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Behavioral Ecology Vol. 11 No. 3: 299-308
© 2000 International Society for Behavioral Ecology
The role of behavioral dominance in structuring patterns of habitat occupancy in a migrant bird during the nonbreeding season
Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA
Address correspondence to P. P. Marra at the Smithsonian Environmental Research Center, PO Box 28, Edgewater, MD 21037, USA. E-mail: marra{at}serc.si.edu .
Received 11 February 1999; revised 9 September 1999; accepted 22 September 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Several species of territorial migratory birds exhibit sexual habitat segregation on their wintering grounds, with some habitats containing mostly males and others mostly females. The objective of this study was to determine if in the American redstart (Setophaga ruticilla) in Jamaica habitat segregation is due to social mechanisms or due to sex-specific habitat specialization. I used habitat-specific patterns of arrival by young males and females, observations of territorial displacements, removal experiments, and simulations of territorial intrusions to differentiate between these two mechanisms. Redstarts were studied in two habitat types, a male-biased mangrove forest and a female-biased scrub habitat. In autumn, male and female hatch-year redstarts initially settled in equal numbers in each habitat, and segregation of the sexes occurred gradually and mostly later in the arrival period. This shift corresponded with an increase in density of older birds and an increase in territorial displacements. Removal experiments showed that vacancies in male-biased habitat were filled more rapidly and with greater frequency than those in female-biased habitat and that vacated male territories in mangrove were replaced more often by females than by males. Simulations of territorial intrusions and analyses of body size indicated that levels of aggression and body size of both males and females were greater in mangrove habitat, suggesting that these factors may be important in determining the outcomes of dominance interactions. I conclude that patterns of sexual habitat segregation in redstarts are structured by the dominance behavior of older and more dominant individuals, and these are mostly males.
Key words: American redstarts, behavioral dominance, habitat specialization, migratory birds, nonbreeding season, removal and playback experiments, Setophaga ruticilla, sexual habitat segregation.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In migratory birds, many species exhibit a habitat distribution pattern in which males and females are spatially segregated during the stationary portion of the nonbreeding period. This is characterized by males and females occurring in different proportions, either at different latitudes (e.g., Ketterson and Nolan, 1976
,
1983;
van Eerden and Munserman,
1995) or at the same latitude but in different habitat types. This
latter pattern is known as sexual habitat segregation and appears to be a
widespread phenomenon during the non-breeding period for migratory passerines
in both the New (e.g., Lynch,
1992; Lynch et al.,
1985; Ornat and Greenberg,
1990; Sliwa, 1991;
Wunderle, 1992;
Wunderle and Waide, 1993) and
Old World (Nisbet and Medway,
1972).
Two mechanisms have been proposed to underlie sexual habitat segregation.
First, the habitat specialization hypothesis proposes that males and females
are each habitat specialists, with males choosing to establish territories in
one type of habitat (hereafter "male-biased habitat") and females
in another (hereafter "female-biased habitat")
(Lynch et al., 1985;
Morton, 1990;
Morton et al., 1987). It
assumes, based on the abundance of each sex, that habitat suitability is
highest for females in female-biased habitat and for males in male-biased
habitat. Second, interference behavior of dominant individuals (e.g., males)
may lead to the exclusion of subordinate individuals (e.g., females) from some
habitats (Gauthreaux, 1978;
Lynch et al., 1985). Such
social dominance can be considered a result of intraspecific competition for
limiting resources and would result in the most suitable habitats becoming
male-biased and less suitable habitats becoming female-biased. Below, I
describe several tests designed to separate habitat specialization from
behavioral dominance mechanisms responsible for structuring patterns of sexual
habitat segregation in a long-distance migrant passerine, the American
redstart (Setophaga ruticilla).
The first test examines the settlement patterns of migrant birds on their wintering quarters. The habitat specialization hypothesis predicts that naive male and female hatch-year (HY) birds, arriving in winter habitats for the first time, should settle preferentially into the appropriate male- or female-biased habitat when they first arrive in autumn. In contrast, the behavioral dominance hypothesis predicts territory settlement patterns of HY redstarts over the first few weeks to be either random with respect to habitat and sex, especially if habitats are of equal suitability in autumn, or skewed toward the male-biased habitat if this habitat is of higher suitability relative to female-biased habitat. Under either scenario, sub-ordinate HY males and females will begin to settle with greater frequency in female-biased habitat, most likely due to the increase of aggressive encounters and resulting territory displacements by older returning redstarts (after-hatch year red-starts; AHY). Thus, the first objective of this study was to quantify the settlement patterns and the frequency of territorial displacements of HY and AHY males and females into known male and female-biased habitats in autumn.
In a second test, I removed individuals from female- and male-biased habitats and examined the frequency and rate of replacement as well as the sex and age of the replacement birds. If sexual habitat segregation is driven by habitat specialization, the frequency and rate of replacement should be equal between the two habitats, whereas behavioral dominance predicts faster replacement in male-biased compared to female-biased habitats because male-biased habitat is assumed to be of higher suitability. The habitat specialization hypothesis predicts that when males or females are removed from their territories in either habitat type, they should be replaced by the same gender, assuming the presence of floaters or of neighboring individuals interested in moving. Alternatively, the behavioral dominance hypothesis predicts the removal of individuals from male-biased habitat may result in a shift in the sex or possibly age (older to younger) of the new territory owner, at least in the absence of older males and presence of excluded subordinates.
On their wintering quarters, both sexes of several species of Neotropical
migrant birds have been shown to defend territories vigorously and exhibit
stereotypical aggressive behaviors (e.g.,
Greenberg, 1986;
Greenberg and Ortiz Salgado,
1994; Greenberg et al.,
1994,
1996;
Holmes et al., 1989;
Rappole and Warner, 1980).
Thus, a third test designed to separate habitat specialization from behavioral
dominance hypotheses involved quantifying this aggressive behavior of
territorial birds. The habitat specialization hypothesis predicts that each
sex will exhibit higher levels of aggression in the habitat type with which it
is most commonly associated. The behavioral dominance hypothesis predicts that
males and females obtaining territories in male-biased habitat do so either
because they are more aggressive, have larger body size (see below), or
possibly both. Increased aggressiveness by individuals in male-biased habitat
would suggest an asymmetry in habitat suitability, a finding inconsistent with
the habitat specialization hypothesis. To test these predictions I performed
playback experiments in the territories of individuals in each habitat type in
autumn and quantified the aggressiveness of their response.
Large body size has been shown to allow some individuals greater access to
limited resources (Fretwell,
1969; Smith and Metcalfe,
1997). Thus, an additional prediction consistent with the
behavioral dominance hypothesis is that individuals with territories in
male-biased habitat, regardless of sex, should be larger than individuals in
female-biased habitat. Thus, I also measured wing chords and tarsus lengths of
individuals occupying both habitat types to determine if body size was a
possible mechanism allowing some individuals to win territorial disputes and
exclude smaller, subordinate birds from male-biased habitats.
The study species was the American redstart (Setophaga ruticilla),
a Nearctic-Neotropical migrant well suited for testing the hypotheses and
predictions outlined above. Redstarts breed in North America and spend the
nonbreeding period in the Caribbean, Central America, and northern South
America (Sherry and Holmes,
1997). They exhibit sexual habitat segregation throughout most of
their winter range (Marra and Holberton,
1998; Sherry and Holmes,
1997), and individuals can be sexed and aged reliably
(Holmes et al., 1989;
Marra et al., 1993;
Pyle et al., 1987;
Sherry and Holmes, 1997).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Research was conducted at the Font Hill Nature Preserve, 13 km west of Black River, St. Elizabeth Parish, in southwestern Jamaica. Redstarts were studied in two habitat types with approximately equal densities but different sex ratios. In mangrove forest, redstart density over 2 years (1994 and 1995) averaged 20.1 ± 0.9 SE/5 ha, of which 65% were male and 35% were female. Second-growth scrub habitat had 20.6 ± 1.4 SE redstarts/5 ha, of which approximately 30% were male and 70% were female.
The mangrove habitat was predominately black mangrove (Avicennia germinans) with small amounts of white (Laguncularia racemosa) and red (Rhizophora mangle) mangrove along the periphery. The mangrove stands had continuous canopies averaging 12 m in height, had almost no ground or shrub level vegetation, and were flooded with up to 1 m of water. Second-growth scrub habitat was predominated by logwood (Haematoxylon campechianum), a 2-8 m tall, thorny tree, with larger, scattered trees (e.g., Bursera simarubra, Terminalia latifolia, and Crescentia alata) and many vines and tangles.
I studied redstarts on three 5-ha study sites in mangrove and two 5-ha sites in second-growth scrub adjacent to these mangrove sites. All sites were gridded at 25-m intervals, which allowed me to locate and map redstart territories. The third mangrove site was necessary to obtain larger sample sizes of females in that habitat type. Removal experiments in mangrove and second-growth scrub were conducted on smaller study plots in nearby areas at Font Hill (see below).
American redstarts were captured using a song playback technique
(Holmes et al., 1989),
measured (tarsus, wing chord, body mass), aged, sexed, and given a unique set
of color-bands. I aged all redstarts as either HY or AHY using skull
ossification and then sexed them using several plumage characters. Criteria
for aging and sexing have been described in detail elsewhere
(Marra et al., 1993;
Pyle et al., 1987;
Sherry and Holmes, 1997), and
were confirmed by observation and recaptures of color-banded individuals of
known sex over several years (Marra PP et al., unpublished data).
Arrival and settlement patterns
In 1994 and 1995, my assistants and I censused redstarts for 8 weeks from
early September to late October. Censuses were conducted in each site twice
per week (2-3 days apart), and alternated between observers. Censuses began at
0600 h on alternating sides of the plot, lasted 2-4 h, and consisted of an
observer walking at a slow pace on each of five 250-m transects that were 50 m
apart. Redstarts were detected by either sight or sound, located, identified
as banded or unbanded, and classified as female, HY male, or AHY male, or, if
sex could not be ascertained with confidence, as a female-plumaged individual.
If an unmarked redstart was seen in that same area again on the next census,
it was captured within the next few days and color-banded, aged, sexed, and
measured. We recorded all territorial displacements, which were defined as a
territorial color-banded bird seen on two consecutive census visits that
subsequently shifted at least one full territory away (ca. >50 m) or
disappeared and was replaced by a neighboring or new redstart.
Removal experiments
Individual American redstarts were removed from one male-biased (mangrove)
and one female-biased (second-growth scrub) site in 1994 and 1996. Because
extensive removal experiments had already been conducted in mangrove at this
same site (Marra et al.,
1993), the major effort of these experiments was to conduct
removals in female-biased habitat. I also made smaller scale removals,
however, in mangrove to control for annual differences in population density
and floater abundance.
Before removal, I mapped territories of all individuals on one 3-ha plot in
female-biased habitat and one 1.5-ha plot in male-biased habitat. Overall, six
observers spent a total of 25 preremoval h mapping the territories of 17
redstarts on the female-biased sites and a total of 12 h mapping the
territories of 16 redstarts on male-biased sites (less time was necessary for
territory mapping in the mangrove habitat because its open vegetation made
following birds easier than in the thicker second-growth scrub). Mapping of
redstarts continued until no further changes in the size and shape of the
territories could be detected (Marra et
al., 1993). After mapping was complete, 12 redstarts in scrub and
6 in mangrove were captured and permanently removed from their territories on
15 October 1994 and 9 November 1996. We visited each site and checked for the
presence of redstarts 1 day, 1 week, and then 2 weeks after removal. Song
playbacks were used to facilitate finding birds and to confirm densities. In
each year, 8 h after removal were spent mapping redstarts in the female-biased
removal plot and 5 h in the male-biased plot.
Simulations of territorial intrusions
I quantified behavioral responses of redstarts using a vocalization
playback in both habitat types in the autumn of 1996. Each playback experiment
consisted of placing a taxidermic mount of an AHY male redstart approximately
0.5 m above the ground in the center of a focal bird's territory. An amplified
speaker was concealed at the base of the model with a speaker cable leading to
a remote tape recorder at a hidden location approximately 15 m away. One
person operated the recorder, while two other observers were stationed
approximately 15 m on the opposite side of the decoy and approximately 20 m
apart. Each experiment consisted of a 10-min broadcast of American redstart
vocalizations at a constant volume. Three different tapes were used, each
containing a mix of AHY male song and AHY male chips in equal proportions and
from different individuals (Kroodsma,
1986). Although chips are the most common vocalization made by
redstarts during the winter, the use of the song—chip combination in
equal proportions produced a stronger and more consistent response from the
redstarts (Holmes et al.,
1989; Marra PP, unpublished data).
Each of the two observers independently scored three parameters on the focal bird as soon as it appeared in the vicinity (about 15-20 m) of the decoy: (1) the total number of dives (defined as a flight over the model accompanied by a sharp drop in flight directed toward the decoy), (2) the total number of separate physical attacks on the decoy (defined as a hit on the decoy), and (3) an overall response score (1 = no response; 2 = mild response with occasional chips and remains in vicinity but always more than 10 m away; 3 = strong response, obviously agitated with close approaches within 2 m of the model; 4 = very strong response, highly agitated and attacks model). Intermediate scores (1.5, 2.5, and 3.5) were also used.
None of the focal redstarts used in these experiments had been previously exposed to a playback that season, although some had responded to a playback in previous years when they were first banded. Birds banded within a season exhibit a reduced response to song playback in that same season, but when exposed to playbacks a year later their responses were at preexposure strength (Marra PP, unpublished data). Experiments on the same day were always conducted on individuals more than 200 m apart to avoid exposing other potential experimental birds to the sound of the playback or sight of the decoy.
Data analysis
I used chi-square analysis to test if (1) the proportion of territorial
displacements differed between habitats, (2) males did more displacing than
females in mangrove, (3) AHYs did more displacing than HYs in mangrove, (4)
the sex ratio of birds removed within each habitat differed from the
replacements, and (5) the proportion of each sex present between habitats
changed after removal. The effects of habitat (mangrove versus scrub) and sex
(male versus female) on the number of dives, attacks, and response score
exhibited by redstarts during playbacks experiments were examined by standard
two-way analysis of variance. Because sample sizes were too small for males in
female-biased habitat to include age (HY versus AHY) in the model, a separate
analysis was conducted on females to test for the effects of habitat and age.
All playback data were natural-log transformed to meet assumptions of equal
variance and normality.
To examine body size relationships, I first calculated the scores of a
principal component analysis based on unflattened wing chord and tarsus
length. A natural-log transformation was performed on the scores from the
first principal component to meet assumptions of normality and equal
variances, and these transformed data were used as an estimate of skeletal
body size. I analyzed these data using a three-way ANOVA including sex (male
verus female), age (AHY versus HY), and habitat (mangrove versus scrub) and
then analyzed the data separately for males and females. All statistical
analyses were made using JMP (SAS
Institute, 1997).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Behavior during the arrival period
I predicted that if sexual habitat segregation was caused by sex-specific habitat specialization, naive HY male and female redstarts, upon arrival in their wintering grounds, would settle differentially into male- (mangrove) and female-biased (scrub) habitats, respectively. In general, I found that male and female HY redstarts initially arrived and settled approximately equally in both habitat types. In 1994, the numbers of HY males were the same in both habitat types through the first 4 weeks and then increased more rapidly in mangrove habitat (Figure 1). The numbers of HY males leveled off between 3.5 and 4 individuals/5 ha in second-growth scrub and approximately 6.5/5 ha in mangrove habitat at the end of the censusing period. The rate of settlement did not differ between habitats in 1995, with mean numbers by week 8 of 3.5 individuals/5 ha in scrub and 3.7/5 ha in mangrove. In 1995, the numbers of HY male redstarts were lower at the end of October than those in the previous year (mean for week 8 of 5.4 ± 1.4 in 1994 versus 3.1 ± 1.5 individuals/5 ha in 1995; t = 2.2, df = 6, p =.07; Figure 1).
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In 1994, HY females settled into both habitats at similar rates through week 6 (Figure 1). During week 7 and 8, however, numbers of HY females increased in scrub, while numbers remained stable in mangrove. Mean number of HY females in mangrove remained constant over the final 2 weeks of October at 4.5 HY females/5 ha, while numbers increased in scrub to 6.0 HY females/5 ha by the end of October. In 1995, HY females exhibited settlement patterns similar to those in 1994, increasing to 5.0 individuals/5 ha in scrub and only 2.0 individuals/5 ha in mangrove.
Because American redstarts exhibit strong site fidelity to their winter
territories of the previous year, testing predictions regarding habitat choice
cannot be done with older (AHY) birds
(Holmes et al., 1989;
Holmes and Sherry, 1992;
Marra and Holmes, in press).
Nevertheless, I quantified AHY arrival patterns to assess changes in numbers
of all redstarts. The patterns of arrival and settlement of AHY redstarts in
1994 were similar to those of HY individuals
(Figure 2). The settlement
patterns of AHY males by habitat diverged, with mean numbers increasing to 8.0
individuals/5 ha in mangrove and never exceeding 2.0 individuals/5 ha in
scrub. By week 8 the mean number of AHY males was 14.7 individuals/5 ha in
mangrove and had yet to asymptote, compared to 2.5 ± 0.5 individuals/5
ha in scrub habitat. For AHY females, there were no differences among habitats
in patterns of settlement in either year. In 1994, AHY females never exceeded
4 individuals/5 ha by the end of October (week 8) in either habitat. In 1995,
AHY females exhibited similar rates of increase to AHY males, however, in
contrast to males, there were no habitat-specific patterns in settlement,
although by week 8 females had not shown signs of asymptoting.
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Significantly more territorial displacements occurred on the mangrove sites
(40/3 plots) compared to scrub sites (4/2 plots) in both 1994 and 1995
(
2 = 8.0, df = 1, p =.007), and these were mainly
males displacing females (2 = 14.4, df = 1, p =.000)
or AHYs (predominantly males) displacing HYs (males and females;
2 = 19.6, df = 1, p =.000;
Table 1). Over both years, 87%
of territorial displacements took place in mangrove, compared to only 13% in
scrub, and the majority (80%) of these displacements were by males or by AHY
individuals (85%). Displacements were by both returning color-banded AHY
redstarts (65%) and by new individuals (35%) establishing site dominance for
the first time.
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Removal experiments
Territory replacement was more rapid and complete in male-biased than in
female-biased habitats. One day after the removals in mangrove in 1994 and
1996, 4 of 6 (67%) of the vacated territories had new redstarts present,
compared to only 1 of 12 (8%) of the vacated territories in scrub
(Figure 3). Furthermore, on the
first day after the removals, new redstarts in mangrove were engaging in
aggressive interactions with neighbors, whereas the one redstart in scrub was
a single foraging bird seen briefly. One week after removals, 100% of the
vacated territories in mangrove had been filled, compared to only 58% in
scrub. Two weeks after removal the percentage of replaced redstart territories
leveled off to 50% in scrub, while the sites in mangrove remained
occupied.
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In scrub, the sex ratio went from a 3:1 ratio of females to males removed
to 5:1 females to males after replacement, but this change was not significant
(2 = 2.66, df = 1, p =.1;
Table 2). In these same years,
I removed a total of four males and two females from mangrove. Combining these
data with those of removal experiments conducted in mangrove in 1989
(Marra et al., 1993) shows
that 13 vacated territories in mangrove were filled within 2 weeks by 7 males
and 7 females, representing a 108% replacement rate. The sex ratio in this
habitat shifted from a 1:3.3 female to male ratio before removal to a 1:1
ratio in the replacement birds (2 = 3.6, df = 1, p
=.06). In comparing between habitats, the proportion of males present declined
equally in mangrove (77% to 50%) and scrub (25% to 17%) as a result of the
removal (2 = 0.14, df = 1, p =.71). In contrast, the
proportion of females increased in both habitats after removal (23% to 50% in
mangrove; 75% to 86% in scrub), but significantly more in mangrove compared to
scrub (2 = 58.12, df = 1, p =.000).
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In mangrove, none of the replacement birds were observed before removal, even though the experiments were done after the main arrival period. It did not appear that any of the replacement in mangrove was due to shifting neighbors. Color-banded neighbors remained on territory and exhibited intense aggressive interactions with new replacement redstarts. This contrasts with scrub habitat, where approximately 50% of the replacement birds observed were color-banded individuals shifting from neighboring territories.
Simulations of territorial intrusions
American redstarts in mangrove habitat responded more aggressively to tape
playbacks than conspecifics in female-biased, scrub habitat
(Table 3). Both male and female
redstarts in mangrove dived significantly more often toward a stuffed AHY male
decoy during the 10-min tape playback than did redstarts in scrub (habitat:
F = 7.7, p =.009; sex: F = 0.83, p = 0.37;
habitat x sex: F = 0.02, p =.89). Only males attacked
the decoy, and this occurred in both habitats (habitat: F = 1.0,
p =.32; sex: F = 4.4, p =.04; habitat x sex:
F = 1.0, p =.32). Response scores were significantly higher
in mangrove (habitat: F = 8.3, p =.007), although males in
scrub also responded aggressively, resulting in a marginally significant sex
effect and habitat x sex interaction (sex: F = 3.9, p
=.06, habitat x sex F = 3.3, p =.08;
Table 3). Because of small
sample sizes of males in scrub, age effects could not be assessed in the full
model. A separate analysis conducted for just females showed that the response
scores in females were higher in mangrove habitat (habitat: F =
19.56, p =.001), regardless of age (F = 1.73, p
=.21; habitat x age: F = 4.1, p =.07).
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Body size
Male American redstarts were significantly larger than females. Within a
sex, no differences were found in male body size across habitats, but females
in mangrove were larger than females in scrub, regardless of age
(Figure 4). In a three-way
ANOVA including sex, age, and habitat, males were significantly larger than
females, and there were no significant interactions (age: F = 0.86,
p =.35; sex: F = 66.12, p =.0001; habitat:
F = 2.39, p =.12; age x habitat F = 0.33,
p =.56; sex x habitat: F = 2.55, p =.11; age
x sex x habitat: F = 0.12, p =.73). When sexes
were considered separately, I found that females in mangrove were larger than
those in scrub habitats, regardless of age (age: F = 0.02, p
=.88; habitat: F = 5.47, p =.02; age x habitat
F = 0.48, p =.49), and there were no differences in male
body size either between age or habitat classes (age: F = 2.03,
p =.16; habitat: F = 0.001, p =.97; age x
habitat F = 0.02, p =.88).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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My results support the hypothesis that dominance behavior of older males excludes females and younger males from preferred mangrove habitat and is the primary mechanism responsible for creating patterns of sexual habitat segregation in American redstarts during the nonbreeding period. Habitat specialization by males and females did not appear to play a role in driving patterns of habitat occupancy in this species.
Arrival and settlement patterns of both hatch-year males and females in
September and early October was random with respect to habitat type, a finding
inconsistent with the habitat specialization hypothesis. Furthermore, the fact
that HY redstarts did not settle disproportionately in mangroves suggests
either that habitats were of equal suitability at the time of settlement or
that HY birds could not detect differences in suitability. In early to
mid-October, however, as older, more dominant redstarts arrived, HY males
continued to settle with greater frequency in mangrove, but HY females began
to increase in abundance in scrub. The latter of these shifts of females was
due to a disproportionate increase in displacements among redstarts in
mangrove habitat. Overall, 87% of the displacements observed were in mangrove
forest, and these were predominately males displacing females and older birds
displacing younger ones, common patterns with dominance hierarchies in birds
(e.g., Balph, 1977;
Wilson, 1975). Furthermore,
both returning color-banded redstarts and individuals arriving for the first
time were responsible for displacements, suggesting that both prior site
dominance and intrinsic dominance determine the outcomes of behavioral
interactions.
Dominance hierarchies form because some critical resource is limiting, and
individuals of varying abilities compete for access to that resource (see
Gauthreaux, 1978). In the case
of American redstarts in Jamaica, food is probably the limiting resource
(Lovette and Holmes, 1995;
Parrish and Sherry, 1994), and
individuals compete over access to territories that will provide sufficient
and consistent food levels for the duration of the nonbreeding period.
Therefore, if behavioral dominance structures patterns of habitat occupancy,
the most intense competition for territories should take place in habitats
that are the most suitable. Removal experiments are an effective and
informative way to assess the importance of dominance behavior and resource
competition in driving spacing patterns. Differential replacement by males and
females in male- and female-vacated territories provides strong evidence for
differences in habitat suitability and for the role of behavioral dominance.
Morton et al. (1987) removed
four male hooded warblers (Wilsonia citrina) and found that two were
replaced by new males and none by females, leading them to suggest that sexual
habitat segregation in winter might be due to innate preferences (i.e, habitat
specialization) by males and females. This idea was further supported by
laboratory studies with hand-reared birds
(Morton, 1990) and additional
field data (Morton et al.,
1993). More recent removal experiments with this species, however,
in female-type habitat found that the sex of the replacement bird could not be
predicted by the sex of the removed territory owner
(Stutchbury, 1994).
When I removed redstarts from male- and female-biased habitat types, replacement occurred in both habitats, mostly by females and younger males, suggesting that territorial exclusion was keeping individuals out of both sites. However, significantly more territories were reoccupied in mangrove compared to scrub, and those territories were reoccupied more rapidly, suggesting that competition for sites there was more intense. In addition, vacated male territories in mangrove were occupied disproportionately by females rather than by males, indicating that mostly females had been excluded from male-biased habitat and that these territories were not sex specific. The more rapid and complete settlement by excluded individuals in one habitat relative to another supports the behavioral dominance hypothesis.
Simulations of territorial intruders with a stuffed decoy accompanied by a
vocalization playback demonstrated that male and female redstarts in mangrove
responded more aggressively than females but only slightly more than males in
female-biased scrub habitats. Higher levels of aggression by redstarts in
mangrove may be due to several factors. First, aggressiveness of individuals
in mangrove may represent a quality intrinsic to those redstarts, possibly
regulated by circulating levels of plasma testosterone (e.g.,
Ketterson and Nolan, 1992;
Wingfield et al., 1987).
Second, differences in measured levels of aggression may represent a
frequency-dependent response. In other words, redstarts in mangrove may have
exhibited higher levels of aggression to a vocalization playback because they
have been involved in interactions more frequently. A third possibility is
that mangrove habitat is of higher suitability, and individuals exhibit higher
levels of resource defense because they have more to lose (e.g.,
Brown, 1964;
Elwood et al., 1998). Finally,
higher levels of aggression may be due to prior residence advantage of older,
returning birds (Beletsky and Orians,
1989; Holberton et al.,
1990; Krebs,
1982). Although my experiments do not allow for differentiation of
these four causes of higher aggression, they do demonstrate that redstarts in
mangrove exhibited higher levels of aggression than individuals in scrub, a
finding consistent with the behavioral dominance hypothesis but not with the
habitat specialization model. Therefore, differences in aggression, regardless
of their ultimate causation, may in part be responsible for determining the
outcomes of behavioral interactions and ultimately habitat occupancy
patterns.
The ability of males to dominate and exclude females and some younger males is also associated with differences in body size. Overall, males were significantly larger than females, and 40% of all displacements were by males displacing females rather than males being displaced by females (10%). Despite this fact, some females were able to persist and establish territories in mangrove habitats. These females were not only more aggressive as indicated by results of playback experiments (see above), but they were also significantly larger than those in scrub habitat. This suggests that body size, at least for females, could be partially responsible for allowing them to persist in mangrove habitat. To test for the effect of female body size in winning antagonistic encounters, neutral-ground experiments between females of small and large body size from both habitats will be required.
In summary, results of removal experiments, combined with data on autumn
settlement patterns, territory displacements, and aggressive behavior, support
the hypothesis that behavioral dominance is responsible for structuring winter
habitat segregation in American redstarts. Patterns of sexual habitat
segregation, at least in Jamaica, appear to be formed by adult males settling
into high suitability habitats and excluding subordinates, which are
predominately females and some HY males. Factors other than sex and age may
affect the ability of some individuals to acquire territories in male-biased
habitat. In winter, both sexes of redstarts exhibit overt agonistic behaviors
involving vocalizations, aerial displays, posturing, and physical contact
(Ficken, 1962;
Holmes et al., 1989;
Sherry and Holmes, 1997), and
this behavior eventually results in displacement or at least territory
boundary adjustments (Marra,
1998). Differences among individuals in these aggressive behaviors
may be partially responsible for the outcomes of dominance interactions and
may explain why some females can acquire territories in male-biased
habitat.
A predicted outcome of behavioral dominance is that birds forced into less
suitable habitat will have lower survival or decline in physical condition.
Marra and Holberton (1998)
measured circulating levels of corticosterone, a hormone associated with
behavioral and physiological changes in energy demand
(Harvey et al., 1984;
Wingfield, 1994) in redstarts
occupying these Jamaican mangrove and scrub habitats in autumn just after
territory establishment and then again in these same individuals in spring.
Their results demonstrated that in autumn, regardless of sex and age,
redstarts had similar baseline corticosterone concentrations across both
habitat types. However, 6 months later, in March at the end of the tropical
dry season, redstarts in the female-biased, scrub habitat had significantly
higher basal corticosterone concentrations, whereas redstarts with territories
in mangrove had corticosterone concentrations similar to those in autumn. High
levels of corticosterone suggest that these birds were in relatively poor
energetic condition. Corticosterone is thought to increase foraging effort in
an attempt to increase or maintain energy reserves
(Astheimer et al., 1992;
Gray et al., 1990;
Wingfield, 1988;
Wingfield and Silverin, 1986).
Redstarts with territories in scrub also lost significantly more body mass
compared to birds in mangrove, had lower annual survival rates
(Marra and Holmes, in press),
and departed later on spring migration
(Marra et al., 1998),
regardless of sex or age. Taken together, these results demonstrate that
population consequences can arise from sexual habitat segregation.
Gauthreaux (1978,
1982) proposed that behavioral
dominance and its consequences, such as the ones I have described here, are
important factors regulating patterns of dispersal and migration within
species. He argued that differential migration in the fall, as birds settle
onto their wintering quarters, results from dominance interactions and can
explain patterns such as latitudinal (Ketterson and Nolan,
1976,
1983,
1985;
Myers, 1981) and altitudinal
(Diamond and Smith, 1973)
segregation of age and sex classes. He reasoned that subordinate individuals
are forced to occupy more southern areas farther from breeding areas and as a
result arrive back to breeding areas later than dominant individuals wintering
closer to the breeding grounds. Empirical evidence, however, has thus far
failed to provide clear support for this hypothesis (Ketterson and Nolan,
1983,
1985;
Rogers et al., 1989; but see
Lundberg et al., 1981). In the
case of American redstarts, intraspecific competition and resulting
segregation among habitats occurs within a site at the same latitude and
elevation and can affect the timing of spring migration
(Marra et al., 1998). In this
way, the data presented here for redstarts, a species exhibiting habitat
segregation, support Gauthreaux's theory
(1978,
1982) that behavioral
dominance and resulting despotic distribution on the nonbreeding grounds may
play a part in influencing dispersal and migration.
Behavioral dominance has been shown to be the underlying mechanism driving
habitat occupancy patterns during the breeding season in many bird species
(see Gauthreaux, 1978).
Furthermore, its role in structuring winter social systems in birds forming
flocks has been well documented (e.g.,
Enstrom, 1992;
Holberton et al., 1990;
Ketterson, 1979; Lahti et al.,
1997,
1998;
Nakamura et al., 1996;
Piper and Wiley, 1989;
Rohwer, 1977;
Slotow and Paxinos, 1997;
Smith and Metcalfe, 1997), and
several studies have also shown that, within flocks, behavioral dominance
results in lower overwinter survival for subordinates
(Desrochers et al., 1988;
Fretwell, 1969;
Kikkawa, 1980;
Smith et al., 1980). Little
information, however, exists regarding the role that intraspecific dominance
behavior plays in regulating habitat use during the nonbreeding season for
territorial long-distance migrant passerines
(Greenberg, 1986). My findings
appear to be the first to identify and evaluate the potential effects of
dominance behavior among sex and age classes in any territorial migrant
passerine in winter. More research on additional species is needed to better
understand the pervasiveness of behavioral dominance and its associated
influences on individual condition and ultimately population dynamics. Habitat
segregation is found throughout most of the winter range of American
redstarts, and behavioral dominance may be the underlying mechanism
structuring this habitat segregation throughout that distribution.
Identification of the fundamental mechanisms involved in habitat choice, such
as was done here, can lead to a better understanding of the factors that drive
the population dynamics of these birds
(Bernstein et al., 1991;
Sherry and Holmes, 1996).
|
ACKNOWLEDGEMENTS |
|---|
This research was made possible by a Doctoral Dissertation Improvement Grant from the National Science Foundation, an Albert Cass Fellowship, a Grant-in-Aid of Research from The Society of Sigma Xi, and a Frank M. Chapman Memorial Fund Grant from the American Museum of Natural History. Additional financial support was provided by the National Science Foundation through grants awarded to Richard T. Holmes (Dartmouth College) and Thomas W. Sherry (Tulane University). This work was only possible thanks to the excellent assistance of several people in the field, especially R. Dobbs, J. Goetz, J. Knight, J. Prather, R. Holmes, A. Strong, J. Barg, and M. Johnson. I would especially like to thank Deb and Richard Holmes, and Pam (Williams) Becsy for their help with logistics in Jamaica. This paper was greatly improved from comments by R. T. Holmes, M. Ayres, D. Bolger, J. Faaborg, R. Ydenberg, P. D. Hunt, and two anonymous reviewers. I am grateful to the Petroleum Corporation of Jamaica for allowing us to conduct this research at the Font Hill Nature Preserve and Yvette Strong and the Natural Resources Conservation Authority for their support of our research in Jamaica. Finally, Robert Sutton, Ann Haynes-Sutton, Pam (Williams) Becsy, Steve and Sue Callaghan, and Peter Williams have provided support and hospitality during my frequent trips to Jamaica. All bird removals were conducted under permits issued by the U.S. Fish and Wildlife Service and the Natural Resources Conservation Authority of Jamaica. Removal protocols were approved by the Institutional Animal Care and Use Committee of Dartmouth College.
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