
often cited cases of adaptive radiation (Roths-
child 1893-1900, Perkins 1903, Amadon 1950,
Raikow 1977, Freed et al. 1987a, James and Ol-
son 1991, Tarr and Fleischer 1995, Fleischer et
al. 1998). Several species of extinct, large,
flightless waterfowl (moa-nalos) show extreme
morphological modification in their apparent
shift into a ratite/grazing mammal/tortoise niche
(Olson and James 1991; Sorenson et al. 1999).
Other avian lineages have not speciated and
have changed morphologically little or not at all
from putative mainland relatives (e.g., Black-
crowned Night Heron, Nycticorax nycticorax
hoactli; Short-eared Owl or Pueo, Asiofiammeus
sandwichensis). Is this variance in levels of spe-
ciation and phenotypic differentiation related
merely to the lengths of time that lineages have
been evolving in the islands (Simon 1987, Car-
HAWAIIAN BIRD MOLECULAR SYSTEMATICS--FIeischer and Mclntosh 53
I I I I : Main
Kaual I I .......... .i.11.i.i.i'11..i!...,.i._....o...11.b:i.i..}...: ....
. (SAmy) Oa I Ts,w: ,65,,w.
(3.7 my) ¾"
- [ e Maui-Nui
w -nk (1.9 my)
:: VaCL? e ......... Hawaii
................................... : .43 my)
Main Hawaiian Islands
(K-At ages)
FIGURE 1. Map of the main Hawaiian Islands (plus inset map of main and leeward Hawaiian Islands). Ages
of the oldest rocks from the main islands based on K-Ar dating are noted. Maui-Nui is composed of the islands
of Maul, Lana'i, Kaho'olawe, and Moloka'i, all of which were connected until about 0.34).4 Ma ago and again
during more recent periods of low sea level.
son and Clague 1995)? Or are there other factors
that have promoted stasis in some lineages and
change in others, regardless of length of time in
the islands? As noted above, the fossil record
provides little resolution of this question. Thus,
estimates of the age of separation from ancestors
outside of the Hawaiian Archipelago, or the age
of a radiation within the islands, can only be
inferred from molecular data.
The Hawaiian Islands and its avifauna are ex-
tremely isolated from continental and other Pa-
cific island avifaunas. This is likely the primary
reason for the relatively low number of indepen-
dent taxonomic avian lineages that occur in the
islands (Mayr 1943, Pratt 1979). While the total
number of such lineages has been increased (and
continues to increase) from recent fossil findings
(Olson and James 1982a, 1991; James and Olson
1991), the islands still appear to have far fewer
independent avian lineages than one might ex-
pect for a tropical archipelago of this size and
topographic diversity, and there may be addi-
tional factors involved that limit the primary di-
versity of the avifauna.
Here we summarize molecular and other data
relevant to systematics and biogeography of the
Hawaiian aviafauna. We first provide a brief
overview of the geological history of the Ha-
waiian Archipelago and its utility for calibrating
rates of molecular evolution (Tarr and Fleischer
1993, Fleischer et al. 1998). We then consider
the origins and phylogenetic histories of each
lineage within the avifauna, addressing exten-
sive and minor radiations, well-differentiated
single species, and undifferentiated (and likely
recent) colonists. We also apply a molecular
clock approach to obtain rough estimates of the
maximum period of time that a lineage could
have existed in the Hawaiian Islands.
GEOLOGICAL HISTORY AND THE
CALIBRATION OF MOLECULAR
EVOLUTIONARY RATES
The Hawaiian Islands have an unusual geo-
logical history (Clague and Dalrymple 1987,
Walker 1990, Carson and Clague 1995; Fig. 1).
They form as the Pacific Plate drifts northwest
over a "hot spot" where magma extrudes from
the earth's mantle through the crust to build
huge shield volcanos (often to >4 km above sea
level). The extreme weight of a new island,
combined with the cooling of the crust as it
moves away from the hot spot, causes a rela-
tively rapid subsidence in island elevation and
area. Subsidence continues slowly beyond this
point, as does erosion, and islands shrink to be-
come small coral and sand atolls and ultimately
undersea mounts (Fig. 1).
The Hawaiian Islands are ordered by age in a
linear pattern, with the oldest main island in the
54 STUDIES IN AVIAN BIOLOGY NO. 22
northwest (Kaua'i at 5.1 Ma) and the youngest
in the southeast (Hawai'i at 0.43 Ma; Fig. 1).
This volcanic conveyor belt provides an excep-
tional system for evolutionary studies, as it sets
up a temporal framework that can be used to
estimate the timing of evolutionary events and
rates of evolution. The age of an island is the
maximum age for a population inhabiting the is-
land. These ages can be used to calibrate rates
of molecular change if phylogenies reveal that
the pattern of cladogenesis parallels the timing
of island formation, and if populations colonize
near to the time of island emergence (Bishop
and Hunt 1988, Tarr and Fleischer 1993, Givnish
et al. 1995, Fleischer et al. 1998).
We used this rationale to calibrate part of the
mitochondrial cytochrome b (cyt b) gene in Ha-
waiian drepanidines (Fleischer et al. 1998). The
overall rate of cyt b divergence, corrected for
minor saturation, transition bias, rate variation
among sites, and potential lineage sorting is
1.6% sequence divergence/Ma. This value is
similar to a rate we estimated for overall restric-
tion site divergence in mitochondrial DNA
(mtDNA) in drepanidines (--2%/Ma; Tarr and
Fleischer 1993). Note that rates calibrated using
this approach are based on a time period of di-
vergence up to only about 4 Ma. Recently,
Moore et al. (in press) showed through simula-
tion modeling that cyt b sequence divergence is
accurate as a predictor of time of divergence
only to about 5 Ma (i.e., about 10% overall se-
quence divergence). Predictions of dates older
than 5 Ma are generally underestimated. Nonlin-
earity of sequence divergence due to saturation
and rate variation among sites appears to be-
come problematic above about 10% overall se-
quence divergence for birds (Krajewski and
King 1996, Randi 1996, Moore and DeFilippis
1997). Thus the drepanidine or other cyt b rates
are not likely to be applicable to events that hap-
pened appreciably earlier than 5 Ma, and caution
must be exercised when making predictions or
calibrations from cyt b sequence divergences
over 10%.
Our drepanidine rates (Trot and Fleischer
1993, Fleischer et al. 1998) are within the range
of estimates for avian and mammalian taxa
based on calibrations derived from relatively re-
cent fossil evidence of cladogenesis. This is true
for both restfiction fragment length polymor-
phisms (RFLPs) in total mtDNA and sequence
divergence in the cyt b gene. Examples of avian
rates include RFLP variation in geese at --2%/
Ma (Shields and Wilson 1987); cyt b sequences
in partridges versus Gallus at 2.0%/Ma (Randi
1996; however, Arbogast and Slowinski [1998],
corrected the divergences using an HKY [Has-
egawa et al. 1985] model with a F-correction to
obtain a rate of about 5.0%/Ma); RFLP variation
in New World quail at 2.0%/Ma (reported in
Klicka and Zink 1997); woodpecker cyt b at
2.0%/Ma (Moore et al. in press); cyt b in cranes
at 0.7%/Ma for Balearicines versus Gruines (old
split) and up to 1.7%/Ma for comparisons within
the Gruines (Krajewski and King 1996); and cyt
b in albatross at 0.65%/Ma (Nunn et al. 1996,
recalculated for total sequence change in Klicka
and Zink 1997). In the crane and albatross stud-
ies the slower rates could be caused by the lon-
ger generation times in these species, or perhaps
by reduced metabolic rates in these larger-bod-
ied taxa (Martin and Palumbi 1993, Rand 1994,
Bromham et al. 1996, Nunn and Stanley 1998).
Alternatively, the difference may relate to the
fossil dates used for calibration: for both studies
these dates are older than 10 Ma, whereas for
all but the partridge/Gallus comparison (Randi
1996) the dates are before 5 Ma. Both studies
attempt to correct for saturation (Krajewski and
King 1996, Nunn et al. 1996), but may severely
underestimate divergence (Arbogast and Slow-
inski 1998). This could be considered an inverse
prediction of the findings of Moore et al. (in
press): using dates older than 5 Ma to calibrate
may result in an underestimate of the rate. Sup-
porting this is a negative correlation between di-
vergence times and divergence rates (Spearman
rho - -0.51, P - 0.042) from Table 2 of Martin
and Palumbi (1993). Avian rates are similar to
most mtDNA/cyt b rates calculated for mammal
taxa (e.g., --2%/Ma; Brown et al. 1979, Irwin et
al. 1991, Stanley et al. 1994, Janacek et al.
1996).
In general, then, calibrated rates of mtDNA
protein coding sequence divergence in birds and
mammals do not appear to vary greatly from
about 2%/Ma. Most rate variation appears to be
correlated with variation in body size and its
correlates (i.e., metabolic rate, generation time;
Martin and Palumbi 1993, Rand 1994), although
some of the variation may be due to differing
selective constraints on proteins in different lin-
eages or to fluctuations in population size (Ohta
1976). In summary, with the exception of the
very rapidly evolving control region (which in
some sections may be evolving an order of mag-
nitude faster than the average for mtDNA; e.g.,
Quinn 1992), most avian and mammalian rate
calibrations based on corrected mtDNA diver-
gence and dates before 5 Ma ago reveal rates at
about, or above, 2% divergence/Ma. Based on
the rather detailed rationale described above we
feel that mtDNA (RFLP or cyt b) sequence di-
vergence between a Hawaiian taxon and its clos-
est non-Hawaiian relatives that is below about
10% would indicate an origin near the time of
or after the formation of the island of Kaua'i.
HAWAIIAN BIRD MOLECULAR SYSTEMATICS--Fleischer and Mclntosh 55
ORIGINS AND EVOLUTION OF THE
HAWAIIAN AVIFAUNA
There were more than 102 species of native
breeding land- or waterbirds (i.e., non-seabirds)
in the Hawaiian Islands (Table 1; constructed
from James and Olson 1991, Olson and James
1991; and H. James, pers. comm.). These 102
species sort into six songbird families (Passeri-
formes) and seven non-songbird families (Table
1). Some families have a relatively large number
of species (i.e., >4) and, in some cases, it is
fairly clear that each group of species in a family
represents an in situ radiation from a single col-
onization (e.g., drepanidines, thrushes). it is
clear that in some families (e.g., anatids, rallids)
there has been more than a single colonization
event, while for others (e.g., corvids, meliphag-
ids) it is difficult to determine how many inde-
pendent colonization events have occurred.
Avian biologists working in the islands have
been fortunate to have an excellent Holocene
fossil record (Olson and James 1982a, 1991;
James and Olson 1991). Without this record, we
would be missing a tremendous amount of in-
formation about distributions, phylogeny, bio-
geography, and ecology of these birds. Even so,
additional fossil taxa continue to be discovered
and, thus, our knowledge remains incomplete.
The advent of genetic studies employing the
polymerase chain reaction (PCR) has opened a
new and exciting avenue for study of these fos-
sils. Our laboratory has had considerable success
amplifying mtDNA sequences from these sub-
fossil remains. Here we summarize what has
been learned about the evolution of Hawaiian
birds from phylogenetic analyses of mtDNA se-
quences from a number of extinct and extant
taxa.
EXTENSIVE RADIATIONS
The drepanidines (Hawaiian finches or hon-
eycreepers) are by far the most speciose group
in Hawai'i, with 33 species known from histor-
ical collections and more than 17 known from
subfossil remains (totaling over 50 species;
James and Olson 1991; H. James, pers. comm.).
The drepanidine radiation is remarkable for its
extreme morphological, ecological, and behav-
ioral diversity (Rothschild 1893-1900, Perkins
1903, Amadon 1950, Baldwin 1953, Raikow
1977, Pratt 1979, Freed et al. 1987a, James and
Olson 1991). However, major adaptive shifts ap-
pear to have modified many characters tradition-
ally used for phylogenetic reconstruction, while
others less subject to selection have been con-
served and provide little or no phylogenetic in-
formation. The somewhat chimeric associations
of morphological traits in the group have even
led to the suggestion that the drepanidines are
not monophyletic (Pratt 1992a,b). Molecular
data may prove especially useful for assessing
evolutionary relationships in this group, and
they do support a cardueline ancestry and, thus
far, monophyly of the drepanidines (Fleischer et
al. 1998; Fig. 2c).
Molecular data may also be effective in esti-
mating a time frame for the drepanidine radia-
tion. The radiation of the drepanidines would
seem quite deep based on their relative degree
of phenotypic diversity. Molecular evolutionary
rate estimates based on DNA-DNA hybridiza-
tion data (Sibley and Ahlquist 1982) are in sup-
port of this prediction with an estimated split of
drepanidines from a cardueline outgroup of
about 15-20 Ma. Molecular rate estimates from
both allozyme (Johnson et al. 1989, Fleischer et
al. 1998) and mtDNA data (Tarr and Fleischer
1993, 1995; Fleischer et al. 1998), however,
strongly contradict the results of Sibley and
Ahlquist (1982) and suggest a basal split that
began about 4 Ma ago and a separation from a
mainland cardueline ancestor (not necessarily
the closest outgroup; Fig. 2c) of <5-6 Ma ago.
These mtDNA results are based on several in-
ternal rate calibrations estimated as outlined
above for cyt b. Sibley and Ahlquist's (1982)
results may be biased by their use of continental
biogeographic points in their calibration (Quinn
et al. 1991) or by use of too distant outgroups
for comparison.
No other avian radiation in Hawai'i is so di-
verse in morphology or number of lineages as
the drepanidines. Extinct flightless rails, classi-
fied as Porzana (Olson and James 1991), in-
cluded perhaps more than 12 species, with as
many as three species on each major island. Un-
til recently it has not been clear whether these
species comprise a single highly radiated clade,
or represent a number of independent coloniza-
tions from mainland or other Pacific island
sources. Molecular phylogenetic analyses (B.
Slikas, S. Olson, R. Fleischer, unpubl. data) in-
dicate that each of the two historically collected
Porzana species resulted from independent col-
onizations. For Porzana palrneri the Kimura 2-
parameter corrected distance (Kimura 1980; dis-
tance and SE calculated in MEGA, Kumar et al.
1993) for 197 base pairs (bp) of ATPase8 was
2.1 ñ 1.1% distant from its closest non-Hawai-
ian Poraana relative. For P. sandwichensis the
ATPase8 Kimura 2-parameter corrected distance
was 5.9 +- 1.8% to its closest non-Hawaiian Por-
aana relative. Molecular analyses of Poraana
taxa known only from subfossil remains are un-
derway.
56 STUDIES IN AVIAN BIOLOGY NO. 22
Old World Ibises (9 spp.)
Spoonball
r-Glossy Ibis
It -white-faced Ibis (Piegaols)
I I Scarlet b s ,,
1 i__Whitelbls (Eudoc. mus)
L- -Lanai Flightless Ibis
.-----New World Ibises (5 spp )
Outgroups
b. I---Hawaiian Hawk, B. solitarius
71J i Galapagos Hawk, B. galapagoensis
(Buteo) -Swainsoh'S Hawk, B. swainsoni
H L--Short-tailed Hawk, B. brachyurus
9t -- Red-tailed Hawk, B. jamaicensis
94 L Old World Buteos (5 spp.)
I "Woodland" Buteo
I - Other Buteo/Parabuteo
L-- Buteogallus urlbltlnga
,-J69 Whlte-browed Rosefinch (Carpodacus thura)
,- [ -I'-'---'-.:._1 ............. House F,nch (C ........... ) Carduelini
' I I Green Honeycreeper (Chlorophanes splza)
' --I I Scarlet-rumped Tanager
r Ll. prnthnmer Tanager (P'rangaru ra) (Ramphøcetusp .......... )
J , j Prothonotary Warbler (Prolonoh'r,a C trea) Emberizinae
J , _ .b__. ____ Brown-headed Cowbird (Mololhrus ater)
Buff-barred Warbler (Phylloscopus pulcher)
: I Townsend's Sohtaire
'-L Ruf.-throated Sohtaire
.... [____"'1____ Omao Myadestes
-b____- Swainso n's Thrush
b Veery Catharus
............. d6y %'ru;R' '(''''i
e ! Dabbltng Ducks
ß ............ _S_o_u ?_ A_ _m _e r c_a_n_ D_ u_ c_k_s .......
--- Thambetochen
[ iL__ __'-___ __'TT2_ U _P?_i_o_c_h_e_n_ ...... _M_o_a
L Diving Ducks and relabves
I I Shelducks & Shelgeese
t "True" Geese & Swans
New World Jays
"OId World" Jays (+ Corvus rnonedula)
Corvus corax - Raven - Eurasia
Corvus corax - Raven - NA
Corvus hawaiiensis- Alala
Corvus corone- Hooded Crow
orvus brachyrhynchos - Amer, Crow1
orvus brachyrhynchos - Amer. Crow2
us kubaryi- Mariana Crow
ß Corvus tnstis - Grey Crow
FIGURE 2. Abbreviated phylogenetic reconstructions for six Hawaiian taxa. a. Summarized maximum parsi-
mony tree based on 407 nucleotide sites of 12s ribosomal RNA (A. Cooper, S. Olson, H. James, R. Fleischer,
unpubl. data). b. Summarized parsimony phylogram based on preliminary analysis of over 1500 bp of mtDNA
sequence (ATPase8, ND2, cyt b, and COI) in Buteo and related taxa (R. Fleischer, P. Cordero, C. Mcintosh, I.
Jones, and A. Helbig, unpublished). c. Summary of relationships of outgroups and drepanidines based on par-
simony analysis of 675 bp of cyt b sequence. d. Parsimony phylogram constructed from 700 bp of cyt b sequence
from two Myadestes and three Catharus taxa with '0ma'o and Turdus outgroup. e. Parsimony tree of two moa-
nalo genera and a wide sampling of other waterfowl taxa showing two moa-nalo genera to be sister taxa and
related to dabbling ducks. Tree is summarized from Sorenson et al. (1999), and based on over 1200 bp of
mtDNA sequence. f. Parsimony phylogram showing summary of jay relationships to Corvus and a sampling of
Corvus taxa based on 1008 bp of cyt b. The 'Alal is most closely related to the Common Raven.
MINOR RADIATIONS
Seven other Hawaiian avian groups have un-
dergone what appear to be minor radiations,
each with fewer than six species (Table 1).
These include thrushes (genus Myadestes), hon-
eyeaters (genera Moho and Chaetoptila), a lin-
eage of owls (genus Grallistrix), several crows
(genus Corvus), flightless ibises (genus Apteri-
bis), and two waterfowl (Anatidae) lineages:
true geese (genus Branta) and the highly modi-
fied dabbling duck relatives called "moa-nalos"
(genera Chelychelynechen, Ptaiochen, and
Thambetochen).
The five species of thrushes were placed orig-
inally in their own genus, Phaeornis, but were
considered aligned with solitaires (Myadestes;
Stejneger 1887, Amadon 1950), robins (Turdus)
or nightingale-thrushes (Catharus; Ripley 1962).
Most of the morphological and other evidence
(e.g., Kepler and Kepler 1983) clearly favors
placement of thrushes in Myadestes (Pratt 1982).
We analyzed variation in about 700 bp of the
cyt b gene of mtDNA (C. Mcintosh and R.
Fleischer, unpubl. data), for the Hawai'i Thrush
(or 'Oma'o, M. obscurus), three Catharus, two
American Myadestes and a Turdus species,
along with outgrou_p taxa. The resulting trees
clearly place the 'Oma'o within the Myadestes
clade, regardless of the tree building algorithm
(i.e., maximum parsimony, Fig. 2d; maximum
likelihood or minimum evolution). We could not
resolve with certainty using this data set whether
the '0ma'o is more closely related to M. geni-
barbis, a Caribbean solitaire, or M. townsendi of
western North America. The Kimura 2-parame-
ter corrected distance between the '0ma'o and
the solitaires is 6.7% for the 700 bp.
HAWAIIAN BIRD MOLECULAR SYSTEMATICS--FIeischer and Mcintosh 57
The meliphagid genera Chaetoptila (Kioea; 2
spp.) and Moho (the '(7)'6s; 4 spp.) may repre-
sent independent colonizations from south Pa-
cific meliphagids (Perkins 1903), although Mayr
(1943) considers both genera derived from a sin-
gle colonist. One species of Moho occurs on
each of Kaua'i, O'ahu, Maul Nui (Maui, Lana'i,
Moloka'i, and Kaho'olawe), and Hawai'i, and
this well-differentiated lineage (Pratt 1979) may
provide an opportunity to estimate a rate cali-
bration. The closest sister groups for the Ha-
waiian meliphagids are unknown, with some au-
thors suggesting Gymnomyza of Fiji and Samoa
(e.g., Mayr 1943) and others favoring Foulehaio
of Samoa or the New Zealand tui's (Prosthe-
madera; e.g., Munro 1944, Pratt 1979). Molec-
ular studies are underway to address the origin
and monophyly of the Hawaiian forms and the
possibility of a rate calibration from the four
Moro species. A calibration could be used to
estimate the date of separation from the most
recent common ancestor. This date is important
because we estimate from our drepanidine cali-
brations that nectarivorous drepanidines evolved
only 2-3 Ma ago, while Givnish et al. (1995)
used a calibration of chloroplast DNA restriction
fragment variation to estimate that bird-pollinat-
ed flowering lobeliads (genus Cyanea) evolved
8-17 Ma ago. Thus it is highly unlikely that dre-
panidines "coevolved" with these plants in the
islands (as was suggested by Givnish et al.
1995). The meliphagids are the only other
known native, obligate nectarivores in the is-
lands and, if they are older, could be the coe-
volved taxon.
At least four crows (Corvus) occurred in the
islands (James and Olson 1991; H. James, pets.
comm.). Three of these are known only from
subfossils; two of which have been described
and the fourth is the highly endangered Hawai-
ian Crow (Corvus hawaiiensis), hereafter re-
ferred to as 'Alala. It is unclear at present wheth-
er these represent a single colonization and sub-
sequent radiation, or multiple colonizations by
the same or different ancestral taxa (James and
Olson 1991). Preliminary phylogenetic analyses
of the 'AlMa and seven other Corvus taxa indi-
cate that it is more closely related to the Com-
mon Raven (Corvus corax) than to more typical
crows, including two South Pacific island crows
(R. Fleischer and C. Mcintosh, unpubl. data;
Fig. 2f). The Kimura 2-parameter corrected se-
quence divergence for 1,008 bp of cyt b between
'AlMa and North American Common Raven is
about 8.4 + 1.0%.
Subfossil bones and owl pellets are all that
remain of four species of long-legged owls
(Grallistrix) that apparently were morphologi-
cally adapted to feeding on birds. While no
DNA analyses have yet been made on this
group, it appears likely that they represent the
results of a single colonization and subsequent
minor radiation.
At least four lineages of waterfowl have col-
onized the Hawaiian Islands. Of these, only two,
the moa-nalos (Olson and James 1991, Sorenson
et al. 1999) and the modern geese (Branta; Ol-
son and James 1991, Paxinos 1998; E. Paxinos
et al. unpubl. data), have speciated beyond a sin-
gle endemic species. All of the moa-nalos
evolved to very large size, flightlessness, and
highly modified cranial morphology. They have
become convergent in morphology to rafites in
terms of postcranial morphology, and one spe-
cies in particular has converged to tortoise-like
cranial morphology. Like the moas of New Zea-
land (Darwin 1859), the moa-nalos occupied a
grazing mammal or tortoise niche (Olson and
James 1991). One genus and species (Chelyche-
lynechen quassus, the Turtlejawed Goose) is re-
stricted to Kaua'i and one (Ptaiochen) to Maui,
but Thambetochen is found on both Maui Nui
and O'ahu, suggesting the genus may have orig-
inated on O'ahu and later walked across the Pen-
guin Bank land bridge (Fig. 1) to Moloka'i. No
moa-nalo is known from the young island of Ha-
wai'i (but see below).
Olson and James (1991) suggested that the
moa-nalos were related to either dabbling ducks
or shelducks (tadornines) on the basis of skeletal
characters, primarily the presence and shape of
their syringeal bullae. Livezey (1996) tentatively
concluded from a cladistic analysis of morphol-
ogy that the moa-nalos were sister to a "true"
geese and swan clade, and not to anatids. Mi-
tochrondrial DNA analyses for two of the three
genera (Thambetochen and Ptaiochen; Sorenson
et al. 1999) have provided a phylogenetic hy-
pothesis and estimates of minimum genetic di-
vergence from anatid outgroups. The two genera
form a well-supported clade that is itself sister
to the "dabbling" ducks, although perhaps
somewhat more similar to several South Amer-
ican Anas or Anas relatives than to North Amer-
ican dabblers (Fig. 2e). Molecular data do not
support a close relationship with either tadorni-
nes or true geese. The distance between the
moa-nalos and their closest anatid outgroup,
based on 1,009 mtDNA sites, is 6.9 _+ 0.5%.
The Nn or Hawaiian Goose (B. sandvicen-
sis) is the only extant representative of what ap-
pears to be a minor radiation of Branta in the
islands (Olson and James 1991, Paxinos 1998;
E. Paxinos et al., unpubl data.). Nene are clearly
derived from Canada Geese (B. canadensis;
Quinn et al. 1991), and distances based on
mtDNA restriction fragment and cyt b sequence
data suggest that the two taxa shared a common
58 STUDIES IN AVIAN BIOLOGY NO. 22
ancestor sometime within the past 1 Ma (Quinn
et al. 1991). At least two, and probably more
than three additional Branta species existed in
the islands (Olson and James 1991, Paxinos
1998; E. Paxinos et al., unpubl. data). One of
these, the "very large Hawai'i goose" is the
largest land vertebrate known from Hawai'i and
is restricted in distribution to the island of Ha-
wai'i (Giffin 1993). The species is highly mod-
ified morphologically with a massive body,
short, stout wings (it was flightless, but may
have used its wings for fighting; S. Olson, pets.
comm.); and cranially quite similar to the moa-
nalos. In fact, it appears to be a superb example
of convergent evolution to the moa-nalos. Mi-
tochrondrial DNA sequence analyses (Paxinos
1998) strongly support placement of the very
large Hawaiian goose Branta and also indicate
a sister taxon relationship with the Nene and its
close, larger relative, B. hylobadistes.
Two species of ibis (Apteribis) have been de-
scribed from subfossil material (Olson and Wet-
more 1976, Olson and James 1991). Apteribis
had stouter legs and shorter wings than other
ibises and were flightless. The two or more spe-
cies were limited to Maul Nui, and the discon-
nection of Maul, Lana'i, and Moloka'i 0.3-0.4
Ma ago may have initiated the speciation
event(s). Analyses of mitochondrial 12S ribo-
somal DNA sequences of Apteribis and 21 other
ibis species (Fig. 2a; A. Cooper, S. Olson, H.
James and R. Fleischer, unpubl. data) indicate
that the closest sister taxon to Apteribis is the
New World White Ibis (Eudocimus albus). The
Kimura 2-parameter pairwise distance between
the two taxa for 407 bp of 12S rRNA sequence
is 3.2 _+ 1.0%.
SINGLE DIFFERENTIATED SPECIES
Two raptors, a duck, and two songbirds rep-
resent single differentiated species. These taxa
apparently colonized the islands and differenti-
ated considerably from their ancestors but did
not undergo subsequent speciation. The two rap-
tors are the endangered Hawaiian Hawk or 'Io
(Buteo solitarius) and an extinct accipiter-like
harrier (Circus dossenus). The 'Io is currently
restricted to the island of Hawai'i but has been
found in fossil form on other islands (Olson and
James 1991; S. Olson, pers. comm.). Like many
other species of Buteo, the 'Io exhibits a light
and a dark color morph. Preliminary phyloge-
netic analyses of more than 1,500 bp of mtDNA
sequence in 18 species of Buteo (R. Fleischer, E
Cordero, C. Mcintosh, I. Jones, and A. Helbig,
unpubl. data) provides weak support for a clade
containing the 'Io, the North American Short-
tailed Hawk (Buteo brachyurus; to which it is
least divergent; Fig. 2b), the North American
Swainson's Hawk (Buteo swainsoni; as suggest-
ed by Mayr 1943), and the endemic Galpagos
Hawk (Buteo galapagoensis). The 'Io does not
have a close relationship with any Old World
Buteo we assessed. The Kimura 2-parameter
(Kimura 1980) corrected sequence divergence
from Buteo brachyurus is only 1.4 + 0.8% for
part of cyt b. We have no molecular data for the
extinct and highly modified Circus.
The Laysan Duck (Arias laysanensis) is a rel-
atively differentiated, small duck whose very
small and vulnerable wild population inhabits
only the tiny leeward island of Laysan. It has
been consistently classified as either a subspe-
cies of the Hawaiian Duck (Arias wyvilliana),
hereafter referred to as Koloa, or of the Mallard
(Arias platyrhynchos) on the basis of morphol-
ogy and allozyme data (see Amadon 1950, Liv-
ezey 1991, Browne et al. 1993). Recent DNA
analyses (Cooper et al. 1996; J. Rhymer, unpubl.
data), however, have strongly countered the
above scenarios, indicating instead that the Lay-
san Duck is differentiated from the Koloa and
Mallard and may be more closely aligned with
the South Pacific Black Duck (Arias supercilio-
sa) clade. The Koloa, on the other hand, does
cluster closely with the North American Mallard
or Mottled Duck (Arias fulvigula) clades. Anal-
yses of mitochondrial control region sequences
of subfossil bones (Cooper et al. 1996) have also
revealed that the Laysan Duck occurred in the
main Hawaiian Islands well into the period of
Polynesian settlement, and in forested habitats
and higher elevations (> 1,500 m) not considered
typical for a dabbling duck. The level of mito-
chondrial control region sequence divergence
between the Laysan Duck and its closest out-
group taxon is about 10%; overall mtDNA di-
vergence is lower than this (J. Rhymer, unpubl.
data).
The fourth "nonradiating" species, the 'Ele-
paio (Chasiempis sandwichensis), is polytypic at
the subspecies level and occurs on the islands of
Kaua'i, O'ahu, and Hawai'i (enigmatically, no
fossils have been found of this species on Maul
Nui; James and Olson 1991). The 'Elepaio is
likely related to Polynesian flycatchers in the ge-
nus Monarcha (Mayr 1943, Amadon 1950) and
is one of the few species for which differentiated
subspecies have been identified on a single small
island (Hawai'i; Pratt 1980). Molecular analyses
of each island subspecies may, however, reveal
differentiation sufficient to elevate them to spe-
cies level.
PROBABLE RECENT COLONIZATIONS
Several taxa show little phenotypic diver-
gence from mainland outgroups, suggestive of a
very recent colonization (Table 1). These in-
HAWAIIAN BIRD MOLECULAR SYSTEMATICS--Fleischer and Mcintosh 59
clude the Black-necked Stilt (Himantopus mex-
icanus knudseni), Hawaiian Coot (Fulica alai),
Common Moorhen (Gallinula chloropus sand-
vicensis), Koloa, Black-crowned Night Heron
(Nycticorax nycticorax hoactli), an eagle (Hal-
iaeetus), and the Short-eared Owl. Of these, only
the Black-crowned Night Heron is not currently
considered to be distinct from mainland forms
at the subspecies or species levels, but the Short-
eared Owl, in spite of its subspecific designation,
is thought to be a post-Polynesian colonist (Ol-
son and James 1991).
The Common Moorhen, Hawaiian Coot,
Black-crowned Night Heron, and Short-eared
Owl are extremely similar morphologically to
outgroup relatives (Amadon 1950), but no DNA
data currently exist with which to assess the age
of their splits. As noted above, the Koloa is a
very close relative of the Mottled Duck and
Mallard (<3% mitochondrial control region di-
vergence; Cooper et al. 1996). The endemic sub-
species of the Black-necked Stilt differs from
North American Black-necked Stilts (H. m. mex-
icanus) by only about 1.5 + 0.6% sequence di-
vergence in 447 bp of mtDNA control region (R.
Fleischer et al., unpubl. data). The North Amer-
ican Black-necked Stilts are considered to be the
closest mainland relatives on the basis of mor-
phology. Cyt b and 12S rRNA sequences from
a subfossil bone of the extinct eagle (Haliaeetus
sp.; Fleischer et al. 2000) are not different from
the Old World White-tailed Eagle (H. albicilla),
and the two species differ by 1.5% for the ATP-
ase8 gene. Skeletal characteristics could not dif-
ferentiate the Hawaiian eagle bones from either
White-tailed Eagle or Bald Eagle (H. leucoce-
phalus; Olson and James 1991). Thus, for at
least three of these seven taxa the supposition of
a recent split from a mainland ancestor and re-
cent arrival in the islands is supported by the
molecular data.
SUMMARY: GEOGRAPHIC ORIGINS AND
TEMPORAL FRAMEWORK
Above we summarize recent molecular sys-
tematic studies of the Hawaiian avifauna. We
use these data to infer, if possible, the closest
living relatives and the geographic origins of the
Hawaiian taxa we sampled. Our biogeographic
analyses indicate (Table 1) that at least 9 or 10
of the --> 21 independent lineages appear to be
of North American or at least Western Hemi-
sphere origin, 4 appear to be of South Pacific or
Australasian origin, 2 or 3 are of Asian origin,
and 5 are of currently unknown geographic or-
igin. Thus Mayr's (1943) conclusion that about
half the Hawaiian avifauna is of American origin
is still supported by our molecular data.
We found a relatively low level of molecular
divergence between the Hawaiian taxa and their
closest non-Hawaiian (mostly mainland) rela-
tives (i.e., from zero to 10.3% sequence diver-
gence for 14 lineages). Based on these results,
none of these Hawaiian lineages split from
mainland ancestors earlier than about 6.4 Ma. In
fact, most of our estimates, although rough and
lacking meaninglhl standard errors, fall well
within the period of formation of the current set
of main islands (i.e., Kaua'i at 5.1 Ma and later,
Fig. 1). Only the drepanidines (10.3%), the
corvids (8.4%), and perhaps the moa-nalos
(6.9%) and the thrushes (6.7%) have Kimura 2-
parameter sequence divergences from mainland
relatives that suggest colonization prior to even
the formation of O'ahu (3.7 Ma), and in each of
these cases we may not have obtained sequence
for the closest mainland outgroup (which we
may not have sampled or it might be extinct).
The overall picture suggests that while native
Hawaiian Drosophila (Beverley and Wilson
1985, Thomas and Hunt 1991, DeSalle 1992,
Russo et al. 1995) and lobeliads (Givnish et al.
1995) may have colonized the archipelago well
before the formation of Kaua'i, thus far we have
little evidence that any bird lineages have done
SO.
These findings lead us to consider factors be-
yond simple isolation by distance and the an-
thropogenically induced Holocene extinction
that may help to explain Hawai'i's low primary
avian diversity. First, the unique geology of the
islands (Carson and Clague 1995) results in a
situation in which individual islands have a lim-
ited "lifespan" (--5-7 Ma) as a high island. Lin-
eages that have colonized older islands, but for
some reason cannot succeed onto younger is-
lands, will be ultimately lost as their island dis-
appears into the sea (this may be especially true
for forms that have evolved to be flightless).
There may be reduced chance for taxonomic di-
versity to build up over long evolutionary peri-
ods relative to archipelagos with longer surviv-
ing islands. Secondarily, what secondary enrich-
ment of avifaunal lineages by speciation that
does occur in the islands may allow "niches" to
be filled (perhaps by now locally adapted taxa)
such that they are no longer available for occu-
pation by new (and not locally adapted) colo-
nists from elsewhere. Thus, primary diversity
could be reduced by competitive exclusion.
Continued paleontological research in the is-
lands combined with studies of DNA sequence
variation should help us to address these hy-
potheses. We hope these new fossils and se-
quences will continue to shed light on the sys-
tematics, biogeography, and timescale of avian
evolution on the Hawaiian conveyor belt.
60 STUDIES IN AVIAN BIOLOGY NO. 22
ACKNOWLEDGMENTS
We thank C. Tarr, S. Olson, H. James. E. Paxinos,
A. Cooper, B. Slikas, J. Rhymer, B. Arbogast, S. Co-
nant, M. Sorenson, T. Quinn, A. Helbig, I. Jones, A.
Driskell, and T. Pratt for information concerning and
discussion of many of the topics covered in this paper,
and C. Tart, B. Slikas, J. M. Scott, reviewer #1, and
especially H. James for comments on an earlier draft
of the manuscript. Samples for many of our analyses
were provided by museum or field collections of tis-
sues and we gratefully acknowledge the cooperation of
C. Kishinami and A. Allison (B. P. Bishop Museum),
S. Conant (University of Hawai'i), E Sheldon (Loui-
siana State University), M. Robbins and B. Slikas
(Academy of Natural Sciences-Philadelphia), P. Bruner
(Brigham Young University-Hawai'i), E. Bermingham
(Smithsonian Tropical Research Institute), S. Olson, P.
Angle, and M. Braun (U.S. National Museum), R.
Cann (University of Hawai'i), S. Rowher and S. Ed-
wards (Burke Museum), and C. Cicero (Museum of
Vertebrate Zoology-Berkeley). We greatly appreciate
permission from Dave Swofford to use PAUP* (a gem
of a program). Funding for many of the results pre-
sented above was provided by the Smithsonian Insti-
tution Scholarly Studies Program, Friends of the Na-
tional Zoo, U.S. National Science Foundation, U.S.
Fish and Wildlife Service, the National Geographic
Society, and the Biological Resources Division of the
U.S. Geological Survey.
Studies in Avian Biology No. 22:61-67, 2001.
EVOLUTIONARY RELATIONSHIPS CONSERVATION
OF THE HAWAIIAN ANATIDS
JUDITH M. RHYMER
Abstract. The Hawaiian Duck or Koloa Maoli (Arias wyvilliana), hereafter retErred to as Koloa, and
Laysan Duck (A. laysanensis) are two endangered species of waterfowl in the mallard complex that
are endemic to the Hawaiian lslands. These nonmigratory, nondimorphic species were thought to be
derived from stray migratory, sexually dimorphic common Mallards (A. platyrhynchos), that subse-
quently lost the dimorphic plumage character. Laysan Ducks currently occur only on the tiny island
of Laysan, while Koloa are found on O'ahu, Hawai'i, and, primarily, Kaua'i. Recent ancient DNA
analysis shows that subfossil bones in deposits on the Big lsland, Hawai'i, belong to the extant Laysan
Duck. Similar fossils have been found on many of the major Hawaiian Islands, indicating that the
species was formerly more widespread. Because of extensive hybridization between introduced Mal-
lards and Koloa and the superficial morphological similarity between the Hawaiian taxa, their taxo-
nomic status and phylogenetic relationships have been controversial. The perception that they may be
subspecies of the Mallard, or even conspecific, has influenced their recovery programs. Molecular
analyses indicate that Koloa and Mallard are distinct but very closely related species, whereas the
Laysan Duck is very distinct from either. Some of the nondimorphic species in the mallard complex,
such as the Laysan Duck, may have evolved from a nondimorphic ancestor rather than the common
Mallard. Repeated bottlenecks, inbreeding, and small population size have likely contributed to a loss
of genetic variation in the Laysan Duck, but it is now possible to plan a captive breeding program to
preserve remaining variation for possible reintroduction of the species to other previously occupied
Hawaiian Islands. Hybridization with Mallards is one of the factors contributing to the decline of
Koloa on O'ahu and Hawai'i. The Kaua'i population represents a stronghold for the species, but
thorough census data and basic information on the ecology of Koloa on Kaua'i, essential for devel-
oping a specific conservation plan, are not available.
Key Words: Arias laysanensis; Arias platyrhynchos; Arias wyvilliana; ancient DNA; hybridization;
molecular phylogeny; reduced genetic variation; species limits.
The Laysan Duck (Anas laysanensis) and Ha-
waiian Duck or Koloa Maoli (A. wyvilliana),
hereafter referred to as Koloa, are endangered
species of waterbirds endemic to the Hawaiian
Islands. Laysan Ducks are restricted to the tiny
370 ha island of Laysan in the northwestern Ha-
waiian chain. They survived a severe bottleneck
in the early part of the century, as their popu-
lation was estimated to have plummeted to fewer
than 10 individuals by 1911 (Moulton and Wel-
let 1984). This precipitous population decline
was caused by overhunting and by habitat de-
struction by introduced rabbits. A ban on hunt-
ing plus extermination of the rabbits allowed
numbers of Laysan Duck to rebound to about
500 birds over the next few decades, but a se-
vere drought in 1993 reduced the population to
fewer than 150 individuals (Cooper et al. 1996),
an indication of the extreme vulnerability of this
species. Harsh environmental conditions on Lay-
san Island likely represent less than optimal hab-
itat for the Laysan Duck.
Recent analysis of DNA isolated from late
Holocene subfossils, found in lava tubes in for-
ested habitats at elevations as high as 1,800 m
on Hawai'i, indicates that they are Laysan Duck
(Fig. 1), an indication that the species was once
found elsewhere in the Hawaiian Islands (Coo-
per et al. 1996). Similar subfossil anatid speci-
mens found on O'ahu, Kaua'i, and Moloka'i
suggest that the range of Laysan Ducks was
once more widespread. This situation is not
unique: remains of over 30 other, now extinct,
passerine and nonpasserine avian species of late
Holocene age have also been found on Kaua'i,
O'ahu, Moloka'i, Maul, and Hawai'i (James and
Olson 1991, Olson and James 1991). These pre-
historic avian extinctions are attributed primarily
to predation by Polynesians and introduced
predators and to habitat destruction (Olson and
James 1991). It may be possible to reintroduce
Laysan Ducks to other islands, provided preda-
tors such as rats, mongoose, feral cats, and dogs
are controlled and wetland and upland nesting
habitats are protected.
Koloa once occurred on all the major islands
in the lower Hawaiian chain except Lfina'i and
Kaho'olawe (Griffin et al. 1989). The only sub-
stantial population is now found on the island of
Kaua'i, in montane areas and on the Hanalei Na-
tional Wildlife Refuge. There are a few birds on
O'ahu, but hybridization with introduced com-
mon Mallards (A. platyrhynchos) is a serious
problem there (Browne et al. 1993). The total
population of Koloa has been roughly estimated
at 2,500 birds, (2,000 on Kaua'i-Ni'ihau, 300 on
O'ahu, 25 on Maui and 200 on Hawai'i; Engilis
and Pratt 1993), but in reality, there are few
61
62 STUDIES IN AVIAN BIOLOGY NO. 22
lOO
A. laysanensis
Subfossil 1
Subfossil 2
63
99 A. platyrhynchos 2
I I A. wyvilliana1
73 A. wyvilliana 2
A. platyrhynchos I
A. sparsa
I I I I I
0.12 0.09 0.06 0.03 0
Kimura's 2- Parameter Corrected Distance
FIGURE 1. Neighbor-joining tree obtained with MECA, based on Kimura's 2-parameter corrected distances
using mtDNA control region sequences (after Cooper et al. 1996). Bootstrap values are shown. Sequences from
Holocene subfossils are compared to those of extant Hawaiian anatids.
good data from which to estimate their current
population size. Surveys do not cover montane
streams and wetlands where most birds reside.
In fact, little is known about their breeding ecol-
ogy, reproductive success, movements, and an-
nual habitat requirements. Specific conservation
action has been limited, except for sporadic re-
leases of captive-reared birds on O'ahu, Maul,
and Hawai'i, which have had marginal success.
Current recovery plans call for wetland protec-
tion and management and removal of the threat
of hybridization (USFWS 1985). Management
will include water level control, predator con-
trol, minimizing disturbance, improved census
techniques, and monitoring of contaminants and
avian disease.
The Laysan Duck and Koloa are thought by
some to be derived from perhaps two waves of
stray migratory Mallards that became isolated
on the Hawaiian Islands and subsequently lost
the Mallard's sexually dimorphic plumage (Wel-
ler 1980). They represent 2 of 14 closely related,
nonmigratory, sexually nondimorphic species
and subspecies in the worldwide mallard com-
plex of waterfowl. The taxonomic status of
many species in this complex has been contro-
versial (e.g., Johnsgard 1961, Palmer 1976,
Young and Rhymer 1998), and the specific sta-
tus of Laysan Ducks and Koloa are no exception
(Weller 1980). Detailed morphological analysis
of the genus Anas by Livezey (1991) placed wy-
villiana and laysanensis as sister species within
a northern hemisphere mallard clade, not supris-
ing given their close geographic distribution and
small body size; they are about one-half to two-
thirds the size of common Mallards. Livezey
(1991) considered them to be lull species, as did
Berger (1972) and the American Ornithologists'
Union (AOU 1983). In other studies, their status
has variously been described as (1) both Laysan
Duck and Koloa as subspecies of the Mallard
(Delacour and Mayr 1945, Johnsgard 1978, Wel-
ler 1980); (2) Koloa as a subspecies of Mallard,
but Laysan Duck as a full species (Ripley 1960);
(3) Koloa as a full species with Laysan Duck as
a subspecies of Koloa (Brock 1951b, Griffin et
al. 1989); and (4) Laysan Duck as a full species
that evolved from Koloa (Warner 1963).
Three issues have been raised that have im-
portant implications for conservation of the Lay-
san Duck and Koloa: (1) recognition of species
limits--are the Laysan Duck and Koloa distinct
species from one another and from the common
Mallard and, therefore, more worthy of protec-
tion? (2) hybridization with introduced spe-
cies-what is the extent of hybridization with
introduced Mallards and is it a possible threat to
the species' integrity of Koloa? (3) loss of ge-
netic variation--have small population size and
population bottlenecks led to a loss of genetic
variation in Koloa and Laysan Duck? These is-
sues are addressed using molecular genetic anal-
yses of mitochondrial and nuclear DNA.
METHODS
MOLECULAR ANALYSIS
As part of a larger study of phylogenetic relation-
ships in the mallard complex of species, blood and/or
muscle or heart tissue samples were collected from
common Mallard (North America, N = 28; Europe, N
HAWAIIAN ANATID CONSERVATIONsRhymer 63
20); Koloa (Kaua'i, N = 19), Laysan Duck (foun-
ders of captive flock, Smithsonian Conservation Re-
search Center, N 15), African Black Duck (A.
sa), the nondimorphic sister species to the mallard
complex (Cooper et al. 1996, Johnson and Sorenson
1998, J. Rhymer, unpubl. data; captive flock, Wildlife
Preservation Trust, N = 1); and Green-winged Teal (A.
crecca; N = 2) as an outgroup (Johnson and Sorenson
1998). DNA was isolated from each sample using stan-
dard procedures (Rhymer et al. 1994).
Mitochondrial DNA (mtDNA )
The two most variable domains of the mitochondrial
control region (631 base pairs, bp, from the 5' and 3'
regions) were amplified using primers developed for
waterfowl (Cooper et al. 1996). DNA sequencing was
done on an ABI automated sequencer (model 373A)
and sequences were aligned using Geneworks ©
(lntelliGenetics, Inc.) and by eye.
Single-copy nuclear DNA (scnDNA)
Five lg of DNA from each individual were digested
with l0 enzymes that recognize six-base sequences.
Fragments in digested samples were separated on
0.7%-1.2% agarose gels and transfered to nylon mem-
branes (MSI Magnagraph) via Southern (1975) blot-
ting. One arian oncogene, v-myc (Alitalo et al. 1983)
and five anonymous single-copy nuclear DNA (scn-
DNA) clones were used as probes, for a total of 30
probe/enzyme combinations. Anonymous scnDNA
clones were obtained using standard procedures
(Quinn and White 1987a, Parsons et al. 1993). Two
hundred ng of probe were labeled with 32p for each
hybridization, and membranes were then exposed to
Kodak XAR film for 24-72 hours.
Amplified fragment length polymorphisms (AFLP)
The amplified tragment length polymorphisms
(AFLP) technique is based on the detection of genomic
restriction fragments by polymerase chain reaction
(PCR) amplification, which produces fing.erprints with-
out prior sequence knowledge (Vos et al. 1995). Pro-
tocols provided with the AFLP © Analysis System I
and AFLP Starter Primer Kit (GibcoBRL) were fol-
lowed. Briefly, this includes an initial restriction di-
gestion of 150 ng genomic DNA with EcoR I and Mse
I, followed by ligation of EcoR I and Mse I adapters,
amplification of the restriction fragments, labeling of
an EcoR I primer with [3,3P]ATP, reamplification with
the labeled EcoR I primer and an Mse I primer, and
separation of labeled, amplified fragments on a 6.0%
denaturing polyacrylamide sequencing gel. Primers
used were EcoR I (AAG) with Mse I (CAG), and EcoR
I (AA) with Ma'e I (CAA).
DNA ,fingerprinting with minisatellites.
Five lg DNA were digested with Hae III, fragments
were separated on agarose gels, and were then trans-
fenced to nylon membranes via Southern blotting using
standard procedures (Loew and Fleischer 1996). Mem-
branes were hybridized with 32p labeled Jeffrey's 33.15
minisatellite probe and exposed to Kodak XRP-1 x-
ray film for 24 hours.
STATISTICAL ANALYSES
Phylogenetic relationships using mitochondrial
DNA control region sequences were estimated using
maximum parsimony (PAUP 3.1.1; Swofford 1993)
and the neighbor-joining algorithm (Saitou and Nei
1987) with Kimura's 2-parameter model (MEGA 1.01;
Kumar et al. 1993). One thousand bootstrap replica-
tions were performed to estimate robustness of tree
topologies and decay indices (the number of additional
steps in the shortest tree(s) without a given node) were
also calculated (Bremer 1988). For AFLPs, alleles at
polymorphic loci were scored as 1 (present) or 0 (ab-
sent), and the resulting data matrix was also analyzed
using maximum parsimony. A strict consensus of most
parsimonious trees was calculated.
For scnDNA data, genetic distances were estimated
for each pair of species according to Nei's (1987)
method for unmapped fragment data, using the anal-
ysis package RESTSITE (vl.1; Nei and Miller 1990),
which allows for the inclusion of multiple individuals
of each taxon analyzed with several probe/enzyme
combinations. Relationships among species were esti-
mated using the neighbor-joining method. Data were
not available for an outgroup for either AFLP or
scnDNA analyses.
Two methods were used to estimate genetic diver-
sity within species. First, band-sharing coefficients
were calculated from Jeffrey's 33.15 minisatellite
DNA data, comparing unrelated individuals of Mal-
lards (N = 5), Koloa (N = 5), and Laysan Ducks (N
5) on the same gel. Second, proportion of polymor-
phic loci (P) were calculated for each species using
AFLPs, as the number of loci at which the most com-
mon allele had a fYequency of less than 0.95 divided
by the total number of individuals in the sample.
RESULTS
RECOGNITION OF SPECIES LIMITS
Phylogenetic analysis of mtDNA control re-
gion sequences indicate that there are two di-
vergent lineages of common Mallards in the
world (Figs. I and 2), one that has a Holarctic
distribution (Mallard 1) and one that is appar-
ently found only in North America (Mallard 2;
Young and Rhymer 1998). The Koloa is very
closely related to the Mallard, particularly lin-
eage 2 (as are the other North American non-
dimorphic mallard species, the Mottled Duck, A.
fulvigula, and American Black Duck, A. rubri-
pes; J. Rhymer, unpubl. data). Divergence of
Laysan Duck from the Koloa/Mallard clade is
well supported (Fig. 2).
The occurrence of two divergent mtDNA
Mallard lineages suggests either retention of an
ancestral polymorphism or hybridization among
taxa in North America. One of the problems that
can arise from analysis of maternally inherited
mtDNA is the possibility that the gene tree is
not congruent with the species phylogeny (Arise
et al. 1990). This possibility prompted analysis
of biparentally inherited nuclear DNA molecular
markers (scnDNA and AFLPs) to determine if
64 STUDIES IN AVIAN BIOLOGY NO. 22
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14
-- A. platyrhynchos I
99 I A. platyrhynchos 2
8
A. wyvilliana
--A. laysanens
A. sparsa
A. crecca
FIGURE 2. Single most parsimonious tree obtained
with PAUP 3.1.1, relating mitochondrial control region
sequences for A. platyrhynchos, A. wyvilliana, A. lay-
sanensis and A. sparsa (length = 127, CI excluding
uninformative characters 0.73, RI = 0.70). Tree
rooted with A. crecca as an outgroup. Branch lengths
are proportional to the number of inferred changes
along each branch. Decay indices are shown below
each node; bootstrap values are shown above
relationships among species suggested by the
mtDNA results would be upheld. Only one lin-
eage of Mallards was found at the nuclear level
and both nuclear DNA datasets support the very
close relationship between the common Mallard
and the Koloa (Figs. 3 and 4). The divergence
between Laysan Duck and Koloa was also high-
ly repeatable, regardless of the nuclear DNA
method employed.
HYBRIDIZATION WITH INTRODUCED SPECIES
Based on morphology, many of the Koloa-like
birds on O'ahu appear to be hybrids. However,
hybrid individuals are increasingly difficult to
identify morphologically after more than one or
two generations of backcrossing to one of the
parental species (e.g., Rhymer et al. 1994). Mo-
lecular methods provide an unambiguous as-
sessment of the extent of hybridization and in-
trogression between species. One putative Ko-
loa/Mallard hybrid has been analyzed with
mtDNA and nuclear markers so far. This indi-
vidual was phenotypically similar to Koloa but
possessed a Mallard 2 mitochondrial haplotype.
Analysis of nuclear DNA using AFLPs indicates
that the hybrid is indistinguishable from Koloa
(Fig. 4). These data suggest that the hybrid in-
dividual was not an F1 but a backcross into the
Koloa. Further, because mtDNA is inherited
only from the female parent, whereas AFLP loci
are biparentally inherited, these data also indi-
cate that the initial cross involved a female Mal-
lard hybridizing with a male Koloa.
Loss OF GENETIC VARIATION
There is considerably less mtDNA haplotype
diversity in both Hawaiian and Laysan Ducks
than in the Mallard. Five to ten haplotypes (with
minor changes) have been found in each of the
two Mallard lineages (Avise et al. 1990; J. Rhy-
mer, unpubl. data), whereas only two haplotypes
are found in the Koloa and one in Laysan Duck
(Fig. 1). Analyses of minisatellite DNA and
AFLPs also indicate an apparent loss of varia-
tion in Laysan Ducks (Table 1). Average num-
bers of scorable bands for the Jeffrey's 33.15
probe were similar for Mallards and Koloa but
much reduced in Laysan Ducks. Similarly, band-
sharing coefficients for Mallards and Koloa are
within the range (0.2-0.5) for unrelated individ-
uals in outbred avian populations (Haig and Av-
ise 1996), while those for unrelated Laysan
A. platyrhynchos
I A. wyvilliana
A. laysanensis
i I I I I I I
0.007 0.006 0.005 0.004 0.003 0.002 0.001 0
Genetic Distance (Nei 1987)
FIGURE 3. Neighbor-joining tree obtained with RESTSITE 1.1, based on scnDNA data using Nei's (1987)
distances for unmapped restriction sites for A. platyrhynchos, A. wyvilliana, and A. laysanensis
HAWAIIAN ANATID CONSERVATION--Rhymer 65
wyvilliana 2
wyvilliana 2
wyvllliana 2
wyvilliana 1
wyvilliana x platyrhynchos 2
wyvllliana 1
wyvilliana 2
wyvilllana 1
wyvilliana 1
wyvilliana 1
wyvilliana 1
wyvllliana 2
wyvilllana 2
platyrhynchos 1
platyrhynchos 2
laysanansis
laysanensia
laysanansis
laysanensis
laysanensis
laysanensls
laysanensis
FIGURE 4. Strict consensus of 53 most parsimonious trees relating variation in AFLP loci of the two Mallard
mtDNA lineages (platyrhyncos 1 and 2), Koloa (wyvilliana 1 and 2 refer to mtDNA haplotypes), and Laysan
Duck (laysanensis). Several individuals are included to illustrate variation within and among taxa. One putative
Koloa x Mallard hybrid with a Mallard 2 mtDNA haplotype clusters with Koloa, suggesting a backcross indi-
vidual
Ducks were extremely high (> 0.8; Table 1). On
two AFLP gels, the proportion of polymorphic
loci (P; corrected for sample size) in Laysan
Ducks was only about one-tenth that of Mallards
with Koloa intermediate to the other two species
(Table l).
TABLE 1. COMPARISON AMONG SPECIES OF NUMBER OF
SCORABLE BANDS (+ SE) AND BAND-SHARING COEFFI-
CIENTS (S), BASED ON JEFFREY'S 33.15 MINISATELLITE
PROBE AND PROPORTION OF POLYMORPHIC LOCI (P), BASED
ON AFLP DATA
Minisatellite DNA AFLP a
/4 scorable bands
N (-+ SE) s N P
Mallard 5 42.8 _+ 0.60 0.22-0.40 4 0.097
Koloa 5 43.4 _+ 0.62 0.30-0.51 16 0.049
Laysan Duck 5 34.6 + 0.26 0.82-0.90 10 0.014
104 of 401 scorable AFLP bands were variable.
DISCUSSION
Genetic analyses of both Laysan and Koloa
provide insights into problems with systematics,
hybridization, and loss of genetic variation of
these endangered species that have important
consequences for their conservation. Small body
size of the two Hawaiian species places them
together in recent systematic treatments based
on detailed morphological analyses (Livezey
1991, 1993), but some plumage characters of the
Koloa are more similar to Mallard than to Lay-
san Duck. Adding to the taxonomic confusion,
however, are results of a recent allozyme study
that showed a deep split between Mallard and
Koloa (an order of magnitude greater than all
anatid and most other avian congeneric genetic
distances previously observed; Arise and
Aquadro 1982), but virtually no differences be-
tween Laysan Duck and Koloa (Browne et al.
1993). In contrast, the analyses of mtDNA and
nuclear DNA in this study show that the diver-
66 STUDIES IN AVIAN BIOLOGY NO. 22
gence of Laysan Duck from a Koloa/Mallard
clade is robust, whereas the Koloa and Mallard
are very closely related (with only a few spe-
cies-specific diagnostic markers). It is possible
that the anomalous protein results stem from the
analyses of different tissue types in different
samples, which could artificially inflate esti-
mates of divergence among taxa.
Using a clock calibration of about 8% se-
quence evolution per million years (calculated
for the more variable 5' end of the mitochondrial
control region by Sorenson and Fleischer 1996),
it is estimated that the Koloa may have diverged
from the North American lineage of Mallards
(Mallard 2) as recently as 130,000 years ago, but
from the Holarctic lineage (Mallard 1) as long
ago as 0.8 million years ago (Ma). Divergence
of the Laysan Duck from both common Mallard
lineages, as well as from the Koloa, also appears
to be on the order of 0.8 Ma. The evolution of
these species from A. sparsa (about 1.7 Ma) is
well supported even when all 14 species and
subspecies in the mallard complex are included
in the analysis (J. Rhymer, unpubl. data). In ad-
dition, some species in the mallard complex,
such as the Laysan Duck, may well have
evolved from the nondimorphic ancestor rather
than the common Mallard (Fig. 2; see also John-
son and Sorenson 1998, Young and Rhymer
1998).
Confusion over the taxonomy and evolution-
ary history of these species has been compound-
ed by the propensity of introduced Mallards to
hybridize whenever possible with some of the
nondimorphic species in the mallard complex,
e.g., Grey Duck (A. superciliosa) in New Zea-
land (Rhymer et al. 1994), Black Duck and Mot-
tled Duck in North America (Johnsgard 1967,
Mazourek and Gray 1994), and the former Mex-
ican Duck (A. diazi; Hubbard 1977). Extensive
hybridization with introduced species can lead
to a kind of genetic extinction of rare native flo-
ra and fauna (Rhymer and Simberloff 1996). As
a result, the specific status of the taxa involved
can be called into question, with important con-
sequences for the protection of some endangered
species (Meffe and Carroll 1994, Avise and
Hamrick 1996). Nevertheless, current thinking
does not consider the retained ability to inter-
breed as sufficient evidence to preclude specific
status and protection (O'Brien and Mayr 1991,
Rhymer and Simberloff 1996).
Hybridization between Koloa and introduced
Mallards on O'ahu has been so extensive that
this population is no longer considered to have
pure Koloa. Removal of the threat of hybridiza-
tion is an essential component for the species
recovery (USFWS 1985). As an aside, the con-
tention that hybridization between Mallards and
closely related nondimorphic species occurs pri-
marily because females of the nondimorphic
species are more attracted to the colorful Mal-
lard male was not upheld in a detailed study of
New Zealand Grey Ducks and introduced Mal-
lards (Rhymer et al. 1994), and the same appears
true for Koloa. Only one known Koloa x Mal-
lard hybrid has been analyzed so far and this
individual resulted from a Mallard female x Ko-
1oa cross. More importantly, there is a popula-
tion of Koloa on Kaua'i that is largely unaffect-
ed by hybridization, so far. Knowledge of the
potential threat and the availability of diagnostic
molecular markers can now help to monitor in-
cursion of hybridization on this island. Apart
from guarding against hybridization, detailed
studies of Koloa ecology are of the utmost im-
portance in understanding its population dynam-
ics. It is the Kaua'i population that will provide
a stronghold for the Koloa, so it is suprising that
little is known about the ecology of this endan-
gered species. Captive breeding programs and/
or translocations are a final resort. It is better to
understand the species' ecology in planning the
prevention of further declines.
The Laysan Duck is in an even more precar-
ious situation with fewer than 150 individuals
surviving the drought of 1993 (Cooper et al.
1996). In this case, a captive breeding program
seems warranted. Results of mitochondrial and
nuclear DNA analyses indicate that repeated
bottlenecks, inbreeding, and/or low population
numbers have probably contributed to a loss of
genetic variation in this species. Only one mi-
tochondrial haplotype remains and the number
of minisatellite DNA bands and polymorphic
loci (using AFLPs) is reduced compared to that
found for either the Koloa or the Mallard. High
levels of band sharing among apparently unre-
lated individuals suggest a history of inbreeding,
similar to those observed in another species of
endangered Hawaiian waterfowl, the Nn
(Branta sandvicensis; Rave et al. 1994). Al-
though few empirical data are available showing
a direct link between loss of genetic variation
(as indicated by molecular markers) and fitness
(Lynch 1996), it is generally understood that
adaptive evolutionary change is the primary
means of responding to selective challenges
(i.e., genetic variation is important for isolated
species to adapt to environmental perturbations).
All indications are that the beleaguered Laysan
Duck does not adapt well to the harsh environ-
mental conditions on Laysan Island. A captive
program should be undertaken to reintroduce the
Laysan Duck to other islands, provided preda-
tors are controlled and the habitat protected. It
is now possible to plan a captive breeding pro-
gram to maximize maintenance of the remaining
HAWAIIAN ANATID CONSERVATION--Rhymer 67
genetic variation in this species (e.g., Haig et al.
1990).
We now know what the conservation issues
are for the endangered Koloa and Laysan Duck
and genetic considerations provide one starting
point for developing comprehensive strategies to
ensure their protection.
ACKNOWLEDGMENTS
I want to thank R. Fleischer for his encouragement
over the years to work on the Hawaiian anatids. DNA
fingerprints, using Jeffrey's 33.15 probe, were done in
his lab at the National Zoological Park, while I was
supported on a Smithsonian Institution Visiting Sci-
entist Fellowship through the Migratory Bird Program.
Thanks to A.J. Jeffrey for the use of his 33.15 mini-
satellite probe. Also thanks to H. James and S. Olson
for thought provoking discussions of evolution in Ha-
waiian waterfowl. Special thanks to D. Heckel for his
encouragement, for allowing me the use of his lab at
Clemson University for mtDNA sequencing and AFLP
analysis, and for support through an NSF EPSCoR
grant to University of South Carolina. I also want to
thank L. Gahan for her expert advice on AFLP tech-
nology and E. Beedle for running sequences. The
scnDNA RFLP analysis was done as part of a larger
project on the North American mallard species com-
plex at the Smithsonian Institufion's Laboratory of
Molecular Systematics under the direction of M.
Braun, while I was supported on a Smithsonian Insti-
tution Molecular Evolution Postdoctoral Fellowship. I
owe a deep debt of gratitude to the late Trish Sawaya
for her many hours of enthusiastic and patient tutelage
in lab techniques during that time.
,(
Studies in Avian Biology No. 22:68-80, 2001.
THE INTERPLAY OF SPECIES CONCEPTS, TAXONOMY, AND
CONSERVATION: LESSONS FROM THE HAWAIIAN AVIFAUNA
H. DOUGLAS PRATT AND THANE K. PRATT
Abstract. The Hawaiian Islands, with their unique geological history and geographic position, pro-
vide an excellent natural laboratory in which to evaluate currently competing biological (BSC) and
phylogenetic (PSC) concepts of the species. Although the BSC as historically applied in archipelagic
situations is shown to be flawed in producing overlumped polytypic species, it nevertheless remains
the preferable concept for most practical purposes. A review of the taxonomic history and species
limits in Hawaiian birds under both concepts reveals that, when properly applied, the BSC yields a
species total remarkably close to that produced under the PSC, contrary to what many proponents of
the latter have supposed. We propose that the widespread adoption of the PSC for conservation
purposes is potentially harmful. The PSC trivializes the species taxon and introduces new problems
of deciding when a population becomes diagnosable, the possibility that species could appear and
disappear in a reticulate fashion, and the likelihood that genetically diagnosable but phenotypically
identical, and therefore not field identifiable, populations could be ranked as species. All of these
problems negatively impact such things as constructing credible and politically defensible lists of
endangered species, the prioritization of limited conservation resources, and the gathering of field data.
We contend the BSC is arguably a more rational concept that better supports the activities of both
scientific and nonprofessional observers. Biological species limits in oceanic archipelagoes worldwide
need to be reevaluated using modern concepts and technologies before rational conservation decisions
can be made.
Key Words: avian conservation; biological species; endangered species; Hawaiian Islands; phylo-
genetic species; polytypic species; species limits.
Avian systematists have recently joined in a
great debate over the definition of species. The
long-accepted biological species concept (BSC)
of Mayr (1942a) has been challenged by a new
one from the field of phylogenetic systematics,
usually called the phylogenetic species concept
(PSC). As defined by Cracraft (1983), a phylo-
genetic species is a population or cluster of in-
dividuals "diagnosably different from other such
clusters, and within which there is a parental
pattern of ancestry and descent." Because diag-
nosability can be established by "any feature or
set of features, ranging from single fixed nucle-
otide substitutions to major phenotypic (but ge-
netically based) features" (Zink and McKitrick
1995), the PSC would elevate virtually all iso-
lated subspecies to species and add many more
based on small populations with one or more
distinctive traits. Zink and McKitrick (1995) and
Zink (1997) summarized the debate and argue
in favor of the PSC, whereas Mayr (1992), with
recent support from Snow (1997) and Collar
(1997), defended the BSC. For popular over-
views of the controversy, see Myers (1988) and
Sibley (1997).
Many might regard this debate as purely ac-
ademic. Recently, however, some conservation-
ists have suggested that the PSC would better
serve their purposes than the BSC, showing that
such esoteric pursuits do, indeed, have relevance
in the "real world." Hazevoet (1996) has even
charged that the BSC "promotes the extinction
of endemic birds," by classifying many distinc-
tive island forms as subspecies. Because conser-
vation efforts often focus only on "full" species
(Collar et al. 1994), there is some validity to
Hazevoet's claim. In this review, we use the avi-
fauna of the Hawaiian Islands to demonstrate:
(1) that proper application of the BSC in archi-
pelagic situations can produce a species list
much closer to one based on the PSC than has
been previously appreciated; (2) that the BSC
itself is sound and that the many problems with
it cited by some conservationists and systema-
tists arise from misapplication of the concept
rather than weaknesses of it; and (3) that the
PSC suffers from its own problems in practice
such that a shift to it could be worse for con-
servation than maintaining the BSC (Collar
1997).
Because Hawai'i is the most isolated oceanic
archipelago, with numerous large and ecologi-
cally varied islands, it has long been regarded as
a superb natural laboratory for the study of evo-
lution and biogeography. With the possible ex-
ception of Galfipagos's birds, Hawai'i's is the
best studied of any insular avifauna, and repre-
sents a much later stage of evolution than that
of Darwin's younger islands, with a much higher
level of endemism. Unfortunately, the Hawaiian
Islands have also suffered considerably more
ecological degradation (for a review, see Pratt
1994; Van Riper and Scott this volume) than the
Galfipagos and have more extinct and endan-
68
SPECIES CONCEPTS IN HAWAIIAN BIRDSPratt and Pratt 69
gered birds than any comparable region. They
also have the largest component of introduced
species of any modern avifauna (Long 1981),
but we will show that even alien birds can teach
evolutionary lessons on islands. Thus Hawai'i's
birds provide all the necessary ingredients for
evaluating the relationship of the competing spe-
cies concepts to each other and to conservation.
They further provide an important counterpoint
to Hazevoet's (1995) use of the Cape Verde Is-
lands avifauna as evidence of the need to aban-
don the BSC.
AVIAN TAXONOMY IN HAWAi'I
Most recognizable forms of Hawaiian birds
were first described as separate species under the
Linnean typological or morphological species
concept. Even some forms no longer regarded
as subspecies were so described (e.g., the three
populations of Hemignathus virens wilsoni; Wil-
son and Evans 1890-1899). All authors of the
"classical period" of Hawaiian bird research
(Wilson and Evans 1890-1899, Rothschild
1893-1900, Bryan 1901, Henshaw 1902a, Per-
kins 1903) used a morphological species con-
cept, although all were evolutionists. Perkins's
(1903) "family tree" of the Hawaiian honey-
creepers, an endemic taxon variously ranked as
the Drepanididae, Drepanidinae, or Drepanidini,
was the first phylogenetic treatment of any Ha-
waiian birds. After the flurry of ornithological
research in the islands around the turn of the
twentieth century, a period of neglect ensued,
with only a few scattered notes and papers on
Hawaiian birds appearing over the next four de-
cades, and avian taxonomy remained static.
Elsewhere during this quiescent period, sys-
tematists, with ornithologists prominent among
them, were formulating the "modern synthesis"
that culminated in Mayr's (1942a) classical def-
inition of the biological species that has been
memorized by generations of biologists. The
BSC is operational, rather than morphological,
and is based on the ability or inability of popu-
lations to interbreed freely. It introduced the
concept of polytypic species (comprising several
subspecies) for clusters of morphological "spe-
cies" that could or would interbreed in nature.
It thereby created the vexing problem of how to
classify distinctive isolated (allopatric) forms
whose ability or willingness to interbreed cannot
be objectively demonstrated. Mayr (1942a) sug-
gested the use of "potential isolating mecha-
nisms" to gain inferences as to what might hap-
pen during a hypothetical future period of con-
tact. He also suggested that systematists look to
the degree of diflrence between related sym-
pattic species as a guideline to evaluate allopat-
tic forms in a given group. We will show that
properly applied, these precepts lead to species
lists that can be corroborated by other procedu-
res, such as phylogenetic analyses and genetic
studies. However, early practitioners of the BSC
too often ignored their own fundamental guide-
lines and engaged in hasty lumping of vaguely
similar forms. One wag has dubbed the period
"Lumparama." In many cases, no reasons other
than general similarity and geographic separa-
tion were ever stated for lumping closely related
forms previously considered separate species
(see numerous examples in Mayr and Short
1970). It was taxonomy by decree.
Virtually all mid-century authors treated geo-
graphically replacing island populations the
same as such populations on continents, even
when differences were striking and consistent.
However, subsequent genetic studies (e.g., Boag
1988) showed that island colonization is a
unique phenomenon that differs fundamentally
from the kind of isolation that results from hab-
itat fragmentation, glacial cycles, and other con-
tinental phenomena. Diamond (1977) showed
that speciation differed on islands as compared
to continents, but his study suflred from the
state of knowledge of the time in that several
assumptions he made about Hawai'i in particular
(e.g., that intraisland subspeciation has not oc-
curred on islands smaller than New Zealand, but
see Pratt 1980; that the Hawaiian Crow, Corvus
hawaiiensis, represents a single colonization
with no subsequent intra-archipelagal dispersal,
but see Olson and James 1982b) have been
shown to be false. The failure to appreciate the
different character of insular allopatry was a ba-
sic misunderstanding that contributed to over-
lumping many island taxa.
The problem was exacerbated by Mayr's
(1942a, 1969) clearly stated belief that allopatric
populations of uncertain status should be con-
sidered subspecies. The "when in doubt, lump"
precept may be appropriate for closely related
isolates on continents (Snow 1997), but we will
show that for traditional studies of archipelagic
speciation, exactly the opposite bias ("when in
doubt, split") is more likely to result in a species
list that will stand up to independent corrobo-
ration. Indeed, every recent study of strikingly
marked insular "subspecies" of which we are
aware has revealed potential behavioral or eco-
logical isolating mechanisms to support recog-
nition of the forms as separate biological spe-
cies. Although Mayr (1942a) introduced the
concept of the superspecies for strongly diflr-
entiated allopatric species (allospecies), he stat-
ed that (p. 170): "It would be an abuse of this
concept if an author were to call every polytypic
species, composed of insular and thus well-
marked subspecies, a superspecies." Again, it
70 STUDIES IN AVIAN BIOLOGY NO. 22
now appears that the real abuse of the superspe-
cies concept is its under use in insular situations.
Subsequently, Sibley and Monroe (1990) modi-
fied the Mayrian definitions for the BSC and rec-
ognized many well-marked island "subspecies"
as allospecies. Even Mayr himself (E. Mayr and
J. Diamond, unpubl. data) has elevated many of
his earlier (Mayr 1945) subspecies to allospe-
cies.
The first review of the Hawaiian avifauna to
apply the "modern synthesis" was that of Bryan
and Greenway (1944), who combined many
geographically replacing morphological species.
Areadon (1950) carried the process further,
lumping many strikingly differentiated island
forms into large polytypic species (his work
dealt mainly with the honeycreepers, but he re-
viewed the other land and freshwater species in
an appendix). His classification exemplifies mid-
century evolutionary thinking. For example,
Amadon (1950) considered plumage color rela-
tively unimportant as an isolating mechanism,
despite the fact that birds are highly visual or-
ganisms. The de-emphasis of coloration as a
guideline to species limits was undoubtedly in-
fluenced by numerous hybridization studies dur-
ing the period that lumped such different-look-
ing continental forms as the three North Amer-
ican flickers (Colaptes spp.; Short 1965), the
various "dark-eyed" juncos (Junco spp.; Mayr
1942b), "Black-crested" and Tufted titmice
(Baeolophus spp.; Dixon 1955), Australian mag-
pies (Gymnorhina spp.), silvereyes (Zosterops
spp.), and many others (reviewed by Ford 1987),
the "Northern" orioles (Icterus spp.; Sibley and
Short 1964), Black-headed and Rose-breasted
grosbeaks (Pheucticus spp.; West 1962), Eastern
and Spotted towhees (Pipilo spp.; Sibley and
West 1959), and numerous others. Some of these
studies have withstood subsequent scrutiny, but
many have not. The trend of the era led to lump-
ing of such other taxa as Glossy and White-
faced ibises (Plegadis spp.; Palmer 1962), Pa-
learctic and Nearctic Green-winged Teal (Anas
spp.; Delacour and Mayr 1945), "Black-shoul-
dered" kites (Elanus spp.; Parkes 1958), the
three "yellow-bellied" sapsuckers (Sphyrapicus
spp.; Howell 1952), and Holarctic rosy-finches
(Leucosticte spp.; Mayr 1927, French 1959),
based solely on inference rather than actual stud-
ies. Most of the latter lumpings have subse-
quently been shown to be erroneous or ill-ad-
vised. We will show that, among Hawaiian
birds, behavioral and genetic studies virtually al-
ways support the premise that those that look
different, are different. Interestingly, although
Amadon (1950) was applying the BSC, his work
largely ignored the relatively little biological
data available at the time and was based almost
entirely on museum skins. But his study was
state-of-the-art, and we should not be surprised
that some of his polytypic "species" have sub-
sequently been shown to be amalgams of several
biological species (see section on 'Alauahios be-
low). Amadon's (1950) classification of Hawai-
ian birds remained the standard for three de-
cades.
The 1970s saw a renaissance in ornithological
field studies in Hawai'i. Many observers, in-
cluding the authors, confronted by overwhelm-
ing potential isolating mechanisms among many
very strikingly marked "subspecies," began to
question Amadon's (1950) taxonomy. H. Doug-
las Pratt conducted a complete review of avail-
able data from a variety of lines of inquiry and
combined it with new information on vocaliza-
tions (Pratt 1996b), foraging behavior, nesting
habits, and ecology to produce the first complete
taxonomic revision of the endemic avifauna
(Pratt 1979) since Amadon (1950). First appear-
ing in a dissertation, his classification was the
basis of that published by Berger (1981), who
did not accept all of Pratt's splits at the species
level. Berger's (and hence most of Pratt's) tax-
onomy was then adopted by the American Or-
nithologists' Union (AOU) Check-list (AOU
1983), which has been followed by most sub-
sequent authors. Pratt et al. (1987) adopted all
of Pratt's (1979) species limits, and in a series
of papers expanding on his dissertation, Pratt
(1982, 1987, 1989, 1992b) defended them, and
all were eventually adopted by the AOU (1985,
1991, 1993, 1995).
Shortly after H. Douglas Pratt's work became
widely known, another new classification ap-
peared in the form of a review of recently dis-
covered subfossil Hawaiian bird remains (Olson
and James 1982b). As further discoveries came
to light, these authors revised their classification
and presented an updated version in tabular form
(Olson and James 199l). Their arrangement of
genera differs irreconcilably (Conant et al. 1998,
Pratt this volume) with that of Pratt (1979) and
the AOU Check-list (AOU 1998) as revised, but
at the species level the two classifications differ
only slightly and could eventually agree totally.
In a footnote, Olson and James (1991) expressed
the view that "distinctive, allopatric, insular
forms" are best regarded as species. Their spe-
cies-level taxonomy is thus the closest yet to ap-
plication of the PSC to the Hawaiian avifauna.
During the 1970s, the first systematic studies
of Hawaiian birds using the new technique of
cladistics appeared. Raikow's (1977, 1986) an-
atomical studies produced the first cladistic phy-
logeny of Hawaiian honeycreepers (Pratt [1979]
was influenced by this technique, but his first
classification was not strictly cladistic). Since
SPECIES CONCEPTS IN HAWAIIAN BIRDSPratt and Pratt 71
then, virtually all analyses of Hawaiian bird evo-
lution have been cladistic. Until recently, cladis-
tic methods did not affect decisions at the spe-
cies level, but the PSC is itself an outgrowth of
cladistic thinking (Cracraft 1983, Zink 1997).
The recent split of the O'ahu 'Amakihi (Hern-
ignathus fiavus; see below) was based solely on
a reconstruction of phylogenetic history through
the study of mitochondrial DNA and shows that
some decisions by proponents of the BSC come
surprisingly close to PSC reasoning. Among Ha-
waiian birds, genetic studies at the molecular
level have usually supported species limits de-
termined by more traditional methods and are an
important independent corroboration of them
(Johnson et al. 1989; Tarr and Fleischer 1993,
1995; Fleischer et al. 1998). Indeed, many recent
splits were not accepted until biochemical data
supported them, but such data are not, in the
operational sense of the BSC, biological (Green-
wood 1997). Rather, biochemical systematists
may base their decisions on the Mayrian tech-
nique of comparing degrees of difference, in this
case genetic, between allopatric forms and those
between related sympatric ones, or on measure-
ments of the length of time allopatric popula-
tions have been evolving independently. Thus
they implicitly subscribe to the BSC but deal
with data that are outside the realm of traditional
isolating mechanisms.
THE SPECIES OF HAWAIIAN BIRDS
The following is a review of all historically
known Hawaiian land and freshwater birds and
one nesting seabird whose species limits have
been controversial. It shows that a near consen-
sus on species limits has developed during the
past decade. All lines of inquiry have contrib-
uted to it, and the result is a species list, based
on the BSC, that differs little from one based on
the PSC. It also suggests that in practice, appli-
cation of the PSC is not as simple as it first
appears.
HAWAIIAN PETREL
The Hawaiian petrel breeds in barren alpine
zones of the Hawaiian Islands, with the main
colony near the summit of Haleakal on Maul.
The birds' range at sea is poorly documented,
but they are believed to remain in the central
Pacific near Hawai'i year-round (Pratt et al.
1987). From the earliest days of its discovery,
the similarity of the Hawaiian Petrel to the Dark-
rumped Petrel (Pterodrorna phaeopygia) of the
Galfipagos was obvious, and virtually all tax-
onomists regarded it as an allopatric subspecies
P. p. sandwichensis. With the advent of tech-
nology that allowed detailed vocal comparisons
of the two populations, differences in voice be-
came apparent. Tomkins and Milne (1991) sug-
gested that these differences were sufficient to
be regarded as isolating mechanisms between
species, and Sibley and Monroe (1993) recog-
nized the Hawaiian Petrel (P. sandwichehsis) as
distinct. This case demonstrates a longstanding
and increasing appreciation among BSC propo-
nents of vocalizations as isolating mechanisms.
Recently, strong genetic divergence of the two
petrels was demonstrated using allozyme elec-
trophoresis (Browne et al. 1997) and as yet un-
published mtDNA studies (G. Nunn fide R.
Fleischer, pers. comm) had similar results. Be-
cause of their genetic diagnosability and geo-
graphic separation, the two forms would clearly
qualify as phylogenetic species.
ENDEMIC DUCKS
The Hawaiian Islands have two endemic
ducks that are apparent derivatives of the Mal-
lard (Arias platyrhynchos). The form wyvilliana
(Hawaiian Duck, hereafter referred to as Koloa)
is known historically from the main islands,
whereas laysanensis was historically restricted
to Laysan. Both endemics were originally de-
scribed as separate species, but Bryan and
Greenway (I 944), Munro (1944), and Amadon
(1950) considered them conspecific but distinct
I¾om the Mallard. Delacour and Mayr (1945)
lumped them all. For the next two decades most
authors (e.g., Brock 1951 a, Bailey 1956, Warner
1963) followed the former taxonomy, but Ripley
(1960) advocated species status for the Laysan
Duck while keeping the Koloa a subspecies of
Mallard. Alternatively, Berger (1972) consid-
ered both endemics fiall species, whereas Weller
(1980) again lumped both with the Mallard. Vir-
tually all of these varied treatments resulted
from subjective treatment of morphological
characters with little consideration given to
some rather obvious potential isolating mecha-
nisms. For example, Mallards and their relatives
are notorious hybridizers, especially in captivity.
Yet Ripley (1960) indicated that captive Laysan
Ducks failed to hybridize with Koloa when they
had the opportunity. In a recent survey of wa-
terfowl collections worldwide, only three of 46
collections holding Laysan Ducks reported that
laysanensis hybridized with another duck spe-
cies (M. Reynolds, pers. comm.). Ripley (1960)
further described numerous ecological peculiar-
ities of the Laysan Duck, but based his taxonom-
ic reasoning solely on morphological characters
such as distinctive downy plumage. For the Ko-
loa, Pratt (1979) pointed out that migratory
ducks form pair bonds on the wintering grounds,
a fact overlooked by previous treatments of this
complex. Koloa breed year-round (Swedberg
1967) and form pairs within sight of occasional
72 STUDIES IN AVIAN BIOLOGY NO. 22
wild Mallards. Swedberg (1967) further states
that even on small ponds the local ducks tend to
avoid wintering migrants, another obvious be-
havioral isolating mechanism. The near total ge-
netic swamping of Koloa by domestic Mallards
on O'ahu (Browne et al. 1993) does not negate
the inference gained from earlier, more natural
situations. Species status for the two endemic
ducks is now also supported by both laboratory
and paleontological studies. Browne et al.
(1993), using allozyme electrophoresis, pro-
posed that A. wyvilliana and A. laysanensis are
sister taxa, separate from A. platyrhynchos. Dis-
covery of subfossil remains of what appeared to
be laysansensis on the main Hawaiian Islands
(Olson and Ziegler 1995) suggested prehistoric
sympatry with wyvilliana. Sequencing of mt-
DNA from the subfossil bones (Cooper et al.
1996, Cooper 1997, Rhymer this volume) indi-
cated that they were close to the Laysan Duck
but not the Koloa, strongly suggesting former
sympatry. Rhymer's (this volume) results differ
from those of Browne et al. (1993) in showing
a close Mallard/Koloa relationship, with the
Laysan Duck very distinct genetically. Whatever
their phylogeny, these three forms appear to be
good species under virtually any species con-
cept.
HAWAIIAN COOT
All authors after Bryan and Greenway (1944)
considered the Hawaiian Coot a subspecies of
the American Coot (Fulica americana) until
Pratt (1987) showed that its differences were of
the same degree as those of other allospecies of
the worldwide coot superspecies, and involved
characters important in species recognition. He
suggested it be classified as F. alai as originally
described, and was followed by Sibley and Mon-
roe (1990), Olson and James (1991), and the
AOU (1993). Because it has consistent diagnos-
tic characters that distinguish it from other coots,
the Hawaiian Coot is also a phylogenetic spe-
cies.
HAWAIIAN STILT
Like the coot, the endemic stilt of the Ha-
waiian Islands has been regarded by most au-
thors as a subspecies of its North American
counterpart, the Black-necked Stilt (Himantopus
mexicanus). It is behaviorally quite similar but
has many distinctive plumage features (Pratt et
al. 1987) as well as adaptations to the unique
Hawaiian environment. Mayr and Short (1970)
recognized eight species of stilt in the superspe-
cies H. himantopus, including the Hawaiian H.
knudseni, rather than engage in "partial dubious
lumping with insufficient knowledge." They
stated that some forms "will undoubtedly prove
conspecific," and virtually no one followed their
split. Olson and James (1991), without com-
ment, ranked the Hawaiian Stilt as a full species.
In light of what we now know about discrete
plumage differences as indicators of relationship
among island birds, that decision was probably
sound. Under the PSC, the Hawaiian Stilt would
unquestionably be a separate species because of
its diagnostic plumage differences, and now mo-
lecular data (Fleischer and Mcintosh this vol-
ume) show large genetic divergence as well. It
likely is a valid biological species.
HAWAIIAN SOLITAIRES
The relationship of the Hawaiian thrushes
(Turdinae) to the American solitaires (Myad-
estes) was hypothesized by the earliest research-
ers (Stejneger 1887, 1889) but was not generally
accepted until Pratt (1982) reviewed and ampli-
fied the evidence supporting it. This classifica-
tion has subsequently been corroborated by new
osteological comparisons (Olson 1996) and ge-
netic studies (Fleischer and Mcintosh this vol-
ume). The various forms exhibit only slight vari-
ation in plumage, but differ strongly in bill mor-
phology and vocalizations. They might all have
been considered conspecific except for the fact
that two of them are sympatric on Kaua'i. The
smaller of those, the Puaiohi (M. palmeri), has
always been considered a separate species, but
mid-century workers regarded all the others as
conspecific. Pratt (1982) documented the vocal
differences mentioned by early researchers and
showed by playback experiments that these were
effective isolating mechanisms, at least between
the Kgma'o (M. myadestinus) of Kaua'i and the
'Oma'o (M. obscurus) of Hawai'i. The status of
the then rare (and probably now extinct) form
of Moloka'i (see Reynolds and Snetsinger this
volume) and the extinct forms of O'ahu and
Lgna'i had to be assessed by inference. Pratt
(1982) recognized the Oloma'o (M. lanaiensis)
as a species on the basis of its reportedly dis-
tinctive song. He found that the named subspe-
cies on Lgna'i (nominate) and Moloka'i (M. lan-
aiensis rutha) could not be differentiated on the
basis of plumage, but maintained the subspecies
because of a reported difference in vocal behav-
ior. Munro (1944) reported that the Moloka'i
bird sang and the Lgna'i one did not. This dif-
ference disappeared, however, when Oloma'o on
Moloka'i fell silent as they became rare and
thinly distributed (pers. obs. based on reports of
various field workers). Although the bird has
been observed, its song has not been heard for
decades. Because the O'ahu specimens had been
lost, Pratt (1982) only tentatively recognized the
',maui (M. woahensis) as an additional species.
Following rediscovery of the two known speci-
SPECIES CONCEPTS IN HAWAIIAN BIRDS--Pratt and Pratt 73
mens of the latter, Olson (1996) re-evaluated the
O'ahu form and considered it a subspecies of M.
lanaiensis pending comparison with subfossil
remains from Maui (which lost its solitaire be-
fore the arrival of ornithologists). He emended
the name to M. lanaiensis woahensis. If this ar-
rangement stands up to further scrutiny, it will
represent a pattern of speciation unique in the
Hawaiian Islands. Whether the three populations
of Oloma'o are phylogenetic species is difficult
to say, given our limited knowledge of them, but
the O'ahu form has a stronger claim to status
under the PSC than the other two because of its
slightly different coloration and longer period of
isolation (Moloka'i and Lna'i were joined with
Maui to form Maui Nui during the last glacia-
tion).
'ELEPA1OS
Hawai'i's monarchine flycatchers comprise
the endemic genus Chasiempis and are distrib-
uted on Kaua'i (sclateri), O'ahu (ibidis; former-
ly gayi but see Olson 1989), and Hawai'i (sand-
wichensis), but are enigmatically absent from the
Maui Nui cluster. The three island forms are
strikingly different in coloration, but their voic-
es, ecology, and general behavior are rather sim-
ilar. Also, sandwichensis exhibits considerable
intraisland variation and has three named forms
(nominate, ridgwayi, and bryani) with zones of
intergradation (Pratt 1980). The three major
forms were first lumped by Bryan and Greenway
(1944), and until very recently no one had chal-
lenged that classification. Pratt (1980) regarded
them as megasubspecies (Amadon and Short
1976) to emphasize the two different levels of
differentiation. Reflecting their previously stated
beliefs about distinctive island forms, Olson and
James (1991) recognized three species without
elaboration, and Olson (1996) maintained that
classification. Conant et al. (1998) were the first
to document behavioral and ecological differ-
ences among 'elepaios. They showed that the
obvious and diagnostic plumage differences are
reinforced by other, more subtle potential isolat-
ing mechanisms. Conant et al. (1998) recom-
mended biological species status for the Kaua'i
'Elepaio (C. sclateri), O'ahu 'Elepaio (C. ibi-
dis), and Hawai'i 'Elepaio (C. sandwichensis),
and we endorse their conclusion.
Whether the three subspecies of the Hawai'i
'Elepaio would be considered phylogenetic spe-
cies is problematical because some of their ob-
served intergradation may be primary and clinal
rather than secondary (Pratt 1980). The three
forms were presumably in constant genetic con-
tact in the recent past, but because of habitat
destruction the very distinctive Mauna Kea pop-
ulation (C. sandwichensis bryani) is now an iso-
late (Scott et al. 1986) with distinctive ecology
as well as plumage. Preliminary studies of one
zone of intergradation between C. sandwichensis
bryani and C. sandwichensis ridgwayi on the
southeastern flank of the mountain have found
evidence of secondary contact with possibly
some assortative mating (E. VanderWerf, pets.
comm.). Thus C. sandwichensis bryani may be
in the very earliest stage of speciation by the
BSC. In a PSC view, none of the three intrais-
land variants would be recognized taxonomical-
ly while they remained in genetic contact, but
presumably "C. bryani" is now a phylogenetic
species.
MILLERBIRDS
The only Old World warblers (Sylviinae) na-
tive to the Hawaiian Islands are restricted to the
Northwestern Hawaiian Islands. The extinct
Laysan Millerbird (Acrocephalusfamiliaris) and
the endangered Nihoa Millerbird (A. kingi) have
long been considered conspecific, but Olson and
Ziegler (1995) split them without elaboration.
Biological support for such a split is presented
by Morin et al. (1997), although they maintained
the single species. Certainly the differences be-
tween them are of the same degree as those ex-
isting between other Pacific island Acrocephalus
(Pratt et al. 1987), and separate species status is
probably warranted. They clearly are phyloge-
netic species. The question has more than aca-
demic significance because of recent proposals
to introduce Nihoa Millerbirds to Laysan (M.P.
Morin and S. L. Conant, pers. comms.). If they
are a different species from the original Laysan
bird, the proposal should perhaps be reconsid-
ered.
DREPANIDINE FINCHES
The finches of Laysan and Nihoa present an
instructive example of differing appearance as
an indicator of biological isolating mechanisms.
They differ strikingly in overall size as well as
relative size of bill. Plumages are similar but di-
agnostically different with females more diver-
gent than males. Amadon (1950) and other mid-
century authors regarded them as conspecific,
but Banks and Laybourne (1977) split them after
reporting very different molt and maturational
sequences. Other authors (e.g., Ely and Clapp
1973, Clappet al. 1977) reported differences in
nesting behavior, and Pratt (1979, 1996a) de-
scribed vocal differences. Because of the many
potential isolating mechanisms, all recent au-
thors have recognized both Laysan Finch (Te-
lespiza cantans) and Nihoa Finch (T. ultima) as
both biological and phylogenetic species. Re-
cently, proof of biological species status was re-
ported by James and Olson (1991), who found
74 STUDIES IN AVIAN BIOLOGY NO. 22
fossil remains of both species together on Mo-
loka'i. Genetically, the two differ to the degree
expected between pairs of closely related but bi-
ologically distinct species (Fleischer et al. 1998).
These finches are one of many examples in
which plumage differences that were dismissed
by mid-century workers accurately predicted bi-
ological species status.
'AMAKIHIS
This is a group of small, black-lored olive
green birds with down curved, short bills. The
extinct Greater 'Amakihi (Hemignathus sagitti-
rostris) of the island of Hawai'i had a longer,
straighter bill and was probably a close relative,
although some authors place it in the monotypic
genus Viridonia. The 'Anianiau (H. parvus), a
Kaua'i endemic, has a shorter, straighter bill and
rather different coloration and, despite its occa-
sional designation as "Lesser 'Amakihi," is
probably not very closely related. Conant et al.
(1998) reevaluated the morphological data and
placed the 'Anianiau in the monotypic genus
Magumma, and Fleischer et al. (1998) found ge-
netic evidence to support their treatment. Both
of these birds appear to have influenced the evo-
lution of "typical" 'amakihis by character dis-
placement: the Hawai'i form H. virens virens
has the shortest bill in the complex, whereas the
Kaua'i 'Amakihi (H. kauaiensis) has the longest
(Pratt 1979). Mid-century authors regarded all
typical 'amakihis as conspecific but almost al-
ways noted the much larger bill of the Kaua'i
bird. The bill is both longer and heavier with
virtually no overlap in measurements with any
other form (Conant et al. 1998). The larger bill
results in different feeding behavior and general
ecology. Vocalizations of the Kaua'i 'Amakihi
are also distinctive (Pratt et al. 1987, Pratt
1996b). Nevertheless, Berger (1981), and the
AOU (1983), failed to follow Pratt's (1979)
split. After biochemical data (Johnson et al.
1989, Tarr and Fleischer 1993) corroborated
Pratt's findings, the split was accepted (AOU
1995), although the Check-list Committee cited
no "traditional" data in support of the change.
Conant et al. (1998) summarized the numerous
potential isolating mechanisms of the Kaua'i
'Amakihi.
Surprisingly, Tarr and Fleischer's (1993) anal-
ysis of restriction-site variation in mtDNA
showed that the O'ahu 'Amakihi (H. chloris),
which had never been considered a biological
species in modern times, was genetically distant
from the morphologically, ecologically, and vo-
cally similar 'amakihis of Maul Nui and Ha-
wai'i. Furthermore, their evidence indicated that
the O'ahu birds were the sister taxon to H.
kauaiensis and therefore could not be conspe-
cific those of Maui Nui and Hawai'i. On this
basis, the AOU (1995) accorded the O'ahu
'Amakihi species status. Then Fleischer et al.
(1998) altered their earlier branching-sequence
hypothesis as the result of a new analysis in-
volving sequencing of mtDNA. They now be-
lieve the O'ahu taxon is, after all, sister taxon to
the Maui/Hawai'i forms. Still, the genetic dis-
tance between the O'ahu 'Amakihi and its sister
taxa is of the same order of magnitude as that
between the Kaua'i and Maui/Hawai'i forms, so
the species status of the O'ahu 'Amakihi is val-
id. This example shows why caution is dictated
in making taxonomic innovations based solely
on a single genetic study. The AOU (1995) de-
cision, though now upheld for different reasons,
could easily have proven incorrect and may have
been premature.
Interestingly, the only clue that the O'ahu bird
might be a separate species prior to the DNA
studies was its distinctive plumage. Again, the
character considered least important by mid-cen-
tury workers was, in fact, the most telling. Male
O'ahu 'Amakihi are more yellow below and
more strikingly two-toned than other 'amakihis,
with the typical pale eyebrow reduced to a small
supraloral spot. Females are even more distinc-
tive in being much less yellow or olive than oth-
ers and especially in retaining as adults the pale
wingbars seen in juveniles of all forms. O'ahu
'Amakihi can be distinguished from those of
other islands with virtually 100% accuracy on
plumage characters alone. Vocal differences,
such as a higher pitched song (Pratt 1996b), may
also exist but have not been adequately investi-
gated.
The same cannot be said of the remaining two
forms. Separate names were originally proposed
for the populations on Moloka'i, Lgna'i, and
Maui, but both Amadon (1950) and Pratt (1979)
found them inseparable. As a group they differ
on average from Hawai'i birds in coloration and
bill length (longer), but overlap is so broad that
only extreme individuals could be diagnosed on
characters alone (Pratt 1979). Thus they form a
biological subspecies H. virens wilsoni. Whether
practitioners of the PSC would consider this
form a species is unclear because despite their
obviously divergent histories, they are not com-
pletely diagnosable on phenotypic characters.
'AKIALOAS
'Akialoas look like giant 'amakihis with ex-
tremely long bills. All forms are extinct, making
biological assessment difficult. Forms are known
historically from Kaua'i, O'ahu, Lgna'i, and Ha-
wai'i, but those from the central islands are
known only from a handful of specimens. Their
classification has produced a nomenclatural
SPECIES CONCEPTS IN HAWAIIAN BIRDS--Pratt and Pratt 75
tangle (Olson and James 1995), and their sys-
tematics is as yet unsettled. Most authors (e.g.,
Berger 1981, AOU 1983, Pratt et al. 1987, Sib-
ley and Monroe 1990) follow Pratt (1979) in
placing 'akialoas in a large genus Hemignathus
defined on the basis of a suite of synapomor-
phies (Conant et al. 1998) in coloration, plum-
age sequence, and degree of sexual dimorphism,
bill shape, and vocalizations, but Olson and
James (1995) segregate them in their own genus
Akialoa. (For a defense of "greater" Hemigna-
thus, see Conant et al. 1998). At the species lev-
el, the situation is historically complicated. Bry-
an and Greenway (1944) lumped all forms, but
Amadon (1950) recognized two species on the
basis of the strikingly diflrent relative bill
lengths of the Kaua'i and Hawai'i forms. Having
seen only two immature specimens of the Lna'i
form and none of the O'ahu one, he included
both with the shorter-billed Hawai'i birds as
Hemignathus obscurus and separated the Kaua'i
'Akialoa (H. procerus emended to H. stejnegeri
by Olson and James 1995). Pratt (1979) and Ol-
son and James (1982b) showed that the Lna'i
and O'ahu 'akialoas were actually closer to the
Kaua'i 'Akialoa in bill length, and lumped all
forms again. The AOU (1983), however, main-
tained Amadon's (1950) split. Pratt et al. (1987:
302) reviewed the situation and pointed out that
if two species are recognized, the line of sepa-
ration had to go between Lna'i and Hawai'i
with resultant nomenclatural changes. They sug-
gested the names Lesser 'Akialoa (H. obscurus)
for the Hawai'i bird and Greater 'Akialoa (H.
ellisianus) for the other three forms; the AOU
(1997) eventually adopted this two-species clas-
sification.
But the situation is complicated by recent pa-
leontological data. James and Olson (1991) de-
scribed a second species of 'akialoa, H. upupi-
rostris, from Kaua'i and O'ahu that was sym-
pattic with the historically known forms. Addi-
tionally Olson and James (1995) reported two
sympatric prehistoric 'akialoas from Maui and a
larger species sympatric with the Lesser 'Aki-
aloa on Hawai'i, all as yet undescribed. Because
the relationships of these forms are unresolved,
Olson and James (1991, 1995) recommend rec-
ognition of all described forms as species: Ha-
wai'i 'Akialoa (Akialoa = Hemignathus obscu-
ra), Maui Nui 'Akialoa (A. lanaiensis), O'ahu
'Akialoa (A. ellisiana), Kaua'i 'Akialoa (A. ste-
jnegeri), and Hoopoe-billed 'Akialoa (A. upu-
pirostris). Interestingly, plumage variation
among the historically known forms is of the
same degree as that in several other groups or
pairs of species (e.g., 'amakihis, Hawaiian soli-
taires, O'ahu and Maui 'alauahios) and is non-
clinal (for illustrations of all forms, see Pratt in
press). This case, perhaps more than any other,
shows the folly of the old "if in doubt, lump"
dictum. Obviously, 'akialoas cannot all be con-
specific no matter what their interrelationships
turn out to be. Presumably, the five species de-
limited by Olson and James (1995) can be con-
sidered phylogenetic as well as biological.
NUKUPU'US
The three island forms of Nukupu'u and the
'Akiap6l'au comprise another group of hon-
eycreepers with long, hooked bills. Each was de-
scribed in the 1800s as a separate species: Hem-
ignathus lucidus from O'ahu, H. hanapepe from
Kaua'i, H. affinis from Maui, and H. wilsoni
from Hawai'i. Bryan and Greenway (1944)
combined all four, but Amadon (1950) separated
the 'Akiapl'au because of its unique straight,
rather than decurved, lower mandible. This tax-
onomy was supported by Olson and James'
(1994) morphological studies and discovery of
a specimen of Nukupu'u supposedly from Ha-
wai'i (Olson and James 1994), indicating pos-
sible sympatry. Thus the Nukupu'u and 'Akia-
p61'au cannot even constitute a superspecies.
Since Amadon's (1950) work, systematists have
ignored the nukupu'u complex, and the AOU
(1983) considered the Kaua'i and Maui forms as
subspecies of H. lucidus. With all three taxa ex-
tinct or nearly so, their classification must de-
pend on careful study of the fewer than 100
specimens scattered among a dozen museums
from Honolulu to Berlin. Ongoing studies by T.
K. Pratt and J. K. Lepson (pers. comm.) reveal
that measurements and coloration consistently,
and in some cases strikingly, distinguish the
three nukupu'us from each other. The PSC
would certainly consider them three species, but
it is likely that by the criteria of the BSC the
same outcome would be reached. Fleischer et al.
(1998) identified the nukupu'us as a good test
case for seeking a match between genetic diver-
gence and sequence of colonizing new islands
as they emerge down the Hawaiian chain.
'ALAUAHIOS
These small warblerlike birds of the genus
Paroreomyza are confined to the central islands
of O'ahu and the Maui Nui complex. Despite
extreme interisland color variation that ranged
from brilliant scarlet to dull gray, Amadon
(1950) considered the four named forms of Pa-
roreomyza conspecific with the two species of
Oreomystis from Kaua'i and Hawai'i. Certainly,
the inclusion of the brilliant scarlet Kkwahie
(P. flammea) of Moloka'i, with yellow and
green birds from O'ahu, Maul, and Lna'i,
should have been a red flag indicating the exis-
tence of more than one species. But Amadon
76 STUDIES IN AVIAN BIOLOGY NO. 22
(1950:166) stated that "variation from yellow to
red is obviously accomplished readily and need
not be considered as necessarily indicating spe-
cific difference." Lumping the Moloka'i, Lana'i,
and Maui forms meant that their striking differ-
ences had to have evolved since the breakup of
Maui Nui, a period we now know to have been
as little as 10,000 years. In fairness, we should
point out that such geological information was
unavailable in the period in which Amadon
(1950) worked. Pratt (1979) hypothesized that
the fact that the Kakawahie was the largest Pa-
roreomyza and had the heaviest bill, and the
Maui/Lna'i form was the smallest with the
smallest bill suggested character displacement
during a period of sympatry on Maui Nui. Olson
and James (1982b) found paleontological evi-
dence of such sympatry and agreed that Paro-
reomyza had to comprise more than one species.
The other two Maui Nui forms, known histori-
cally from Lna'i (montana) and Maui (newto-
ni), are very similar, differing only in that the
Lgna'i birds are slightly brighter dorsally. No
one since Bryan and Greenway (1944) has ever
suggested that they are other than a single bio-
logical species, the Maui 'Alauahio (P. mon-
tana), but whether they qualify as phylogenetic
species is problematical. The slight but consis-
tent color differences they exhibit, rather than
evolving in 10,000 years, may represent frag-
ments of a former interisland cline, such as that
shown by 'elepaios on Hawai'i (Pratt 1980), in
which paler birds inhabited the lower and drier
parts of Maui Nui and darker ones the rain for-
ests of Haleakalg. The relatively few specimens
from west Maul do appear somewhat interme-
diate in dorsal coloration. Questions such as at
what point the fragments of a f)rmer cline be-
come phylogenetic species show that the PSC is
not free of subjective judgments (Collar 1997,
Snow 1997). The O'ahu 'Alauahio (P. macula-
ta), now possibly extinct, was considered con-
specific with the Maui/Lgna'i bird by Olson and
James (1982b), but later (James and Olson 1991 )
they joined other authors in separating it. Its bill
is intermediate between those of P. fiammea and
P. montana but the coloration of both males and
females is clearly different and diagnostic (Pratt
et al. 1987).
'/KEPA
Representatives of the drepanidine "cross-
bills" (Loxops) were known from Kaua'i,
O'ahu, Maui, and Hawai'i, with a distinct taxon
on each island. Most forms are small birds with
yellow or gray bills, the males red or orange-
yellow, the females gray-green, and neither sex
with any bold black patterning or other mark-
ings. The Kaua'i form is so distinctive that it
was at first placed in its own genus Chrysomi-
tridops (Wilson 1890). It is larger, with a pro-
portionally larger blue bill. Both sexes are pat-
terned in yellow and green with a prominent
dark mask and pale forehead, although males are
brighter than females. Bryan and Greenway
(1944) recognized two species of Loxops: L. ca-
eruleirostris ('Akeke'e) for the Kaua'i form, and
L. coccineus ('kepa) for the O'ahu, Maui, and
Hawai'i forms. Despite the striking plumage dif-
ferences, which he did not consider great, Ama-
don (1950) believed it "by no means improbable
that they all would interbreed freely were their
ranges to overlap" and considered them all con-
specific. Pratt (1979) showed that the plumage
and bill differences were paralleled by others in
vocalizations, but his recommendation of a re-
turn to Bryan and Greenway's classification was
not adopted by Berger (1981). Thus the AOU
(1983) maintained Amadon's single species of
'fkkepa. Further research by Pratt (1989) and
others (summarized by Lepson and Freed 1997,
Lepson and Pratt 1997) revealed fundamental
differences in nest construction and ecology. As
a result, the AOU (1991) finally recognized the
'Akeke'e as a separate species. This is yet an-
other case in which plumage differences pre-
dicted potential isolating mechanisms in other
aspects of the birds' biology.
The status of the three named forms of 'ke-
pa is less clear because the O'ahu form (wol-
stenholmei) is extinct and known from only a
few specimens, and the Maui one (ochracea) is
very rare if not extinct and was never common
in historical times. Males of each fbrm can be
distinguished with near 100% accuracy on col-
oration alone, but females are more difficult to
identify visually. Whether the color differences
are sufficient isolating mechanisms, in the ab-
sence of other data, for recognition of O'ahu and
Maui 'akepas as biological species is moot (Pratt
1989), and their status as phylogenetic species
is likewise unclear. Perhaps biochemical data, as
yet unavailable, will reveal clearer differences.
'APAPANES
The 'Apapane (Himatione sanguinea) is
found in montane forests throughout the main
Hawaiian Islands with no geographic variation.
A now extinct related form on low, unforested
Laysan was long regarded as a subspecies, but
Olson and James (1982b, 1991) regarded it as a
species (H. freethi) without comment. Schlanger
and Gillett (1976) had considered the Laysan
Honeycreeper a relict of the days when Laysan
was a high island, but Olson and Ziegler (1995)
believed it to be a colonizer from the main is-
lands that has speciated on Laysan. With dis-
tinctive coloration (orangish rather than bright
SPECIES CONCEPTS IN HAWAIIAN BIRDS--Pratt and Pratt 77
crimson body feathering, dingy pale brown rath-
er than white undertail coverts), a shorter bill,
and distinctive cranial osteology, it is unques-
tionably a species under the PSC. Olson and
Ziegler (1995) split it on the basis of unspecified
osteological differences. Overlooked in most
discussions are several obvious potential isolat-
ing mechanisms of the Laysan Honeycreeper:
distinctive song and song phenology (Rothschild
1893-1900); different feeding behavior (includ-
ing often walking on the ground to forage
among flowers; Fisher 1903); different nest
placement and structure (Schauinsland 1899,
Bailey 1956); and, most obviously, totally dif-
ferent habitat. A previously unreported anatom-
ical difference, noticed by H. Douglas Pratt in
preparing illustrations (Pratt in press) is that the
Laysan bird has differently shaped tips to its pri-
maries, lacking or possessing in very reduced
form the truncation that produces the 'Apapane's
wing noise. It now appears highly unlikely that
these birds, adapted to two different worlds,
could successfully interbreed, much less do so
freely. Although Fancy and Ralph (1997) con-
sidered it a subspecies, future authors, including
Pratt (in press), will likely split it, bringing the
BSC and PSC into agreement on 'apapanes.
SUMMARY
A wealth of new morphological, behavioral,
ecological, and genetic data have dramatically
changed the systematics and taxonomy of Ha-
waiian birds. For example, a comparison of
Amadon's (1950) classification of Hawaiian
honeycreepers with the one we outline above
shows that for 40 named taxa, the number of
biological species (if all that have been proposed
are accepted) swells from 23 to between 34 and
38, the final figure depending upon the classifi-
cation of 'fikepas and nukupu'us. Correspond-
ingly, the number of taxa designated as subspe-
cies has dwindled from 17 to 6 or as few as 2!
These two poorly differentiated taxa (Maui Nui
'amakihi and Lfina'i 'alauahio) amount to small
pickings indeed over which to debate the BSC
versus PSC. The status of the 25 undifferentiat-
ed, and therefore unnamed, island populations
('O'fi [Psittirostra psittacea], 'Apapane, and
'I'iwi on six islands, the three Maul Nui 'ama-
kihis, and 'kohekohe [Palrneria dolei] on Mo-
loka'i and Maui) does not change. Likewise, the
19 named populations of songbirds that are not
honeycreepers have increased from 10 to 15 spe-
cies, with one subspecies sunk, one in dispute,
and one subspecies of Hawai'i 'Elepaio inter-
grading clinally with the nominate race, and an-
other isolated but with limited and, as yet, little
understood secondary contact.
Why is interisland endemism at the species
level so striking in Hawai'i? The answer lies
partly in the geographical setting: the Hawaiian
Archipelago comprises moderately large islands
with relatively few offshore islets and atolls in-
habitable by landbirds. Distances between main
island groups average 58 kin, a formidable
crossing for most sedentary songbirds. Birds
newly colonizing one island from another could
become quickly isolated genetically by weight
of numbers. Because the pool of potential im-
migrants on neighboring islands is much smaller
than would be the case if the source area were
a continent or much larger island, conspecifics
would arrive infrequently, and in low numbers
they would enter a resident population number-
ing in the hundreds of thousands at least. Thus,
adaptation to local conditions would proceed al-
most immediately without significant genetic in-
put from ancestral populations, and evolution of
endemic forms could proceed rapidly (Freed et
al. 1987a).
Grant (1994) found that Hawaiian native
finches exhibit less variability in bill measure-
ments than Galfipagos finches and attributed the
difference to greater specialization in feeding
habits, greater genetic distance among species,
and near absence of hybridization. All of these
comparisons relate to the very different geologic
history of Hawai'i (Fleischer et al. 1998) as
compared to the Galfipagos, a tighter cluster of
islands of relatively much younger age (Grant
1986). Species saturation was achieved in both
archipelagos primarily by adaptive radiation of
descendants of very few successful transoceanic
colonizations (Diamond 1977, Juvik and Austr-
ing 1979), but levels of differentiation fit each
unique situation. Because Hawaiian bird popu-
lations become genetically isolated virtually
from the start, they can quickly evolve differ-
ences in plumage and voice, both of which are
effective isolating mechanisms. Thus they soon
become both biological and phylogenetic spe-
cies, with only a brief period of intermediacy.
The most straightforward case of this has been
proposed by Fleischer et al. (1998), who provide
genetic data indicating that the four 'amakihis
originated from interisland colonizations that
followed shortly after emergence of new islands
in a conveyor-belt fashion as the archipelago
moved across a mid-ocean "hot spot."
Nevertheless, interisland colonizations in Ha-
wai'i obviously proceeded in both directions to
produce the species-rich faunas of each island as
well as the several examples of intra-archipelag-
ic double invasions (Myadestes on Kaua'i, Pa-
roreomyza on Maui Nui, 'akialoas on several
lands, etc.). Also, some Hawaiian birds are
widespread in the islands with no detectable in-
tedsland variation. The three Maul Nui 'amakih-
78 STUDIES IN AVIAN BIOLOGY NO. 22
is and the two populations of 'kohekohe are
fragments that were panmictic during recent pe-
riods of lower sea level, but other undifferen-
tiated populations belong to species that disperse
widely with relatively frequent intra- and inter-
island movements. Despite huge historical pop-
ulations and the widest geographic range possi-
ble, two of those, the 'Apapane and 'I'iwi, are
among the least genetically diverse of honey-
creepers (Tart and Fleischer 1995, Jarvi et al.
this volume). Both may have suffered recent se-
vere genetic bottlenecks then expanded their
populations and ranges, and the recently extinct
'O'fi, which has not been investigated geneti-
cally, probably exhibited the same pattern. Ab-
sence of interisland variability in five species of
Hawaiian waterfowl reflects large scale interis-
land movements and reproductively cohesive
populations, as confirmed by banding studies
(Engilis and Pratt 1993). The fact that far-rang-
ing species move in both directions shows that
not all speciation in Hawai'i has resulted from
Fleischer et al.'s (1998) conveyor belt. Virtually
all oceanic island avifaunas, though always de-
pauperate in number of species as compared to
continental areas, have very high levels of en-
demism (Stattersfield et al. 1998). Isolated, geo-
logically old archipelagos with large interisland
distances, such as the Marianas, Carolines, Tua-
motus, Marquesas, and many others, can be ex-
pected to exhibit species-level endemism com-
parable to that of Hawai'i as their avifaunas are
re-examined for the presence of potential isolat-
ing mechanisms.
Reflecting upon the history of avian system-
atics and taxonomy in Hawai'i, we repeatedly
see that coloration, long regarded as relatively
insignificant in determining species limits, may
be the first and most reliable indicator. Consis-
tent, unique vocalizations or discretely different
bill size or shape also virtually always corre-
spond to interspecific boundaries. In every case
in which species limits determined on these bas-
es have been tested by biochemical or paleon-
tological data, decisions based on an enlightened
use of traditional phenotypic investigations have
been upheld. Far from being single characters
that identify species, appearance and vocaliza-
tions predict where other more subtle isolating
mechanisms exist. Because the Hawaiian Islands
could well be regarded as the quintessential oce-
anic archipelago, the lesson is clear: island birds
that look or sound different are very unlikely to
be conspecific. Allopatric populations that have
only average rather than diagnostic differences
are little diverged genetically and can be rec-
ognized as subspecies. The old prejudice that
similar allopatric populations should be classed
as subspecies until proven otherwise has not
withstood the test of actual practice on oceanic
islands, and the underlying assumptions that
produced it must now be questioned or discard-
ed, at least for insular taxa. Properly applied to
island endemics, the BSC produces species lim-
its comparable to those of the PSC, and further
allows for the recognition of subspecies, a cat-
egory the PSC would essentially eliminate
(Snow 1997, Zink 1997). Because the taxonomy
of island birds elsewhere in the tropical Pacific
is still based largely on studies done in the first
half of the century, we can anticipate a major
increase in the number of biological species rec-
ognized in the region when the data are re-eval-
uated with the insights gained from the Hawai-
ian experience. However, we caution future
workers not to follow their predecessors in mak-
ing taxonomic changes based solely on infer-
ence.
SPECIES CONCEPTS AND
CONSERVATION
Our paper began with, and was largely
prompted by, the conflict between the BSC and
PSC as debated by Hazevoet (1996) and Collar
(1996). Because of the Hawaiian Islands' ex-
tremes of location and geologic history, their
birds define the issue better than any other iso-
lated insular avifauna. However, the outcome is
unexpected: most diagnosable, allopatric taxa
can be argued to be biological species on the
criteria that they either (1) are not sibling spe-
cies, or (2) were formerly reproductively isolat-
ed in sympatry but now live apart in contracted,
relictual ranges, or (3) are genetically and mor-
phologically distinct to a degree similar to re-
lated biological species living in sympatry. A
few recognizable taxa do not qualify by these
criteria, but we question whether these are either
truly diagnosable (e.g., Maui 'Amakihi) or evo-
lutionary units (three subspecies of Hawai'i
'Elepaio).
Changing views of biological species limits in
Hawai'i has had surprisingly little impact on the
course of conservation efforts because the U.S.
Endangered Species Act of 1973 does not focus
on, nor limit endangered status to, full species
only. No named Hawaiian taxon deserving in-
creased protection was omitted from the list be-
cause of its designation as a subspecies. Al-
though undiagnosable and unnamed populations
were not considered federally, a few were in-
cluded in an otherwise parallel list of popula-
tions protected by the state of Hawai'i. Actual
recovery efforts have been less encompassing,
however, and reflect the need to engage in triage.
Faced with a depressing list of 32 endangered
birds, 13 of them on the brink of extinction, state
and federal agencies focused their limited per-
SPECIES CONCEPTS IN HAWAIIAN BIRDS--Pratt and Pratt 79
sonnel and funding on managing tractable spe-
cies such as NCn½ (Branta sandvicensis), Koloa,
Laysan Duck, Newell's Shearwater (Puffinus au-
ricularis newelli), and Hawaiian Crow, or 'AI-
ala. Beginning in the 1980s, recovery efforts be-
gan to focus on restoration and protection of
habitat, to the benefit of entire bird communities.
In the mid-1990s, special programs were initi-
ated for two more endangered birds, the Puaiohi
and Po'ouli (Melamprosops phaeosoma). The
fact that these projects were funded, and not one
to restore the Hawai'i 'Amakihi on Moloka'i,
shows that even with a program that focuses on
populations, conservationists' attentions in Ha-
wai'i as well as worldwide (Collar 1997) are in-
evitably closely tied to the species concept.
On what few phenotypic or genetic characters
should one describe a phylogenetic species? Re-
cent introductions of the endangered Laysan
Finch, with subsequent rapid evolution in bill
size (Conant 1988a), present proponents of the
PSC with some yet-to-be resolved issues. For
example, do diagnosable populations that
evolved through founder effects and local ad-
aptation in only two decades qualify as phylo-
genetic species? If not, at what point would
they? Further, if introductions result in the cre-
ation of populations that are diagnosably distinct
(Conant 1988b), and therefore are "new" phy-
logenetic species, how can this technique con-
tribute to the conservation of the parent popu-
lation? A related situation is that some intro-
duced birds in Hawai'i, such as House Sparrows
(Passer domesticus, Johnston and Selander
1964), may already be phenotypically diagnos-
able. Conservationists are unlikely to regard
such introduced populations as endemic phylo-
genetic species. As Fleischer (1998) has pro-
posed, artificially fragmented populations of en-
dangered species in Hawai'i could become diag-
nosable at the molecular level through genetic
drift and presumably therefore qualify as phy-
logenetic species. Recovery actions cannot save
endangered species when new "species" are
created from recently fragmented or introduced
populations.
A second problem with the PSC is the pos-
sibility that species can appear and then disap-
pear in a reticulate fashion (Zink 1997) because
their delimitation does not require genetic iso-
lation. Consider again the example of the 'Ele-
paio on Mauna Kea. Because its range is almost
exactly congruent with that of the endangered
Palila (Loxioides bailleui), it will be strongly af-
fected by efforts to restore habitat for that spe-
cies. If plans to connect the upper forests of
Mauna Kea (the range of Chasiempis sandwich-
ensis bryani) with the rain forests of Hakalau
Forest National Wildlife Refuge (where C. s.
ridgwayi occurs) succeed, broad contact be-
tween two now isolated forms of 'Elepaio, each
a potential phylogenic species, could be re-es-
tablished, resulting in extensive interbreeding.
As our Hawaiian examples show, automatic
splitting of all populations with diagnosable dif-
ferences (Cracraft 1997) under the PSC is not as
simple in practice as it sounds (Collar 1997) and
could undermine the use of such time-honored
and successful management techniques as rein-
troduction and habitat restoration. We agree with
Collar (1997) that the PSC would trivialize the
species concept and severely stretch limited re-
sources without providing any rational basis for
formulating conservation priorities.
Even when, as in the United States, conser-
vation authorities are enlightened about the
sometimes arbitrary way that species limits are
applied and protect endangered populations of
whatever status, alpha taxonomy is still far more
than just an academic exercise. Much more is
involved in the conservation of island birds than
just the decision as to which ones are officially
listed as endangered. Often, the only information
available on birds of remote islands comes from
recreational birders, who seek out endemic spe-
cies and generally ignore those that are "just
subspecies" (see for example Pratt 1990, Wauer
1990a,b). One can argue the rationality of that
mindset, but no one can deny that in the eyes of
recreational birders, conservationists, and the
general public, species status has almost magical
properties. It is quite possible that many island
species worldwide could become endangered or
extinct without anyone noticing because birders
ignored forms ornithologists called subspecies.
Witness the case of the Island Scrub-jay (Aphel-
ocoma insularis) endemic to Santa Cruz Island
off California. Few birders were even aware of
its existence before it was recognized as a spe-
cies, but almost immediately afterwards, a small
industry developed for the sole purpose of en-
abling people to see the bird (Atwood and Col-
lins 1997). Had this been an endangered species,
we believe the increased population monitoring
would have contributed data valuable to the
bird's recovery. An example of the latter phe-
nomenon is the case of Bicknell's Thrush (Ca-
tharus bicknelli). No one voiced concern about
its conservation status until it was elevated to
species status (Thurston 1998).
Attention f¾om birders may be important even
before a bird is listed as endangered. For ex-
ample, the O'ahu 'Elepaio was rarely sought out
except on Christmas Bird Counts because, as a
subspecies, it did not score differently with bird-
ers. Thus, its sudden population crash in the past
two decades (Pratt 1994) went largely unnot-
iced. Now that it is a candidate for species status
80 STUDIES IN AVIAN BIOLOGY NO. 22
(Conant et al. 1998) as well as for listing as an
endangered species (Conant 1995), birders have
become more interested (Pratt 1993), and re-
search on the species has resumed (VanderWerf
et al. 1997, VanderWerf 1998a). Now, young
visitors to Honolulu's Hawai'i Nature Center
have their own species of 'Elepaio and 'amakihi
on which to focus their local pride and interest.
The fact that ecotourists would visit a locality
for the sole reason of observing an endemic
bird, or that school children take pride in and
learn about their local avian specialty, increases
public awareness and interest, especially in
small countries with limited resources (Wille
1991) in whose hands the fate of many species
ultimately lies.
Collar (1997) cited the numerous valuable
contributions of recreational birders to taxono-
my through their worldwide travel, tape record-
ing, photography, and note taking on breeding
biology and general natural history and behav-
ior. Janzen et al. (1993) even refer to birders as
"parataxonomists" in recognition of their con-
tributions. We support Collar's (1997) observa-
tion that birders are today the ornithologist's
most important ally in clarifying species limits
and conservation status of birds, and managers
of parks and reserves should encourage and fa-
cilitate birding rather than discourage it as has
all too often been the case in some Hawaiian
reserves (Pratt 1993, pers. obs.).
Conservationists and the general public need
a rational and observable basis for species rec-
ognition. By increasing the number of trivial
look-alike "species" to a bewildering and over-
whelming degree, adoption of the PSC could de-
stroy scientific credibility with governmental of-
. ficials and the general public who have little in-
terest in or knowledge of the subtleties of tax-
onomic philosophy. The BSC makes intuitive
sense through its use of observable isolating
mechanisms and the subspecies category for in-
termediate stages, and provides a credible basis
for conservation strategies. Although Hazevoet
(1996) may be correct that "taxonomic neglect"
promotes extinction of island birds, his proposed
solution of switching to the PSC will actually
increase such neglect by augmenting the taxo-
nomic workload, providing a confused taxono-
my for conservation practices (Collar 1997), and
recognizing "species" that defy common sense.
Besides, his main goal (increasing the number
of recognized species on islands) can be accom-
plished within the BSC without all of the dis-
advantages of the PSC. Proper application of the
BSC, including a long overdue review of the
taxonomic status of island taxa worldwide, will
do far more for avian conservation than adop-
tion of the phylogenetic species concept.
ACKNOWLEDGMENTS
We thank J. M. Scott for the initial inspiration for
this paper, and R. C. Fleischer for thought provoking
comments and insights from his unpublished data. S.
Conant, M. Morin, and M. Reynolds kept us apprised
of current conservation efforts in the Northwestern Ha-
waiian Islands. J. K. Lepson and E. VanderWerf shared
their unpublished museum and field observations with
us. Colleagues J. V. Remsen and F. Sheldon contrib-
uted thoughts to our formulation of the species concept
debate and commented on the manuscript.
Studies in Arian Biology No. 22:81-97, 2001.
WHY THE HAWAI'I CREEPER IS AN OREOMYSTIS: WHAT
PHENOTYPIC CHARACTERS REVEAL ABOUT THE PHYLOGENY
OF HAWAIIAN HONEYCREEPERS
H. DOUGLAS PRATT
Abstract. A Phylogenetic Analysis Using Parsimony (PAUP) of 39 phenotypic characters of myol-
ogy, osteology, tongue morphology, bill morphology, plumage and coloration, behavior, and ecology
produced a tree that strongly supports, with a few exceptions, current American Ornithologists' Union
classification of Hawaiian honeycreepers (Drepanidinae). These results are compared with those from
three different biochemical and genetics laboratories and those of a cranial osteology study. The
honeycreepers, including the aberrant genera Melamprosops and Paroreomyza, are shown to be mono-
phyletic and a subgroup of the Fringillidae. The Maui Parrotbill Pseudonestor xanthophrys is related
to thin-billed taxa rather than to the drepanidine finches. The genus Hemignathus, the present limits
of which have been widely challenged, is shown to be strongly supported by a large suite of characters,
except that the parrotbill may belong in it and the 'Anianiau (H. parvus) should be removed from it
and placed in its own genus Magumma. Hemignathus can be divided into four or five subgenera. The
generic pairs Chloridops/Loxioides, Himatione/Palmeria, and Vestiaria/Drepanis can justifiably be
lumped as Loxioides, Himatione, and Drepanis respectively. The genera Paroreomyza and Oreomystis
are not closely related, and the latter includes the Hawai'i Creeper (O. mana). Synapomorphies of the
two species of Oreomystis include: lack of adult sexual dimorphism; lack of wing-bars; distinctive
juvenal plumages; bill shape and coloration; foraging behavior; flocking behavior; juvenal begging
calls; and a simple, narrow, nontubular tongue unique among honeycreepers. Hypothesized relation-
ships of the Hawai'i Creeper with '.kepas (Loxops) based on mtDNA studies, or to 'amakihis (H.
virens and relatives) based on osteology, are incompatible with hypotheses based on a wide range of
other characters.
Key Words: Drepanidinae; Hawai'i Creeper; Hawaiian honeycreepers; Hemignathus; Magumma; Or-
eomystis; Pseudonestor.
The classification of the Hawaiian honeycreep-
ers (Drepanidinae) has been controversial since
the American Ornithologists' Union (AOU
1983) abandoned the longstanding classification
of Amadon (1950) in favor of a new one based
on Berger's (1981) use of my revision (Pratt
1979). This classification has been followed in
most general references since, including Scott et
al. (1986), Pratt et al. (1987), Sibley and Monroe
(1990), and the AOU (1983, 1991, 1998), but its
use has not been without criticism. Amadon
(1986) felt that "the genera of the Hawaiian
honeycreepers have been bandied about in rather
cavalier fashion," and Olson and James (1995)
bemoaned the wide acceptance of my classifi-
cation "among non-taxonomists without any
consideration having been given to its merits."
Olson and James (1982) introduced a different
classification, based largely on osteological stud-
ies, that has evolved in subsequent works (James
and Olson 1991; Olson and James 1991, 1988,
1995), but has not as yet been widely adopted.
The two schools have come to agreement on
several points, and the remaining differences in-
volve primarily the limits of the genera Loxops
and Hemignathus and the placement of the Ha-
wai'i Creeper (Oreomystis maria of AOU 1998
or Loxops maria of James and Olson 1991) and
'Akikiki or Kaua'i Creeper (O. bairdi). James
(1998) conducted a phylogenetic analysis of cra-
nial osteology, the first study to include all taxa,
both historical and subfossil. Her phylogeny (for
historically known taxa only) is presented by
Fleischer et al. (this volume). Recently, various
allozyme (Johnson et al. 1989, Fleischer et al.
1998) and mtDNA studies (Tarr and Fleischer
1993, 1995; Feldman 1997; Fleischer et al.
1998; Fleischer et al. this volume) have sug-
gested patterns of relationship that challenge
both AOU (1998) and James and Olson's (1991)
taxonomy. Because genetic technologies are still
advancing, hypotheses of relationships based on
them must be considered tentative. Each suc-
ceeding study seems to change the picture, the
various methods show little concordance in their
results, and the various laboratories do not agree
even when performing essentially the same anal-
yses. To their credit, the authors of these studies
have been very conservative in recommending
taxonomic changes. Molecular studies virtually
never mention phenotypic characters, the tradi-
tional tools of systematists, because they con-
sider such "adaptive" characters too subject to
the vagaries of natural selection to be evolution-
arily informative (R. Fleischer, pers. comm.).
Also, no genetic study of Hawaiian honeycreep-
ers has addressed the possibility that past hy-
bridization could have a profound effect on per-
81
82 STUDIES IN AVIAN BIOLOGY NO. 22
ceived patterns of divergence, although hybrid-
ization has been shown to have played a major
role in the adaptive radiation of the similar-aged
Darwin's finches (Grant 1994). Although DNA
studies may ultimately answer all phylogenetic
questions, I agree with Raikow (1986) that con-
cordance testing with more traditional methods
is still the only reasonable way to evaluate their
hypotheses. In this volume, Fleischer et al. do
exactly that by using data from mtDNA along
with phenotypic osteological characters to assess
the phylogenetic placement of the Po'ouli (Me-
larnprosops phaeosorna). In the two decades
since my first effort (Pratt 1979), many new pos-
sible phenotypic synapomorphies have been dis-
covered and others re-evaluated. Clearly now is
the time to provide a cladistic analysis of this
eclectic mix of traditional phenotypic characters,
so that meaningful comparisons with genetic
studies can be made.
METHODS
Scientific names used herein are those of the AOU
(1998) unless otherwise noted. I conducted phyloge-
netic analyses of 39 characters (Table 1) derived from
studies of myology, osteology, tongue morphology,
bill morphology, plumage and coloration, behavior,
and ecology using PAUP* (Swofford 1999) and
MacClade 3.01 (Maddison and Maddison 1992). Table
2 shows the data matrix. The first 3 characters were
segregated to simplify some manipulations done with
them. The 26 taxa include the chaffinches (Fringilli-
nae) and cardueline finches (Carduelinae) as out-
groups. Groups are coded as possessing a character if
any included species does so. Question marks indicate
gaps in the data. I have liberally used vernacular names
for three reasons: 1) to be as taxonomically noncom-
mittal as possible in entering the data; 2) to make my
trees directly comparable to others presented in this
volume that also use Hawaiian names; and, most im-
portantly, 3) because these are the only available
names that have remained unambiguous for two cen-
turies.
Phenotypic data are admittedly subject to some ma-
nipulation by the investigator because characters can
be described in various ways. Thus the coding of sev-
eral characters requires explanation. in Character 21,
for example, long sickle-shaped bills are found among
'akialoas (Hemignathux spp.) and in the 'l'iwi (Ves-
tiaria coccinea) and mamos (Drepanis spp.), but they
differ between the two groups in the nature of the bony
support (Baldwin 1953). By combining two features,
Character 21 codes this character without introducing
known homoplasy. Tongue shape (Character 15) and
bill shapes (Characters 19 22) could have been ap-
proached several different ways, but I found that qual-
itative descriptions worked better than quantitative
ones. I also did not order these characters because
whether they represent transtbrmational series is un-
certain. Character 26 ('amakihi coloration) represents
a suite of possibly synapomorphic characters that ap-
pear to have evolved in tandem. 'Amakihi coloration
includes: 1) plumage olive green dorsally; 2) under-
parts yellow to olive green, paler than dorsum; 3) lores
narrowly dark gray or black; 4) bill dark gray to black,
usually with bluish base to mandible; 5) females and
juvenals like males but less yellow; and 6) juvenals
with at least faint wingbars. These characters must be
grouped because they are not independent of one an-
other.
I applied similar techniques and the same data set
(plus other characters) in a different analysis that will
be explained under the discussion of the Hawai'i
Creeper below.
RESULTS
With all characters at the same weight, I con-
ducted a heuristic search that yielded a total of
390 equally parsimonious trees. From those, a
50% majority rule consensus tree (Fig. la) was
computed that had a length (L) of 130 steps, a
consistency index (CI) of 0.546, and a retention
index (RI) of 0.720. The numbers on the lines
indicate the percentage of trees that possess the
branch shown. The result produced some appar-
ent anomalies. Although the two 'alauahios (Pa-
roreomyza montana and P. rnaculata) and the
Kgkgwahie (P. fiarnrnea) stand apart as I pre-
dicted (Pratt 1992b), the Po'ouli remains imbed-
ded in the largest clade even though it also lacks
the "defining characters" (Pratt 1992a), Char-
acters 1-3 in Table 1, that presumably cause Pa-
roreomyza to segregate in the tree. The differ-
ence for the Po'ouli is that it possesses an inter-
orbital septum (Characters 11-12) like those of
other Hawaiian honeycreepers (Zusi 1978;
James and Olson 1991; Fleischer et al., this vol-
ume). Such a topology requires that the "defin-
ing" characters be secondarily lost in Melam-
prosops. This hypothesis lacks credibility be-
cause: 1) only these three among the 46 char-
acters are virtually exclusive to Hawaiian
honeycreepers as compared with all other pas-
serines; 2) they probably represent gene com-
plexes rather than single loci; and 3) they were
favored by natural selection in the Hawaiian en-
vironment and retained in most of the drepani-
dine taxa, so it is difficult to discern how a re-
versal would be advantageous. If, as hypothe-
sized by Pratt (1992a), drepanidine odor is a de-
fense against predation, then for a lineage to lose
it and have to compensate for the loss by the
redevelopment of energy-taxing predator mob-
bing behavior (which dreps with the odor also
lack), is certainly counterintuitive if not unpar-
simonious. Similarly, the loss of lingual wings
(or conversely the development of a squared-off
base to the tongue) seems unlikely to have oc-
curred more than once among the honeycreepers
because it has happened only one other time
(among sunbirds) in the entire passerine order.
A strict consensus tree of the same data set (Fig.
lb; L = 125, CI = 0.576, RI = 0.715) collapsed
HAWAI'I CREEPER--Pratt 83
many of the nodes and revealed a lack of reso-
lution among most taxa (but note that the Hem-
ignathus/Pseudonestor clade, discussed below,
survives, as do pairings of mamos and 'I'iwi,
Palila and Kona Grosbeak, and the two creep-
ers).
Consequently, I conducted a second analysis
giving Characters 1-3 a weight of 2, with all
others remaining weighted at 1. This run pro-
duced 150 equally parsimonious trees. The ma-
jority-rule consensus tree (Fig. lc; L = 136, CI
= 0.551, RI = 0.723) has a much more intuitive-
ly satisfying topology and is also more consis-
tent with the findings of Fleischer et al. (this
volume) and Pratt (1992a) with regard to Me-
lamprosops. Furthermore, its topology is so ro-
bust that most of it survives in a strict consensus
tree (Fig. ld; L = 125, CI = 0.576, RI = 0.715).
These consensus trees support a number of
hypotheses, some of which have taxonomic im-
plications: 1) the Hawaiian honeycreepers, in-
cluding Melamprosops and Paroreomyza, are
monophyletic; 2) Melamprosops and Paroreo-
myza independently diverged from the "main
line" of drepanidine evolution very early, before
the "defining characters" of Pratt (1992a, b)
evolved; 3) the drepanidine finches form a clade
that does not include the 'O'fi (Psittirostra psit-
tacea), Lina'i Hookbill (Dysmorodrepanis mun-
roi), or the Maui Parrotbill; 4) the genera Chlor-
idops and Loxioides are sister taxa, as suggested
by James and Olson (1991); 5) the 'amakihis,
'akialoas, and "heterobills" form a clade that
corresponds to the currently recognized genus
Hemignathus (AOU 1998) except that 6) the
'Anianiau (H. parvus) is not included in it, as
suggested by Conant et al. (1998); 7) Pseudo-
nestor may be a Hemignathus; it is more closely
related to the thin-billed taxa than to the drepan-
idine finches as suggested very early by Perkins
(1903) and later by Bock (1970) and Pratt
(1979) but not accepted by the AOU (1983); 8)
the remaining honeycreepers may divide into
two clades along the traditional "red" vs.
"green" lines; 9) several of the "red" genera
are closely related and possibly warrant merger;
10) Paroreomyz. a is not closely related to Or-
eomystis; which 11) includes the Hawai'i Creep-
er. Several of these require further comment.
DISCUSSION
DREPANID1NE FINCHES
Amadon (1950) placed all the drepanidine
finches (except the hookbill, which he regarded
as an aberrant specimen) in the genus Psittiros-
tra rather than recognizing the five genera pre-
viously named, most of which at the time would
have been monotypic. This arrangement also re-
flected his hypothesis that these birds' finchlike
characters were secondarily derived from a thin-
billed ancestor. Greenway (1968) split the genus
into Psittirostra for the 'O'fi and Loxioides for
the rest, and Banks and Laybourne (1977) ad-
vocated re-establishment of the original five
genera, primarily on the basis that Amadon's
Psittirostra was morphologically too broad, and
breaking it up reflected degrees of phenotypic
divergence comparable to those among various
mainland finch genera. With a cardueline ances-
try fairly well established, Amadon's large Psit-
tirostra also appeared to represent a paraphyletic
assemblage based on plesiomorphies (Pratt
1979). Olson and James (1982b) maintained
Amadon's Psittirostra but recognized five sub-
genera. Later (James and Olson 1991), they rec-
ognized all five genera, several of which by then
had gained new members described from pre-
historic remains, and added several new finch-
like genera. Although my phylogeny would sup-
port Greenway's (1968) classification, I would
caution against making any sweeping taxonomic
changes at this time. This study included rela-
tively few characters that could differentiate the
finch genera, so the apparent monophyly of the
group could easily be an artifact. Any changes,
with the possible exception of the merger of
Chloridops and Loxioides suggested by both this
study and James and Olson (1991 ), should await
publication of James's (1998) dissertation, new
fossil discoveries, and ongoing studies based on
ancient DNA extracted and amplified from pre-
historic remains (R. L. Fleischer, pers. comm.).
MAUl PARROTBILL
Not only does the parrotbill cluster with the
thin-billed taxa contra previous classifications
(Raikow 1977, AOU 1983), but it may belong
in the genus Hemignathus. Once the conflation
of its huge but fundamentally different bill with
the large bill of the 'O'fi (Raikow 1977) is elim-
inated, the similarities of the parrotbill to the
hemignathines, especially the 'Akiap61'au (H.
munroi), are overwhelming. Synapomorphies
are as varied as a modified jaw muscle (Zusi
1989) and juvenile call notes (pers. obs.). Inter-
estingly, the mtDNA phylogeny of Fleischer et
al. (1998, this volume) also supports a close 'Ak-
iap61'au/parrotbill relationship, although not
necessarily the current composition of Hemig-
nathus (see below). The parrotbill's tongue
(Character 16) is unique among the honeycreep-
ers, elongated with lateral and terminal projec-
tions. It looks very much like a drepanidine tu-
bular tongue that has simply been unrolled, and
can easily be seen as derived from a tubular an-
cestor. However, osteological studies (James
1998, Fleischer et al. this volume) group the par-
84 STUDIES IN AVIAN BIOLOGY
TABLE 1. CHARACTER STATES FOR PAUP* ANALYSES OF HAWAIIAN HONEYCREEPERS
NO. 22
Characters used in Figure 1
Defining characters of Hawaiian honeycreepers (Pratt 1992a):
1. Drepanidine odor
0. Absent
1. Present
2. Proximal end of tongue
0. With prominent "lingual wings."
1. Squared off, with no large backward projections.
3. Mobbing behavior
0. Present
1. Absent
Anatomy:
4. Pattern of insertion of the 3 branches of M. flexor digitorum longus (Raikow 1978)
0. ABB
1. ABA
5. Condition of M. peroneus brevis tibial head (from Raikow 1978)
0. Absent
1. Present
6. Condition of M. pterygoideus retractor (Zusi 1989)
0. Not enlarged
1. Highly enlarged
7. Tibial head of the shank muscle M. peroneus brevis (Raikow 1977, 1978)
0. Absent
1. Present
8. Coracoidal head of the upper forelimb muscle M. deltoideus minor (Raikow 1977)
0. Absent
1. Present
*9. Condition of M. plantaris (Raikow 1977)
0. Present
1. Absent
2. Variable within taxon.
10. Solid bony palate (Sushkin 1929, Amadon 1950)
0. Absent
1. Present
11. Interorbital septum thickness (Zusi 1978)
0. Thin, single-walled
1. Thick, double-walled
2. Thick, double-walled but with thin area in center
12. Fenestration of interorbital septurn (Richards & Bock 1973, Zusi 1978)
0. Large fenestrae
1. Solid
2. Small fenestrae or none (variable)
13. Floor of cranial fenestra in profile (Zusi 1978)
0. With hump or upward protrusion
1. Flat
14. Palatine process of the premaxilla (Bock 1960, Richards & Bock 1973)
0. Present
1. Absent ( fused) with lateral flange at anterior end
2. Absent (= fused) with reduced lateral flange
Tongue adaptations:
'15. Overall shape
0. "Nontubular, fleshy above, corneous below and caudolaterally" with "a rounded
tip edged with small papillae" (James et al. 1989).
1. As above but "far less fleshy, more slender" (Gadow 1899).
2. Straight and shallowly troughlike (Richards and Bock 1973).
3. Thin, tubular for half or more of length.
4. Fleshy but narrow, with spoonlike tip (Bock 1978).
HAWAI'I CREEPER Pratt 85
TABLE 1. CONTINUED
Characters used in Figure I
'16. Tongue margins
0. Smooth, not raised dorsad (Gadow 1899, Gardner 1925, Clark 1912, Amadon
1950, Raikow 1977, James et al. 1989).
1. Slightly raised, with short lateral and terminal laciniae at distal end
(Gadow 1899, Richards and Bock 1973).
2. Slightly raised, with long lateral and terminal laciniae
(Rothschild 1893-1900).
3. Strongly raised and curved inwards progressively toward tip,
lateral laciniae interlaced distally (Gadow 1899, Raikow 1977).
'17. Seed-cup modifications
0. Mixed within taxon.
1. No specialization for seeds
2. Seed-cup tip (Gadow 1899, Amadon 1950)
Bill morphology (mostly pers. obs.).'
18. Nasal Operculum (Raikow 1977, James et al. 1989)
0. Not expanded downward
1. Partially developed
2. Expanded downward to nearly cover nostril
19. Finchlike bill shape
0. Finchlike
1. Finchlike but elongated (i.e. tanager-like)
2. Not finchlike
*20. Unique morphologies
0. Bill shape represented elsewhere among passerines
1. Heavy, hooked maxilla
2. Heavy, parrotlike bill
3. Slightly crossed bill tips
4. "Heterobill" morphology
'21. Sickle-shaped bills
0. Not sickle-shaped
1. Sickle-shaped, thin
2. Sickle-shaped, thick
22. lnflation of bill
0. Bill not inflated
1. Bill highly inflated, subglobose
*23. Profile of gonys
0. Strongly convex
1. Slightly convex
2. Straight to slightly concave
3. Strongly concave
Plumage and Coloration (pers. obs.)
24. Sparrow-like streaking
0. Present at least in juveniles
1. Never present
*25. Juvenal plumage
0. No age-related plumage variation
1. Juvenile distinct but patterned like adult female
2. Juvenile patterned differently from either adult
26. Presence of "amakihi coloration" (see text for details):
0. Not present
1. Present
2. Present with secondary modifications
3. Present with loss of distinctive female and juvenile plumages
27. Purring or cooing wing note in flight
0. No
1. Yes
86
TABLE 1. CONTINUED
STUDIES IN AVIAN BIOLOGY
NO. 22
Characters used in Figure 1
28. Primaries with truncate tips
0. No
1. Yes
29. Plumage texture
0. Soft, non-shiny
1. Shiny or hardened
*30. Predominant plumage colors
0. Yellow-green, yellow, or red
1. Black, red, and/or yellow
2. Brown and black
3. Dull green or gray
4. Variable in group
Behavior and ecology
'31. Song quality
0. Canarylike (Perkins 1903, Pratt 1996a)
1. Dissonant whistles, bell-like and mechanical sounds
(Perkins 1903, Bryan 1908, Pratt 1996a)
2. Lively, quiet chittering (Engilis 1990, Kepler et al. 1996)
3. Lively whistles interspersed with call-like notes
(Pratt 1992b, Pratt 1996a)
4. Song of simple trills or warbles (Perkins 1903, Henshaw
1902, Pratt 1996a)
*32. Song complexity (Newton 1973; Pratt 1979, 1996)
0. Complex
1. Mixed complex and simple
2. Simple
*33. Distinct juvenal call beyond fiedging
0. Absent or unrecognized
I. Rapid juvenal begging calls in flocks (Scott et al. 1979; Fig. 2)
2. Evenly spaced "sound beacon" from solitary chick
(BNA; pers. ohs.)
34. Whisper songs (Pratt 1979, 1996a, b)
0. No whisper song
1. Whisper songs similar to primary songs.
2. Whisper songs distinct from primary songs.
35. Nest sanitation
0. Absent at some point in nesting cycle (Newton 1973; van Riper
1980a; Pletschet and Kelly 1990; Morin 1992a, b; BNA)
1. Throughout nesting cycle.
*36. Primary adult diet (Perkins 1903, Berger 1981, BNA)
0. Seeds
1. Soft fruits
2. Nectar
3. Mixed
4. Invertebrates
37. Nest construction roles (Newton 1976, Morin 1992b, BNA)
0. Construction by female only.
1. Construction mainly by female with limited help from male.
2. Construction by both sexes.
38. Size of territory (Newton 1976, BNA)
0. Large texTitories.
1. Small territories in immediate area of nest.
*39. Display flights over breeding area (Newton 1976, Morin 1992a, BNA)
0. Absent
1. Present
HAWAI'I CREEPER--Pratt 87
TABLE 1. CONTINUED
Characters used in Figure 1
*40. Presence of red in plumage
0. Yes
1. No
'41. Bill color
0. Pale throughout (may have darker tip)
1. Pale with dark culmen
2. Brown or gray with pale base
3. Black with bluish base to mandible
4. All black
*42. Attenuation of bill
0. None
1. Slight
2. Moderate
3. Pronounced
4. Extreme
*43. Presence of yellow in plumage (adult male)
0. Yellow head only
1. No yellow (or very little)
2. Yellow underlying entire plumage, nowhere bright
3. Yellow throughout plumage, with bright areas
4. Nearly all yellow.
*44. Black or gray feathering in face
0. None
1. Broad, not confined to lores
2. Confined to lores
*45. Presence of wing bars
0. Never present
1. Faint in juveniles, absent in adults
2. Present in juveniles only
3. Present in some adults
*46. Color pattern of crown and supraloral area
0. Uniformly colored
1. Indistinct pale eyebrow
2. Bold, distinct eye stripe
3. Contrasting crown and forehead
4. Pale supraloral fleck
Notes: All characters ordered except those with asterisks. Citations for every data point not given. Summaries are cited where useful. The abbreviation
BNA refers to the Birds of North America series of the American Ornithologists' Union (Baird 1994; Fancy and Ralph 1997, 1998; Lepson 1997,
Lepson and Freed 1997, Lepson and Pratt 1997, Pratt et al. 1997, Sixnon et al. 1997, Lindsey ct al. 1998; Olson 1998a,b,c; Snetsinger 1998; Baker
and Baker 2000a,b; Sykes et al. in press).
rotbill with two other taxa that have strongly
hooked bills (')'fi and hookbill), but different
tongues. This grouping could easily be viewed
as the result of homoplasy or just superficial re-
semblances. It is reminiscent of Raikow's (1977:
113) clustering of the parrotbill with the 'O'fi on
the basis of their vaguely similar bill shape and
the fact that such placement was "not refuted by
other characteristics." That placement is now re-
futed by many other characters, and the parrot-
bill, despite its large bill, clearly belongs among
the thin-billed taxa. However, I do not suggest
merger of Pseudonestor and Hemignathus until
the relationships are better understood, even
though my findings seem to show that, with
Pseudonestor excluded, Hemignathus is para-
phyletic.
HEMIGNATHUS AND moxoPs
Except for the Pseudonestor problem, the
above results clearly support current AOU
(1998) taxonomy that restricts Loxops to the
'akepas and groups the 'amakihis, 'akialoas, and
heterobills in Hemignathus. However, the cur-
rent inclusion of the 'Anianiau in the latter ge-
nus is not justified. For a detailed discussion of
the reasoning behind these conclusions, see Co-
nant et al. (1998). DNA studies also support rec-
ognition of a monotypic Magumma for the 'An-
ianiau. Tarr and Fleischer's (1995) restriction-
88
TABLE 2.
TABLE 1
STUDIES IN AVIAN BIOLOGY NO. 22
DATA MATRIX FOR PAUP* ANALYSIS OF HAWAIIAN HONEYCREEPERS USING CHARACTER STATES FROM
Character state
Taxon 1 2 3 4 5 6 7 8 9 10 11 12 13 14 lfi 16
Chaffinches 0 0 0 I 0 0 0 0 0 0 0 0 0 0 0 0
Cardueline finches 0 0 0 0 1 0 0 1 0 I 1 I 1 1 0 0
Telespiaa finches 1 I I 1 ? 0 0 1 0 l 1 1 I I 0 0
Palila I I I ? ? ? ? ? ? ? 1 1 1 ? 0 0
koa finches 1 I ? ? ? ? ? ? ? ? 1 I 1 ? 0 0
Kona Grosbeak I 1 ? ? ? ? ? 9 ? ? I 1 I ? 0 0
'6'a I 1 I 0 1 0 0 1 0 ? I I 1 ? 0 0
Lfina'i Hookbill ? ? ? ? ? ? '? ? ? ? I 1 1 1 0 0
Po'ouli 0 0 0 '? ? ? ? ? ? ? 2 2 1 ? 4 0
KfikSwahie/'alauahios 0 0 0 ? ? ? ? ? ? 0 0 0 1 2 2 1
Maui Parrotbill 1 1 I ? ? 1 ? ? ? ? 2 2 I ? I 2
Hawai'i Creeper 1 1 1 ? ? '? ? ? 1 ? 2 2 1 I 2 1
'Akikiki 1 1 I 0 I ? 0 l 0 ? 2 2 1 ? 2 1
'kepas/'Akeke'e 1 I 1 ? ? ? ? ' ? I 2 2 1 1 3 3
'Anianiau 1 I I ' ? ? ? ? ? ? 2 2 I ? 3 3
Greater 'Amakihi I 1 ? ? ? ? ? ? ? ? 2 2 l ? 3 3
'amakihis I I 1 0 1 0 I 1 1 ? 2 2 1 2 3 3
'akialoas 1 I ? 0 I 0 I I 0 I 2 2 I 1 3 3
nukupu 'us 1 1 ? 0 I ? ? ? ? ? 2 2 I ? 3 3
'Akiap61fi'au 1 I 1 0 1 1 0 1 0 ? 2 2 I ? 3 3
'Ula-'ai-hawane l 1 ? ? ? ? ? ? ? ? 2 2 I ? 3 3
'Apapane 1 I 1 0 I 0 1 I 1 1 2 2 I 1 3 3
',kohekohe I 1 1 I 1 0 1 1 I ? 2 2 1 ? 3 3
'I'iwi 1 I l 0 1 0 0 I 1 1 2 2 I 2 3 3
Black Mamo I 1 '7 ? ? ? ? ? ,? ? ? ? 1 ? 3 3
Hawai'i Mamo 1 1 ? ? ? ? ? ? ? ? ? ? 1 ? 3 3
fragment mtDNA study of a limited number of
taxa found the 'Anianiau widely separated from
the 'amakihis in a clade of its own. Fleischer et
al.'s (1998, this volume) mtDNA sequencing
study included additional taxa and grouped the
'Anianiau with the heterobilled 'AkiapOl'au (H.
munroi) and the parrotbill. James's (in Fleischer
et al., this volume) osteological phylogeny, how-
ever, maintains the grouping of the 'Anianiau
with the 'amakihis, which may reflect the su-
perficial resemblance that led to the former
name "Lesser 'Amakihi" and my own (Pratt
1979) uncritical placement of this species in
Hemignathus before closer scrutiny (Conant et
al. 1998).
James and Olson (1991: Table 14) restricted
Hemignathus to 'akialoas ald the heterobills,
and later (Olson and James 1995) subdivided it
and placed the former in a new genus Akialoa.
They grouped the 'amakihis with the 'rkepas,
'Anianiau, and Hawai'i Creeper in Loxops. Thus
constituted, Loxops would be close to Amadon's
(1950) characterization (Pratt 1979, Conant et al.
1998). James's (1998) newly analyzed osteolog-
ical data (Fleischer et al., this volume) provide
no support for such an arrangement. In fact, her
phylogeny not only supports restriction of Lox-
ops to 'gkepas, but can be interpreted as sup-
porting a large Hemignathus as currently rec-
ognized. The 'amakihis, heterobills, and akialoas
are members of a single clade even on osteolog-
ical grounds, but the picture is complicated by
the inclusion of the "red" honeycreepers in the
same clade. This result reveals one of the weak-
nesses of single-character or single-complex
analyses. With only one suite of characters, the
computer program has no way of distinguishing
homoplasy or parallelism from synapomorphy.
The bill morphologies among the "red" birds
(i.e., short down-curved bills, long sickle-bills,
etc.) parallel those found in Hemignathus, but
other characters (i.e., behavior, plumage type,
sequence of plumages, and vocalizations) show
that these resemblances are not synapomorphic
with similar morphologies among the "green"
birds (Perkins 1903, Amadon 1950). I suspect
that a combination of the osteological data with
my own would resolve this discrepancy and
bring James's (1998) phylogeny and mine into
substantial agreement. With the red birds re-
moved, James's uppermost clade fairly closely
approximates Hemignathus as currently delim-
ited (AOU 1998).
Fleischer et al.'s (1998) mtDNA sequence
phylogeny supports neither an enlarged Hemig-
nathus nor an enlarged Loxops. In it, the heter-
HAWAI'I CREEPER--Pratt 89
TABLE 2. EXTENDED.
Character state
17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39
0 0 0 0 0 0 I 0 I 0 0 0 0 4 ? 2 0 0 1 0 0 0 0
0 0 0 0 0 0 1 0 I 0 0 0 0 4 0 0 0 I 0 0 0 1 1
1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 0
2 0 0 0 0 I 0 I I 0 0 0 0 0 0 0 0 1 0 0 1 1 1
2 0 0 0 0 0 1 1 1 0 0 0 0 0 ? ? ? ? ? 0 ') ? ?
2 0 0 0 0 I 0 1 0 0 0 0 0 0 0 0 ? 1 ? 0 9 ? 1
1 1 1 1 0 0 0 1 1 0 0 0 0 0 0 0 0 0 ? I ? 1
1 1 2 1 0 0 0 1 ? 0 0 0 0 0 v ? ? ? ? v v ? ?
I ? I 0 0 0 0 1 I 0 0 0 0 2 2 0 0 0 I 4 2 ? 0
1 1 2 0 0 0 1 1 1 0 0 0 0 0 3 1 0 2 1 3 ? I 1
1 0 2 2 0 0 0 1 1 2 0 0 0 0 4 2 2 2 0 4 1 0 0
1 1 2 0 0 0 2 I 2 0 0 0 0 3 4 2 1 0 1 4 1 I 0
I 1 2 0 0 0 2 1 2 0 0 0 0 3 4 2 I 2 1 4 ') ? '
1 2 2 3 0 0 2 1 1 0 0 0 0 0 4 2 0 2 0 4 0 I 1
I 2 2 0 0 0 2 1 1 0 0 0 0 0 4 2 0 2 1 3 1 1 0
1 2 2 0 0 0 2 1 0 3 0 0 0 0 4 2 ? ? ? 4 ' ' '
I 2 2 0 I 0 3 I 1 I 0 0 0 0 4 2 0 2 0 3 1 0 1
1 2 2 0 1 0 3 1 1 1 0 0 0 0 4 2 ? ? ? 3 ' ? ?
I 2 2 4 1 0 3 I 1 I 0 0 0 0 4 2 '? ? ? 4 ' ? '
1 2 2 4 I 0 1 I 1 I 0 0 0 0 4 2 2 2 1 4 0 ? 0
1 2 1 0 0 0 1 1 2 0 ? 0 1 1 ' ' ? ? ? ' ? ? '
I 2 2 0 0 0 2 1 2 0 I 1 1 I I 0 0 0 I 2 2 1 1
1 2 2 0 0 0 2 1 2 0 1 0 1 1 1 0 0 2 1 2 0 I 1
1 2 2 0 2 0 3 1 2 0 1 1 1 1 1 0 0 0 I 2 I I 0
I 2 2 0 2 0 3 1 0 0 1 0 0 I I ' ? ? ? 2 ? ? '
I 2 2 0 2 0 3 1 0 0 1 0 1 1 1 ' ? ? ? 2 ? ? '
obills group with the parrotbill and 'Anianiau,
the 'amakihis are sister-group to the red birds,
and the Hawaii Creeper is sister-group to the
'akepas. The analysis does not include the
Greater 'Amakihi or the 'akialoas. According to
R. Fleischer (pers. comm.) the branching se-
quence among the thin-billed honeycreepers is
not well defined by the techniques used in their
study, so I believe we should await further de-
velopments before tinkering with a taxonomy so
well supported by phenotypic characters.
Although the phenotypic data support a large
Hemignathus, they also support the recognition
of four (or five if Pseudonestor is included) sub-
genera within it: Hemignathus for the hetero-
bills; Akialoa for the 'akialoas; Chlorodrepanis
for the "typical" 'amakihis; and Viridonia for
the Greater 'Amakihi. The latter two cannot be
combined as has been done in the past (Green-
way 1968) because such a construct would be
paraphyletic. In fact, future studies should con-
sider the possibility that the Greater 'Amakihi,
like the 'Anianiau, warrants a genus of its own.
THE "RED-AND-BLACK" GENERA
Every study reviewed herein shows that the
members of this subgroup, recognized from the
time of Perkins (1903), do indeed form a well-
defined clade. R. C. Fleischer (pers. comm.), on
the basis of the small degree of genetic differ-
ence between them, believes all of the "red"
genera could justifiably be merged. On pheno-
typic grounds, the genera Vestiaria and Drepan-
is differ solely on a relatively minor red-to-yel-
low color shift, hardly a generic-level distinction
by modern standards, but my earlier suggestion
(Pratt 1979) that they should be merged was not
accepted by Berger (1981). Also, the 'Apapane
and ',kohekohe (Palmeria dolei) are close
structurally and behaviorally, although the lat-
ter's unique plumage features make it look su-
perficially rather different. The lumping of Him-
atione and Palmeria is not as strongly supported
by my phylogeny as the Vestiaria/Drepanis
merger.
HAWAI'I CREEPER
So now we come to the one species whose
taxonomic position is the subject of the widest
disagreement among competing evolutionary
hypotheses and hence the namesake of this pa-
per. The Hawai'i Creeper is a small, drab Ha-
waiian honeycreeper endemic to the island of
Hawai'i (Scott et al. 1979). Its dull gray-green
90 STUDIES IN AVIAN BIOLOGY NO. 22
Majority rule
7.2_7
100 100
7..7 '100
60
100
Majority rule
10o
10o
100 100
IO0
IO0
100 100
Chaffinches
Carduelme tinches
Telespza finches
Palila
Kona Grosbeak
koa finches
Lana'i Hookbill
Po'o-uli
-- Maul Parrotbill
'akialoas
-- 'akepas/'Akeke'e
Hawai'i Creeper
'Akikiki
'Apepene
-- 'riwi
Hawai'i M arno
Kakawahie/alauahios
Chaffinches
Cardueline finches
Telespiza finches
1100L Palila
Kona Grosbeak
koa linches
Lana"i Hookbill
Maui Parrotbill
'Akiapola'au
'amakhis
Greater 'Amakihi
'akepasfAkeke'e
Hawai" Creeper
Akikiki
Anianiau
Ula-'ai-hawane
Apapane
Akohekohe
Back Mamo
HawarIMamo
Po'o-uli
Kakawahie/alauahios
Stnct
b
Strict
Chaffinches
Carduehne tinches
Telespiza finches
Palila
Kona Grosbeak
koa finches
Po'o-uli
Mau parrotbill
Hawai'i Creeper
'Apapane
Hawah M arno
Chaffinches
Cardueiine finches
-- r- Loxioides
Psittirostra
Dy,morodrepania
Peudonextor
Hemigthus (Viridonia)
Hemigthus
I I Hemigmthus (Akialoa)
I Hemigthus (H.)lucidm
I I ' Hemigmthm (H.)munroi
I 0 .... ysris ....
Oreomvstia irdi
- Hemignathu parvus
iri;ps
Hi--lone
Pabr
DrepanB,erea
Drenia p'ca
Melampros()p.
Poreomvza
HAWAI'I CREEPER--Pratt 91
coloration and generally inconspicuous behavior
may have contributed to the fact that the Ha-
waiians did not distinguish it from the Hawai'i
'Amakihi (Hemignathus virens; Perkins 1903).
It was first described (Wilson 1891) as Hima-
tione mana, but Amadon (1950) included it in
his large genus Loxops as one of the subspecies
of the "Creeper," a "species" subsequently
shown to be a grouping of five species in either
2 (Pratt 1979, 1992b) or 3 (Olson and James
1982b, James and Olson 1991) genera. The
O'ahu, Moloka'i, and MauiFLana'i components
of Amadon's "Creeper" are now placed in the
enigmatic genus Paroreomyza, which now ap-
pears to represent a very early divergence in the
evolution of the honeycreepers (Tarr and
Fleischer 1995, Fleischer et al. 1998, this study).
The genus Oreomystis comprises the remaining
two species, the 'Akikiki or Kaua'i Creeper, O.
bairdi, and the Hawai'i Creeper, O. mana. John-
son et al. (1989), Feldman (1997; phylogeny re-
produced in Freed 1999) and Fleischer et al.
(1998, this volume) present strong allozyme,
mtDNA, and osteological evidence that O. bair-
di is the sister-group of Paroreomyza, although
the placement of that clade varies among the
studies. For this relationship to hold, the hon-
eycreepers' squared-off tongue base (Character
2) would have to have evolved twice indepen-
dently, an unlikely prospect as discussed earlier.
This study achieved very different results (Fig.
1 ) in which Paroreomyza and Oreomystis bairdi
are as fax apart as any other two drepanidine
genera. Tarr and Fleischer's (1995) restriction-
site study supports this finding, but is out of step
with their later mtDNA sequence analyses.
On osteological grounds, Olson and James
(1982) and James and Olson (1991) place the
Hawai'i Creeper in their large Loxops and con-
sidered it closely related to the 'amakihis (Olson
and James 1995). However, James's (1998) phy-
logeny (see Fleischer et al., this volume) shows
it only as a sister group to most of the other thin-
billed honeycreepers, a position rather close to
where it appears in my study (except that the
'Akikiki is paired with it). Thus the osteological
phylogeny and mine actually differ more strik-
ingly on the placement of O. bairdi than on that
of the Hawai'i Creeper. The osteological phy-
logeny, if correct, would require either the cre-
ation of a new monotypic genus for the creeper
or the recognition of a huge genus Drepanis that
would include everything f¾om the creeper to
heterobills to mamos. If the red birds were re-
moved from this assemblage as suggested
above, the creeper could be in Hemignathus. In-
terestingly, Feldman's (1994) independent
mtDNA study showed the Hawai'i Creeper as
sister group to the red honeycreepers which
clade in turn formed an unresolved trichotomy
with the 'amakihis and 'gkepas. Although dis-
tinctive, this hypothesis is closer to those de-
rived from osteology and this study than to the
other mtDNA results. Fleischer et al. (1998, this
volume) hypothesize on the basis of mtDNA se-
quencing that the Hawai'i Creeper forms a clade
with the 'gkepas which in turn is sister to an odd
assemblage that includes the heterobills, parrot-
bill, and 'Anianiau. So is this enigmatic little
bird an odd offshoot of its own, sister to the
'Apapane (Himatione sanguinea) and 'I'iwi, a
non-crossbilled 'gkepa, or an Oreomystis?
The question of whether Oreomystis is related
to Paroreomyza is independent of whether the
Hawai'i Creeper and the 'Akikiki are congeners.
So numerous are the phenotypic similarities of
the Hawai'i Creeper to the 'Akikiki that manu-
script reviewers of Pratt (1992b) questioned
even considering them separate species, let
alone members of different genera. The Hawai'i
Creeper is vaguely similar in overall coloration
to female and juvenile 'amakihis, female 'dcepa
(Loxops coccineus), and both sexes of 'Akeke'e
(L. caeruleirostris; Scott et al. 1979, Pratt et al.
1987), but differs in important details. Unlike
'amakihis and 'rakepas, adults are not sexually
dichromatic. They have a broad gray mask,
shaped more like the black mask of L. caerulei-
rostris than the narrow black lores of 'amakihis.
Unlike 'amakihis but resembling 'gkepas, nei-
ther adults nor juveniles ever have wing-bars.
And unlike both 'amakihis and 'gkepas, juve-
niles have a distinctive plumage with pale feath-
ering in the lores and over the eye. In plumage
features, the Hawai'i Creeper closely resembles
Oreomystis bairdi, which also lacks sexual di-
chromatism as an adult, has a distinctive pale-
faced juvenile plumage, and lacks wing-bars.
The creeper's bill is nearly straight with a
concave gonys (Pratt 1992b), pale except for a
dusky tinge, variable in extent, along the cul-
men. In overall shape it is somewhat interme-
diate between that of an 'amakihi and that of an
'gkepa (without crossed tips) and resembles that
FIGURE l. Phylogenetic trees of Hawaiian honeycreepers: a) unweighted tree, 50% majority-rule consensus;
b) unweighted strict consensus tree; c) majority rule tree with Characters 1-3 weighted 2; d) strict consensus of
weighted trees, with AOU (1998) scientific name equivalents and Hemignathus divided into four subgenera. See
Tables 1 and 2 for data and coding. See text for analysis details.
92 STUDIES IN AVIAN BIOLOGY NO. 22
lO
5
Oreomystis
bairdi
0. mana
5 --
o I I
0 2 4
Time (seconds)
FIGURE 2. Juvenile begging calls of the 2 species of Oreomystis. O. bairdi recorded 6 August 1997 by David
Kuhn near the Mohihi Trail above Koa'ie Stream, Alaka'i Wilderness Preserve, Kaua'i (not archived). O. maria
recorded by the author 4 May 1977 at Keauhou Ranch, Ka'u District, Hawai'i (Cornell Laboratory of Orni-
thology, Library of Natural Sounds No. 05274). Audiospectrograms prepared on a Macintosh computer using
Canary¸ software program.
of Oreomystis bairdi in nearly every detail ex-
cept that it is somewhat thinner, light gray rather
than pale pink, and has somewhat more dark
pigment above (Pratt et al. 1987). Because their
bills are nearly identical in shape, the most par-
simonious hypothesis would seem to be that the
two creepers share a common ancestry, but bill
shape does not argue strongly against an 'akepa
relationship for them both.
The nuthatch-like foraging of the Hawai'i
Creeper differs from that of Oreomystis bairdi
only in that the chosen substrates average larger
for the latter (Pratt 1992b). Of all the 'amakihi
species, the Kauai 'Amakihi (H. kauaiensis) is
the most frequent bark-picker, but it would never
be characterized as nuthatch-like (Conant et al.
1998). Nor does the Hawai'i Creeper forage in
any way resembling the feeding of either species
of Loxops (Lepson and Pratt 1997, Lepson and
Freed 1997). Following fledging, tightly struc-
tured family groups of both Hawai'i Creeper
(Scott et al. 1979, Pratt et al. 1987) and 'Akikiki
(Pratt 1992b, Conant et al. 1998) forage together
with frequent begging notes from the juveniles.
Both may eventually join larger mixed-species
flocks with 'amakihis, 'akepas, and other species
(Pratt et al. 1976, Lepson and Freed 1997, pers.
obs.). Similar tightly structured family foraging
groups with distinctive calls have not been re-
ported in 'amakihis or 'akepas (Lepson and Pratt
1997, Lepson and Freed 1997), although they
both join looser flocks. Because the hypothe-
sized ancestor of the drepanidines was a seed-
eating cardueline finch, the nuthatch-like forag-
ing of the two creepers can be viewed as a syn-
apomorphy.
The song of the Hawai'i Creeper is a short
trill similar to that of O. bairdi, but many other
drepanidine species also sing short trills, so adult
songs reveal little about relationships (Scott et
al. 1979, Pratt et al. 1987, Pratt 1992b, Pratt
1996). One noteworthy difference is that songs
of both Oreomystis are highly stereotyped,
whereas those of such potential relatives as
HAWAI'I CREEPER--Pratt 93
'amakihis and 'akepas are highly variable even
when uttered by the same individual (Pratt
1979,1996; Pratt et al. 1987). The begging notes
of Hawai'i Creeper juveniles flocking with their
parents after fledging are very similar to those
of juvenile 'Akikiki (Fig. 2) in similar context,
which were first recorded in 1997 and are thus
not included in recently published tapes (Pratt
1996). The individual notes of 'Akikiki juve-
niles are slightly shorter and cover a somewhat
wider frequency range than those of the Hawai'i
Creeper, but they have a similar syncopated
rhythm, with notes grouped in short bursts (Fig.
2). Although a few other Hawaiian honeycreep-
ers (e.g. Pseudonestor xanthophrys, Hemigna-
thus munroi) have distinctive juvenile begging
notes that persist long after fledging, none have
the same sound or rhythmic pattern of the two
creepers. No long-persisting juvenile begging
notes have been reported among either 'amakih-
is or 'akepas, nor among cardueline finches, and
thus the juvenile calls appear to be another syn-
apomorphy linking the two Oreomystis.
But it is the tongues that present the most
enigmatic observations. The Hawai'i Creeper's
tongue is narrow and nontubular, with a notched,
slightly frayed tip (Richards and Bock 1973) and
resembles the tongue of O. bairdi in virtually
every detail (Pratt 1992a). Such a tongue tip dif-
fers strikingly from that of the hypothetical an-
cestral Hawaiian honeycreeper (Raikow 1977),
is found only in the Hawai'i Creeper and the
'Akikiki, and, unlike that of the parrotbill, is dif-
ficult to envision as a derivative of the highly
derived drepanidine tubular type. The most like-
ly explanation for two taxa sharing in detail such
a complex derived morphology is that they both
inherited it l¾om a common ancestor. The sim-
ple, notched tongue certainly appears to be a de-
fining synapomorphy in Oreomystis.
If Raikow (1977, 1985, 1986) is correct that
the tubular drepanidine tongue defines a major
clade of the Drepanidinae that includes both the
"green" and "red" groups, Oreomystis cannot
belong to it unless its distal tongue morphology
is secondarily derived from the tubular form. Of
course, such derivation is clearly possible. Both
the DNA and osteology trees of Fleischer et al.
(this volume) require this secondary derivation
for the Hawai'i Creeper but not the 'Akikiki. My
unweighted tree (Fig. la) shows the two-mem-
ber Oreomystis as one branch of an unresolved
trichotomy with the "red" clade on the one hand
and the "green" clade on the other, but my
weighted tree (Fig. l c) places it, like both of
those of Fleischer et al. (this volume), in a po-
sition that requires secondary derivation of the
Oreomystis tongue from a tubular ancestor.
This result prompted me to conduct an addi-
tional analysis that focused on the "green"
birds, including all species-level taxa and addi-
tional characters (40-46 in Table 1) that, for rea-
sons mentioned earlier, could not be used with
the broader sample of taxa. I included the three
Paroreomyza species and the monotypic Psitti-
rostra for comparative purposes and so that the
relationships of Pseudonestor would also be re-
examined. All characters were unweighted in
this analysis, and Character 35 (nest sanitation)
was ordered rather than unordered as previously.
Table 3 is the data matrix for this analysis. A
heuristic search of the 46 characters produced
180 trees, from which majority-rule and strict
consensus trees (Fig. 3; L = 109, CI = 0.661,
RI = 0.732) were derived. This time, the two
Oreomystis sorted out as the sister group to the
entire clade defined by the tubular tongue (but
including Pseudonestor), which I believe is a
reasonable placement for it. Note that the earlier
pairing of Oreomystis with 'Anianiau did not
hold up in this more detailed analysis, and I re-
gard it as an artifact.
Problems of possible homoplasy complicate
analysis of another anatomical feature that has
figured prominently in the taxonomic history of
the creepers. Raikow (1976) found that some
Hawaiian honeycreepers, like many other pas-
serines, have lost the plantaris, a minor muscle
of the shank. Of the taxa he studied, only the
'amakihis and the "red" genera Himatione, Pal-
meria, and Himatione lacked the plantaris. Un-
fortunately, he included neither an 'akepa nor
any of the "creepers" (which were all then con-
sidered conspecific) other than Oreomystis bair-
di. Nevertheless, Raikow (1977) separated "the
Creeper" generically from the 'amakihis based
on the loss of the plantaris in the latter. If the
loss of the plantaris is a uniquely derived char-
acter state within the honeycreeper taxon, then
the logical conclusion is that the taxa that share
this condition form a clade ('amakihis plus the
red-and-black birds), a grouping that appears in
Fleischer et al.'s (1998) mtDNA tree. Subse-
quent dissections (S. L. Olson, pers. comm.) re-
vealed that the Hawai'i Creeper lacks the plan-
taris, a result that might also seem to support a
relationship to 'amakihis. How useful is loss of
the plantaris as a key to phylogeny? Clearly, it
cannot be considered a synapomorphy in any
broad sense, because it has occurred several
times among passetines generally, and at least
twice among the Carduelinae (Raikow 1976,
1977, 1978). Furthermore, avian muscles have
been shown to be subject to evolutionary rever-
sals (i.e., to become re-established in a lineage
after loss; Raikow et al. 1979) as well as suffi-
ciently variable individually to present problems
for phylogenetic studies based on few specimens
94 STUDIES IN AVIAN BIOLOGY NO. 22
TABLE 3. DATA MATRIX FOR PAUP* ANALYSIS OF "HEMIGNATHINE" SPECIES OF HAWAIIAN HONEYCREEPERS USING
CHARACTER STATES FROM TABLE ]
Character state
Taxon I 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Psittirostra 1 1 1 1 1 0 0 I 0 ? 1 1 1 .9 0 0 1 1 1 I 0
Paroreomyza
maculata 0 0 0 ? ? ? ? ? ? 0 0 0 1 2 2 1 1 1 2 0 0
Paroreomyza
montana 0 0 0 ? ? ? ? ? ? 0 0 0 1 2 2 1 1 1 2 0 0
Paroreomyza
fiammea 0 0 0 ? ? ? ? ? ? 0 0 0 1 2 2 1 I I 2 0 0
Pseudonestor 1 1 1 ? ? I ? ? ? '? 2 2 1 ? 1 2 1 0 2 2 0
Oreomystis
maria
Oreomystis
bairdi
Loxops cocci-
Loxops caeru-
leirostris
Hemignathus
sagittirostris 1 I ? ? ? ? ? ? ? ? 2 2 1 ? 3 3 I 2 2 0 0
Hemignathus
virens
Hemignathus
tiara
Hemignathus
kauaiensis
Hemignathus
parvus
Hemignathus
ellisianus
Hemignathus
obscurus
Hemignathus
lucidus han-
apepe
Hemignathus
lucidus luci-
dus
Hemignathus
lucidus affin-
is
Hemignathus
munroi
I 1 1 ? ? ? ? '? I ? 2 2 1 I 2 1 1 1 2 0 0
1 1 1 0 1 ? 0 1 0 ? 2 2 1 ? 2 I 1 1 2 0 0
I 1 I ? ? ? ? ? ? 1 2 2 I 1 3 3 1 2 2 3 0
1 1 1 ? ? ? ? ? .9 ? 2 2 1 .9 3 3 I 2 2 3 0
1 I 1 0 I 0 I 1 1 ? 2 2 1 2 3 3 1 2 2 0 1
1 1 1 0 I 0 ? 1 1 ? 2 2 1 2 3 3 I 2 2 0 1
1 1 I 0 1 0 ? I 1 ? 2 2 1 2 3 3 1 2 2 0 1
l 1 1 ? ? ? ? ? ? ? 2 2 I ? 3 3 1 2 2 0 0
1 1 ? 0 1 0 1 1 0 1 2 2 I I 3 3 1 2 2 0 1
1 1 ? ? ? ? ? 1 0 1 2 2 1 1 3 3 1 2 2 0 I
1 1 ? ? ? ? ? ? ? ? 2 2 1 ? 3 3 I 2 2 4 1
I 1 ? ? ? ? ? ? ? ? 2 2 1 ? 3 3 1 2 2 4 I
1 1 ? ? ? ? ? ? ? ? 2 2 I ? 3 3 1 2 2 4 1
I 1 I 0 1 I 1 1 0 ? 2 2 1 ? 3 3 I 2 2 4 1
(Raikow et al. 1990). Further complicating mat- though the placement of that genus among the
ters is the lack of information on the plantaris others remains controversial. The phenotypic ev-
condition of 'akepas, the Greater 'Amakihi, and idence in this case, which includes certain and
the 'Anianiau. Thus the hypothesis that the plan- probable synapomorphies of plumage sequence,
taris has been lost more than once in drepanidine coloration, bill and tongue morphology, vocali-
evolution is by no means far-fetched, and the zations, social behavior, and ecology are too nu-
usefulness of this character in reconstructing merous and varied to be dismissed out of hand,
phylogeny is severely compromised. Neverthe- as has been done in recent molecular studies,
less I included it (Character 9) in my analyses none of which have even mentioned this striking
as an unordered character. conflict of genetic and phenotypic data. Nor in
The case for inclusion of the Hawai'i Creeper my opinion can so many similarities be credibly
in Oreomystis based on "traditional" taxonomic attributed to convergence or homoplasy.
data is straightforward, unequivocal, and sup- R.L. Fleischer (pets. comm.) has suggested that
ported by every tree topology in this study, al- a past hybridization event could produce the re-
HAWAI'I CREEPER Pratt 95
TABLE 3. EXTENDED.
Character state
22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46
0 0 1 1 0 0 0 0 0 0 0 0 0 ? 1 ? 1 ? 1 0 1 0 0 1 0
0 1 1 1 0 0 0 0 0 3 1 0 2 1 3 ? ? ? I 1 0 3 1 3 2
0 1 1 1 0 0 0 0 0 3 1 0 2 1 3 ? 1 1 1 1 0 3 2 1 0
0 1 1 1 0 0 0 0 0 3 1 0 2 1 3 ? ? ? 0 1 0 1 0 0 0
0 0 1 1 2 0 0 0 0 4 2 2 2 0 4 1 0 0 1 1 2 3 2 1 2
0 2 1 2 0 0 0 0 3 4 2 1 0 1 4 1 0 0 1 1 0 2 1 0 0
0 2 1 2 0 0 0 0 3 4 2 1 2 1 4 ? ? ? 1 1 0 1 0 0 0
0 2 1 1 0 0 0 0 0 4 2 0 2 0 4 0 1 1 0 0 0 1 0 0 0
0 2 1 1 0 0 0 0 0 4 2 0 2 1 4 2 ? 0 1 0 0 3 1 0 3
0 2 I 0 2 0 0 0 0 4 2 ? ? ? 4 ? ? ? 1 3 3 2 2 0 1
0 3 1 1 1 0 0 0 0 4 2 0 2 0 3 0 1 1 1 3 2 3 2 2 1
0 3 1 1 1 0 0 0 0 4 2 0 2 ? 3 1 ? ? 1 3 2 3 2 3 4
0 3 1 1 1 0 0 0 0 4 2 0 2 1 3 1 0 0 1 2 3 3 2 2 1
0 2 1 1 0 0 0 0 0 4 2 0 2 I 3 1 1 0 1 1 1 4 0 0 0
0 3 1 1 1 0 0 0 0 4 2 ? ? ? 3 ? ? ? 1 2 4 3 2 1 1
0 3 1 1 1 0 0 0 0 4 2 ? ? ? 3 ? ? ? 1 2 4 2 2 2 1
0 3 1 1 1 0 0 0 0 4 2 ? ? ? 4 ? ? ? 1 4 4 3 2 1 0
0 3 1 1 1 0 0 0 0 4 2 ? ? ? 4 ? ? ? 1 3 4 3 2 1 0
0 3 1 1 1 0 0 0 0 4 2 ? ? ? 4 ? ? ? 1 4 4 3 2 1 2
0 1 1 1 1 0 0 0 0 4 2 2 2 1 4 1 ? 0 1 4 4 3 2 1 0
sults seen here, but considers convergence more has clearly played a role (Grant 1986, 1994), and
likely. The name Oreomyza ( = Oreomystis) per- as Freeland and Boag (1999:584) pointed out, "it
kinsi was based on a possible hybrid specimen of is extremely difficult with existing data to differ-
which one parent was a Hawai'i Creeper (Amadon entiate between the effects of lineage sorting and
1950:176-177), so hybridization is neither unprec- hybridization." Recently, P. R. Grant (pers. comm.
edented nor unreasonable. Furthermore, if Tarr and fide Thane Pratt) reported a pattem of hybridiza-
Fleischer (1995) and Fleischer et al. (1998) are tion and subsequent backcrossing among the
correct that the drepanidine radiation resulted from Geospizinae that, if it occurred among Hawaiian
a recent rapid burst of speciation, then hybridiza- honeycreepers, could explain the apparent conflict
tion need not indicate "next-of-kin" relationship, of phenotypic and genotypic data for the Hawaii
especially because intergeneric hybrids are fairly Creeper. In such a scenario, hybrids would involve
frequent in birds (Bledsoe 1988a). In the similarly primarily, or only, male Oreomystis mating with
rapidly evolving Darwin's finches, hybridization female '5.kepas or 'amakihis. Given the song vari-
96 STUDIES IN AVIAN BIOLOGY NO. 22
Pffttirostra
Paroreomycamaculata
100 Paroreomyzamontana
Par or eornyza flammea
88 Pseudønestør
Hemignathus lucidus affinis
Hemignathus lucidus hanapepe
I Hemignathus munroi
I Hemignathus lucidus lucidus
'- 6 .em ignathm virens
I 1[ Hemignathusfiava
L4 Hemignathus kauaiensis
72[' tternignathux ellisianus
- Hemignathus ob*curus
Hemignathus sagittirostris
Hemignathus lucidus hanapepe
Hemignathus lucidus lucidus
. Hernignathus virens
Hernignathus fiava
Hernignathus kauaiensis
-- Hemignathus ellBianus
Hemgnathu sagittirostri,
100 --
t___ Loxop caeruleirostris Loxop5 caeruleirostris
Hemignathus parvu,* Hemignathus parvu.*
lOO [-- Oreom¾stis mana
Oreomstis bairdi Oreomystis mana
ß Oreom?tis bairdi
FIGURE 3. Species-level phylogeny of "hemignathine" Hawaiian honeycreepers plus Paroreomyza and Psit-
tirostra. Left, 50% majority-role consensus tree; right, strict consensus tree. Taxonomy follows AOU (1998).
ation of the latter two groups and the relative uni-
formity of Oreomystis songs, non-Oreornystis fe-
males might be more likely to mate with a male
Oreomystis than Oreomystis females to mate with
a non-Oreomystis male. Offspring of such matings
would then mate preferentially with Oreomystis or
hybrids because males would sing the songs of
their fathers and females would respond to songs
of their fathers. If the birds with mixed ancestry
became the ancestors of the Hawai'i Creeper, then
they could retain all of the phenotypic synapo-
morphies of Oreomystis but possess mtDNA,
which represents solely the female line of descent,
"stolen" from another species. Ongoing studies of
nuclear DNA (R. Fleischer, pers. comm.) may help
to solve this problem. Of course, the past hybrid-
ization event might not have involved the Hawai'i
Creeper at all; it could instead be the reason why
the 'Akikiki tums up in the "wrong" place in
some phylogenies. Indeed, the molecular and os-
teological phylogenies reviewed here are more
similar in their placement of the Hawai'i Creeper
than the 'Akikiki.
Removal of the Hawai'i Creeper from the genus
Oreomystis at this stage would clearly be prema-
ture, especially because we would have no un-
equivocal alternative. At present, the DNA labo-
ratories offer us three different hypotheses. This
analysis of phenotypic characters shows very
strong support for the current taxonomy, which is
somewhat weakly corroborated by osteological
studies and one mtDNA analysis. Furthermore,
plausible hypotheses can be offered to explain the
observed lack of genetic and phenotypic congru-
ence. Until nuclear DNA studies are completed
and possible hybridization is addressed, the pro-
dent course is to avoid taxonomic changes based
solely on molecular data. If future studies prove
that the evolution of the Hawai'i Creeper was en-
tirely independent of Oreomystis bairdi, then the
large number and varied character of apparent syn-
apomorphies of these two species will represent
one of the most remarkable and noteworthy ex-
amples of convergence ever demonstrated. That
finding would be exciting, but the burden of proof
clearly lies with those who would remove the Ha-
wai'i Creeper t¾om Oreomystis. Why is the Ha-
wai'i Creeper an Oreomystis? Because that is what
the most consistent available evidence shows it to
be.
HAWAI'I CREEPER--Pratt 97
SUMMARY
This study shows that the alpha taxonomy of
the Hawaiian honeycreepers currently in use
(AOU 1998) has a solid foundation in pheno-
typic characters. None of the taxa, with the pos-
sible exception of Hemignathus, are paraphylet-
ic, and generic limits, with a few minor excep-
tions, are reasonable. Hypothesized relationships
at variance with current usage and based on ge-
netic studies must be considered preliminary and
tentative until consistent results are achieved.
Taxonomic and sequence changes suggested by
these results include: 1) the merger of Chlori-
dops and Loxioides, or at least adjacent place-
ment in the taxonomic order; 2) removal of the
'Anianiau from Hemignathus and classification
as Magumma parva; 3) recognition of four sub-
genera of Hemignathus (Hemignathus, Akialoa,
Chlorodrepanis, and Viridonia); 4) the place-
ment of Pseudonestor adjacent to Hemignathus
in taxonomic sequence, or even merger of the
two genera; 5) lumping of Vestiaria into Dre-
panis and probably also Palmeria into Hima-
tione; and 6) movement of Melamprosops and
Paroreornyza to the beginning of the sequence,
preceding Telespiza.
ACKNOWLEDGMENTS
I thank D. Kuhn for recording the 'Akikiki juveniles
for this study. Students and staff of the Louisiana State
University Museum of Natural Science helped in nu-
merous ways: D. Lane and M. Cohn-Haft assisted in
preparation of the audiospectrograms, F. Burbrink
taught me how to use PAUP and MacClade, and J. V.
Reinsen and F. H. Sheldon made numerous suggestions
that improved the manuscript. Colleagues R. L.
Fleischer, H. James, S. Olson, L. Freed, T Pratt, J.
Lepson, B. Slikas, C. Mcintosh, and R. Raikow made
valuable input by their challenging comments and
sharing of unpublished information. J. M. Scott, S. Co-
nant, and J. Rotenberry made helpful comments on
earlier versions of the manuscript.
Studies in Avian Biology No. 22:98-103, 2001.
PHYLOGENETIC PLACEMENT OF THE PO'OULI, MELAMPROSOPS
PHAEOSOMA, BASED ON MITOCHONDRIAL DNA SEQUENCE
AND OSTEOLOGICAL CHARACTERS
ROBERT C. FLEISCHER, CHERYL L. TARR, HELEN F. JAMES, BETH SLIKAS, AND
CARL E. MCINTOSH
Abstract. The Po'ouli (Melamprosops phaeosoma) is a small oscine songbird first discovered on
Maui in the early 1970s and originally described as a member of the Drepanidini (Hawaiian honey-
creepers). A recent study suggested that the Po'ouli may not be a drepanidine because it lacks most
of a small set of drepanidine synapomorphies (e.g., specialized tongue morphology and distinctive
odor). We conducted phylogenetic analyses of the Po'ouli and a number of drepanidine and potentially
related songbird taxa. Our character sets included mitochondrial DNA sequences (obtained for Me-
lamprosops via PCR of DNA isolated from museum specimens) and osteological characters. Analyses
support the placement of the Po'ouli within the drepanidine clade, although the position of the Po'ouli
within the clade is not strongly supported by either data set. Our results indicate that the Po'ouli is
relatively distinct phylogenetically among drepanidines. If a goal of biodiversity conservation is to
retain as much genetic diversity as possible then the Po'ouli should be considered a species of very
high priority for conservation efforts.
Key Words: ancient DNA; Drepanidini; Melamprosops phaeosoma; mitochondrial DNA; osteology;
phylogeny; Po'ouli.
In 1973 a new genus and species of Hawaiian
bird was discovered by a group of student re-
searchers in a small area of rainforest on the
north slope of Haleakal Volcano on Maui. It
was described from two collected specimens as
the first new, living species of Hawaiian hon-
eycreeper (Drepanidini) to be found in over 50
years (Casey and Jacobi 1974). Later, however,
doubts arose concerning whether this small,
brown, snail-eating bird is a drepanidine or some
other type of songbird (Pratt 1992a). It was giv-
en the scientific name Melamprosops phaeoso-
ma, and the common Hawaiian name Po'ouli
(which means "black-faced" in reference to its
prominent black mask). The Po'ouli is now on
the verge of extinction. Recent and intensive ef-
forts to locate the species has resulted in detec-
tion (and marking) of only three individuals (S.
Reilly and M. Collins, pers. comm.; Reynolds et
al. this volume). It is possible that this number
represents the entire living population for the
species.
Although the Po'ouli differs in morphology,
behavior and ecology from other living Hawai-
ian birds (Pratt et al. 1997b), its phylogenetic
uniqueness and closest relatives remain uncer-
tain (Bock 1978, Pratt 1992a). According to
Pratt (1992a), Melamprosops completely lacks
the few synapomorphies that define the Drepan-
idini, most notably the unique musty odor and
specialized tongue characteristics. It also differs
from all known drepanidines in plumage color
and pattern, bill morphology, vocalizations, diet
(i.e., specialization on snails), and other aspects
of behavior (Pratt 1992a). Knowledge about the
relationships and phylogenetic uniqueness of the
Po'ouli will help in deciding how much effort
should be expended to recover the species (Faith
1992, Krajewski 1994). Here we present cladis-
tic analyses of mitochondrial DNA sequences
and skeletal morphology that indicate that this
troubling (and troubled) little bird is a Hawaiian
honeycreeper, albeit an extremely distinctive
one.
METHODS
SAMPLED TAXA
We compared DNA and skeletal characters of Me-
lamprosops to a sampling of taxa from within the Dre-
panidini, Carduelini, Fringillini, Emberizinae, and oth-
er outgroups. Common and scientific names of North
American and Hawaiian taxa follow the AOU Check-
list (1998). Common and scientific names of other
taxa, and subfamily classifications, are from Monroe
and Sibley (1993).
Drepanidini analyzed for mtDNA sequence or os-
teology (see Figs. I and 2) include Nihoa Finch, Te-
lespiza ultima; Lay_san Finch, T. cantans; Palila, Lox-
ioides bailleui; '0'0, Psittirostra psittacea; Lfina'i
Hookbill, Dysmorodrepanis munroi; Maui Parrotbill,
Pseudonestor xanthophrys; Kaua'i Creeper, Oreomys-
tis bairdi; Hawai'i Creeper, O. mana; Maui 'Alauahio,
Paroreomyza montana; 'Akeke'e, Loxops caeruleiros-
tris; 'kepa, L. coccineus; 'Akiap61'au, Hemignathus
munroi; Lesser 'Akialoa, H. obscurus; 'Anianiau, H.
parvus; Kaua'i 'Amakihi, H. kauaiensis; O'ahu 'Ama-
kihi, H. fiavus; Maui 'Amakihi, H. virens wilsoni; Ha-
wai'i 'Amakihi, H. v. virens; 'I'iwi, Vestiaria cocci-
nea; Hawai'i Mamo, Drepanis pacifica; 'Apapane,
Himatione sanguinea; and ',kohekohe, Palmeria do-
lei.
Carduelini analyzed include the White-browed Ro-
sefinch (Carpodacus thura, Genbank number
98
PLACEMENT OF PO'OULI Fleischer et al. 99
69
92
! White-browed Rosefinch
Carduelini
Buff-barred Warbler
FIGURE l. Phylogenetic tree constructed using a maximum parsimony criterion from mitochondrial DNA
cytochrome b sequences. The phylogram is one of two maximum parsimony trees of (weighted) length 1255
and CI of 0.53. The numbers at particular nodes are the percentage of trees containing the node following a
500 repetition bootstrap. Nodes with percentages below 50% are not noted. These nodes are assumed to be
unresolved and their branches collapse to a polytomy. See Methods for scientific names of taxa exhibited here.
AF015765), House Finch (C. mexicanus; Fleischer et
al. 1998), Common Rosefinch (C. erythrinus), Purple
Finch (C. purpureus), Spot-winged Grosbeak (Mycer-
obas melanozanthos), Evening Grosbeak (He6Ieri-
phona ve67ertina), Desert Finch (Rhodopechys obso-
leta), Golden-winged Grosbeak (Rhynchostruthus so-
cotranus), European Greenfinch (Carduelis chloris),
Pine Siskin (C. pinus) Red Crossbill (Loxia curviros-
tra), Yellow-fronted Canary (Serinus mozambicus),
Grey-headed Bullfinch (Pyrrhula erythraca), Pine
Grosbeak (Pinicola enucleator), and Asian Rosy Finch
(Leucosticte arctoa). The Common Chaffinch (Frin-
gilla coelebs) is a fringilline outgroup.
Emberizines include the Green Honeycreeper (Chlo-
tophanes spiza; Fleischer et al. 1998), Scarlet-rumped
Tanager (Ramphocelus passerinii; U15717), Summer
Tanager (Piranga rubra; U15725), Prothonotary War-
bier (Protonotaria citrea; this study), Brown-headed
Cowbird (Molothrus ater; this study), Northern Car-
dinal (Cardinalis cardinalis), Black-and-white Warbler
(Mniotilta varia), Vesper Sparrow (Pooecetes grami-
neus), White-lined Tanager (Tachyphonus rufus), Red-
winged Blackbird (Agelaius phoeniceus), and Saffron
Finch (Sicalisfiaveola). Outgroups are the House Spar-
row (Passer domesticus) and the Buff-barred Warbler
(Phylloscopus pulcher; Y10732).
MITOGHONDRIAL DNA
DNA was isolated from samples taken from the only
two Melamprosops museum specimens that exist. The
tip of one small secondary feather was removed from
the B. P. Bishop Museum specimen (holotype: BBM-
X147112; under the care of C. Kishinami and A. Al-
lison), and a small piece of skin from the ventral open-
100 STUDIES IN AVIAN BIOLOGY NO. 22
e
Desert :inch
Golden-winged Grosbeat{
Carduelini Europ. ean Greenfinch
'ine Siskin
[-- Red Crossbill
[--Yellow-fronted Canary
Common Rosefinch
__ Grey-headed Bullfinch
-- Pine Grosbeak
ß -- Purple Finch
i ................ -:....A,s.i .a,n,,..R.,o. sy .F..i..n .c..h. ............
............................ L;n'fhficn .........
parrow
FIGURE 2. Phylogenetic tree constructed using a maximum parsimony criterion from a matrix of osteological
characters. A strict consensus of 128 optimal trees found by repeated random searches of these data (500
replicates, closest addition sequence with ten trees held at each step, initial tree improved upon with TBR branch
swapping; optimal tree length 286 steps). See Methods for scientific names of species included in the tree.
ing was taken from the American Museum of Natural
History specimen (paratype: AMNH-810456; under
the care of G. Barrowclough). Museum specimen
DNA was isolated in a small laboratory dedicated to
ancient DNA analyses using "ancient DNA" proce-
dures (e.g., Cooper et al. 1996, Paxinos et al. 1997).
Modem DNA analyses were conducted in a laboratory
separated by >500 m from our ancient laboratory.
Briefly, DNA was isolated by digesting skin or feather
pulp overnight at 55 ø C in a DTT-SDS-EDTA buffer
with proteinase K, followed by phenol and chloroform
extractions and centrifugal dialysis to remove buffer
and other solutes (as in Paxinos et al. 1997).
We amplified and sequenced two regions of mtDNA
from the museum and modern specimens (Fig. 1) using
the polymerase chain reaction and specific primers: (1)
675 bp of the Cytochrome b (Cyt b) gene in two over-
lapping pieces (see Fleischer et al. 1998); and (2) 224
bases of the 5' end of the mitochondrial control region
(CR; Tarr 1995). Cyt b and CR sequences were also
obtained for some non-drepanidine songbird species
from Genbank (see Fig. 1). The Cyt b sequence was
PLACEMENT OF PO'OULI Fleischer et al. 101
amplified only from the AMNH specimen, and ana-
lyzed with 18 other drepanidine taxa as reported in
Fleischer et al. (1998). The CR segment was amplified
from the BPBM specimen only, and from an additional
6 drepanidine species. PCR controls were negative
(i.e., no apparent product produced) for the study skin
amplifications for both Cyt b and CR. Sequences were
produced either manually as in Fleischer et al (1998)
or on an ABI-373 automated DNA sequencer as in
Greenberg et al. (1998), and were aligned with Se-
quencher 3.0. Phylogenetic reconstructions and other
analyses utilized PAUP*4.0d64 (D. Swofford, pers.
comm.) and MacClade 3.01 (Maddison and Maddison
1992), and are described in the results section below.
OSTEOLOGY
A subset of data froin a separate study of cranial
osteology and phylogeny in the drepanidines (James
1998) was used to determine if the Po'ouli is supported
as part of the drepanidine clade. The original study
involved 72 characters and 55 species of drepanidines,
including 17 fossil species that became extinct follow-
ing hutnan settlement of the archipelago less than two
thousand years ago (James and Olson 1991). For the
present study, the fossil taxa were excluded in order
to specifically examine the phylogenetic placement of
Melamprosops relative to extant or historically extinct
drepanidines. Twenty-one other species of nine-pri-
maried oscines were included so that other potential
relationships might be revealed. Passer domesticus
was included as an outgroup. The resulting matrix had
45 terminal taxa and 57 informative characters.
The osteological matrix was analyzed using a par-
simony criterion. All characters were mn as ordered
characters except for seven multistate characters that
were run as unordered because the states were not
judged to be sequential. Ten characters had an essen-
tially binary distribution of states except that a few
taxa showed intermediate conditions. In these in-
stances, the intermediate condition was scored as a
third state, but the character was assigned a weight of
0.5 for the parsimony analyses, to prevent intermediate
conditions froin exerting an undue influence on tree
length. All other characters were unweighted.
RESULTS
MITOCHONDRIAL DNA
Cladistic parsimony analyses of the Cyt b se-
quences consistently place the Po'ouli within the
Drepanidini (Fig. 1). We initially ran a heuristic
search in PAUP* with replicated, random addi-
tion and no character weighting, and obtained
seven equally most parsimonious trees for dre-
panidines and carduelines. A maximum likeli-
hood (ML) estimate of the transition-to-trans-
version ratio was then made using the tree with
the lowest ML score (ts:tv -- 4.0:1). This ratio
was used to weight transversional changes, and
a heuristic search generated two maximum par-
simony trees of length 1255 (unweighted for the
same topology is 685 steps) and a consistency
index of 0.53 (Fig. 1). Placement of Melampro-
sops within the Drepanidini, however, occurs re-
gardless of whether transversions are weighted
4.0:1, 10.0:1, or unweighted relative to transi-
tions (although weighting and additional out-
group taxa does affect the topology of drepani-
dine relationships). Forcing the Po'ouli from the
Drepanidini to the Carduelini (in MacClade;
Maddison and Maddison 1992) increases the
length of the tree (unweighted) in Figure 1 by
12 additional steps. This constrained tree is sig-
nificantly longer than that of Figure I based on
both parsimony (Kishino-Hawegawa test, t =
2.69, P = 0.0072; Kishino and Hasegawa 1989)
and maximum likelihood (G = 52.71, P <
0.001; Felsenstein 1988) tests. Making Melam-
prosops the sister to each emberizine clade also
significantly increases tree length (by 20-27 ad-
ditional steps; Kishino-Hasegawa test, t = 3.56,
P < 0.001).
Distance analyses further support a drepani-
dine relationship for Melamprosops. Kimura 2-
parameter and gamma-corrected distances were
lower for comparisons of the Po'ouli and dre-
panidines (0.086 -+ 0.002, range 0.062-0.102)
than for comparisons of the Po'ouli and cardue-
lines (0.147 + 0.005, range 0.142-0.152) or
berizines (0.196 -+ 0.010, range 0.170-0.218).
The CR sequence analyses also place the
Po'ouli within the Drepanidini. First, three sin-
gle-base deletions found in the Fringillini and
Carduelini CR sequences do not occur in dre-
panidines nor in Melamprosops CR sequence
(Table 1). Second, 1000 replication bootstraps of
maximum parsimony trees (with gaps and trans-
versions weighted 10:1 or 5:1 over transitions;
heuristic search) reveal 88% and 90% support,
respectively, for monophyly of the drepanidines,
including the Po'ouli. Last, forcing the Po'ouli
from the Drepanidini into the Carduelini (i.e.,
sister to Carduelis chloris) or Emberizinae (i.e.,
as a sister to Melospiza georgiana) increases un-
weighted tree length by 4 and 10 steps, respec-
tively. The constrained trees are significantly
longer (Kishino-Hasegawa test, t = 2.15, P =
0.032 when sister to Carduelis; t = 2.32, P =
0.021 when sister to Melospiza).
OSTEOLOGY
Parsimony analysis produced 128 equally
most parsimonious trees from which we derive
a strict consensus tree (Fig. 2). The Po'ouli is
nested within the drepanidine clade in all of the
128 trees. Moving the Po'ouli outside the dre-
panidine clade to a position as sister to either
cardueline terminal taxa or cardueline resolved
clades adds 9 to 23 additional steps to the total
tree length. Making the Po'ouli a sister taxon to
Fringilla or any emberizine outgroup adds 13 to
20.5 steps.
102 STUDIES IN AVIAN BIOLOGY NO. 22
TABLE 1. LISTED ARE 67 VARIABLE NUCLEOTIDE SITES (OF 224 TOTAL) FROM THE 5'-END OR LEFt DOMAIN OF
THE MITOCHONDRIAL CONTROL REGION ASSESSED FOR ONE EMBERIZINAE (MELOSPIZA GEORGIANA; GREENBERG ET AL.
1998) AND TEN FRINGILLINAE, INCLUDING THREE FRINGILLINI (FRINGILL4; MARSHALL AND BAKER 1997), ONE CAR-
DUELINI (CARDUELIS; MARSHALL AND BAKER 1997), AND SIX EXTANT MEMBERS OF THE DREPANIDINI (TARR 1995)
Melospiza georgiana
Fringilla teydea
Fringilla montifringilla
Fringilla coelebs
Carduelis chloris
Paroreomyza montana
Loxioides balleui
Telespiza cantans
Hemignathus parvus
Hemignathus kauaiensis
Himatione sanguinea
Melamprosops phaeosoma
1 2 3 4 5 6
1234567890123456789012345678901234567890123456789012345678901234567
TAGCCACGACACCTTATTATGAA-CCACTAGTGA-A-AACACTCCCGTAGGTATATTCAATAGATAG
.... TGTA.-.T ..... A.C..TA..T .... A..-.-.G.TA..T...T .... -.GCTTC.TA.C..
.... T.TAG-..AC ......... -..T.CC.GA.-.-.G.TA ...... T .... -.GCTTC.TA.C..
C .... G...T .......... A..-A.T .... A..-.-.G.TA ...... T .... -.GCTTC.TAGC.A
.CAAT.A .... GT ....... A.TAA.CT...GA.-G-.GA.A..T .... ACAT-GCCTGCCTAGC..
.CA...A...GATC ..... C.CTA.AC.AG.GAGG.TGG ....... ACT ....... C..C.T..C..
.CA.T.A .... G .... C..C.CCAA.T.AC.C..G.G.G ........ GT ...... C...C.T .....
.CA...A...GGT.C.C...ACCA.AC.A ..... G.G.G ..... NNNNN ...... C...C.TT.C..
.CA...A...GA ...... G.ATCAAAC.A..A..G.NNG ....... AGT .... G .... TC.T..C..
.CA.T.A...GA ........ ACCCAAC.A..A..A.A.G...C...CAC .... AG.C.TC.T..CC.
.C..TTA...G ........ C.CTAAAC.ATCAC.G.NNG .... A.T..T...CG..C.TC.T..C..
.CA.T.A ........ C ..... TTC.AT.A..A..G.NNG...NN-NNNNN ...... GCTTC.T..C..
Note: Melamprosopx phaeosoma sequence is froin this study. A "." indicates identity of the nucleotide to the topmost base and an "N" indicates
a base that could not be calle& A "-" indicates a gap or deletion in the sequence. Note the three insertions found in all drepanidines relative to
l¾ingillines (at sites 35, 37, and 54). In addition, there are three drepanidine transversional synapomorphies (22, 26, and 29). See Fig. 1 for common
names of drepanidine taxa.
DISCUSSION
In spite of Pratt's (1992a) assessment that the
Po'ouli might not be a drepanidine, we find con-
sistent evidence to the contrary. Pratt (1992a)
notes that the Po'ouli should be considered a
"nine-primaried oscine of uncertain affinities,"
and that it "does not look, smell, act, or sound
like a Hawaiian honeycreepen" Our DNA evi-
dence places Melamprosops within the drepani-
dines, and osteological characteristics indeed
make the Po'ouli "look" like a honeycreeper.
How does one reconcile the apparent morpho-
logical, ecological, and behavioral distinctive-
ness of the Po'ouli (Pratt 1992a; Pratt et al.
1997b, this volume) with our results? Two ex-
planations may account for this: (1) some of the
phenotypic traits that Pratt emphasizes (i.e.,
those associated with foraging mode and feed-
ing) may be affected by adaptive radiation and
thus we might expect to see wide diversity in
their character states; and (2) some of the 17
extinct drepanidine species known only from
fossils may have shared these traits with the
Po'ouli, thus making it different only in the con-
text of living or historically extinct taxa. We do
not know what factors effected the evolution of
the brownish coloration and the black facial
mask, nor why Melamprosops (and apparently
Paroreomyza; Pratt 1992b) lack the distinctive
drepanidine odor.
While our results indicate that the Po'ouli is
a Hawaiian honeycreeper, the relationships of
the Po'ouli within the drepanidines are not well
resolved by the mtDNA data (Fig. 1). Majority
rule bootstrap analysis results in collapse of sup-
porting branches such that Melamprosops be-
comes a basal drepanidine lineage. On the strict
consensus for the morphological trees, the
Po'ouli joins at a node proximal to the finch-like
species but distal to most other living drepani-
dines. It is not depicted as the sister group of
any living drepanidine species. Thus, in both
mtDNA and osteological trees the Po'ouli ap-
pears to represent a unique drepanidine lineage.
Its lineage may have diverged from other dre-
panidine lineages prior to evolution of the syn-
apomorphic characters defined by Pratt (1992a).
How phylogenetically distinct is the Po'ouli
among living drepanidines? To answer this we
estimated the contribution of each taxon to the
PLACEMENT OF PO'OULI--Fleischer et al. 103
total minimum evolution score for the Cyt b tree
in Figure 1. In PAUP*, we constrained the tree
topology, pruned a taxon from the tree, then re-
calculated the ME score. The process was re-
peated for each drepanidine taxon; each ME
score was subtracted from the total ME score to
provide a phylogenetic "distinctiveness" score
(U) for the taxon (essentially that of Faith 1992).
The Po'ouli had the highest U (0.044) among
the 19 drepanidines (mean and SE of U for the
other 18 taxa was 0.015 +_ 0.002). To evaluate
the Po'ouli's distinctiveness in the osteology-
based tree we constrained the tree in Figure 2 in
MacClade 3.01. A drepanidine taxon was re-
moved and the length of the reduced tree was
subtracted from the length of the total tree. The
procedure was repeated for each of the 23 dre-
panidines, and revealed that the Po'ouli was the
fourth most distinctive taxon based on osteology
(after Maul and Kauai creepers and the 'Akia-
p61'au). Thus we consider the Po'ouli to be
phylogenetically unique among the drepanidi-
nes, and the taxon that individually contributes
most to extant drepanidine phylogenetic diver-
sity.
The closest corrected genetic distance be-
tween the Po'ouli and other drepanidines is
0.062. Applying a corrected internal rate cali-
bration for Cyt b in honeycreepers of about
0.016 +_ 0.005/MY (from Fleischer et al. 1998)
suggests that the Po'ouli split from its nearest
living drepanidine relative about 3.8 +_ 0.9 MY
ago (fairly early in the drepanidine radiation;
Tarr and Fleischer 1995, Fleischer et al. 1998).
Of course extinct fossil drepanidines (James and
Olson 1991) not included here, such as Xestos-
piza, may turn out to be more closely related
genetically. Nonetheless, in comparison to other
extant drepanidines, the Po'ouli has had a long,
independent evolutionary history. This long pe-
riod of independent evolution can perhaps ex-
plain some of Melamprosops' unique phenotyp-
ic characteristics. Such phylogenetic distinctive-
ness also increases the Po'ouli's conservation
value, in that the species represents a significant
fraction of the genetic diversity of the drepani-
dines (Faith 1992, Krajewski 1994). Along with
its singular ecological, behavioral, and morpho-
logical characteristics, the Po'ouli's unique evo-
lutionary history convinces us that serious ef-
forts should be undertaken to avoid its impend-
ing extinction.
ACKNOWLEDGMENTS
We gratefully acknowledge C. Kishinami and A. Al-
lison of the B. P. Bishop Museum, and G. Barrow-
clough of the American Museum of Natural History,
for allowing us to sample from the precious Po'ouli
specimens under their care. The Smithsonian Institu-
tion's Walcott and Wetmore Funds, the National Geo-
graphic Society, and the Friends of the National Zoo
provided funding for our Hawaiian honeycreeper re-
search. We thank T Pratt and S. Reilly for providing
information and discussion, and D. Pratt, C. van Riper
and S. Conant for reading and evaluating the results in
the manuscript.
Status and Trends
Studies in Avian Biology No. 22:106-107, 2001.
STATUS AND TRENDS--INTRODUCTION
J. MICHAEL SCOTT AND CHARLES VAN RIPER, III
The first postcontact attempts to assess the
status of Hawai'i's birds were the collection of
birds by naturalists of Cook's third voyage of
exploration (Medway 1981). Additional 18 th and
19 th century attempts to document the occur-
rence of birds in Hawai'i were sporadic and in-
completely reported, and are documented in de-
tail elsewhere (Olson and James 1994a). In the
last decade of the 19 th century and in the first
years of the 20 th century, there was renewed in-
terest in the birds of HawaiT Henry Palmer col-
lected for Walter Rothschild, and S. B. Wilson
obtained specimens that resulted in publication
of his and Evans's monumental works on the
avifauna of Hawai'i (Wilson and Evans 1890-
1899, Rothschild 1893-1900). The Nihoa Finch
(Telea19iza ultima) was described in 1917 (Bryan
1917) and the Nihoa Millerbird (Acrocephalus
familiaris) in 1924 (Wetmore 1924), but the
Po'ouli (Melamprosops phaeosoma) would not
be described until 1973 (Casey and Jacobi
1974). During this same period, Henshaw
(1902a) and Perkins (1903) added much to our
knowledge of the turn of the century status and
distribution of birds in Hawai'i. It was not until
George C. Munro's efforts to survey the avifau-
na of the islands from 1935 to 1937 that anyone
would attempt to systematically ascertain the
20 th century status of HawaiTs native avifauna
(Munro 1944).
The husband and wife team of Charles and
Elizabeth Schwartz conducted an 18-mo survey
of the game birds of the territory of Hawai'i
(Schwartz and Schwartz 1949). The objectives
of this survey were "to ascertain the game birds
present on the Hawaiian Islands, their distribu-
tion and abundance and factors upon which their
welfare depends." Several surveys of the Lee-
ward Islands followed (Bailey 1956, Amerson
1971, Amerson et al. 1974, Clapp et al. 1977,
Woodward 1972). Richardson and Bowles
(1964) conducted an exhaustive survey of
Kaua'i, one that resulted in the last documented
field observations of the 'Akialoa (Hemignathus
ellisJanus). Their observation that all of the spe-
cies known to have occurred on Kaua'i could
still be found there resulted in the state of Ha-
wai'i setting aside the Alaka'i Swamp as a re-
serve.
John Sincock and Gene Kridler, both of the
U.S. Fish and Wildlife Service, set up a statis-
tically defensible set of transects allowing an es-
timate of the population size of Laysan Finch
(Tele19iza cantans) and the Nihoa Millerbird in
the Leeward Islands (Conant et al 1981, Conant
and Morin this volume). These transects have
since been monitored continuously and consti-
tute the first estimate of the numbers of Hawai-
ian birds that included variances. Sincock fbl-
lowed his efforts in the Leeward Islands by es-
tablishing a set of transects in the Alaka'i
Swamp that were used to establish the popula-
tion size of the endangered forest birds of Kaua'i
(reported in Scott et al. 1986). Interagency ef-
forts were initiated in the 1950s to monitor the
numbers of waterbirds (Engilis and Pratt 1993)
and to assess the number and distribution of the
NSn8 (Hawaiian Goose, Branta sandvicensis;
Black and Banko 1994). In 1976, nearly 100
years after its discovery (Wilson and Evans
1890-1899), the first ever attempt to estimate
the population size of the Palila (Loxiodes bail-
leui) was conducted (van Riper et al. 1978). That
effort established that the Palila was more abun-
dant than previously thought, thus documenting
the value of statistically based surveys of the
entire range of a species. Winston Banko pro-
vided an exhaustive review of the literature on
Hawaiian birds and documented all known re-
cords (Banko 1979, 1980a,b,c,d; 1981a,b;
1984a,b; 1986)
The second range-wide survey of the Palila
occurred in 1980 (Scott et al. 1984) and used the
variable circular count. This census method has
been used in all subsequent attempts to estimate
population size of the Palila (Jacobi et al. 1996).
It was in part the success of the Palila surveys
that prompted the Hawaiian Forest Bird Survey
(HFBS) 1976-1981 (Scott et al. 1986), an effort
to survey all the forest bird habitat in Hawai'i.
The HFBS was initiated in the forests of Ka'fi
on Hawai'i in 1976 and ended deep in the heart
of the Alaka'i Swamp on Kaua'i in 1981. The
objectives of this survey were to determine the
numbers, distribution, habitat associations, and
possible limiting factors of the endangered forest
birds of the high islands of HawaiT The only
islands not surveyed were O'ahu (Shallenberger
and Vaughn 1978) and the privately owned
Ni'ihau. Since completion of this HFBS, seg-
ments of HFBS transects have been surveyed
irregularly (Reynolds et al. this volume). The
challenges of estimating the number of birds in
Hawai'i were the motivation for an international
symposium on estimating the number of terres-
trial birds (Ralph and Scott 1981).
106
STATUS AND TRENDScott and van Riper 107
Authors in this section report on more recent
efforts to assess the numbers of Hawai'i's avi-
fauna. David Ainley and his coauthors use a
combination of field observations and modeling
to assess the status of the Hawaiian subspecies
of Townsend's Shearwater (Puffinus auricularis
newelli), hereafter referred to as Newell's Shear-
water, whereas the late Miklos Udvardy and An-
drew Engilis report on 50 years of data on the
migratory Northern Pintail (Anas acuta). Mich-
elle Reynolds and Thomas Snetsinger describe
their eftbrts to monitor the status of the rarest
birds in Hawai'i, reporting on thousands of per-
son-days of field effbrt. Paul Baker describes the
status and distribution of the rarest of Hawai'i's
terrestrial birds, the Po'ouli (Melamprosops
phaeosoma) and finds three birds remaining.
The dilemma of what management actions are
dictated by such a rare species has challenged
the talents of scientists and managers alike.
Studies in Avian Biology No. 22:108-123, 2001.
THE STATUS AND POPULATION TRENDS OF THE NEWELL'S
SHEARWATER ON KAUA'I: INSIGHTS FROM MODELING
DAVID G. AINLEY, RICHARD PODOLSKY, LEAH DEFOREST, GREGORY SPENCER, AND
NADAV NUR
Abstract. We assessed the status of the endenic subspecies of Townsend's Shearwater, hereafter
referred to as Newell's Shearwater (Puffinus auricularis newelli), on Kaua'i, Hawaiian Islands, where
the only sizable population of this species renains. First, to index recent population trends, we ana-
lyzed data gathered on the 1,000-2,000 fledglings attracted to lights and picked up annually by the
"Save Our Shearwaters" (SOS) Program over a 17-year period, 1978 1994. Second, to calibrate and
to provide a denographic context to these data, we quantified breeding productivity and ruortality in
a nountain colony and nortality due to anthropogenic factors in the urban corridor that encircles the
breeding areas during seven years: 1980 1985 (summary of previous study), 1993, and 1994. Finally,
we entered rates of productivity and nortality into a Leslie ruodel to integrate these data, to evaluate
the demographic importance of different sources of nortality, and to assess the utility of SOS in
mitigating nortality frown anthropogenic factors.
During 17 years of data collection, an average 1,432 fledglings that were attracted to lights were
picked up by SOS each year; 90% were banded and released alive. Considering all of Kaua'i during
the study period, more fledglings were picked up, if breeding effort and success were higher, and the
full noon occurred in early October well before the mid-nonth peak of fledging. Overall, the annual
totals of fledglings (1) gradually decreased on the southern shore, where the level of urbanization (and
lighting) has grown to double that of the entire remainder of the island; (2) remained approxinately
stable on the eastern shore (moderate urbanization); but (3) increased narkedly on the northern shore,
where urbanization is low but grew dranatically during the study period. The relationships to urban-
ization were corroborated by natural experiments when lighting was curtailed. Research in the breeding
colony revealed (1) a high incidence of nonbreeding (46% of burrow occupants) even among expe-
rienced adults, typical of nany petrel species; (2) predation (2.5% of individuals) on subadults and
adults in the colonies by introduced house cats (Felts catus) and Barn Owls (Tyro alba); and (3)
breeding success (0.66 chicks/pair) conparable to other shearwaters with stable populations. Research
in the urban corridor revealed, conservatively, that (1) about 15% of an estimated 9,600 fledglings
produced each year are picked up by SOS, (2) annual nortality of fledglings following light attraction
during autmnn is about 10%, and (3) annual mortality to adults and subadults frown collisions with
power lines during spring and smnner (without light attraction) is 0.6-2.1%/yr. Only 15 of the 23,000
fledglings (<0.1%) initially banded by SOS have been recovered in subsequent years, but recoveries
show that first breeding occurs at about 6 yrs of age and that 1-yr-olds do not visit Kaua'i.
A Leslie model, using paraneters deterruined for the Newell's Shearwater, suppleruented by those
frown the very closely related Manx Shearwater (P. p. puffinus), indicated a balanced/stable population
when extrinsic nortality of anthropogenic origin was excluded. Factoring in predation on adults and
subadults in the colonies and mortality of fledglings and adults/subadults due to collisions with human-
nade structures produced decadal declines of 30-60% in the population, with variation depending on
the parameter values used. The nodel also showed that the SOS prograin is critical to reducing the
rate of population decline. Predation frown introduced animals proved to be the nost important cause
of decline, but collisions with structures by adults and nortality of fledglings following light attraction
were also significant.
Key Words: bird inpacts; cat predation; Hawai'i; Kaua'i; light attraction; Newell's Shearwater; oce-
anic island; population nodel; Puffinus auricularis; transnission line; urbanization.
Many populations of tropical seabirds that nest on
oceanic islands with large human populations have
been decimated by introductions of mammalian
predators, habitat destruction, and urbanization,
though the details are known only generally. Sev-
eral large tropical petrels are now endangered or
recently extinct, for example, the Bermuda Petrel
(Pterodroma cahow), Jamaican Petrel (Pt. hasita-
ta), Madeiran Petrel (Pt. mollis madeira), Fiji Pe-
trel (Pt. macgillivrayi), and Magenta Petrel (Pt.
magentae, of New Zealand; Croxall et al. 1984,
Warham 1990, Ehrlich et al. 1992, Nettleship et
al. 1994). Included in this group are those petrels
nesting among the main Hawaiian Islands, the en-
demic subspecies of Townsend's Shearwater (Puf-
finus auricularis newelli), hereafter referred to as
Newell's Shearwater, and Dark-romped Petrel (Pt.
phaeopygia sandwichensis), both of which are list-
ed by the U.S. Endangered Species Act (USFWS
1982a). Newell's Shearwater and Dark-romped
Petrel have been extirpated from most of their for-
mer nesting islands, but on Kaua'i they are still
relatively abundant (Telfer et al. 1987, Harrison
1990).
108
NEWELL'S SHEARWATER DEMOGRAPHYAinley et al. 109
The Newell's Shearwater, or 'A'o, was con-
sidered extinct as of 1908, but on Kaua'i in 1947
it was rediscovered and, in 1967, confirmed to
be breeding (King and Gould 1967, Sincock and
Swedberg 1969). A small breeding population
has been confirmed recently on the island of Ha-
wai'i (Reynolds et al. 1997a, Reynolds and
Ritchotte 1997), and the species may also nest
in very low numbers on Moloka'i and O'ahu
(Harrison 1990). Rediscovery of Newell's
Shearwater coincided with rapid growth in ur-
ban development on Kaua'i, when hundreds of
fledglings were found, having been attracted to
and, typical of all petrels (Reed et al. 1985), ap-
parently blinded by man-made lighting as the
birds made their way from nest to ocean on their
nocturnal fledgling flight (King and Gould
1967). This annual "fallout" became a major
source of mortality, because fledglings die after
being run over by cars or colliding with lights,
utility poles and wires, and buildings (Byrd et
al. 1984, Telfer et al. 1987). Shielding lights re-
duced attraction by as much as 40% in experi-
mental areas (Reed et al. 1985); for example, a
reduction in the intensity of yard lights at the
Hanalei Plantation Hotel in 1965 reduced the
fallout there significantly (King and Gould
1967). New building codes established in the
late 1980s request measures to shield lights
(State of Hawaii 1987); however, compliance
has been inconsistent (D. Ainley and R. Podol-
sky, pers. obs.).
Attempting to decrease the mortality associ-
ated with fallout, the U.S. Fish and Wildlife Ser-
vice (USFWS) and the State of Hawaii, Depart-
ment of Land and Natural Resources (DLNR),
organized the "Save Our Shearwaters" (SOS)
Program in 1978 (Telfer et al. 1987, Rauzon
1991). Residents who found fallen shearwaters
were encouraged, by advertisements in the news
media, to place them in bird boxes at "Shear-
water Aid Stations." The captured birds were
then picked up each morning and taken for re-
lease from a coastal cliff. In the 17 years through
1994, about 23,000 shearwaters have been re-
trieved, banded, and released (T Teller, unpubl.
data).
The current relatively high abundance and
easy access of the Newell's Shearwater on
Kaua'i provided the opportunity to understand
the species' ecology in the context of interac-
tions with human activity, and to test the utility
of SOS before the species' status becomes des-
perate and conservation attempts costly. What is
learned may help to protect this and similar sea-
birds as development and tourism spread to
more and more tropical islands (e.g., Croxall et
al. 1984, Croxall 1991). We report here our find-
ings during a study that included both fieldwork
and analysis of existing unpublished data gath-
ered by SOS and by government researchers
since the late 1970s. The assembled information
provided inputs into a demographic model of
population growth under various scenarios of
mortality. The model was used to evaluate the
impact of three important factors indicated in the
field studies: predation of adults from introduced
animals, mortality of fledglings after fallout, and
mortality of adults from collisions with power
lines. In addition, we use the population dynam-
ic model to project long-term stability of the
Newell's Shearwater population on Kaua'i.
METHODS
FIELDWORK
We conducted fieldwork in a mountain colony above
Kalheo (Fig.l), where the species breeding biology
was studied in the early 1980s as part of an effort to
determine whether Newell's Shearwaters could be
cross-fostered by the much more abundant Wedge-
tailed Shearwater (P. pacificus; Byrd et al. 1984). Ac-
cess to the colony was difficult but nevertheless was
easier by far than to any other colony known for New-
ell's Shearwater. Elevation of the Kalheo colony is
about 600 m. We searched for burrows among the veg-
etation on the >65 degree slopes between May and
November 1993. Burrows were marked and a line of
small sticks was erected across entrances to indicate
burrow use when brushed aside by entering or depart-
ing birds; we also noted the presence or absence of
excrement and feathers. We used a miniature infrared
TV camera (Furhman Diversified, Inc.) on a stiff co-
axial cable "snaked" down each burrow to determine
the presence of eggs or chicks. Once an egg or chick
was found, we rechecked the nest's status monthly. We
attempted to set up a second study colony at a site
called Kaluahonu, on the southern part of the island,
but found that few birds still nested there compared
with the early 1980s. In 1994, due to a shortfall in
funding and a request from the committee overseeing
the project (see Acknowledgments), we diminished
work in the Kalheo colony and allocated our efforts
elsewhere. Therefore, we checked contents of burrows
found the previous year on four occasions between late
August and mid-November. We compared our findings
on breeding productivity with the results of Teller
(1986), who participated in the cross-fostering studies
from 1981 to 1985. Results over the seven seasons
were combined in the demographic model described
below.
To guard against intrusions of feral cats (Fells catus)
and rats into our study colony, we placed a network
of live-capture traps at the entrance to our ridge-top
trails. Traps were baited every three days. In addition,
we carried no food of our own into the colony for fear
of attracting mammals.
To assess survival from the proportion of colony
occupants that may have been banded by SOS (when
birds were fledglings), we captured adult shearwaters
by blocking the burrow entrance just before dark and
waiting nearby. Upon arrival, the birds sat by the en-
trance and could be picked up easily. We checked
110 STUDIES IN AVIAN BIOLOGY NO. 22
NORTHSHORE
PRINCEVILLE
THE HAWAllAH
these birds for bands and banded them if none was
present. We quantified mortality due to collisions with
power lines during summer and to fallout during au-
tumn; results are reported elsewhere (Ainley et el.
1995, Podolsky et al. 1998).
ANALYSIS OF SOS DATA
To assess temporal and regional trends in the num-
ber of birds retrieved, we analyzed data contained in
annual reports of the SOS program from 1980 to 1993
(project W-18-R, Hawaii DLNR), as well as raw data
computerized by SOS from 1987 to 1993. We did not
use data from 1978 or 1979 in most analyses because
effort by the citizenry was reduced in the first two
years of the program relative to subsequent years (cit-
izens learned of the program each fall through adver-
tisements in newspapers and radio).
A ledger on which persons could record the place
where each bird was found was provided by SOS at
each shearwater station. In 10-15% of cases the spe-
cific pickup locality was not recorded, and in some of
these (e.g., when a citizen was commuting to/from
work) it was likely that birds were turned in at stations
some distance from the pickup locality. Beginning in
1982, to determine geographic variation in the relative
strength of fallout, SOS divided Kaua'i into ten dis-
tricts (Fig. 1) and apportioned the birds of unknown
locality to the various districts according to the SOS
station at which these birds were turned in (Telfer et
al. 1987). We combined the districts into broader
regions, a procedure that further diluted the effect of
any incorrect apportionment. The regions, and the dis-
tricts/drop-off stations comprising them, were (see Fig.
1): (1) Northshore--Hanalei-Princeville; (2) East-
shore--K¾1auea-Anahola, Kapa'a, LYhu'e, Westin La-
goons (Kaua'i Sur0 Hotel; and (3) Southshore--K-
loa-Po'ipfi, KalSheo, Hanapfipfi-Waimeae, MSnS-Kek-
aha (including Barking Sands Naval Air Station). NS-
pali-K6ke'e is included in the Northshore, but being
mostly wild land, it contributed little to SOS data.
In analyses where year was an important consider-
ation, we did not use data from autumn 1992 or from
1993, because Kaua'i was much different in ways crit-
ical to our study. Hurricane Iniki devastated human
structures on the island in September 1992, just before
the shearwaters had begun to fledge and SOS would
have swung into action. The hurricane obliterated all
bright lights; all hotels were closed due to damage and
fewer than 10% of street lights or power lines were
left standing. Life on Kaua'i did not return to normal
until summer 1994. Hurricane Iwa, in 1982, did not
pass over Kaua'i until November, after shearwater fall-
out had been completed, so the fallout data were not
affected and were included in analyses.
To maintain robust sample sizes in the data, we
made some reasonable assumptions to categorize cer-
tain data rather than discarding them from analysis.
First, dead adults were distinguished from dead fledg-
lings in the 1987-1993 SOS data, but this was not the
case in the 1980-1986 data. With no organized search
effort in 1987-1990, the average number of dead
adults/subadults found was 17/yr (see Results). So, to
estimate the number of dead fledglings reported by
SOS each autumn, 1980-1986, we assumed that the
age ratio and search effort were the same as in 1987-
1990 and, therefore, subtracted 17 "adults" from the
total number of dead shearwaters reported in each of
those years.
Second, dead adults reported during spring and sum-
mer were logged by SOS beginning in 1987. It was
not until 1991-1992, however, that a concerted search
effort for adults/subadults was made, in effect, equal
NEWELL'S SHEARWATER DEMOGRAPHY--Ainley et al. 1 11
to the effort for fledglings in autumn. In 1991, some
especially interested and knowledgeable citizens (C.
Berg, C. Orr, and K. Viernes) undertook this task and
it was continued by us in 1993 and 1994. We assumed
that patterns revealed in 1991-1994 were similar to
those in the older SOS data. Next, we assumed that
"adults" reported as dead in the SOS data after 15
September of each year included many individuals in-
correctly aged for two reasons. First, in SOS records,
peaks in number of dead birds recorded as "adults"
(many of which are flattened and thus hard to assess)
corresponded exactly to peaks of fledglings (Ainley et
al. 1995). Second, few adults visit the colonies and no
banded adults/subadults have been found after this date
(see Results). Adult shearwaters desert their young a
week or two before the fledgling departs (see Warham
1990); therefore, we considered all birds found after
15 September (the beginning of the fledging and fall-
out period) to be fledglings. To be sure, a few adults
are found after that date (T Teller, pers. comm.).
Finally, it was not until 1982 that stainless steel
bands were used by SOS on all fledglings. Prior to
then, most were banded with monel bands. Therefore,
our analyses based on return rates of banded birds do
not include the data for the 1978-1981 cohorts, assum-
ing that the monel bands were lost rapidly as a result
of immersion in sea water (Boekelheide and Ainley
1989).
To assess trends in SOS totals in the context of ur-
banization, we indexed the urbanization of Kaua'i in
two ways. Ultimately, we were interested in the num-
ber and dispersion of shearwaters, the number and dis-
persion of lights to attract them, and the number of
people available to report birds or carcasses to SOS.
Not having direct data on urbanization (e.g., the rate
at which building permits were issued), we chose two
surrogates. First, we used growth in numbers of year-
round human residents (data from the U.S. Census Bu-
reau, 1930-1990), and compared these among the
three regions to which the SOS data had been parti-
tioned (Fig. 1). From this population are the persons
who participate in SOS, with participation depending
only on the acts of encountering a shearwater, picking
it up, and delivering it to an SOS station. In the small,
close community of residents (currently 48,000 per-
sons), more and more persons would know about SOS
as the years passed and the proportion of interested
persons would not decrease. Efforts to advertise SOS
remained constant throughout the period. Next, to in-
dex trends in growth of the infrastructure developed
for the tourist industry (i.e., coastal hotels, condomin-
iums, lighted tennis courts and driving ranges, etc.),
which would not necessarily track the requirements of
permanent residents, we obtained data from the state
of Hawai'i on the number of passengers using the
Lu'e Airport each year from 1960 to 1993. This in-
frastructure (and attendant lights) would be the source
of fallout. Tourists would not know about SOS.
The following assumptions were used to relate
trends in the SOS data to urbanization. First assump-
tion: the number of fledglings retrieved by SOS in any
year is proportional to breeding population size and
reproductive success. Reproductive output, or at least
SOS totals, appears to have exhibited no continuous
trend through time, except for the occasional outlying
year (see Results). Second assumption: the number of
fledglings reported to SOS is strongly affected by the
number and distribution of lights to attract them. This
effect of lights, proposed also by Teller et al. (1987),
was verified experimentally when lighting was severe-
ly reduced at the Hanalei Plantation Hotel in the 1960s
(King and Gould 1967), at the Kaua'i Surf/Westin La-
goons Hotel after 1983, and throughout Kaua'i as a
result of Hurricane Iniki during 1992-1993 (see Re-
sults). Third assumption: the number of citizens pres-
ent on Kaua'i also directly affects the number of birds
reported. The latter two factors (i.e., number and dis-
tribution of lights plus number of persons available to
encounter birds) would determine the proportion of
fledglings produced that were attracted to lights, went
aground, and were picked up. Final assumption: be-
cause the shearwater population incurs a cost through
mortality from fallout (i.e., some birds die regardless
of SOS), the cost, if high enough, can lead to popu-
lation decline (i.e., too many fledglings die due to ef-
fects of urbanization). It is possible that the proportion
of fledglings attracted and picked up could become
saturated (i.e., an asymptote is reached whereby ad-
ditional lights and people do not lead to more birds
retrieved). This would argue also, however, for fallout
cost to reach a maximum early in the growth of urban
development (an important consideration; see below).
MODELING
We developed a population-dynamic model for the
Newell's Shearwater, using assumptions similar to
those used by others in analogous contexts (e.g., Si-
mons 1984, Beissinger 1995, Shannon and Crawford
1999), to project population trajectory with and with-
out mortality due to anthropogenic factors and to quan-
tify the relative impact of those threats. We used a
Leslie model (Leslie 1945), which combines age-spe-
cific fecundity and survival to estimate population
growth rates. Due to lack of information about year-
to-year variation in demographic parameters, which is
the case for the vast majority of demographic studies
of wild, long-lived vertebrates, we assumed average
(constant) values for the parameters. Owing to lack of
data regarding age-related variation in demographic
parameters among shearwaters and other procellari-
iforms (e.g., Bradley et al. 1989, Wooller et al. 1989),
and consistent with the efforts of other researchers, we
also made the simplifying assumption of age-constant
survival and reproductive success for individuals that
have reached adulthood.
Our approach, first, was to determine the combina-
tion of parameter values that produced a stable popu-
lation. Against this, current population parameters
could be compared to show that, in the absence of
recent anthropogenic activity, Newell's Shearwaters
can maintain their numbers. Second, we used conser-
vative, best estimates for each parameter and compared
population projections that did and did not include var-
ious factors affecting population growth. The factors
considered were: (1) mortality of fledglings attracted
to lights and subsequently grounded during autumn
(fallout), (2) mortality of adults and subadults that col-
lide with utility structures during spring and summer,
(3) predation of adults and subadults in the breeding
112 STUDIES IN AVIAN BIOLOGY NO. 22
F- ESTIMA]EO / MEASURED
130
.110
1 oo
20 I 90
o
lO
4o
2o
o lo
o
'o B
u MEAN 1.7%
D
m 1 91-94MEAN61/YR .! I
] 87-90 MEAN 17/Y"
o 8%90 MEAN
20
<
1980 1988 1990 1980 1985 1990
FIGURE 2. Summary of SOS data for Newell's Shearwaters on Kaua'i, Hawaiian Islands: (A) total fledglings
retrieved annually, 1980-1994; (B) percentage of fledglings that died in captivity during those years; (C) the
number of fledglings, and (D) number of adults, respectively, as reported dead on the road (not retrieved). The
number of dead fledglings was estimated for years prior to 1987 (see Methods).
colonies, and (4) reduction of mortality to fledglings
as a result of the SOS program in autumn.
For all analyses, we used the computer package
STATA (Computer Resource Center 1993). Averages
are reported with + 1 SE.
RESULTS
BREEDING EFFORT AND SUCCESS
Telfer (1986) monitored 36-47 burrows in the
Kalaheo colony during 1981-1985, and we
monitored 58-65 burrows, including many in
Telfer's sample, in 1993-1994. Among the bur-
rows checked in 1981-1985, the proportion in
which breeding adults occurred (i.e., eggs or
chicks found) averaged 46.5% + 6.4% (range
30% to 62%). In 1993, the proportion was 26%,
although this is a minimum as some eggs prob-
ably were lost before we finished our search for
burrows (which took two months). In 1994, our
effort was insufficient to derive an estimate of
reproductive effort (see Methods). In 1993, 58
burrows were visited by shearwaters (88%);
thus, a high level of nonbreeding (no eggs laid)
was apparent. Not determined in 1981-1985 was
the proportion of burrows that actually were ac-
tive (i.e., used regularly regardless of whether
an egg was laid).
Among nests in which eggs were laid, an av-
erage 66.0% _+ 6.4% (range 49-75%) succeeded
each year, from 1981 to 1985; in 1993 only 27%
succeeded and in 1994 81% succeeded. Like
Telfer in 1981-1985, we could not ascertain the
cause of mortality of most chicks. Only three of
the 1994 chicks were from burrows in which
eggs were laid in 1993; conversely, among the
sites that produced chicks in 1994, 11 were ac-
tive but none of these produced eggs or chicks
in 1993. In total, the Newell's Shearwater pro-
duced 0.66 chicks/breeding pair/yr during the
1981-1985 period.
On average, 1,432 fledglings were reported to
SOS each year, ranging from 950 (1992) to
2,200 (1987; Fig. 2A). Some of the variation
was explained by differences in the timing of
moon phases from one year to the next. It ap-
pears that when the full moon occurs in mid-
October, the peak of fledging (Telfer et al. 1987,
Ainley et al. 1997b), as in 1981, the total num-
ber of individuals found during all of the fledg-
ling period (mid-September to early November)
is much lower than if the full moon occurs at
the periphery of peak fledging, i.e., in early or
late October (Fig. 3). Breeding effort and suc-
cess probably also affect the number of fledg-
lings picked up; for instance, 1987 was a year
when ocean productivity in the shearwaters'
feeding grounds was unusually high (see Dis-
cussion) and the number of fledglings picked up
was higher than expected. Nineteen eighty-seven
NEWELL'S SHEARWATER DEMOGRAPHY--Ainley et al. 113
2OO0
$?
¸
lOO0
FIGURE 3.
DATE OF FULL MOON IN OCTOBER
The total number of fledgling Newell's
Shearwaters on Kaua'i, Hawaiian islands, retrieved by
SOS each autumn (Sept-Nov), 1980-1994, as a func-
tion of how closely the full moon coincided with the
peak of fledging (mid-October). The point for 1987
was not used to generate the regression line (r 2 =
0.572, F. = 7.36, P = 0.009; see text). Number by
black and white circles indicates yean
was also a year when the full moon did not oc-
cur during the middle of fiedging and, thus, the
two factors (high ocean productivity, timing of
full moon) combined to produce high fallout
numbers. Finally, curtailment of lighting, as
Hurricane Iniki accomplished in 1992-1993
(and even into 1994 somewhat), brought fewer
fledglings to ground (Fig. 2A). The same pattern
can be seen locally at the Kaua'i Surf/Westin
Lagoons Hotel when lighting was adjusted dur-
ing renovations in 1983 (Fig. 4B) as subsequent
fallout was much lower.
MORTALITY
Breeding colony
We found one fresh adult carcass and six skel-
etons of adults or subadults in the colony during
1993. In 1994, we found 23 dead shearwaters.
All were skeletons of adults that had been killed
in the early spring during courtship two months
before our first visit, and each had marks on the
sternum to suggest eating by a cat. Almost all
dead birds were found in the lower two-thirds
of the study area indicating that the cat entered
the colony from the sugarcane fields below the
colony rather than using our access above the
colony. Telfer (1986) found cat predation to be
significant especially during the second year of
his five year study.
We caught one cat and eight rats during 1993,
but caught neither rats nor cats in 1994. Each
year, we found rat droppings deposited through-
out the colony before our arrival. During our
work at night in 1993, we often saw or heard
introduced Barn Owls (Tyro alba). Barn Owls
prey on Newell's Shearwaters (Byrd and Telfer
1980), and it was clear that they homed in on
the Newell's Shearwater vocalizations that we
occasionally played from a tape recorder (Ainley
et al. 1995). During the day or evening only, we
infrequently saw Short-eared Owls (Asio fiam-
meus), but whether they prey on shearwaters is
not known.
Urban corridor
The number of fledglings that died each year
during SOS processing averaged 1.7% of the to-
tal turned in (Fig. 2B). The number of fledglings
logged by SOS as dead on the road, but not de-
posited at SOS stations, averaged an additional
6% of the total each year (Fig. 2C). Almost all
of these birds were checked for bands.
During 1991-1994, when a concerted search
for dead adults was conducted, 42-72 were
found in spring and summer each year (mean =
61 _+ 7/yr; Fig. 2D; see also Ainley et ah 1995,
Podolsky et al. 1998). Before the directed
search, an average 17 _+ 2 dead adults were re-
ported per year by SOS (1987-1990). In 1993-
1994, among 30 adults that could be sexed (not
overly smashed), the male:female ratio was 8:9,
and 7 (23%) were breeders. The average mass
of dead adults was 381 _+ 8 g (N = 35), a value
important to our estimate of adult survival (see
below).
RATES OF BAND RECOVERIES
Recoveries and band-return rates of fledgling
and adult shearwaters were unexpectedly low.
None of 15 fledglings banded in 1993-1994 and
none of 52 banded in the study colony during
1980-1985 were picked up subsequently by
SOS.
In 1993, we captured nine adults in the col-
ony, but none had been banded previously. Only
1 of 30 adults/subadults found dead in 1993-
1994 was banded. That one individual had been
banded as a fledgling by SOS during fallout on
the Southshore. Thus, we found 1 (2.6%) banded
birds among 39 adults/subadults examined in the
colony in 1993-1994. Similarly low band re-
turns are evident in a sample of 14 adults banded
in 1983 (T Telfer, unpubl. data). These birds
were attracted one night to a camp light in the
K6ke'e forest (Fig. 1). One of these birds (7.1%)
was subsequently recovered upon hitting a pow-
er line.
An equally low recovery rate is evident
among adults found dead along power lines and
roadways. Thus far, only 15 of the 23,000 fledg-
lings banded and released by SOS have been
recovered as adults or subadults during subse-
quent years (Table 1). Excluding data from the
114 STUDIES IN AVIAN BIOLOGY NO. 22
EASTSHORE WITHOUT WESTIN 769 - 54
400 - A
300 -
200-
NORTHSHORE 217 ß 31
C
-200
SOUTHSHORE 357 & 34
400
E
300
200
0
-200
YEAR
WESTIN ONLY 240 ñ 53
400 - B
300 -
-200 - *
EASTSHORE I009 & 60
400- D
300 '
200 '
-200 '
YEAR
FIGURE 4. Deviations from the mean number of Newell's Shearwater fledglings on Kaua'i, Hawaiian Islands,
retrieved by SOS each year, 1980-1994, on the: (A) Eastshore with data from the Kaua'i SurfF½/estin Hotel
(district) removed [Y = -2201 + 26.2X; r 2 0.365, se 10.9, P = 0.038]; (B) Kaua'i Surf F½/estin Lagoons
Hotel only [Y = 2723-31.6X; r 2 - 0.381, se 12.7, P = 0.032]; and totals for (C) Northshore [Y = -2062 +
24.1X; r 2 - 0.543, se 6.9, P = 0.006], (D) Eastshore [P 0.7], and (E) Southshore [P = 0.8].
first few years, when weak monel bands were
used, the recovery rate was only 0.1% (12 of
12,443 birds banded in 1982-1990 and recov-
ered in 1989-1994). Looked at in another way,
among 351 adults reported to SOS, from 1987
to 1994 (when search effort was quantified), 12
(3.4%) had been banded. Three-fourths of the
recoveries occurred during the past four years,
when search effort was much greater than it had
been (Ainley et al. 1995). No birds <2 yrs of
age have been recovered.
POPULATION TRENDS
For all of Kaua'i, numbers of fledglings
picked up each year were about the same during
the period 1980-1990 (Fig. 2A). Thereafter,
even after 1987 numbers declined each year (in-
cluding years beyond those of this study,
through 1997; SOS unpubl. data, T Telfer, pers.
comm.). Results separated by region of retrieval
showed a steeply growing number of fledglings
for the Northshore (Fig. 4C, D, and E). No slop-
ing trend was evident for the Eastshore (Fig.
4D), unless data for the Kaua'i Surf/Vqestin La-
goons Hotel were analyzed separately (Fig. 4B).
Then, positive growth in the number of fledg-
lings was evident (Fig. 4A). Similarly, no slop-
ing trend was evident for the Southshore overall,
although a decline not evident in the other
regions is apparent after 1988 (Fig. 4E).
The growing number of SOS-processed birds
on the East- and especially the Northshore oc-
curred in concert with the doubling and quadru-
pling, respectively, of urban development (size
NEWELL'S SHEARWATER DEMOGRAPHYAinley et al. 115
TABLE 1. THE TiME OF YEAR THAT BANDED NEWELL'S SHEARWATERS OF KNOWN AGE WERE RECOVERED ON
KAUA'I FROM 1980 TO 1994 a
Age (Yr) May June July August
<18 18 25 1 8 15 22 29 6 13 20 27 3 10 17 24 31
2-3 I I I I 2 I 1
4-5 1 2 1 1
->6 1 1
a Dates represent the first day of one-week periods.
of the human population) since 1970 (Fig. 5A).
On the Southshore, where the human population
has always exceeded that elsewhere on Kaua'i,
it also increased during 1970-1990, but in this
case it was returning to a level reached previ-
ously in the 1940s. The infrastructure to support
tourists (lights included), indexed by the number
of persons passing through the Lihu'e Airport,
increased more than 12-fold in recent decades
3O
2O
15
l0
0
ß NORTHSHORE
¸ EASTSIIORE
ß SOUTHSHORE
1930 1960 1990
30
2.0
.
ß
197¸ 90
Indices to urbanization of Kaua'i, Ha-
1960
FIGURE 5.
waiian Islands: (A) Number of permanent residents on
North-, East-, and Southshores, 1930 1990 (cf. Fig. 1);
(B) Number of passengers at Lu'e Airport (mostly
tourists who need to reside at hotels, condominiums,
etc.), 1960-1993 (data from State Airports Commis-
sion). Another commercial but private airport opened
in Princeville ca. 1980 (but no data on passengers are
available).
(Fig. 5B). We hypothesize that this growth, too,
with its accompanying lights, probably affected
the ability of urban areas to attract fledglings.
Many coastal hotels, restaurants, sporting facil-
ities, etc., have been built to accommodate these
tourists and the resident population to service
them. To summarize, then, on portions of Kaua'i
where urbanization has been increasing recently,
more and more fledglings have been recovered
by SOS; where urbanization has been even dens-
er and more widely spread for a long time, no
trend in SOS retrievals has occurred. We hy-
pothesize that either the proportion of fledglings
attracted to lights and the retrieval capabilities
of SOS have become saturated in those areas, or
an increasingly greater proportion of fledglings
are being attracted and the shearwater popula-
tion has suffered greater mortality due to fallout
and, in effect, has declined (see Discussion). In
other words, the decline is masked because an
increasing proportion of fledglings are being at-
tracted to lights.
POPULATION MODELING
To put our results into perspective, we devel-
oped a Leslie model (Leslie 1945), that incor-
porates the various parameters of productivity
and mortality. Before doing this, and in order to
estimate mortality rates, we had to estimate the
total number of fledglings produced on KauaT
The average 9,636 fledglings/yr was derived by
multiplying three values: (1) 84,000, the esti-
mated total population of Hawaiian Newell's
Shearwaters (excluding fledglings; Spear et al.
1995); (2) 0.637, the proportion of total popu-
lation of breeding age, i.e., 6 yrs or older, de-
rived from the stable age distribution (see be-
low); and (3) 0.547, the proportion of adults that
bred in any given year (see below). The result
was 14,600 breeding pairs, which produced 0.66
fledglings per pain Our estimate of fledgling
numbers does not correct for the few that would
occur on Hawai'i (where radar studies indicate
far fewer Newell's Shearwaters than on Kaua'i;
Ainley et al. 1997b, Reynolds et al. 1997a).
PARAMETERS USED IN THE POPULATION MODEL
Five demographic parameters were required
in the Leslie model: survival of adults (i.e., those
116 STUDIES IN AVIAN BIOLOGY NO. 22
32 64 q28 256 5:2 qooo 4000 8ooo
LOG BODY MASS
FIGURE 6. Relationship between body mass and an-
nual adult survival among procellariiforms; data ex-
tracted from Galllard et al. (1989) and Dunning (1992).
A significant relationship (P - 0.045) exists between
log (adult survival) and log (body mass).
birds physiologically mature); survival of juve-
niles and subadults (i.e., birds between fledging
and 12 months of age and those after the first
year of life but before adulthood, respectively);
age of first breeding; reproductive success; and
breeding probability (i.e., the probability that an
adult will breed in a specific year). Before dis-
cussing model results, we present values for
these parameters here, incorporating empirical
results and those from the literature.
Annual survivorship
Annual survivorship, as in most seabirds, has
not been studied in Newell's Shearwater. We es-
timated annual adult survival to be 0.905, a val-
ue reported for a population of the very closely
related Manx Shearwater (P. p. puffinus; taxon-
omy summarized in Ainley et al. 1997a), whose
numbers have been stable and which has been
exhaustively studied since the 1950s (Brooke
1990). This value is consistent with those re-
ported for procellariiforms of similar mass
(Croxall and Gaston 1988) and with an allome-
tric relationship to body mass (381 g; see above)
among procellariiforms (Fig. 6). From this re-
gression, the predicted value for adult survival
of a Newell's Shearwater was 0.904 -+ 0.017,
with an approximate 95% prediction interval of
0.870-0.934.
Juvenile and subadult survival
Juvenile and subadult survival also have not
been studied in Newell's Shearwater and are
poorly known in procellariiforms and most wild
birds. The well-studied Manx Shearwater, again,
can provide some insight. After adjusting for
dispersal, Brooke (1990) estimated that 33.3%
of Manx Shearwater fledglings survived from
fledging to breeding age (age 6 yrs or older). We
incorporated this value into the simulations for
Newell's Shearwaters, after considering the fol-
lowing patterns in the few other seabird species
for which empirical data are available. Annual
survival of juvenile and subadult alcids (e.g.,
Common and Thick-billed murres [Uria aalge
and U. Lornvia], the size of which is similar to
Newell's Shearwater) at ages 1, 2, and 3 yrs,
respectively, is 60%, 82-83%, and 95-96% of
the adult value; from the fourth year on, suba-
dults have attained 100% of the adult value (Nur
1993, De Santo and Nelson 1995; S. Beissinger
and N. Nur, unpubl. data). A similar pattern has
been observed among male Western Gulls (Lar-
us occidentalis; Spear et al. 1987), South Polar
Skuas (Catharacta maccormicki; Ainley et al.
1990), also similarly sized to Newell's Shear-
water, as well as among the heavier-bodied Ad-
lie Penguin (Pygoscelis adeliae; Ainley and
DeMaster 1980) and African Penguin (Sphenis-
cus dermersus; Shannon and Crawford 1999).
This pattern of age-specific survival was main-
tained by us for the Newell's Shearwater while
scaling survival upward to achieve a total sur-
vival of 0.333 between fledging and age 6 yrs.
The result was annual survival estimates of
0.654, 0.78, 0.89, and 0.905 in the first four
years of life, and 0.905 for each year of life
thereafter (within 1 SE of 0.904, the value ob-
tained from the allometric regression, above).
These survival values, consistent with those
for other seabird species, if anything, may be a
bit high rather than too low. For example, sur-
vival from fledging to age 6 yrs in a growing
population of Cory's Shearwater (Calonectris
cliomedea; Mougin et al. 1987) was estimated to
be in the interval 0.230-0.334; Simons (1984)
assumed survival from fledging to breeding age
of 0.268 for a stable population of Dark-rumped
Petrels; and for five alcid species, survival to
average breeding age ranged 0.244-0.345 (Hud-
son 1985). As pointed out below, given an adult
survival of 0.905, survival from fledging to
breeding age would need to be at least 0.333 to
produce a stable population; therefore, we re-
tained this estimate.
Age of first breeding
On the basis of an average age of first breed-
ing in the Manx Shearwater of six to seven years
(Brooke 1990) and data presented in Table 1, we
assumed that no Newell's Shearwater breeds be-
fore age 6 yrs, and from age 6 yrs onward, all
individuals breed with probability, p (see be-
low). Among 15 banded, known-age Newell's
Shearwaters recovered by SOS during the past
several years (Table 1), essentially all <5 yr of
age were found t¾om the period of late-egg lay-
ing onward, suggesting that they did not breed.
NEWELL'S SHEARWATER DEMOGRAPHY--Ainley et al. 117
Of the two birds 6-7 yrs old, one was found in
the prelaying period, consistent with a bird ar-
riving early enough to breed. We further esti-
mated that 1-p fraction of 6-yr-old Newell's
Shearwaters would not breed in a given year.
The result of this assumption is that the actual
mean age of first breeding is between 6 and 7
yrs in all of our simulations, which is consistent
with values not just for Manx Shearwater but
also for the other shearwater species for which
empirical data are available: 7 yrs in the Short-
tailed Shearwater (Bradley et al. 1989) and 9 yrs
in Cory's Shearwater (Mougin et al. 1987).
Longevity
We assumed a maximum age of 36 yrs for
Newell's Shearwater. This corresponds to the
maximal age observed among other shearwaters
(e.g., Bradley et al. 1989).
Productivity
We used a breeding success value of 0.66
fledglings/breeding pair, a value determined in
our study, to simulate the current trajectory of
the Kaua'i population. In the Manx Shearwater,
reproductive success was 0.70 (Brooke 1990), a
value consistent with that reported for Short-
tailed Shearwater (Wooller et al. 1989). We used
0.70 to simulate a balanced Newell's Shearwater
population.
The low numbers of fledglings picked up by
SOS during 1992 and 1993 may be due to sev-
eral factors: (1) strong E1 Nifio conditions that
negatively affected food availability and, thus,
shearwater breeding success (see below); (2) the
possibility that Hurricane Iniki killed many
birds, forcing a need for much new pairing and
construction of burrows, two factors that result
in lower breeding success in other seabirds (but
this is unlikely; see above); (3) an absence of
bright lights (which attract fledglings) on Kaua'i
for many months after the storm (see above);
and (4), at least for 1992, the effect of the full
moon during fledging (Fig. 3). None of these
explanations are likely to explain the pattern en-
tirely, however, because the numbers of fledg-
lings found by SOS continues to decline even
through 1998 (SOS, unpubl. data; T Telfer, pers.
comm.). We hypothesize that recently we have
begun to see the effects of the costs of fallout
and adult mortality on the stability of the shear-
water population (see below).
The low number of birds turned in during fall
1978 was certainly a result of the start-up nature
of the SOS program. The large number found in
1987 was unusual, but is consistent with that
year being at the start of one of the strongest La
Nifias of recent decades. At that time, unusually
productive waters existed in the eastern tropical
Pacific, where Newell's Shearwaters feed (cf.
Ribic et al. 1992, Spear et al. 1995). Thus, in
1987, breeding success may have been unusu-
ally high, and, in that year, the timing of the full
moon would not have decreased the numbers of
fledglings found.
It is not known whether the fewer fledglings
found in some years, as a function of moon
phase, is due to their greater ability to see struc-
tures in the moonlight (hence, fewer crashes), or
whether fledglings are attracted away from civ-
ilization by the very bright moon (as suggested
by Reed et al. 1985). The moon is clearly the
brightest light source around and is low on the
horizon just after sunset; our surveys indicated
that most fallout occurs during the three hours
after sunset (Ainley et al. 1995). Also hypothe-
sized as a possibility by Reed et al. (1985), but
determined to be false by us, is that moon phase
affects the fledging rate, i.e., young may not
fledge during the bright full moon (Ainley et al.
1995).
Breeding probability
The breeding probability parameter refers to
the proportion of adults occupying a burrow in
which no egg is laid. In Newell's Shearwater,
46% of occupied burrows produced an egg dur-
ing the 1981-1985 period. Some of these bur-
rows were surely occupied by prebreeding in-
dividuals. Assuming that (1) all 4- and 5-yr-old
Newell's Shearwaters occupied burrows but did
not breed (see above), (2) all individuals >5 yr
of age occupied burrows and bred with proba-
bility p (see above), and (3) 4- and 5-yr-olds
composed 15.9% of all individuals 4 yr or older
(as determined from simulations described be-
low), we can solve for the fraction of breeding-
aged individuals that bred. Dividing 46% by
84.1% (proportion of burrow-holding population
that has the potential to breed) yields an annual
breeding probability of 0.547. In the Manx
Shearwater, 20% of adults that had bred previ-
ously do not breed in a given year (Brooke
1990); in Short-tailed Shearwater, 12% of adults
do not attend the colony and 19% maintain bur-
rows but do not lay an egg (i.e., breeding prob-
ability is 0.69; Wooller et al. 1989).
There are two sources of uncertainty concern-
ing our estimate of breeding probability. First,
sampling error is associated with the estimate of
46% of pairs breeding among those occupying
burrows (SE = 0.035; 95% CI = 0.39-0.53).
Second, uncertain is our assumption that 15.9%
of burrows are occupied by prebreeding individ-
uals (i.e., that all 4- and 5-yr-olds occupy bur-
rows but do not breed and that 2- and 3-yr-olds
do not occupy burrows). If 3-, 4- and 5-yr-olds
occupy burrows, this implies that 22% of bur-
118 STUDIES IN AVIAN BIOLOGY
TABLE 2. PARAMETER ESTIMATES USED IN LESLIE MODELS UNDER DIFFERENT SCENARIOS
NO. 22
Best estimate: Newell's Shearwater
Balanced: W/O Power line W/Power line W/Power line
Manx mortality, predation, or mortality, predation, mortality, and fallout,
Shearwater fallout and fallout but W/O predation
Survival: adult 0.909 0.905 0.896 0.904
Survival: fledgling
to adulthood 0.333 0.333 0.239 0.327
Age first breeding 6-7 6-7 6-7 6-7
Breeding success 0.70 0.66 0.634 a 0.634 a
Breeding probability 0.80 0.547 0.547 0.547
X 1.000 0.968 0.939 0.963
0.66 chicks fledge per breeding pair but 4% of fledged chicks die in fallout (not rescued by SOS); therefore, 0.66 x 0.96 - 0.634.
rows are occupied by prebreeders; alternatively,
if only 5-yr-olds occupy burrows, this implies
that 11% of burrows are occupied by prebreed-
ers. In turn, this implies that breeding probabil-
ity may vary between 0.60 (if only 5-yr-olds
hold burrows) and 0.50 (if 3-, 4- and 5-yr-olds
all hold burrows). We used 80% breeding prob-
ability for simulating a balanced population
(Manx Shearwater), but 54.7% for simulating
the contemporary Newell's Shearwater popula-
tion.
The factors that affect breeding probability in
Newell's Shearwater are not known for certain.
Why reproductive effort was so low especially
in 1993 is difficult to ascertain. As in 1983, the
year that Telfer (1986) found the fewest burrows
with eggs, 1993 was a year of major E1 Nifio.
Characteristic of such years, seabirds forgo re-
production because of a lack of food reserves
(Schreiber and Schreiber 1984, Ainley and Boe-
kelheide 1990). The 1993 breeding season also
closely followed the devastation of Hurricane
Iniki (September 1992). We saw some evidence
of terrain slumping and a few uprooted trees at
Kalaheo. Thus, the high level of nonbreeding
could have been related to storm damage, but
we saw little evidence of major burrow exca-
vation, and many burrows used in 1993-1994
was not unusual for this population. It is not
clear why breeding probability is low in the
Newell's Shearwater (54%), but it may result
from a high level of mate loss (itself a result of
excessive mortality, see below) because, among
seabirds, breeders who have lost their mates usu-
ally cannot obtain a new one quickly (e.g., Ain-
ley and DeMaster 1980, Boekelheide and Ainley
1989). It could be, too, that our estimates are
biased.
SIMULATION OF A BALANCED POPULATION
Incorporating values from the Manx popula-
tions (Table 2), our model produced a population
that was nearly balanced but still declined slow-
ly at 0.65% per year (X, the finite population
growth rate = 0.994). Thus, after 10 years, the
population will have declined by 6.3%. Increas-
ing adult survival from 0.905 to 0.909, however,
produced a stable population: X = 1.000. An
adult survival rate of 0.909, within 1 SE of Broo-
ke's (1990) estimate of 0.905, is statistically rea-
sonable.
Substituting a breeding probability of 0.547
and a reproductive success of 0.66 in the model,
i.e., Newell's Shearwater values, produced a
population that declined at 3.2%/yr (X = 0.968).
This is our best estimate of the current popula-
tion trajectory of the Newell's Shearwater in the
absence of additional mortality due to fallout,
collisions with power lines, or from introduced
predators (see below). In other words it is an
idealistic scenario. The main factor affecting the
declining growth rate was the fact that breeding
probability was 0.547, rather than 0.8. Substi-
tuting 0.547 into the model was by itself suffi-
cient to reduce population growth rate from
1.000 to 0.978. A breeding success of 0.66 (ver-
sus 0.70) and adult survival of 0.905 (versus
0.909) were of minor influence in lowering pop-
ulation growth rate, accounting for an additional
drop from 0.978 to 0.968.
POPULATION STABILITY WITH MORTALITY OF
FLEDGLINGS DURING FALLOUT
We next added mortality to fledglings during
fallout to the simulation, i.e., attraction to lights
and subsequent death owing to a complex of fac-
tors (see Introduction). This mortality occurs in
spite of the efforts of SOS.
On the basis of the SOS data gathered by an
opportunistic effort, the percent of fledglings
that died annually, among those encountered by
SOS, was 7.7% (see above; Fig. 2). However,
on our night surveys in which search effort was
quantified, 43% of fledglings were found dead
(Ainley et al. 1995, Podolsky et al. 1998). The
discrepancy with SOS must be due partly to dif-
ferent areas being surveyed, our sampling of ar-
eas that were less frequented by citizens (e.g.,
NEWELL'S SHEARWATER DEMOGRAPHY--Ainley et al. 119
TABLE 3. FLEDGLING MORTALITY AS A FUNCTION OF
MORBIDITY AND DISCOVERY RATES a OF NEWELL'S
SHEARWATERS ON KAUA'I, HAWAIIAN ISLANDS
Discovery rate
Morbidi-
ty rate 100% 80% 67% 50%
7.7% 0.011 0.014 0.017 0.023
15% 0.022 0.028 0.033 0.044
25% 0.037 0.046 0.056 0.074
43% 0.064 0.080 0.096 0.127
a Morbidity - percentage dead among downed fledglings; discovery -
percentage of downed fledglings found by SOS.
sugarcane fields, secondary roads), and the re-
luctance of the public to salvage dead birds for
SOS. The true mortality could be approximated
better if we knew the number of birds that citi-
zens rescued from our circuits each night before
we passed through. Our regular checks of SOS
shearwater drop-off stations in the vicinity of
our circuits, however, revealed a few (1-5) but
not disproportionately large numbers of addi-
tional live birds. Clearly, a greater proportion of
each year's fledgling cohort dies than is revealed
by SOS data. This hypothesis is supported by
the fact that SOS reported none of 44 dead birds
tagged and left in place by us during autumn
1993 and 1994 (Ainley et al. 1995, Podolsky et
al. 1998). Thus, the true morbidity, i.e., proba-
bility that a downed fledgling dies, is likely be-
tween 7.7% and 43% of all fledglings. In our
simulations, we considered these extremes as
well as intermediate values of 15% and 25%.
Finally, we estimated the proportion of all
downed fledglings encountered by the public
and (if alive) brought to SOS stations, i.e., dis-
covered. An extreme assumption would be that
citizens discovered (and recorded) all downed
fledglings. This scenario is unlikely, because
some fledglings fall in inaccessible areas, such
as sugarcane fields (which occupy a huge pro-
ponion of Kaua'i's coastal plain and are crossed
by many kilometers of power lines), as well as
other factors that could prevent discovery (e.g.,
birds moved by predators, birds hiding in the
bushes). On the other hand, without recording
them, some citizens find birds and release them
into the ocean at the beach (probably jeopard-
izing the shearwaters, which are not anatomi-
cally prepared to deal with surf). The proportion
of individuals that escape on their own are not
our concern here. Therefore, we have considered
four scenarios: 100%, 80%, 66.7%, and 50% of
all downed fledglings are discovered by SOS.
Combining four levels of morbidity and four
levels of discovery yields 16 combinations of
total fledgling mortality (Table 3). We recognize
that the two dimensions, morbidity and discov-
TABLE 4. POPULATION GROWTH RATES ()k) IN RELA-
TION TO FLEDGLING MORTALITY, ADULT, AND SUBADULT
MORTALITY AND PREDATION OF NEWELL'S SHEARWATER
ON KAVA'l, HAWAIIAN ISLANDS
Adulffsubadult power line-caused mortality
Fledgling
mortality None Low Medium High
Without predation from introduced animals:
0.02 0.966 0.965 0.963
0.04 0.965 0.963 0.962
0.06 0.964 0.962 0.960
0.08 0.963 0.961 0.959
0.10 0.961 0.960 0.958
With predation from introduced animals:
0.02 0.941 0.939
0.04 0.939 0.938
0.06 0.938 0.937
0.08 0.937 0.936
0.10 0.936 0.934
0.962
0.960
0.959
0.958
0.957
ery, are likely related: the more fledglings that
come down in areas not covered efficiently by
citizens, the higher the level of morbidity, since
many fledglings will not be able to recover (e.g.,
it would take days, if ever, for a shearwater to
extricate itself from the tall, dense foliage of a
sugarcane field). However, our intention is mere-
ly to indicate the range of fledgling mortality
likely to be sustained by this population. Total
fledgling mortality due to fallout for the 16 dif-
ferent combinations of morbidity and discovery
ranged 1.1% to 12.7%. Thus, in the most opti-
mistic scenario, 1,432 out of 9,636 fledglings are
downed and 7.7% of the 1,432 die (110/9,636
= 0.011). In the most pessimistic scenario, 2,864
fledglings are downed and 43.1% of these die
(1,232/9,636 = 0.128).
We simulated the effects of fledgling mortality
due to fallout, allowing the fraction of fledglings
dying to vary from as low as 0.02 to as high as
0.10, where all other parameter values corre-
sponded to our best estimate model (Table 2).
High fledgling mortality (0.10) lowered 2t by
0.5%, compared to low fledgling mortality
(0.02; Tables 4, 5; Fig. 7A).
POPULATION STABILITY WITH SUBADULT AND
ADULT MORTALITY DUE TO POWER LINE
COLLISIONS
As indicated above, about 61 subadults and
adults have been found dead as a result of power
line collisions each year. This by no means in-
cludes all such individuals, as an adequate
search of inland power lines, of which there are
about 40 km across sugarcane fields, was be-
yond our resources (Ainley et al. 1995, Podolsky
et al. 1998). We assumed true island-wide mor-
tality to be either 122 birds (i.e., twice the mea-
sured level: "low power line mortality"), 244
120 STUDIES IN AVIAN BIOLOGY NO. 22
TABLE 5. COMPARISON OF POPULATION GROWTH
RATES () AT DIFFERENT LEVELS OF SPONTANEOUS ES-
CAPEMENT BY DOWNED NEWELL'S SHEARWATER FLEDG-
LINGS ON KAUA'I, HAWAIIAN ISLANDS, WITH AND WITH-
OUT PREDATION FROM INTRODUCED ANIMALS AND
WITHOUT THE SOS PROGRAM
25% of dovned fledglings 0% of dovned fledglings es
escape cape
Population Differcnce Population Difference a
Fledgling
mortality Grovth rate Grovth rate
1000 -
800 -
600 '
Low-level po;ver line mortality for adults/subadults, oo
vithout predation:
0.02 0.958 0.0071 0.955 0.0096
0.06 0.955 0.0073 0.952 0.0099 -
0.10 0.952 0.0075 0.949 0.0102 '
Lov-level pover line mortality for adults/subadults, 000-
with predation: -
0.02 0.934 0.0062 0.932 0.0085
0.06 0.932 0.0063 0.930 0.0087
0.10 0.929 0.0066 0.926 0.0091 Boo -
a Absolute difference in h, comparing population growth rate for a pop-
ulation with (see Table 4) and without SOS program (in which 25% or
0%. respectively, of thc 1,432 fledglings turned in each year would escape
on their own).
birds (i.e., 4 X 61, "medium power line mor-
tality"), or 350 dead birds ("high power line
mortality"; see Ainley et al. 1995, Podolsky et
al. 1998, for derivation). In addition, such mor-
tality is apparently age specific: subadults appear
more vulnerable than breeding adults. First, as
noted above, 20% of the birds found and nec-
ropsied by us were active breeders, yet an esti-
mated 35% of such birds exist in the population
(on the basis of the model, 0.637 0.547). Sec-
ond, an additional sample of 15 known-aged
(banded) subadult and adult individuals killed by
power lines (Table 1) indicated that only two
(13%) were 6 yrs of age or older (i.e., of breed-
ing age); the remainder were 2-5 yrs of age
(subadults). Thus, the two samples yielded sim-
ilar adult:subadult ratios.
On the basis of these data, we assumed either
24, 48, or 70 dead breeders per year (122, 244,
or 350 X 0.2). Dividing 24, 48, and 70 by the
total number of adults at the colony yielded mor-
tality rates of 0.046%, 0.092%, and 0.131%, re-
spectively, for the three levels of power line
mortality. For subadults ages 2-5 yrs (Table 1),
depending on the level of power line mortality,
we derived mortality rates of 0.60%, 1.20%, and
1.72%, respectively.
We simulated population growth rate incor-
porating these levels of subadult and adult mor-
tality, together with a range of fledgling (fallout)
mortality values (Table 4). The effect of high
subadult and adult power line mortality com-
pared to no such mortality was to lower popu-
lation growth rate by 0.5% for a given level of
600
400
COLLISIONS
A FLEDGLING
MORTALITY:
0 4 lb 1 2b
. 8 ADULT
MORTALITY:
NONE ß
HIGH A 2.1%
YEAR
FIGURE 7. Results of simulations shoving effects
on population growth in the Nevell's Shearvater
caused by: (A) fledgling mortality of 0, 4, and 10%
due to fallout; and (B) no versus high adulffsubadult
mortality due to collisions vith pover lines. The hor-
izontal line indicates 50% population level.
fledgling mortality. Low and intermediate sub-
adult and adult power line mortality generated
intermediate levels compared to high and no
power line mortality. It appears that the magni-
tude of the effect of power line mortality on
population growth rate is roughly comparable to
the estimated effect of fledgling mortality (i.e.,
depressing the population growth rate by as
much as 0.5%). We considered the high level of
power line mortality to be the best estimate of
such (Ainley et al. 1995, Podolsky et al. 1998).
Nevertheless, for analyzing effects of predation
and efficacy of the SOS program, to err on the
side of caution given the uncertainties involved,
we used our most conservative estimates of
power line mortality.
POPULATION STABILITY WITH PREDATION OF
BURROW OCCUPANTS
Mortality due to predation from introduced
animals should be considered additional to mor-
tality already discussed, since most studies of
shearwaters have been conducted at sites where
NEWELL'S SHEARWATER DEMOGRAPHY---Ainley et al. 121
predation of subadults and adults is low. Some
Manx Shearwaters are taken by Great Skuas
(Catharacta skua) and large gulls (Larus spp.),
but numbers of these avian predators are ex-
tremely low because of control programs (Fur-
ness 1987). Predation by humans had a marked
effect on the Cory's Shearwater population
(Mougin et al. 1987).
We found 30 dead subadults and adults among
the estimated 600 individuals in the Kalheo
colony (about 150 burrows X 2 yrs X 2 individ-
uals/burrow/yr; Ainley et al. 1995). This yielded
a crude estimate of 5% mortality among burrow
holders. We modeled this as an extra 2.5% mo-
rality averaged over all adults and subadults (ex-
cluding 1-yr-olds). We chose to use 2.5% mor-
tality (rather than 5%) to reflect the fact that
some individuals killed might have been tran-
sients and not burrow holders, and some non-
breeders of breeding age might not have been
present at the burrows at all, as in the Short-
tailed Shearwater (Wooller et al. 1989; see
above). As shown below, even 2.5% mortality
of subadults and adults has a dramatic effect on
population growth rate. We have not considered
mortality of adults or chicks due to predation by
rats, for we have no data on rat predation, a most
difficult factor to quantify (Thompson 1987,
Sero 1995, Sero and Conant 1996).
We also considered that predation, especially
from owls, is age specific. Active breeders are
inconspicuous, so we assumed that they incurred
a very low predation rate, whereas 4- and 5-yr-
olds, who attempt to gain both a burrow and a
mate, are most conspicuous of all and suffered
the highest predation rate. We assumed that in-
active breeders (individuals that bred in a pre-
vious year, but not the current year) and 2-and
3-yr-olds incur intermediate levels of predation.
Taking into account our subjective assessment of
predation risk, 2- and 3-yr-olds were assigned a
mortality rate due to predation of 5%; 4- and 5-
yr-olds a rate of 10%; and breeding age individ-
uals (whether active or inactive) a predation rate
of 1%. Averaged over all individuals 2 yrs of
age or older, mortality due to predation was
2.5%.
The effect of predation on population growth
was dramatic (Tables 4, 5). Simulations indicat-
ed a decline of 0.023-0.024 in the finite popu-
lation growth rate, depending on the level of
mortality assumed for fledglings, subadults, and
adults. Thus, the two most important factors in
determining population growth (and in this case,
decline) were the low breeding probability com-
pared with that of stable shearwater populations
(0.547 versus 0.80) and the apparently high mor-
tality rate due to introduced predators. The two
may well be related; loss of mates (due to pre-
dation, hurricanes, or power line collision, see
above) may lead to a reduced breeding proba-
bility for the current or subsequent breeding sea-
son.
POPULATION STABILITY WITH SOS REDUCTION OF
FLEDGLING MORTALITY
There is little information regarding the num-
ber of fledglings that come to ground but then,
in the absence of SOS, spontaneously escape to
the sea. Here, to assess the impact of SOS, we
consider two possibilities: 0% and 25% of
downed fledglings escape on their own. Telfer
et al. (1987) proposed that few fledglings that
fallout would be capable of survival on their
own. In fact, we observed two fledglings who
took off after being grounded (it was windy and
they were in a large, unobstructed expanse--
empty parking lots; Ainley et al. 1995).
In the simulations (Table 5), 2.0-10.0% of all
fledglings were assumed to have died as a result
of hitting power lines, etc., just as was imple-
mented in the simulations shown in Table 4, and
then an additional 1,432 (due to not being res-
cued by SOS participants, assuming 0% spon-
taneous escape) or 1,074 (assuming 25% spon-
taneous escape) fledglings die. The decline in
population growth rate in the absence of SOS
was 0.62-0.75% if 25% of downed fledglings
escaped on their own, and ranged 0.85-1.02%
in the absence of spontaneous escape. Therefore,
the SOS program has had a significant effect on
population growth of the Kaua'i population:
fledgling mortality, in the presence of SOS, low-
ered the population growth rate by 0.12-0.62%
but, in the absence of SOS, lowered it by an
additional 0.62-1.02%.
MODELED POPULATION TRAJECTORIES
Finally, we modeled the population trajectory
for the Kaua'i population of Newell's Shear-
waters under four scenarios, assuming an arbi-
trary starting population size of 1,000 individu-
als (of all ages >1 yr; Fig. 8A). All scenarios
assumed a "low" level of subadult and adult
mortality due to power lines and 4% mortality
of fledglings due to fallout (see above). Scenar-
ios 1 and 3 assumed the continued operation of
the SOS program, but scenarios 2 and 4 assumed
no such program, and further assumed that 25%
of downed fledglings spontaneously escape (see
above). Scenarios 1 and 2 included no provision
for mortality due to introduced predators; sce-
narios 3 and 4 included such mortality.
We also considered results for these scenarios
with values of breeding probability and repro-
ductive success from the Manx Shearwater (Ta-
ble 2, Fig. 8B; Brooke 1990). After all, Newell's
Shearwater eggs raised in the absence of pred-
122 STUDIES IN AVIAN BIOLOGY NO. 22
lOOO
800
600
400
2OO
000
800
600
400
%.. A -- No Introduced Predators
z No Introduced Predators, No SOS
ß Introduced Predators
D Introduced Predators. No SOS
NEWELL'S SHEARWATER
B
MANX SHEARWATER
YEAR
FIGURE 8. Results of simulations showing effects
on population growth of shearwaters in the face of
low-level mortality to fledglings due to fallout (SOS
in operation), low levels of mortality to adults/suba-
dults due to collisions, and low levels of predation on
adults/subadults in the breeding colonies, assuming:
(A) demographic parameters estimated currently for
the Newell's Shearwater, and (B) demographic param-
eters estimated for the Manx Shearwater.
ators (by Wedge-tailed Shearwaters) attained a
success equal to that of the Manx Shearwater
(Byrd et al. 1984). Moreover, Manx values,
when combined with other parameter values,
produced a population declining slightly, where-
as Newell's values produced a population de-
clining steeply (see above). If one concludes that
the Newell's population is declining slightly
rather than steeply, one should adopt Manx val-
ues. Whatever values one uses, however, quali-
tatively similar results are produced: the cessa-
tion of the SOS program would accelerate the
decline of the Newell's Shearwater population
by two fold (in the absence of predation).
DISCUSSION
Comparing the spatial and temporal patterns
in the SOS data with those evident in urbaniza-
tion, as well as modeling results, we interpret
the trends seen in fallout as follows. The shear-
water population on the Southshore is decreas-
ing. The increased urbanization there, which is
compensated somewhat by the slightly increased
use of shielded lights (since 1987), should lead
to more shearwaters being found, all else being
equal. The opposite pattern observed, however
(no increase in fallout), is consistent with an
added cost (mortality that is not uncompensated)
and a declining population. The severe reduction
in the size of the Southshore colony at Kalu-
ahonu (few occupied burrows present in 1992-
1993 compared to the early 1980s; Ainley et al.
1995) is consistent with this trend. In fact, be-
cause our inputs to the demographic model were
gathered on the Southshore (Kalaheo colony,
routes to quantify mortality), our model results
duplicate well what we propose is happening to
the Southshore Newell's shearwater population
on the basis of SOS results.
In contrast to the Southshore, shearwater col-
onies on the Eastshore and Northshore are fac-
ing increased urbanization (well beyond histor-
ical levels; Fig. 5A) and, as predicted with more
lights, more birds are being reported to SOS
(Fig. 4A, C). The very recent growth in urban-
ization is so dramatic that the increased use of
shielded lights (although still minimal) must be
having little compensatory effect on shearwater
fallout. Due to mortality and ensuing population
decline, the fallout pattern for the North- and
Eastshore eventually should duplicate the trend
seen on the Southshore: level or decreasing fall-
out. Indeed, following our study, the number of
fledglings found in 1995, 1996, 1997, and 1998
(T. Telfer, pers. comm.) continued the "unex-
plained" gradual lowering of SOS totals that be-
gan in 1992 (or even 1987).
In the absence of fallout, power line-caused
mortality, and introduced predators, the model
showed that the Kaua'i population of Newell's
Shearwaters should be able to maintain its num-
bers, i.e., no other important factors affect pop-
ulation instability. The SOS program goes far to
reduce one of these mortality factors, death of
fledglings due to fallout. Even with SOS, how-
ever, there is significant mortality of fledglings;
>2% and as much as 10% or more of fledged
shearwaters likely die as a result of fallout. Mor-
tality of subadults and adults due to power line
collisions also depresses population growth, but
depending on the actual rates obtained, it may
or may not be as important. Firm quantification
of the significance of power line-caused mortal-
ity among subadults and adults awaits further
study. In the absence of the SOS program, how-
ever, fallout-caused mortality of fledglings
NEWELL'S SHEARWATER DEMOGRAPHY--Ainley et al. 123
would likely be more important than power line-
caused mortality of subadults and adults.
Evidence points clearly to two factors that im-
portantly affect population growth of the New-
ell's Shearwater: low breeding probability and
high rates of predation on adults and subadults.
The cause of the low breeding probability are
not readily apparent, but rates would be exac-
erbated by mortality of breeders and prebreeders
due to predation, disturbance by predators, and
collisions with power lines. Otherwise, even if
the Newell's Shearwater breeding population is
not currently declining (i.e., the model is wrong
and the SOS results are not a valid index of pop-
ulation size), our results indicate the vulnerabil-
ity of the Newell's Shearwater population. A re-
duction in the production and survival of fledg-
lings will only be felt many years later, at the
time when such fledglings would have begun
breeding. Remember, the longevity of this spe-
cies is about 30 yrs, and not even one generation
has passed since urbanization began to expand
rapidly. We ask, Are the low SOS totals con-
tinuing past 1987 and the unusually low banded-
bird recovery rates finally indicating decreased
survival? Seen in this context, mortality of
adults and subadults due to collisions is still of
great concern for recovery of Newell's Shear-
water (see USFWS 1982a).
Alternative hypotheses exist, of course, to ex-
plain some of the trends revealed by our re-
search and simulations. The regional difference
in trends could be a result of an increasing pop-
ulation of shearwaters on the Northshore due ei-
ther to immigration from colonies on the South-
shore (in turn to help explain the decrease there)
or much better breeding success on the North-
shore than on the Southshore. A shift from the
Southshore to the Northshore is problematic giv-
en the high degree of philopatry characteristic
of procellariiforms (Warham 1990). The very
low recovery rate of shearwaters initially band-
ed as fledglings by SOS could be a result of a
lower-than-natural survival rate of these birds
(deemed to have been "rescued" by SOS only
because they were able to fly away). Another
possibility is that the large majority of fledglings
picked up by SOS were produced on the North-
shore--and eventually recruited to Northshore
colonies as adults--but having reached the sea
were attracted back to land by coastal lights on
the more brightly lighted South- and Eastshores.
Until 1995, the Northshore had lacked the power
lines that effectively "sample" adults and su-
badults in the population, although following
completion of our study high, deep arrays of
lines have been installed. Thus, sampling effi-
ciency may have increased and we can see
whether or not the number of banded birds
found also increases. Additional research in the
colonies on the Northshore also could easily de-
termine whether many banded shearwaters nest
there.
In conclusion, then, the population of New-
ell's Shearwaters on Kaua'i appears to be de-
clining. On the basis of demographic modeling,
the prospects appear to be poor for the continued
existence of a robust population of this species
on this island. A reversal of the indicated pop-
ulation trends will be possible only with more
strict controls of lighting (such as on the Big
Island, where the astronomical observatories re-
quire minimal upward light radiation), fencing
and predator control in several important shear-
water breeding areas, and, possibly, the burying
of power lines in a few especially critical areas
(Ainley et al. 1997a, Podolsky et al. 1998).
ACKNOWLEDGMENTS
T. C. Telfer (Hawaii DLNR) introduced us to shear-
waters and petrels on Kaua'i, contributed much in-
sight, lent equipment to us, and provided access to past
data from the SOS program. He chose not to accept
authorship of this paper. Assistance, too, was provided
by R. Voss and K. Viernes (USFWS), Kilauea Point
National Wildlife Refuge. C. Berg was very helpful
and supplied much information early on that improved
our knowledge of Kaua'i. We also thank Kaua'i Elec-
tric Company and the Electric Power Research Insti-
tute (EPRI) for funding, and the coordination provided
by J. Huckabee and M. Fraser (EPRI). The counsel
received from the EPRI Scientific Advisory Panel was
also of great value: D. Boersma (University of Wash-
ington), G. Breece (Georgia Power and Southern Com-
pany Services), S. Conant (University of Hawai'i), E.
Colson (Pacific Gas and Electric, and Colson and As-
sociates), E. Flint (Pacific Islands Office, USFWS), L.
Ginzburg (Applied BioMathematics), and S. Kress
(National Audubon Society). Finally, B. A. Cooper, R.
H. Day, M. Fraser, T C. Telfer, L. B. Spear, S. Conant,
and several anonymous reviewers provided many good
comments on the manuscript.
Studies in Avian Biology No. 22:124-132, 2001.
MIGRATION OF NORTHERN PINTAIL ACROSS THE PACIFIC
WITH REFERENCE TO THE HAWAIIAN ISLANDS
MIKLOS
D. E UDVARDY AND ANDREW ENGILIS, JR.
Abstract. Northern Pintails (Arias acuta) regularly occur as winter visitors on most Pacific islands
with suitable habitat. Their breeding distribution includes both sides of the Pacific Rim. While large
populations breed in Siberia and winter in California, numerous North American breeders also winter
in areas near the Sea of Japan, Hawaiian Islands, and other Pacific island groups. Though pintail flights
across the Pacific have not been well documented, scrutiny of banding returns shows that an exclusive
Califomia-Hawai'i flyway does not exist, as was earlier proposed. Data support a more complex
movement of birds from numerous breeding locations in the Holarctic. We summarize movements of
Holarctic nesting pintails to wintering grounds in the Hawaiian Islands that include birds originating
from northeastern Siberia, Alaska, and the interior prairie provinces and states of North America. We
also summarize pintail movements to other Pacific archipelagoes. Finally, to close the circle around
the North Pacific, we summarize movements of birds between Canadian and Alaskan breeding grounds
to wintering sites in Japan. We also discuss other panmictic, Holarctic migrants and their colonization
attempts in Hawai'i.
Key Words: Anas acuta; banding return; Holarctic; migration; Northern Pintail; Oceania; panmixis.
The primary interest of a faunist is in establish-
ing the list of species that regularly occur in the
area under scrutiny. Data of a species' regular
occurrence increase knowledge of their total dis-
tribution, which is the aim of the zoogeographer.
Regularly occurring species are recognized as
influential members of local ecosystems; thus,
they play a prominent role in ecogeographical
studies. Often less attention is paid to scarce,
rare, or irregularly occurring species, for chance
seems to determine their detection, and their role
in community ecology appears negligible.
Regarding these "lesser" elements of local
fauna, interest increases when a chance visitor
comes from afar. Lately, the study of rarities be-
came important on two accounts. First, it is re-
alized that bird species are to an extent dynamic;
the "stray" individuals caught outside of their
regular distributional range are all potential col-
onists. The trends in their occurrence outside the
"normal" range and throughout a longer time
period may reveal the nature and extent of the
pioneering tendency of the species. Second, it is
also realized that species composition of faunas
fluctuates; thus rare visitors may reveal trends in
faunal changes.
Holarctic waterfowl are among the most suc-
cessful colonizers owing to their exceptional
powers of flight between breeding and non-
breeding areas. Their ability to move long dis-
tances and tendency for dispersal have resulted
in establishment of waterfowl on many remote
land masses where food and freshwater re-
sources are available (Weller 1980).
As with all remote oceanic islands, the Ha-
waiian Archipelago received its endemic avifau-
na through over-water dispersal and subsequent
local speciation. The Hawaiian avifauna consists
of year-round residents (the landbirds) and sea-
sonal but regular visitors (seabirds that come to
breed, and Anseriformes and Charadriiformes
that winter in Hawai'i). Thirty-three species of
migratory waterfowl have been recorded in the
Hawaiian Islands (Pyle 1997). Ten species are
annual visitors with Northern Pintail (Anas acu-
ta), Northern Shoveler (Anas clypeata), Lesser
Scaup (Aythya affinis), American (Anas ameri-
cana) and Eurasian (A. penelope) wigeons, and
Green-winged Teal (Anas crecca) accounting for
95% of those birds wintering in the islands (En-
gilis 1988).
Our focus in this paper, the pintail, is a reg-
ularly occurring winter visitor in Hawai'i and is
a scarce or irregular visitor to other Pacific is-
land groups. Reliable but general historical ac-
counts claim that pintail came in large numbers
to Hawai'i (Munro 1944). Earlier evidence is
suggested by the fact that the Hawaiians recog-
nized two species by name: pintail (Koloa
Mapu) and shoveler (Koloa Moha), indicating
that they were an obvious component to the Ha-
waiian avifauna before Captain Cook discovered
the islands in the 1770s. Surveys have docu-
mented migratory ducks exceeding 10,000 birds
in the mid-1950s (Medeiros 1958). We exam-
ined the data from biannual waterbird surveys
conducted on most lowland wetlands since the
1940s (Table 1). We omit data collected from
1960 through 1977 (Ni'ihau, Hawai'i, and Mo-
1oka'i not regularly surveyed during those peri-
ods). These data, summarized in Engilis (1988),
confirm that the population size of wintering
pintails in Hawai'i have declined tenfold. This
decline has led to added interest by conserva-
tionists to address habitat needs in the Hawaiian
Islands benefiting migratory waterfowl and
124
PINTAlL MIGRATION IN THE PACIFIC--Udvardy and Engilis 125
TABLE 1. CENSUS OF PINTAILS IN HAWAI'I
Year Total Pintails
1950 1,593
195l 1,875
1952 7,094
1953 8,226
1954 1,950
1955 2,653
1956 3,045
1957 1,619
1958 1,126
1959 1,249
1978 897
1979 490
1980 923
1981 377
1982 150
1983 60
1984 235
1985 150
1986 501
1987 203
Notes: Data from 1950 to 1959 l¾om Meideros (1950-1959). Counts
were taken on Maul, Hawai'i, O'ahu, and Kaua'i. Data from 1978 to
1987 from Engilis (1988). During 1960-1977 not all islands were sur-
veyed and records are sketchy. The period of 1978 1987 represents the
best modern data set as all eight main islands including Ni'ihau were
surveyed.
shorebirds. Understanding pintail movements to
Hawai'i will assist in these efforts.
Medeiros (1958) documented the movement
of pintails between the Hawaiian Islands and
North America, speculating a California-Hawai'i
flyway. Although this connection is correct, the
true migration patterns are more complex. We
analyzed banding data from the U.S. Migratory
Bird Management Office (MBMO), Yamashina
Institute for Ornithology, Japan, and the Russia
Bird Ringing Center. Included in our data col-
lection was a summary of available literature,
examination of specimens from the American
Museum of Natural History (AMNH), National
Museum of Natural History (USNM), and Bern-
ice P. Bishop Museum (BPBM), examination of
bird observation records from the Hawaii Rare
Bird Database (HRBD), and fieldwork conduct-
ed by us (Udvardy 1958-1960 and Engilis
1984-1997). These sources enabled us to gather
considerable amounts of data indicating that pin-
tails from at least half of the species circumpolar
distribution are potential winter visitors to Ha-
wai'i and that their movements across the Pacific
are complex. In the following discussion we try
to document these assumptions.
NORTHERN PINTAlL MIGRATION TO THE
HAWAIIAN ISLANDS
Of the 2,811 pintails banded in Hawai'i, 107
have been recovered on the North American
mainland and 16 have been retrapped on the is-
lands. Additionally, a pintail banded on Maui in
October 1952 was reported taken a month later
from Pukapuka (Danger) Atoll in the Tuamotu
Archipelago. Significantly, the Tuamotus are al-
most due south from the Hawaiian chain, as are
the Line Islands, where two pintails were recov-
ered two to three months after same-year autum-
nal banding in North America (MBMO data).
Medeiros' analysis of these returns lead him to
the conclusion that the islands' wintering pintail
population is not blown off course but are delib-
erately flying from central California to, and re-
turn there from, their wintering areas in Hawai'i.
Of the above mentioned 107 Hawai'i-banded
pintails, 45 were recovered in the San Francisco
Estuary, California (Fig. 1). These returns also
confirmed that pintails return to the islands one
or several years after the initial banding there.
Thus, pintails repeatedly and deliberately visit
Hawai'i to spend the winter, with some flying
further southward after having used the islands
in transit (Medeiros 1958). Medeiros speculated
that the autumnal flight probably used the north-
erly trade winds that originate outside central
California, while for the return flight in the
spring the ducks probably are helped by the
westerlies.
According to the MBMO banding/recovery
data, 165 pintails have been banded in Hawai'i
and recovered (including 16 in Hawai'i) be-
tween 1953 and 1960 (Fig. 1). The data reveal
that the high number of California returns in the
total of Hawai'i-banded ducks matches the dis-
tribution pattern, at banding, of 14 pintails band-
ed from 1951 to 1954 in North America and
later recovered in the Pacific (Fig. 2). In addi-
tion, the proportion of California's share in the
total of 165 records is 77.6% against all other
localities; if we compare California only with
the coastal entities of Alaska, British Columbia,
Washington, and Oregon, the proportions are
128 against 24, or 84.2%.
In order to assess the relation of mainland
populations of pintail to the population visiting
the Hawaiian Islands, according to the banding
and recovery results, we have compared the fig-
ures of banding effort, recoveries, and hunting
pressure on the Pacific coastal areas of North
America for the years of Medeiros's project (Ta-
bles 2, 3). We excluded Alaska from these tables
because there were no data available for hunting
pressure or banding efforts in Alaska for the
1950s.
Comparing the data in Tables 3 and 4, we
concluded that during the 1950s, California pin-
tails were indeed providers of over 90% of the
birds annually harvested by hunters in the tem-
perate Pacific Coast of North America and also
126 STUDIES IN AVIAN BIOLOGY NO. 22
FIGURE 1. Northern Pintails banded in Hawai'i and recovered anywhere.
of pintails annually banded there. The recoveries
in California are predominately from the fall
when hunting pressure is at its highest. Also,
pintails arrive in California earlier than most
species of migratory waterfowl, boosting the
California figures (Miller 1985). These facts,
overlooked by Medeiros, contributed to the pre-
dominance of California in the Hawaiian band-
ing and recovery data. However, California re-
mains a critical area for pintail, supporting over
50% of those wintering in the United States
(Heitmeyer et. al. 1989); thus it probably serves
as a principle staging area for Hawaiian-bound
pintails. This still needs to be confirmed through
modern marking and tracking studies. We note
that banding recoveries support the notion that
pintails could equally originate from other Pa-
cific Coast localities such as Mexico, Oregon, or
Washington (Figs. 1, 2).
A second pattern of movement can be seen
from birds banded in Hawai'i and recovered in
the Arctic. Five birds banded in Hawai'i in the
1950s were recovered in the Arctic: one in the
Aleutian Islands; another in the Yukon-Kuskok-
win Delta, an important breeding ground in
western Alaska; and two on Alaska's South
Coast (Fig. 1). One bird was recovered in the
Anadyr Region of eastern Russia (lat. 62 ø 5' N,
long. 179 ø 1' E). The later bird was a hatching-
year male banded on Maui, Hawai'i, 22 Febru-
ary 1954. It was shot on the breeding grounds
29 May 1960. These multiple recoveries strad-
dling the Bering Sea provide another migration
link from the Holarctic to the Hawaiian Islands.
We speculate that Arctic nesting pintail probably
make the transoceanic flight direct from south-
ern Alaska/Siberia to the Hawaiian Islands, in-
tercepting the leeward islands (e.g., Midway and
Laysan), resting, and then moving to the main
islands. Just as plausible, however, is a move-
ment of Alaskan birds south along the Pacific
Coast of North America, into California, and
then across the Pacific. This movement may be
indirectly supported by banding evidence of
Alaskan birds as nearly 80% of those recovered
have been taken in California (Austin and Miller
1995). The early arrival of pintails to Califor-
nia-males arrive in numbers by late August
(Miller 1985)-could allow time for birds to re-
fuel and make the flight to the Hawaiian Islands.
Again, this high return rate of Alaskan-banded
PINTAIL MIGRATION IN THE PACIFIC--Udvardy and Engilis 127
FIGURE 2. Northern Pintails banded anywhere and recovered in the Pacific Ocean (triangles recovery
location, dots = banding location).
pintails can be biased by the high number of
birds shot in California.
POPULATION DEMOGRAPHY OF PINTAIL
WINTERING IN THE HAWAIIAN ISLANDS
From Medeiros's banding data we note that
Hawai'i had a sex ratio skewed towards females
(Table 4). This is atypical for what has been re-
ported for pintails (and other ducks) of North
America, where males tend to outnumber fe-
males in most studies on the wintering and
breeding grounds (Bellrose et al. 1961, Miller
1985, Rienecker 1987, Austin and Miller 1995,
Migoya and Baldassarre 1995). The higher num-
ber of males recorded in waterfowl populations
has been speculated to be the result of a high
mortality rate (increased predation due to habitat
fragmentation) of adult females during the
TABLE 2. HUNTING PRESSURE a ON PINTAIL 1950--1956 AT PACIFIC COASTAL AREAS
Year British Columbia Washington Oregon California
1950 69,600 109,500 (est.) -- 1,945,300
1951 94,830 114,900 -- 2,966,000
1952 72,620 111,250 -- 4,659,000
1953 94,940 97,800 -- 4,599,500
1954 93,940 112,600 -- 3,461,600
1955 70,490 128,200 -- 3,312,700
1956 71,940 117,700 -- 3,526,000
Totals 568,360 791,950 913,620 (est.) 24,470,100
Yearly Mean 81,194 113,136 130,517 3,495,729
a Figures represent reported birds taken by hunters during the legal hunting season of each year. Source: state and provicial hunting records obtained
in writing by M.D.E Udvardy.
128 STUDIES IN AVIAN BIOLOGY NO. 22
TABLE 3. BANDING OF PINTAIL 1950--1956 AT PA~ TABLE 4. SEX RATIOS OF BIRDS BANDED IN THE HA-
CIFIC COASTAL AREAS WAIIAN ISLANDS (MEDEIROS 1950-1959)
British Sex ratio
Year Columbia Washington Oregon Calirnia Year N (Males to Females)
1950 28 110 234 9,334 1951 417 0.63
1951 26 774 544 19,360 1952 856 0.84
1952 31 656 102 17,570 1953 644 0.65
1953 0 433 574 16,737 1954 446 0.94
1954 5 143 1,000 16,514 1955 478 0.50
1955 5 625 2,931 21,475
1956 0 988 1,651 15,759
Total 95 3,729 7,036 116,749
Source: U.S. Migratory Bird Management office records.
breeding season (Johnson and Sargeant 1977).
The disproportionate numbers of females seen in
Hawai'i may therefore be the result of female
pintail's tendency to exhibit philopatty to their
winter quarters (Rienecker 1987, Anderson et al.
1992), coupled with the effort required to reach
the Hawaiian Islands. In addition, pintails un-
dergo a sex-segregated migration as males move
to molting grounds earlier than females, in some
cases arriving months earlier (Fuller 1953, Oring
1964, Salomonsen 1968, Bellrose 1976). Both
sexes appear prone to wander, particularly young
birds, as is revealed in the specimen record. Of
the 42 pintail specimens examined from Pacific
islands, 25 were hatching-year birds and 17 were
adults. Medeiros's trapping and banding data
also revealed a decline in pintail age ratio
throughout his study (Table 5). This decline was
also reflected in the Pacific flyway pintail pop-
ulation and was the result of a severe drought in
the prairie provinces of Canada depressing con-
tinental waterfowl populations (Ducks Unlimit-
ed 1990).
The timing of pintail migration to Hawai'i has
apparently changed in the past five decades. The
decline of pintails in North America has been
well documented, and we have seen a similar
decline in Hawai'i (Engilis 1988, Ducks Unlim-
ited 1990, Austin and Miller 1995). Not only has
there been a decline in numbers, but the period
of arrival has decreased as well. In the 1950s,
Medeiros documented birds arriving, in num-
bers, as early as mid-September. His banding re-
cords revealed that the early arrival was marked
by small flocks of males, followed by females
and hatching-year birds that arrived in October.
Pintail numbers peaked in November. This sex-
segregated migration pattern has been docu-
mented for other waterlbwl in North America,
particularly in California where male pintail
comprised over 90% of the total birds arriving
in August but only 53% of the total wintering
population once females arrived (Miller 1985).
By the mid-1980s to present, pintail arrival
patterns changed in HawaiT A more abbrevi-
ated migration occurs with the main bulk of pin-
tail arriving in the islands, marked by hatching-
year birds (based on the timing of their body
molt; A. Engilis, unpubl. data) by late October,
peaking in November, and stabilizing at a few
hundred birds through the winter. We speculate
that the early arrival of male pintails to Hawai'i
was lost during the years of continental decline
(mortality?) from 1975 to 1985 leading to the
observed, abbreviated migration and decline in
Hawai'i. In the late 1990s, a few early flocks
have again been observed in late September;
most are comprised of male birds (A. Engilis
and A. J. McCafferty, pets. obs.). During the
same period, pintail numbers have increased on
the continent (USFWS 1996b).
MOVEMENT OF NORTHERN PINTAlL
ACROSS THE PACIFIC
To complete the assessment of pintails mi-
grating across the Pacific, we assembled data for
pintail banded in North American and recovered
in Eurasia. One movement of birds between the
continents has been documented, with part of the
population breeding in eastern Siberia and win-
tering in the western United States (Dement'ev
and Gladkov 1952, Henny 1973). Again the
banding recoveries (N = 423) yield a more com-
plex pattern of movement across the North Pa-
cific than first thought. To make sense of these
data, we combined the patterns of movement
into three groups.
TABLE 5. RATIOS OF WINTERING NORTHERN PINTAlL
ADULTS TO JUVENILES IN THE PACIFIC FLywAY AND THE
HAWAIIAN ISLANDS BASED ON BANDING RECORDS (MED-
EIROS 1950--1959)
Year Hawai'i Pacilic Flyway a
1951 1.19 3.50
1952 2.07 3.70
1953 0.51 0.50
1954 0.72 0.50
a Extrapoled from Bellrose et al. 1961.
PINTAlL MIGRATION IN THE PACIFIC--Udvardy and Engilis 129
FIGURE 3. Northern Pintail banding recoveries in Asia below 50 ø N; birds banded in North America (triangles
= recovery location, dots = banding location).
GROUP 1
Three birds were recovered in Europe and one
in western Siberia. The first bird, a drake, was
banded in northern California and shot eight
years later in western Siberia. Another drake,
also from California, and was recovered two
years later from the Arctic coast of Russia's
Kara Sea. A third, an immature drake from the
Canadian maritime province of Nova Scotia,
was found in Chechia two and a half years later.
These records provide an example of the mech-
anism whereby these circumpolar, wetland spe-
cies mix their genotype so that no specialization
could occur, supporting the notion that the Hol-
arctic pintail population remains panmictic and
opportunistic, thus adapted to varying climate
conditions (Udvardy 1969:180-181). The last of
these cases defies all speculations; an adult fe-
male from northern California that was found
six years later in the Ukraine (Rienecker 1987,
1988).
The remaining 420 pintails mentioned above
were divide into two groups: those recovered in
Asia below 50 ø N (group 2) and those above it
(group 3).
GROUP 2
Below the 50 ø N parallel, 21 North American-
banded pintails have been recovered in Japan, 1
in Korea, and 2 in Sakhalin Island, Russia. Of
these 24 birds, all were winter visitors: 5 were
banded on the Aleutian Islands; a scattering
came from the tundra or northern parklands of
Canada; 11 were in a cluster from the southern
Canadian and northern U.S. prairies; and another
scattering originates in California and other
western states (Fig. 3). These data corroborate
Henny's data (1973) and, in addition, show that
there is an unknown, but sizable number of
North American pintails that regularly winter in
the region of the Sea of Japan, the area which
is also a wintering ground for some portion of
the East Asian breeding population (Dement'ev
and Gladkov 1952, Ornithological Society Japan
1974, Meyer de Schauensee 1984). Further, four
female pintails, all banded within 5 days of one
another on the Aleutian Islands, were recovered
in Japan: three of them 40, 52, and 64 days after
their banding date, respectively. The fourth was
recovered, also in Japan, a year later. These tour
females, banded in "immature" plumage, ex-
130 STUDIES IN AVIAN BIOLOGY NO. 22
2O ø
2½
FIGURE 4. Localities where Northern Pintails have been recorded in the Pacific Ocean (banding, sight and
specimen records). Sources: Reichenow (1899, 1901), Schnee (1901), Baker (1946), Gallagher (1958-1959),
Yocum (1964), Fosberg (1966), Amerson (1969), Ely and Clapp (1973), Palmer (1976), Pratt et al. (1987),
Engilis (1988), Stinson et al. (1997), specimens from American Museum of Natural History, National Museum
of Natural History, Bernice P. Bishop Museum, and sight observation records Hawaii Rare Bird Database).
emplify the regularity of visiting and returning
to winter grounds (cf. philopatry of Rohwer and
Anderson 1988), reminding us of similar data
from Medeiros's banding returns in the Hawai-
ian Islands. It is tempting to suggest a Canada-
Japan flyway on a great circle route from the
North American prairies through the Aleutian
Chain, Kamchatka, and the Kuri! Islands.
GROUP 3
The remaining 396 banded birds recovered in
Asia were there predominantly as spring-sum-
mer arrivals because 338 of them were found
from April to July, 55 in the fall months, and
only 3 in the winter. Beside Henny (1973), a
number of publications deal with drought dis-
placement of pintails to Alaska and beyond
(Derksen and Eldridge 1980; Hestbeck 1995,
1996). Thus, there is a sizable movement be-
tween breeding grounds in eastern Siberia and
wintering areas in North America. It is not
known whether these birds fly over the ocean or
in a great circle route or follow a coastal route
along the Pacific Rim.
To close the circle around the pintails of the
Hawaiian Islands, we looked at the rest of Oce-
ania (Fig. 4). Our scrutiny of the pertinent lit-
erature, banding records, and museum speci-
mens shows that every island group of central
Oceania has received pintail visitors, often in
numbers. We mention here two special cases as
extremes. During the period when the Marshall
Islands were German colonies, Anton Reichen-
ow reported in 1899 about an autumnal duck
migration viewed at Jaluit Atoll by reliable pub-
lic officers and documented by specimens sent
to the Berlin Museum as pintails, Green-winged
Teals, and Canvasbacks (Aythya valisineria).
"In ununterbrochener Folge ungeheure keilfor-
mige Schwiirme" (large numbers in uninterrupt-
ed sequence of enormous v-shaped flocks)
moved over the atolls of Bikar, Utirik, Ailuk,
Jemo, Likiep, and Wotje from north to south in
the fall, and back again in May (Reichenow
PINTAIL MIGRATION IN THE PACIFIC--Udvardy and Engilis 131
1899, 1901). Another observed migration to-
ward north and north-east in the vicinity of
Kwajalein Atoll was documented in May 1900
(Schnee 1901).
The pintail is also an uncommon, but regular
winter visitor to the Mariana Islands, occurring
regularly on the main islands of Guam (numer-
ous sites), Saipan (Lake Susupe), and Tinian
(Hagoi Marsh; Stinson et al. 1997). Kuroda
(1961) linked the pintail that reach Micronesia
to the "Nearctic Hawaiian Flyway" (cf. Baker
1953), referring to the now unrecognized North
American race (A. acuta tzitzihoa). However,
with the prevailing storms across Japan moving
east and southeast, it is conceivable that the
North American connection to the Marianas are
actually birds originating from the "Canada-Ja-
pan" corridor.
SUMMARY OF COLONIZATION EVENTS
BY HOLARCTIC MIGRANTS IN HAWAI'I
The winter range of Northern Pintail is per-
haps the most widespread distribution area of all
species of waterfowl (Palmer 1976, Austin and
Miller 1995). Pintail are prone to disperse and
wander as is evident by the banding, observa-
tion, and specimen information synthesized
here. The species has been recorded on all con-
tinents except Antarctica and shares ancestry
with the endemic island form in the Southern
Hemisphere, Eaton's Pintail (Arias eatoni). Hol-
arctic species prone to wandering have given
rise to the majority of known endemic water-
birds and most landbirds of North Pacific islands
(Fleischer and Mcintosh this volume). The ma-
jority of the species that have colonized are
those whose resources naturally fluctuate, both
on a regional and seasonal pattern. Many of
these are representative of highly volatile spe-
cies such as fringillid finches, frugivorous
thrushes, waterbirds (rallids, shorebirds, and
ducks), and raptors, the latter whose populations
erupt relative to fluctuating small mammal num-
bers. Colonization events have been rarely doc-
umented on island groups, and although pintail
have yet to be recorded nesting in Hawai'i, other
Holarctic migrants have. We summarize three
cases where colonization has led to, or is sus-
pected to have lead to, a Hawaiian breeding pop-
ulation of a Holarctic migrant.
FULVOUS WHISTLING-DUCK
The Fulvous Whistling Duck (Dendrocygna
bicolor) apparently reached Hawai'i under its
own power in 1982 when a flock of six birds
suddenly appeared on O'ahu (Leishman 1986).
They began nesting on O'ahu's North Shore, ex-
panding to nearly 30 birds in under five years.
Dispersal records of individual birds were doc-
umented on Moloka'i, Maui, and Kaua'i during
the late 1980s. After the decline of wetlands and
aquaculture on O'ahu's North Shore in 1992, the
population of Fulvous Whistling Ducks crashed
dramatically, so that by 1998 only one bird re-
mained on the James Campbell National Wild-
life Refuge (A. Engilis, Jr., pets. obs.). It is of
interest to note that the whistling duck has high
populations on the Pacific Coast of North Amer-
ica only in western Mexico. Thus it is conceiv-
able that these birds originated from there, as
could migratory pintail as stated earlier. A Mex-
ico-Hawai'i tie is also suggested by other va-
grants that have occurred in Hawai'i: e.g., Little
Blue Heron (Egretta caerulea), Laughing Gull
(Larus atricilla), and Great-tailed Grackle
(Quiscalus mexicanus; Pyle 1997).
PIED-BILLED GREBE
The Pied-billed Grebe (Podilymbus podiceps)
has bred in Hawai'i since the mid-1980s. A sin-
gle bird arrived to overwinter in 1984 on 'Ai-
makapfi Pond, located on the Kona Coast of Ha-
wait It left in the spring of 1985. Two birds
returned the following fall, remained, and gave
rise to a population on the pond that remained
stable at a dozen birds throughout the late 1990s
(R. David, unpubl. data). These two birds re-
mained and have given rise to a population on
the pond that remains stable at about a dozen
birds. Dispersal records on Kaua'i, Maui, and on
other wetlands of the island of Hawai'i are be-
coming more frequent in recent years, probably
representing young birds that may have origi-
nated from 'Aimakapfi Pond (HRBD, unpubl.
data).
GREAT BLUE HERON AND WHITE-FACED IBIS
Although they have not yet been recorded
breeding, two Holarctic ciconids are now regular
residents in small numbers, the Great Blue Her-
on (Ardea herodias) and White-faced Ibis (Ple-
gadis chihi). Great Blue Herons continue to
wander through the chain and at times form
small groups, often roosting among nesting col-
onies of Cattle Egrets (Bubulcus ibis) and Black-
crowned Night Herons (Nycticorax nycticorax).
What drives these birds to disperse to the Pa-
cific islands remains unclear, as do the mecha-
nisms of how they navigate to the islands year
after year (wintering shorebirds and waterfowl).
Mayr (1953) discussed the migration of birds
across the Pacific speculating that historically
the islands of the Pacific were more massive,
thus providing better opportunity for coloniza-
tion. He also suggested two patterns affecting
Holarctic birds, that of route abbreviation and
route prolongation. The Northern Pintail might
more readily fall into the latter group of mi-
132 STUDIES IN AVIAN BIOLOGY NO. 22
grants, a species whose migration patterns have
been elongated as a result of global climate
changes and expanding breeding range north-
ward, away from traditional wintering grounds.
Baker (1953) further alluded to the fact that oce-
anic islands provide excellent wintering grounds
due to the absence of mammal and reptilian
predators. Both authors discussed their findings
with an emphasis on northern nesting shore-
birds, including those species where the majority
of the known population winters in the Pacific:
Bristle-thighed Curlew (Numenius tahitiensis),
Pacific Golden Plover (Pluvialisfulva), Wander-
ing (Heteroscelus incanus) and Gray-tailed (H.
brevipes) Tattlers, and Bar-tailed Godwit (Li-
mosa lapponica; Baker 1951, Mayr 1953).
Finally, migration out over the Pacific Ocean
has rarely been observed, owing to paucity of
observers and opportunities. A great "corridor"
of migrating Alaska pintails was observed in the
fall in southern British Columbia, and another
one moving from Alaska southwest across the
Pacific has been postulated (Bellrose 1976,
Campbell 1990) and backed by observations
(Martin and Myres 1969). We uncovered one
specimen of American Wigeon (AMNH
131716) collected by C. H. Townsend in 1891
from the USS Albatross, "500 miles NW of
O'ahu", documenting yet another species'
movement across the Pacific. Perhaps new tech-
nologies for tracking large birds (satellite telem-
etry and Doppler radar) may help shed light on
these movements. The evidence bears out a
complex setting for migratory waterfowl in the
Pacific, fortunately observers of the past had the
foresight to band pintails to help us elucidate
these movements herein. What has become clear
is that pintail remain a regularly occurring com-
ponent of the Pacific island avifauna, represent-
ing a link to the mechanics of island coloniza-
tion from the Holarctic faunal region.
ACKNOWLEDGMENTS
In assembling the data for this paper we received
enthusiastic help and data from many fellow wildlifZ
researchers such as C. Kessler, B. H. Powell, J. M.
Sheppard, K. Smith, and G. J. Wiles, all of the U.S.
Geological Survey. The following provided banding
data for our studies: B. Trost of the U.S. Fish and
Wildlife Service for information on pintail banded in
North America; M. Yoshii of the Yamashina Institute
for Ornithology for information on pintail in Japan; in
the 1960s, A. Vinckurov of the Russia Ringing Center,
Moscow, for data on pintails in Russia. The original
hunter and banding data frmn the 1950s has been cour-
teously provided by the departments of wildlife of Ha-
wai'i, Alaska, British Columbia, California, Oregon,
Washington, and the U.S. Fish and Wildlife Service.
B. O'Hara and A. Morton of Ducks Unlimited created
all figures and M. Doyle helped with many of the tech-
nical details while working on the data. We would also
like to thank M. LeCroy (AMNH), P. Angle (USNM),
and C. Kishinami and R. L. Pyle (BPBM) for access
to specimens and assistance while working with col-
lections. K. Evans and J. M. Scott provided helpful
comments on the manuscript. The junior author thanks
M. Udvardy and family for their support of the manu-
script after M.D. E's untimely passing.
Studies in Avian Biology No. 22:133-143, 2001.
THE HAWAI'I RARE BIRD SEARCH 1994-1996
MICHELLE H. REYNOLDS AND THOMAS J. SNETSINGER
Abstract. We compiled the recent history of sightings and searched for 13 rare and missing Hawaiian
forest birds to update status and distribution information. We made 23 expeditions between August
1994 and April 1996 on the islands of Hawai'i, Maui, Moloka'i, and Kaua'i totaling 1,685 search
hours, 146 field days, and 553 person days. During our surveys we found four critically endangered
birds: the Po'ouli (Melamprosops phaeosoma, five to six individu',fis), Maui Nukupu'u (Hemignathus
lucidus affinis, one individual), 'I'iwi (Vestiaria coccinea) on Moloka'i (one individual), and the
Puaiohi (Myadestes palmerk 55-70 individuals). Detection rates for each species were 0.013, 0.002,
0.012, and 0.318 detections/hr, respectively. Although not visually confirmed during our surveys,
auditory detections, unconfirmed sightings, and other reports suggest the possible existence of '0'fi
(Psittirostra psittacea) on Hawai'i, Kaua'i Nukupu'u (Hemignathus lucidus hanapepe), and Maui
',kepa (Loxops coccineus ochraceus) in perilously low numbers. Six undetected forest bird popula-
tions, Kfima'o (Myadestes myadestinus), Kaua'i ')'6 (Moho braccatus), Bishop's '6'0 (Moho bishopi),
'0'fi on Kaua'i, Greater 'Akialoa (Hemignathus ellisianus), and Kfikfiwahie (Paroreomyza fiammea)
have high probabilities of being extinct. Oloma'o (Myadestes lanaiensis) from Moloka'i are probably
extirpated from the areas searched on that island but may persist on the unsurveyed Oloku'i Plateau.
Key Words: bird survey; critically endangered; extinct; Hawai'i; 'I'iwi; Nukupu'u; Po'ouli; Puaiohi.
Descending from a small number of original col-
onizers, Hawai'i's native plants and animals are
an evolutionary panoply. Species underwent ex-
plosive adaptive radiation and specialization in
the world's most isolated island chain (Carlquist
1974, Scott et al. 1986, Freed et al. 1987a, Ho-
warth et al. 1988, James and Olson 1991, Olson
and James 1991, Wagner and Funk 1995, Pratt
and Pratt this volume). Striking examples of spe-
ciation occurred among the lobelioids, fruit flies,
land snails, and Hawaiian honeycreepers (Frin-
gillidae: Drepanidinae), with more than 50
known species having evolved from one cardue-
line finch colonizer (Johnson et al. 1989, Tarr
and Fleischer 1995).
The isolation that allowed such unique adap-
tations also predisposed the ecosystem to vul-
nerability due to human caused and stochastic
natural disturbances. Multiple pressures have re-
sulted in catastrophic species extinctions; habitat
destruction and nonnative species introductions,
including ungulates, mammalian predators,
pathogens, and disease vectors, have had the
most extensive and detrimental effects on Ha-
wai'i's island ecosystem (Atkinson 1977, Ralph
and van Riper 1985, Scott et al. 1986, Loope et
al. 1988, Atkinson et al. 1995). Recent fossil ev-
idence indicates at least 50% of the original avi-
fauna went extinct after the arrival of the Poly-
nesians about 400 AD, and today 75% of the
historically known native birds are either extinct
or endangered (James and Olson 1991, Olson
and James 1991, Ehrlich et al. 1992).
Coincident with increased human develop-
ment and the spread of the Culex mosquito since
the 1900s, HawaiTs remaining native avifauna
has experienced a steady decline with low-ele-
vation and specialized species suffering partic-
ularly heavy losses (Baldwin 1953, Warner
1968, Scott and Kepler 1985, van Riper et al.
1986, Pratt 1994). Many species that were abun-
dant or common into the early 1900s had low
population densities during the extensive U.S.
Fish and Wildlife Service (USFWS) Hawaiian
Forest Bird Surveys (HFBS) of the 1970s and
1980s (e.g., '(5'fi [Psittirostra psittacea], Maui
'kepa [Loxops coccineus ochraceus], '(5'0
[Moho spp.], Hawaiian Crow [Corvus hawaiien-
sis] or 'Alalfi, Moloka'i's Oloma'o [Myadestes
lanaiensis rutha], and Kfima'o [Myadestes my-
adestinus]; Bryan and Seale 1901, Henshaw
1902a, Perkins 1903, Bryan 1908; Banko 1980a,
1980b, 1981a, 1984a, 1986; Scott et al. 1986).
Today the existence of more than half Hawai'i's
critically endangered (Mace and Lande 1991)
birds is seriously in question (Pratt 1994,
USFWS 1996a).
The Convention on International Trade in En-
dangered Species and the World Conservation
Union (WCU 1982) have set 50 years of no
sightings as the arbitrary limit to declare species
extinction. This may be a useful definition in
some cases, but it is hardly appropriate when
periodic intensive search effort or surveys by
qualified personnel make it possible to evaluate
the likelihood of extinction objectively. While
most of Hawai'i's endangered endemics are rare,
often cryptic species that inhabit remote, rainy,
and treacherous terrain where search effort is ir-
regular (further complicated by difficulties in
gaining access to rare bird habitat on both public
and private lands), the periodic survey and in-
tensive search methodology initiated in Hawai'i
in the 1960s (Richardson and Bowles 1964, Sin-
133