We determined habitat preferences for males and females of nine species of dichromatic warblers in the Sian Ka'an Reserve, Quintana Roo, Mexico. We found significant habitat segregation in the American Redstart (Setophaga ruticilla), Common Yellowthroat (Geothlypis trichas), Magnolia Warbler (Dendroica magnolia), and Northern Parula (Parula americana), and we confirmed previously reported habitat segregation in the Hooded Warbler (Wilsonia citrina). Possible differences in habitat distribution were found in the Black-and-white Warbler (Mniotilta varia), Prothonotary Warbler (Protonotaria citrea), and Black-throated Green Warbler (Dendroica virens). Only migratory Yellow Warblers (Dendroica petechia) showed no sign of sexual segregation. In all five cases where there is a significant difference between successional stages, males occupied the more mature habitat. The overall frequency and spatial pattern of recaptures were similar between sexes. Received 29 March 1989, accepted 26 January 1990.
Estacion Biologica Donana, Consejo Superior de Investigaciones,
Avenue Maria Luisa s/n, Seville, 41113 Spain, and
2National Zoological Park, Washington, D.C. 20008 USA
HABITAT segregation between the sexes was
first described for American Kestrels (Falco
sparverius, Mills 1976) and Eastern Great Reed
Warblers (Acrocephalus orientalis, Nisbet and
Medway 1972). More recently the first species
of Neotropical migrant land bird was found to
display intersexual segregation. Male and fe-
male Hooded Warblers (Wilsonia citrina) defend
territories in different habitats (Lynch et al. 1985,
Morton et al. 1987). Males were common in ma-
ture forest, and females occurred in a variety of
scrub habitats. However, the overall frequency
of habitat segregation among Neotropical mi-
grants has not been established. Sexual habitat
segregation has important implications for un-
derstanding the life history and demography
of particular species and for assessing the pos-
sible effects of habitat alteration. We report the
results of a survey of the most common dichro-
matic migratory wood warblers found in the
Northeastern Yucatan Peninsula. The results
summarize two different surveys; each author
conducted one survey. We used two techniques
(mist-netting and visual-auditory surveys),
which produced complementary data sets.
Where the data can be compared, the results are
generally in agreement. The data sets together
provide information on all of the common di-
3 To whom reprint requests should be sent.
539
chromatic warblers in the Sian Ka'an Reserve,
Quintana Roo, Mexico.
METHODS
Study area.--The fieldwork was conducted in the
Sian Ka'an Biosphere Reserve and surrounding ejidos
(rural land cooperatives) in the northeast coastal re-
gion of the Yucatan Peninsula. The reserve receives
1,200 mm/yr of rainfall, primarily during a rainy sea-
son from June to November. The area supports a high
abundance and diversity of Nearctic migrants during
the nonbreeding season (Waide 1980, Lynch 1989).
We conducted surveys in coastal dune scrub, man-
grove scrub, seasonally flooded scrub, low forest, me-
dium-height subdeciduous forest, medium-height
subperennial forest, pasture, and postclearing succes-
sional scrub. These habitats represent the major vege-
tation types of the eastern Yucatan Peninsula (Miran-
da 1958, Olmsted et al. 1983).
Within each habitat where we mist-netted, the veg-
etative cover was categorized and estimated for an
imaginary circle centered at each of 24 net sites. The
categories include (a) herb, grass, or fern; (b) scrub
(1-4 m); and (c) trees (4 m+). Cover was estimated to
one of five classes, each representing 20% (e.g. cover
class 1 = 1-19%, class 2 = 20-39%). A quantitative
description of the habitats is presented (Table 1). Me-
dium-height subperennial forest was not sampled in
an equivalent fashion, but it has greater stature (mean
canopy height = 13-15 m), fewer deciduous canopy
trees, and a moister, shadier understory than subde-
ciduous forest.
To analyze the bird survey data, we pooled the
TABLE 1.
plot.
LOPEZ ORNAT AND GREENBERG [Auk, Vol. 107
Habitat structure measurements of study plots. Numbers are means (+SD) based on 24 points per
Plot size Canopy ht. Vegetative cover Mist-net
(ha) (m) Trees Shrubs Herbs hours
Second growth
1-2 yr 1.5 1.1 + 0.3 0 2.6 + 0.9 2.6 + 1.6 1,105
3-4 yr 1.5 1.6 + 0.6 0.4 + 0.6 3.1 + 1.0 2.0 + 1.0 1,230
7-8 yr 3.0 3.7 + 1.1 2.6 + 1.0 1.5 + 0.7 1.2 + 1.0 1,250
Mangrove scrub 1.5 2.1 + 1.2 1.6 + 0.8 4.0 + 0.8 0.4 + 0.6 576
"Sabana" 1.5 2.1 + 1.5 1.2 + 1.6 2.0 + 1.3 2.7 + 1.0 1,656
Low forest 1.5 5.5 + 1.6 3.6 + 0.5 1.6 + 0.9 0.6 + 0.6 1,728
Medium forest 2.5 11.0 + 1.6 4.1 + 0.6 0.9 + 0.3 0.2 + 0.1 1,404
habitats in two ways. The mist-netting data (Table 2)
are compared for open habitats (second growth 3-4
yr of age or younger and sabana, a marshlike habitat),
scrub (7-8-yr-old second growth and mangrove scrub),
low forest (seasonally flooded low forest), and me-
dium forest. To analyze the broad-scale visual survey,
we contrasted scrub habitats (from pasture to 7-8-yr-
old second growth), subdeciduous, and subperennial
forests.
Mist-netting.--In each of the vegetation types (ex-
cept subperennial forest), we established grids that
consisted of 3 parallel lines with 8 mist nets (2 x 12
m, 30 mm mesh) on each line. Nets were spaced 15-
25 m apart along the lines, and 50-70 m between the
lines. The total areas netted varied between habitats
from 1.5 to 3.0 ha. Nets were opened at dawn (ca.
0600) and closed 6 h later. Nets were opened for at
least three consecutive days in each habitat during
the autumn, winter, and spring of 1985/1986 and of
1986/1987 for a total of 9,372 net hours. All of the
habitats were sampled each year in midwinter. Ad-
ditional netting was done in September-October and
April in some habitats. Because only ground-level
mist nets were used, the relative numbers of individ-
uals captured do not reflect differences in species'
abundance between different habitats (Lynch 1989).
Visual surveys.--The Sian Ka'an Reserve and nearby
areas were surveyed during the winter of 1987/1988
and of 1988/1989. The surveys were designed only
to determine sex ratios, not to estimate relative abun-
dance. A particular habitat patch or trail was selected
for each survey, and the sex of each dichromatic war-
bler was recorded. Effort was made to select sites that
were away from edge situations and could be un-
ambiguously assigned to one of three major habitats:
scrub, subdeciduous, or subperennial forests. Each site
was visited only once each winter.
Criteria used to distinguish sexes.--Sex was deter-
mined for all species by plumage characteristics. The
criteria were developed from the USFWS banding
manual (1984) and supplements from Pyle et al. (1987).
There is a likelihood of some error for subtle dis-
tinctions (such as between first-year male and female
American Redstarts, and male and female Magnolia
Warblers. For participants in the visual surveys, in-
terobserver consistency was tested both with mist-
netted and observed birds, and it was found to be
high for both. For Magnolia Warblers, observer clas-
siftcation from plumage characters was checked in-
dependently against wing chord (using a cutoff of 58
mm or greater for males), and they were consistent
97% of the time. Resident Yellow Warbler females
were distinguished from migratory females by their
grayer upperparts and duller yellow underparts.
TABLE 2. Ratio of males to females in mist-netted samples of warblers. Data were pooled to conduct Chi-
square contingency test for heterogeneity in sex ratio. a
Medium
Open Scrub Low forest forest P
Black-and-white Warbler 8:7 0:3 5:15 1:1 NS
Prothonotary Warbler 15:6 1:2 4:2 1:2 NS
Yellow Warbler 4:6 6:7 0:0 0:0 NS
American Redstart 2:19 6:3 4:10 4:3 <0.025
Hooded Warbler 3:11 1:20 9:10 8:1 < 0.01
Common Yellowthroat 25:27 b 22:12 8:0 0:0 <0.025
' Data were pooled to make the following comparisons: Black-and-white Warbler, American Redstart, and Hooded Warbler open+scrub habitat
vs. forest; Prothonotary Warbler and Common Yellowthroat open habitat vs. scrub+ forest; and Yellow Warbler open habitat vs. scrub.
Significant heterogeneity exists between the recently cleared fields (11:24) and the sabana or marsh-like habitat (14:3).
T^BLE 3. The percentage of males that comprises sightings of dimorphic warblers in scrub and forest habitats
(sample size in parentheses).
Species Scrub Subdeciduous Subperennial
Black-and-white Warbler 58 (12) 55 (20) 48 (62)
Northern Parula a 37 (83) 59 (27) 67 (48)
Black-throated Green Warbler 47 (30) 50 (40) 63 (72)
Magnolia Warbler a 36 (99) 55 (64) 60 (101)
American Redstart 35 (113) 74 (90) 80 (139)
(adult males) a 16 48 47
Hooded Warbler a 11 (72) 67 (83) 89 (97)
Significant (P < 0.05) heterogeneity based on Chi-square contingency test pooled forest vs. scrub data.
Statistical tests.--Testing for differences in the pro-
portion of males in different habitats was by a Chi-
square contingency test. For the visual data, tests com-
pared forest and scrub habitats. Because of variable
and sometimes small sample sizes, the mist-net data
were also grouped. In all cases, adjacent habitats along
the successional gradient were pooled. However, be-
cause of the differences in distribution across the
successional gradient, habitats were grouped in dif-
ferent ways.
RESULTS
Prothonotary WarbIer.--The Prothonotary
Warbler (Protonotaria citrea) was a common tran-
sient (mainly in autumn). The few mist-net cap-
tures in scrub and forest habitat showed no skew
in sex ratio. However, most birds captured in
open habitats were males. The difference in sex
ratio between open and other habitats was not
significant.
Black-and-white WarbIer.--Black-and-white
Warblers (MniotiIta varia) were found primarily
in forests. The mist-nets yielded a high pro-
portion of females in the low forest, but sample
sizes for other habitats were generally small and
the difference between pooled forest and open-
scrub samples was not significant. Visual sur-
veys indicated an even sex ratio for scrub and
forest habitats.
Northern ParuIa.--Northern Parulas (ParuIa
americana) were found in most terrestrial hab-
itats in Sian Ka'an, but were most common in
older secondary-scrub with a substantial num-
ber in the canopy of the subperennial forest.
Few were mist-netted. Based on the visual sur-
veys, Northern Parulas had a significantly fe-
male-biased sex ratio in scrub and male-biased
sex ratio in the taller forests (Table 3).
Yellow Warbler.--During winter most of the
Yellow Warblers (Dendroica petechia) in the Sian
Ka'an area were migrants. Yellow Warblers were
common, but had a very restricted habitat dis-
tribution. They were most common in the nat-
ural scrub vegetation (mangrove and coastal
scrub), and uncommon in postclearing succes-
sion. In the open and scrub habitats considered
here, Yellow Warblers displayed an overall even
sex ratio with no indication of interhabitat vari-
ation. When additional data from coastal scrub
were included, the overall sex ratio was also
equal (30:32).
Magnolia Warbler.--Magnolia Warblers (D.
magnolia) were common in every habitat except
recently cleared fields, although they were more
common in forest than scrub. They were cate-
gorized only by sex in the visual surveys (Table
3). There was a small but significant bias to-
wards females in the scrub and towards males
in the forest habitats.
Black-throated Green WarbIer.--Black-throated
Green Warblers (D. virens) were most common
in forest, and were uncommon in secondary
scrub with high densities of Acacia and other
leguminous trees. Based on the visual surveys
(Table 3), we found a nonsignificant trend to-
wards an increased proportion of males in taller
forest habitat.
Hooded Warbler.--Hooded Warblers were in
every habitat except mangrove scrub. Based on
mist-netting (Table 2), we found 8 times as many
males as females in medium forest, but only 13%
as many males as females in open and scrub
habitats (P < 0.001). The structurally interme-
diate low forest had an intermediate sex ratio.
Similar results were obtained in the visual sur-
vey (Table 3) with the proportion of males rang-
ing from 11% in scrub to 89% in tall forest hab-
itat (overall Chi square, P < 0.001).
American Redstart.--American Redstarts (Se-
tophaga ruticiIIa) were numerous in all habitats
with at least some woody vegetation. Mist-net-
ting data (Table 2) show that almost all birds in
the open habitat were females, whereas males
made up 29-67% of the small samples captured
in scrub to subdeciduous forest. There was no
consistent trend within scrub and forest habi-
tats. Perhaps, because of a larger sample size
(particularly for forest habitats), the difference
in sex ratio was clearer with the visual survey
data. Males made up 74-80% of the forest ob-
servations, and only 35% of the scrub obser-
vations (P < 0.001). The proportion of adult
males, where no problem in accurate determi-
nation by plumage should exist, also increased
dramatically between scrub and forest habitat.
Common Yellowthroat.--The Common Yellow-
throat (Geothlypis trichas) was the most common
warbler in open habitats, but it was absent from
all forest types except seasonally flooded low
forest. Mist-net captures were significantly
skewed towards females in the open pastures
and fields (11:24), and male-biased for the older
second-growth scrub habitats (30:12). In the
natural open habitat, "sabana," males were more
common (14:3).
Recaptures.--Of the individual warblers from
four species (Table 4), 21% (n = 223) were re-
captured after at least 30 days from their first
capture. Although there was considerable in-
terspecific variation, there was no significant
difference in site tenacity between the sexes.
Females were recaptured at a slightly and non-
significantly higher rate (males, 16%; females,
24%). The mean distance between captures and
recaptures (activity radius, Table 4) was similar
for both sexes in all species, with the possible
exception of the American Redstart.
DISCUSSION
Some degree of habitat segregation by sex is
the rule for dimorphic warblers that migrate
through or winter in the northeastern Yucatan
Peninsula. In all five species where there is a
significant pattern, males occupy the more ma-
ture habitat along the successional gradient. In
addition, the Black-throated Green Warbler
showed a nonsignificant trend in the same di-
rection. The one exception was in migratory
populations of the Prothonotary Warbler. This
exception is noteworthy because Prothonotary
Warblers have been found commonly in male-
female pairs during winter in Panama (Morton
1980, pers. obs.). However, although the sex
ratio is female-biased in open habitats, it is not
significantly different from the samples from
other habitats. Furthermore, sex ratio was based
on a small sample of transient individuals.
In the Hooded Warbler, Morton (1990) has
argued that the proximate mechanism for sex-
ual habitat segregation is an innate difference
in the response to simple cues. Support for this
hypothesis comes from two experiments. In one,
a removal experiment, females failed to occupy
mature forest when the resident males were
removed (Morton et al. 1987). In a laboratory
experiment, naive hand-reared males and fe-
males showed distinct preferences for plant
height and habitat structure (Morton 1990). In-
nate differences in habitat preference should
lead to relatively invariant differences in hab-
itat occupied. Habitat segregation in this species
is, in fact, nearly complete, particularly when
fine-scaled habitat measures are analyzed with
multivariate techniques (Lynch et al. 1985).
However, few of the species show habitat seg-
regation that is as clearly defined as in the
Hooded Warbler. In the case of Magnolia War-
biers and Northern Parulas, the magnitude of
the segregation was small, although statistically
significant. In these situations, the role of dom-
inance interactions between the sexes may be
more important. Experiments similar to those
conducted on Hooded Warblers would make an
interesting comparison. We found no support
for the idea that females behave as "floaters" in
the nonforest habitat. The overall frequency and
pattern of recaptures was similar between the
sexes.
Perhaps a more facultative basis for habitat
segregation explains the apparent differences
between studies for the same species. Holmes
et al. (1989) reported no consistent habitat seg-
regation between the sexes of American Red-
start in four Jamaica study areas. Another ex-
planation is that the same degree of habitat
segregation occurs in Jamaica and Mexico, but
the study in Jamaica focused on a more narrow
and structurally intermediate range of habitats.
Two possibilities have been presented for the
evolution of habitat segregation in Hooded
Warblers (Lynch et al. 1985). One explanation
holds that differences in sex roles during the
breeding season may lead to asymmetrical dom-
inance relationships in the winter. Males, the
larger and more aggressive sex, are able to ex-
clude females from the better habitat. An alter-
native hypothesis is that the two habitats rep-
resent different adaptive peaks. Males and
females are best adapted for feeding and avoid-
TABLE 4. Activity radius (mean [___SD] intercapture distance) and recaptures for four species of warblers. The
sex ratio of recaptures is not significantly different from the sex ratio of captures in any species (Chi-square
contingency test); sample sizes are in parentheses.
Species Sex Activity radius (m) Captures Recaptures
Black-and-white Warbler M 87 ___ 44 (33) 14 3
F 65 ___ 32 (39) 26 9
American Redstart M 37 + 21 (16) 16 3
F 93 ___ 35 (47) 35 10
Hooded Warbler M 100 ___ 81 (33) 21 6
F 82 ___ 40 (42) 42 9
Common Yellowthroat M 80 + 37 (43) 41 3
F 57 ___ 38 (33) 36 4
ing predators in their preferred habitats. We
cannot help distinguish these two hypotheses.
However, these observations and others (for
Black-throated Blue Warblers, Dendroica caeru-
lescens; Wunderlie pers. comm.) suggest that
habitat preference is not an arbitrary feature of
a particular sex for a particular species. Rather,
there seems to be a repeated pattern: male war-
biers are associated with forest and females with
more open habitats.
ACKNOWLEDGMENTS
We thank James F. Lynch for comments on earlier
drafts of the manuscript. We also thank Thomas W.
Sherry and two anonymous referees for their careful
reviews, and Mauro Berlanga, Oscar Barrera, James
Lynch, Daniel Niven, Dana Bradley, David and Jill
Heath, and Rosa Maria Vidal for assistance in field-
work. We thank Barbara McKinnon de Montes and
Amigos de Sian Ka'an, A.C., for support during field-
work. We thank SEDUE for use of the facilities at the
Sian Ka'an Biosphere Reserve. Research was funded
by grants from the Direcci6n General de Investi-
gaci6n Cientifica y Tecnica, Ministerio de'Educaci6n
of Spain, and the National Ecology Research Center
of the U.S. Fish and Wildlife Service.
LITERATURE CITED
HOLMES, R. T., T. W. SHERRY, & L. REITSMA. 1989.
Population structure, territoriality and overwin-
ter survival of two migrant warbler species in
Jamaica. Condor 91: 545-561.
LYNCH, J. F. 1989. Distribution of overwintering
Nearctic migrants in the Yucatan Peninsula: I.
General patterns of occurrence. Condor 91: 515-
545.
ß , E. S. MORTON, & M. E. VAN DER VOORT. 1985.
Habitat segregation between the sexes of over-
wintering Hooded Warblers (Wilsonia citrina). Auk
102: 714-721.
MILLS, G. S. 1976. American Kestrel sex ratios and
habitat separation. Auk 93: 740-748.
MIRANDA, F. 1958. Estudios acerca de la vegetacion.
Pp. 215-271 in Los Recursos Naturales del Sureste
y su aprovechamiento, parte II: Estudios partic-
ulates. Mexico City, Inst. Mexicano Recursos Nat.
Renovables (IMERNAR).
MORTON, E.S. 1980. Adaptation to seasonal changes
by migrant landbirds in the Panama Canal Zone.
Pp. 437-457 in Migrant birds in the Neotropics
(A. Keast and E.S. Morton, Eds.). Washington,
D.C., Smithsonian Inst. Press.
1990. The evolution of habitat segregation
by sex in the Hooded Warbler: experiments on
proximate causation. Am. Nat. 135: 319-333.
, J. F. LYNCH, K. YOUNG, & P. MELHOP. 1987.
Do male Hooded Warblers form nonbreeding ter-
ritories in tropical forest? Auk 104: 133-135.
NISBET, I. C. T., & L. MEDWAY. 1972. Dispersion, pop-
ulation ecology, and migration of Eastern Great
Reed Warblers A crocephalus orientalis wintering in
Malaysia. Ibis 114: 451-494.
OLMSTED, I. C., A. LOPEZ ORNAT, & g. DUP,q. 1983.
Vegetacion. Pp. 41-64 in Sian Ka'an, estudios pre-
liminares. Puerto Morelos, Q. Roo, Mexico,
CIQRO-SEDUE.
PYLE, P. D., S. N. G. HOWELL, R. P. YUNICK, & D. F.
DESANTE. 1987. Identification guide to North
American passerines. Bolinas, California, Slate
Creek Press.
U.S. FISH AND WILDLIFE SERVICE. 1984. Bird banding
manual. Washington, D.C.
WAIDE, g. g. 1980. Resource partitioning between
migrant and resident birds: the use of irregular
resources. Pp. 331-352 in Migrant birds in the
Neotropics (A. Keast and E. S. Morton, Eds.).
Washington, D.C., Smithsonian Inst. Press.