Behavioral Ecology Vol. 12 No. 6: 706-715
© 2001 International Society for Behavioral Ecology
Male Seychelles warblers use territory budding to maximize lifetime fitness in a saturated environment
a Zoological Laboratory, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands b Department of Zoology, University of Melbourne, Parksville, Victoria 3052, Australia c Department of Marine Ecology, Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, The Netherlands
Address correspondence to J. Komdeur, Zoological Laboratory, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands. E-mail: j.kmodeur{at}biol.rug.nl .
Received 27 October 2000; revised 18 January 2001; accepted 13 February 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In cooperatively breeding species, helping at the nest and budding off part of the natal territory have been advanced as strategies to increase fitness in an environment that is saturated with territories. The importance of helping or territory budding as a determinant of lifetime reproductive success (LRS) has been debated because the potential benefits of both strategies could not be separated. Here we test the causes and the immediate and future fitness consequences of single dispersal decisions taken by male Seychelles warblers (Acrocephalus sechellensis). Males breeding in high-quality territories (high food abundance) have significantly higher LRS than similar-aged males budding off part of the parental territory. Initially, budders have a low reproductive success (because of limited food resources or absence of a breeding partner). However, they have a long life span and inherit high-quality territories through site dominance, by which they gain higher LRS than breeders on low-quality territories, helpers, or floaters. Experimental creation of male breeding territory vacancies showed that most young males became budders because of intense competition for high-quality territories. The translocation of warblers to the previously unoccupied Aride Island shows that males behave according to the expected fitness benefits of each dispersal strategy. In the absence of competition for territories on Aride, all young males bred in high-quality territories. However, after saturation of high-quality habitat with territories, most males became budders rather than breeders on low-quality habitat, helpers, or floaters.
Key words: Acrocephalus sechellensis, budding, dispersal, helping, lifetime reproductive success, Seychelles warbler, territory inheritance.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In many taxa there is variability among individuals in age at first breeding, and frequently the delay in reproduction extends past the time of sexual maturity (Bourke, 1997
;
Brown, 1987;
Emlen, 1995;
Lawton and Lawton, 1986;
Riedman, 1982;
Stacey and Koenig, 1990;
Taborsky, 1994;
Zack and Stutchbury, 1992).
The main reason for delayed reproduction is the forfeiture of fitness costs
associated with missed or suppressed reproductive opportunities or with
gaining reproductive status in inferior territories
(Cockburn, 1998; Emlen,
1994,
1997;
Sibley and Calow, 1986;
Studd and Robertson, 1985;
Wittenberger, 1979). In only
3% of bird species with delayed reproduction do individuals remain with their
parents on their natal territory
(Cockburn, 1998;
Emlen, 1995). Remaining
offspring providing alloparental care to close relatives can indirectly
increase the number of their genes in future generations, whereas budders can
increase their direct fitness by "budding off" a portion of the
natal area as their own breeding territory. For more than twenty years
researchers have debated how remaining nonterritorial individuals improve
their fitness through helping others to breed (reviewed by
Cockburn, 1998; Emlen,
1991,
1994;
Heinsohn et al., 1990). This
research has been hampered by the fact that the potential fitness effects of
delayed dispersal, helping, and budding behavior could not be separated due to
individuals using mixed strategies. In addition, few studies have been long
enough to investigate the fitness benefits accrued to helpers and budders
(Arcese, 1989;
Chepko-Sade and Halpin, 1987;
Emlen, 1995), and experimental
studies under natural conditions have yet to be performed
(Balshine-Earn et al., 1998;
Emlen, 1991,
1995). In this study, we
tested the causes and the immediate and future fitness payoffs (e.g.,
territory inheritance) of remaining and dispersing tactics used by male
Seychelles warblers (Acrocephalus sechellensis).
Until 1988, the entire world population of Seychelles warblers was confined
to Cousin Island (29 ha), where it had reached carrying capacity since 1973.
Given this and the vulnerability of one small island in the Indian Ocean, an
additional breeding population was successfully established on Aride Island
(68 ha) in September 1988 (Komdeur,
1992). The warblers are insectivorous, usually have clutches of a
single egg (91.0%, n = 223), are single brooded, and have high annual
adult survival (81.1%, 334 bird-years). Once paired, the breeding pair remains
in the same territory until the death of one member of the pair. Territories
differ in quality, measured in terms of insect prey availability
(Komdeur, 1992). Young birds
are excluded from breeding due to habitat saturation and are more likely to
stay on high-quality natal territories because of higher foraging success
leading to increased survival (Komdeur,
1992). In addition, remaining female offspring increase their
lifetime fitness by helping, through which they gain indirect benefits and
parental experience (Komdeur,
1996a). Because helpers are mainly females (88%, n =
271), we assume that males must have developed other strategies to increase
their fitness.
In this study we had two principal aims. First, we wanted to describe reproductive tactics and the fitness consequences of young males born in a saturated, high-quality environment on Cousin Island. We analyzed the fates and fitness consequences of all tactics used: breeding, floating, and remaining as helper or nonhelper. We used 14 years of data from an individually marked population of which the behavioral parents (breeders) for all the produced young are known. For an entire cohort of males, the dispersal tactics, every nesting attempt, and its outcome are known throughout their lives. Second, we sought to establish whether the lifetime payoffs of the tactics predicted the observed dispersal behavior after experimental manipulation of the habitat. We tested this by creating male breeding vacancies that differed in reproductive prospects and then monitoring whether males using lower fitness-related tactics took over the available vacancies. In addition, the transfers of same-aged male warblers, with different previous background, to the unoccupied island of Aride allowed us to test the extent to which the fitness payoffs associated with the dispersal tactics on Cousin island also hold true in the new situation on Aride. We also expected that the dispersal tactics of males born on Aride gradually change over time when competition over territories becomes more intense.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and data collection
The entire population of Seychelles warblers on Cousin Island (115-123 groups, 310-400 birds) was under study from December 1982 till October 1996. Between 23 and 29 September 1988, 29 color-ringed adult warblers (16 males and 13 females; all between 3 and 5 years old) were transferred from Cousin Island to Aride Island by motorboat. On the high-quality habitat on Aride (see below), all breeding groups and their male offspring were studied from September 1988 to March 1997. Data were based on individually color-ringed males, ringed as nestlings, of which the dispersal, settlement patterns, and reproductive success were monitored monthly after hatching. All territories were checked regularly for 1 h (every 2 weeks, 1985-1991; every 4 weeks, 1982-1984, 1992-1997) for nests with a clutch or young and for presence of color-ringed birds to assess dispersal and survival of birds. As warblers rarely colonize other islands by themselves [out of 2156 ringed adults, only one bird (0.05%) is known to have flown from Cousin Island to Cousine Island], we assumed that missing birds had died if they were not found on other territories on the same island. We recorded the status of each male each month during the male's entire adult life using the following definitions. A helper was a male present on the natal territory engaged in helping at the nest. A nonhelper was a male present on the natal territory that did not help at the nest if a nest was present. A budder was a male that defended part of the parental territory against his parents and other warblers to acquire a territory (budded territory) for himself, in the absence of a vacancy. A floater was a male that was rarely present on the natal or a particular breeding territory; in contrast, helpers, nonhelpers on the natal territory, and budders could be engaged in exploratory forays searching for reproductive vacancies and could be absent from their natal territories for 1-5 days (Komdeur, 1991
), but they had
not severed the ties with their natal group. A breeder was a male that
obtained a vacant breeding territory with a female partner when he had not
been a helper, a nonhelper, a budder, or a floater after reaching maturity.
When a helping, nonhelping, budding, or floating male eventually acquired a
breeding territory with a female partner, these males were still referred to
as helpers, nonhelpers, budders, or floaters, respectively, because we wanted
to quantify the fitness of males initially performing each of these strategies
upon reaching the age of maturity.
Territory and habitat quality
Territory quality, which was not determined by the presence of nest sites
and nest predators (Komdeur,
1991,
1994a,b),
was measured in terms of insect prey available. Because the warblers are
insectivorous, taking 98% of their insect food from leaves
(Komdeur, 1991), the quality
of a territory depends on insect prey available and amount of foliage.
Territory quality was therefore expressed as mean number of prey invertebrates
available within a territory. The quality of territories was assessed every 3
months (Cousin: June 1982-June 1996; Aride: September 1988-June 1996). Before
translocation of birds, the area of low- and high-quality breeding habitat
present on Aride Island was estimated as follows. The total vegetated area of
Aride Island (62.7 ha) was subdivided into 36 plots of 132 x 132 m.
Within each plot a subplot of 50 x 50 m (the same size as an average
warbler territory on Cousin) was mapped, and the insect quality of this plot
was measured monthly from September 1987 to September 1998. The method used to
measure territory quality on Cousin and Aride and area quality on Aride is
presented elsewhere (Komdeur,
1992,
1994a). Because the quality of
breeding territories remained constant between years
(Komdeur, 1996b), territory
and area quality was expressed as the average quality over the whole research
period and divided into low quality (lqt: 0-3000 insects present) and high
quality (hqt: >3000 insects present). On Aride Island the total area of
high-quality and low-quality breeding habitat was calculated as the total area
of high- and low-quality plots, respectively (see Methods, Experimental
removals and translocations). We defined saturation of high-quality habitat as
the complete occupation of high-quality habitats with territories. We
calculated annual saturation index of high-quality habitat on Aride Island as
the quotient of the number of territories in this habitat in a given year and
the number of territories at first saturation of high-quality habitat (i.e.,
24 territories; see Results).
Fitness accounting
Lifetime reproductive success (LRS) is expressed as the total number of
yearling offspring produced over a male's lifetime. The analyses on Cousin
were restricted to males born on high-quality territories in the years
1982-1986 who reached at least 8 months of age (the minimum age of
reproduction), died before the end of the study period, and did not fill
experimentally created breeding vacancies (see below; n = 46). Ages
were based on known hatching date. On Cousin, we excluded the younger cohorts
because their LRS was not yet known, as some males are still alive. On Aride,
however, because some of the cohort males are also still alive at present, we
calculated the reproductive performance over their first 5 years of life to
gain adequate cohort sizes for analyses. Because cohorts were equally spread
over the years (Cousin: 8, 9, 9, 10, and 10 males; Aride: 15, 11, and 13
males), we did not examine for cohort variation. In all years between 1982 and
1996 on Cousin, the density of warblers (300-326 adults), and territories of
different qualities (hqt: 15-18; lqt: 100-105 territories) remained the same
(Komdeur, 1996b).
LRS was calculated as Vh + Vb,
where Vh = indirect helping benefits, and
Vb = direct breeding benefits. The indirect helping
benefit, which is the production of additional related yearlings as a result
of the activities of the male helper, beyond the expected reproduction of the
focal breeding without the male helper, is estimated as
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). To express
Vh in offspring equivalents accrued to the helper, we
multiplied Rm,o in the expression of
Vh by a factor of 2 because the coefficient of relatedness
to both classes of young (additional sibs "produced" by the helper
and offspring produced by the breeder) is 0.5.
The fitness obtained through direct reproduction of the male is given by:
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) given the conditional expression of the breeder—helper
distinction and the asymmetry in choosing the breeder or helper role (male
reproducers never become helpers, and male helpers never become reproductives
in their natal territories; Richardson et
al., 2001).
Experimental removals and translocations
The extent to which males discriminate among breeding opportunities
according to likely reproductive potential, and the extent to which
competition for territories that vary in reproductive potential contributes to
changes in male dispersal tactics were analyzed by a removal experiment and a
translocation experiment. Experimental removals accelerate the natural process
of breeder replacement and make the behavioral mechanisms of competition for
reproductive status more accessible to study. Within a season, territories
chosen for removals were separated from each other by at least four
territories to avoid mutual interactions.
First, we selected five high-quality and five low-quality breeding territories with highest and lowest reproductive potential, respectively (see Results), on Cousin Island. Each territory contained an unaided breeding pair and was situated next to one high-quality budded territory with second-highest reproductive potential (see Results) containing a male without a breeding partner. The male of the breeding pair was removed and translocated to Aride, and the budding male was observed on successive days after removal. This experiment was conducted 23-29 September 1988.
Second, the translocation of warblers to Aride Island allowed us to test
the influence of male status and habitat quality on dispersal tactics used by
these males. We transferred 16 male warblers that were of similar age (3-5
years) but had a different status (five breeders on high-quality territory,
five breeders on low-quality territories, three budders, two helpers, and one
floater) from Cousin Island to the unoccupied island of Aride, with high- and
low-quality breeding habitat available (5.6 ha and 62.4 ha, respectively). The
males were released in the low-quality habitat and subsequently followed
weekly to monitor the habitat in which they eventually established
territories. In addition, with increasing competition over territories, we
expected males born on Aride to discriminate among the various dispersal
tactics according to likely reproductive potential. On Aride Island, there was
no competition over high-quality vacancies until October 1990, but thereafter
the high-quality habitat had become completely saturated with territories
(Komdeur, 1992). On Aride we
distinguished two male cohorts born on high-quality territories: Cohort
Abefore consisted of 15 males born between October 1988 and January
1990 that had reached the reproductive age of 8 months before 1 October 1990
(the time of first saturation of the high-quality habitat); cohort
Aafter consisted of 24 males born between February 1990 and January
1992 that had reached 8 months of age after 1 October 1990. The internal
controls in this study are the dispersal and settlement pattern of two male
cohorts born on the saturated, high-quality habitat on Cousin Island. Cohort
Cbefore consisted of 14 males born between October 1988 and January
1990, and cohort Cafter consisted of 19 males born between February
1990 and January 1992.
Statistical analysis
Means are expressed with standard deviations, the presented probability
values are two-tailed, and the null hypothesis was rejected at p
<.05. We analyzed normally distributed continuous data of different
categories using ANOVA with post-hoc Tukey testing to establish group
identities; the relationship between similar data and a continuous variable
was analyzed by means of linear regression. The relationship between
proportions and a continuous variable was analyzed by means of logistic
regression; proportions in a contingency table were analyzed using a
log-linear modeling approach, where all frequencies were increased by 0.005 to
avoid high numbers of cells with zero scores. We tested repeated measures of
normally distributed, continuous data of different categories with
multivariate analysis of variance (MANOVA). Differences between repeated
measures within categories and differences between categories within repeated
measures were tested by constructing the appropriate A- and C-matrices for
hypothesis testing. We used SYSTAT 7.0
(1997) for analyses.
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RESULTS |
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Variance in LRS on Cousin
The total number of yearlings produced by 46 adult male warblers was 153 (Figure 1), of which 64 were males. The highest observed LRS of a male was 10 yearlings (n = 2), but the average LRS was 3.3 ± 3.0 yearling per male. Of the observed males, 26.1% died without having produced offspring of their own. Only a few males were successful: of the 153 yearlings, 82 (53.6%) were produced by only 11 (23.9%) adult males. The production of male yearlings was 39.1% [(64-46)/46 x 100] more than the total sample of adult males. Recruitment on high-quality territories was therefore significantly higher than adult mortality, and hence competition for high-quality vacancies was intense.
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Dispersal strategies and LRS on Cousin
Table 1 summarizes the
demographic benefits and duration of dispersal strategies and reproductive
life span of males using different strategies. The average age at which males
became breeders, budders, helpers, or floaters was 1.0-1.2 years, which was
similar for all strategies. The dispersal strategies affected both annual
reproductive success and longevity, and consequently LRS. The best option for
male yearlings to gain highest LRS is breeding immediately on high-quality
territories, whereas the second best option is budding on high-quality
territories. Males starting as budders had the same high longevity as those
breeding immediately on high-quality territories. Budding males started the
budding process in their natal territories at an average age of 1.1 years old,
expanded their budded territory at the expense of adjacent territories, and
lived in the budded area for, on average, 2.6 years (two examples of this
process are illustrated in Figure
2). The shortest and longest period a male lived in a budded
territory was 0.9 and 6.2 years, respectively. Even though nearly all budders
(90.5%; n = 21) acquired a mate at a later stage during the budding
process, annual reproductive success in the budded territory was low and
similar to annual indirect reproductive success of helpers on high-quality
territories, to annual direct reproductive success of floaters, and to
breeders on low-quality territories (Table
1). However, reproductive potential was not sacrificed by budding.
By the average age of 3.7 years, budders had left their budded territory and
filled high-quality breeding vacancies, either on their natal territories or
on adjacent territories (33.3% and 66.7%, respectively; n = 21). The
annual reproductive success on these newly acquired territories was comparable
to that of males breeding on high-quality territories at 1 year of age
(Table 1). Considering each
dispersal strategy separately, males starting as budders had significantly
lower LRS than males breeding immediately in high-quality territories but
significantly higher LRS than males starting either as a helper, a floater, or
a breeding bird on low-quality territories at 1.0-1.2 years of age
(Table 1). Males using one of
the last three strategies had a two to five times lower longevity, with
virtually no successful reproduction (Table
1). All floaters (n = 5) and 50% of the helpers
(n = 6) died without having acquired a breeding territory.
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Even though males born in high-quality territories can expect to gain highest lifetime reproductive success by breeding immediately in high-quality territories, only a few did so (15.2%, Table 1) because of the shortage of high-quality breeding vacancies. In all years from 1982 to 1996, in the high-quality habitat production of adult males was significantly higher than could be accommodated in the male breeding vacancies (annual mean: 7.1 ± 2.4 and 1.7 ± 1.3, respectively; paired t test: t = 11.11, df = 14, p <.001), whereas in the low-quality habitat the number of adult males produced was equal to the number of male breeding vacancies (annual mean: 22.7 ± 5.0 and 19.3 ± 2.9, respectively; t = 1.84, df = 14, ns). Of 316 breeding vacancies for males, 91.8% were on low-quality and only 8.2% were on high-quality territories. Even though competition for low-quality breeding vacancies was less, most male offspring that were not breeding immediately in high-quality territories (n = 46-7 = 39) budded off a portion of their natal territory (53.8%), whereas a small fraction filled breeding vacancies on low-quality territories (17.9%), became floaters (12.8%), or remained with their parents as helpers (15.4%) (Table 1). Although some of the budders and helpers did eventually fill a breeding vacancy, budders, helpers, and floaters were never observed switching between the strategies of budding, helping, and floating. These findings suggest that competition for high-quality territories and LRS payoffs have caused the males to become budders on Cousin. This led us to test two concomitant predictions. First, budders on high-quality territories should fill high-quality breeding vacancies only. Second, in the absence of habitat saturation on Aride, young males born on high-quality habitat should establish breeding territories in the unsaturated high-quality habitat immediately after reaching independence. However, after saturation of the high-quality habitat, young, mature males born in high-quality territories should remain on their natal territories as budders; they should not become breeders on low-quality territories, helpers, or floaters.
Facultative dispersal on Cousin and Aride
Removals on Cousin Island
The relative quality of the breeding vacancy significantly influenced the
budder's dispersal behavior. On Cousin Island, all five experimental
high-quality breeding vacancies were filled by budders from adjacent
high-quality territories within 2 h after the removal of the senior breeding
male. However, none of the five low-quality vacancies were filled by budders
from adjacent high-quality territories. These were all filled by males born on
low-quality territories (two-tailed Fisher's Exact test, p
=.008).
Translocation to Aride Island
The 16 males with different dispersal status translocated to Aride Island
all established territories in the high-quality habitat during the month after
translocation. Before saturation of the high-quality habitat, all males
belonging to cohort Abefore left their natal territories at 0.7
± 0.2 years of age (n = 15). Most of these males established
new territories in the high-quality habitat, some filled breeding vacancies on
high-quality territories, but none became budders, helpers, floaters, or
breeders on low-quality habitat (Figure
3). After the high-quality habitat became saturated, none of the
cohort Aafter males established territories on the high-quality
habitat directly. The fraction of these males filling high-quality breeding
vacancies was the same as before saturation
(Figure 3). Most cohort
Aafter males became budders on their natal territories, few became
helpers, breeders on low-quality territories, or floaters. The first males
seen helping, breeding in lower-quality territories, and floating were
observed in 1991, 1991, and 1996, respectively. On Cousin Island, however,
most males of cohorts Cbefore and Cafter became budders;
none established new territories in the high-quality habitat, and few became
helpers, floaters, or breeders on low-quality habitat
(Figure 3). The change in the
frequency of budding before (cohort Abefore) and after saturation
of high-quality habitat on Aride Island (cohort Aafter) compared
with the control groups on Cousin Island (Cbefore and
Cafter) was significant (Figure
3).
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2 of final fit = 8.99, p
=.110), the strategy most contributing to the interaction strategy x
time period is the number of budders. After fitting the model, the most
outlying cell (Freeman-Tukey deviate) remains the low number of budders on
Aride before saturation (The number of territories on high-quality habitat increased linearly from 13 in September 1988 to 24 in September 1990 to 39 in September 1993. From 1993 onward, the number of territories on the high-quality habitat has remained stable between 39 and 41 territories (Figure 4). Mean annual territory size remained the same from 1988 to 1990, but declined from 1991 to 1996 (Figure 4).
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Between 1990 and 1992, all budders converted their budded territory into permanent, high-quality breeding territories by enlarging their territory at the expense of the natal territory and surrounding territories (n = 15; see also next section). These territories were still present at the end of the study period (March 1997). As a consequence, more territories became established in the already saturated, high-quality habitat (Figure 4). The annual increase in number of territories on high-quality habitat until 1993 was the same as before saturation (mean annual increase: 1990-1993; 5.0 territories [n = 3 years]; 1988-1990; 5.5 territories [n = 2 years]). From 1993 onward, however, only a few of the then-budded territories became permanent, high-quality breeding territories (10.5%, n = 19; Figure 5). Most disappeared (89.5%) because the budder ascended to high-quality territories by taking over breeding vacancies either on his natal territory or on adjacent territory, after which the budded area merged with adjacent territories. The higher the competition over highquality territories (measured as the saturation index) in a given year, the smaller the size of the budded territory in the next year, and the lower the fraction of budders still present on their budded territories (Figure 5). The average age at which budders filled breeding vacancies was 2.7 ± 1.0 years (n = 17).
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Reproductive performance in relation to age and habitat
saturation
Using longitudinal data, we investigated age-related changes in territory
size and reproductive success of the two male cohorts on Aride Island
(Figure 6). Annual territory
size of cohort Abefore males (which established new territories or
filled breeding vacancies at 1 year of age) remained stable over their first 5
years of life (MANOVA: F4,52 = 0.83, ns) and did not
differ between dispersal strategies (MANOVA: F1,13 = 0.77,
ns; strategy x age: F4,52 = 2.27, ns;
Figure 6). Reproductive success
of these males was low in their first year of life but increased in their
second year of life (univariate test for difference contrast:
F2,13 = 17.7, p <.001). From 2 to 5 years of
age, no further improvement in reproductive success was evident (all
univariate tests for difference contrasts: F2,13 <
0.80, ns). Total reproductive success after 5 years was similar for both
strategies (F1,13 = 0.44, ns).
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After saturation of the high-quality habitat, annual territory size of cohort Aafter males differed between dispersal strategies (MANOVA: F2,19 = 939, p <.001). There was also an effect of age on territory size, but this effect was different for males following different dispersal strategies (MANOVA: age: F4,76 = 6.38, p =.002; strategy x age: F8,76 = 39.6, p <.001). Territory size of males that had filled high-quality breeding vacancies at 1 year of age tended to decline when they were 4 and 5 years old because the budded territories increased in size at the expense of these territories (MANOVA difference contrast: 1>2 [change in territory size from age 1 to 2]: F1,19 = 0.00, ns; 2>3: F1,19 = 0.00, ns; 3>4: F1,19 = 3.78, p =.067; 4>5: F1,19 = 3.47, p = 0078; Figure 6). In comparison with males breeding immediately on high-quality territories, annual territory size of same-aged budders was significantly lower during their second and third year of life, but had become similar in their fourth and fifth year of life (MANOVA hypothesis testing: age 2: F1,19 = 535, p <.001; age 3: F1,19 = 149, p <.001; age 4: F1,19 = 0.09, ns; age 5: F1,19 = 2.38, ns; Figure 6).
After saturation of the high-quality habitat, reproductive success differed between dispersal strategies and between ages (MANOVA: strategy: F3,20 = 11.4, p =.001; age: F4,80 = 5.22, p <.001; strategy x age: F12,80 = 3.08, p <.005). Reproductive success of budders increased from 2 to 3 years of age, but remained the same from 3 to 5 years of age (MANOVA difference contrast: 2>3: F1,19 = 14.9, p =.001; 3>4: F1,19 = 0.025, ns; 4>5: F1,19 = 1.83, ns; Figure 6). Compared with same-aged males breeding immediately on high-quality territories, budders produced fewer yearlings during their second year of age, but the same number of yearlings from 3 to 5 years of age (MANOVA hypothesis testing: age 2: F1,19 = 73.4, p <.001; age 3 to 5: all F1,19 < 0.4, ns; Figure 6). Overall, total reproductive success (RS) over the first 5 years of life of budders was significantly lower than total RS of males breeding immediately on high-quality territories but was significantly higher than total RS of helpers on high-quality territories and higher than breeders on lower quality territories (Figure 6).
The average size of territories and reproductive success of six unassisted breeding pairs (the same breeding birds which remained on the same territories during the period October 1988-October 1993) had decreased considerably after October 1990 when all the space in the high-quality habitat was occupied. During the 2 years before saturation, these breeding pairs occupied larger territories and had higher annual reproductive success than during the 3-year period after saturation (mean territory size: 0.25 ± 0.03 ha vs. 0.15 ± 0.01 ha, paired-sample t test: t = 7.22, df = 4, p <.001; mean annual reproductive success: 2.75 ± 0.69 vs. 1.03±0.34, t = 6.24, df = 4, p =.004).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Dispersal strategy and perception of reproductive potential
Variation in reproductive success among territories is a common feature of most noncooperative (e.g., Bensch and Hasselquist, 1991
; Bollmann et
al., 1997; Both and Visser,
2000; Lundberg and Alatalo,
1992; Stutchbury and
Robertson, 1988; Tye,
1992) and most cooperative breeding systems (e.g.,
Nias and Ford, 1992;
Stacey and Koenig, 1990;
Stacey and Ligon, 1991;
Walters et al., 1992). It is
clear that many species can assess territory quality and that the selection
pressure to do so is high (sensu Ens et
al., 1995; Lucas et al.,
1997). Many studies have shown that individuals of
noncooperatively breeding taxa increase their reproductive success after
moving (e.g., Baeyens, 1981;
Beletsky and Orians, 1987;
Petersen and Best, 1987; but
see Newton and Marquiss, 1982)
and that poorer territories are less likely to be occupied
(Krebs, 1971;
Wauters and Dhondt, 1990).
However, for cooperatively breeding species, not only must sufficient
resources exist within a given territory to support additional animals
(Blackwell and Bacon, 1993),
but also some form of fitness benefit for both the dominant pair and the
subordinate is necessary
(Lindström,
1986; Macdonald and Carr,
1989). Without such relative benefits, alternative behavioral
strategies, principally dispersal, will be favored. In other words, apart from
assessing territory quality, mature offspring should be able to perceive which
dispersal strategy would maximize their future inclusive fitness (sensu
Lucas et al., 1997).
In this study we assessed the relative costs and fitness benefits of
different dispersal strategies used by male Seychelles warblers born in
high-quality territories on the islands of Cousin and Aride. Dispersing and
breeding in high-quality territory or staying on their natal territories as
budders yield the longest life span (Cousin: dispersing and breeding: 8.4
years; budding: 8.2 years), as compared to helping, floating, or breeding on a
low-quality territory. Furthermore, breeding in a high-quality territory upon
reaching reproductive maturity yields the highest LRS because of high annual
reproductive success. The second-best reproductive option for a male's whole
life is budding. Although most budders acquired a breeding partner, annual
reproductive success during the budding process was low and comparable to
helping, floating, or breeding in low-quality territory. However, the future
beneficial component of budding is the guarantee that the male will survive to
become the primary breeding male on a high-quality territory. Male helpers
caused a significant reduction in the reproductive success of their parents.
An experimental study showed that this was due to greater depletion of food
resources (Komdeur,
1994b).
Young male Seychelles warblers do sample different territories all over the
island before making a choice where to settle, as shown by observational
(Komdeur, 1991) and by
radiotelemetry studies (Komdeur J, Daan S, Madsen V, and Tinbergen JM,
unpublished observations). Our observations and experiments clearly
demonstrate that young males also assess the relative costs and benefits of
different dispersal strategies. Despite the high fitness returns of breeding
on high-quality territory, only a few males on Cousin became breeding males in
high-quality territories. We think this was due to high competition for these
territories for three reasons. First, in the high-quality habitat on Cousin,
the number of adult males produced exceeded the number of male breeding
vacancies. Second, experimentally created high-quality male breeding vacancies
were filled immediately by nonbreeding budders from adjacent territories.
Third, on Aride, with no shortage of high-quality habitat and breeding
partners, all translocated Cousin males that were using different dispersal
strategies at the time of translocation established high-quality breeding
territories. In addition, all males born on Aride either established
high-quality territories or filled breeding vacancies in high-quality
territories before reaching 1 year of age. After saturation of the
high-quality habitat on Aride, with no shortage of breeding partners and
unoccupied, lower-quality habitat, few males obtained high-quality breeding
territories. If males were unable to breed in a high-quality breeding
territory, most males took the second best reproductive strategy of remaining
in their natal territories to become budders (Cousin: 63%); few used
strategies yielding lower fitness benefits. None of the experimentally created
low-quality male breeding vacancies were filled by budders from adjacent
high-quality territories, but all by males from low-quality territories.
However, it is unclear why some males became helpers. First, they do not need
to help in return for being permitted to stay in their natal territory
(pay-to-stay hypothesis; Gaston,
1978; Taborsky, 1984,
1985). We have never observed
breeders responding aggressively toward related nonhelping male offspring
(which include future budders that remain in their natal territory) or to
nonhelping floaters (which occasionally return to their natal territory for a
total period of up to 2 weeks during a year floating;
Komdeur, 1991). Second, unlike
female helpers, male helpers caused a significant reduction in the
reproductive success of their parents
(Komdeur, 1996a). Compared to
female helpers, male helpers do not contribute to nest building and incubating
the clutch, providing less offspring care and competing for food resources
(Komdeur, 1996a). Third,
helping never results in inheritance of a breeding spot. All breeding spots
were inherited by budders that, compared with helpers, were more abundantly
present and had site-dominance over territory inheritance
(Komdeur and Edelaar, in
press). Fourth, helping never results in siring offspring with the
helper's mother (Richardson et al.,
2001). Potentially, helping males gain breeding experience, for
which there is observational and experimental evidence in the Seychelles
warbler (Komdeur, 1996a).
In addition, it is unclear why some males became floaters. The floaters of the cohort studied between 1982 and 1986 (this study) are short-lived and do not produce any offspring. However, of all the floaters studied up till 1999 (n = 16), 18.8% (n = 3) did eventually fill a breeding vacancy, which happened in 1997 after the death of many breeding males due to torrential rains (Blaakmeer K, unpublished observations). The three floaters that acquired a breeding territory produced offspring and have reached ages older than the 1-2 years of floaters of this study; one was 4 years old, and two (still alive at present) were at least 3 and 4 years old.
Costs of missed opportunities
In male Seychelles warblers, the cost of helping, floating, or settling on
a low-quality territory seems to be a cost of missed opportunities because it
never results in obtaining a high-quality territory later and a high
reproductive success (fitness). It could be that not all males are capable of
using those dispersal tactics yielding the highest fitness. For example,
compared with males with a good body condition, males with a relatively worse
condition may be less able to compete for high-quality breeding territories or
to gain part of the natal territory through fighting and subsequent budding.
Instead, such males may gain a higher fitness as helpers or floaters. In
addition, it is potentially easier for a helper or a floater to inherit a
vacant territory than for a territory holder to do so because territory
switching rarely occurs. Most breeding birds (99.1%; n = 314)
remained in their low-quality breeding territories until their death
(Komdeur, 1991). This
inflexibility of established breeders, despite the possibility of higher
reproductive success elsewhere, is common
(Aebischer and Coulson, 1990;
Ens et al., 1995;
Korpimaki, 1988;
Picman, 1987). If territory
switching is a possibility—as it is in some species
(Beletsky and Orians, 1987;
Curry, 1988;
Krebs, 1971;
Newton and Marquiss,
1982)—the relative advantage of budding decreases
(Kokko and Sutherland, 1998).
Dominant status over territory inheritance upon the death of the same-sex
adult is linked to budding and not to helping and is independent of the male's
age (Komdeur and Edelaar, in
press). The absence of territory switching and the presence of
site dominance over territory inheritance may explain why it pays for
Seychelles warbler males to stay and bud in a saturated environment. We favor
this explanation because it appears to be the most parsimonious; additional
work is required to determine both beneficial and detrimental effects for the
parents of tolerating a budding son and for the participants in the
interaction. Experiments in which the male's body condition is changed
(through supplementary feeding or handicapping the bird) are needed to show
whether the dispersal strategy used is state dependent.
Ideally, the LRS and fitness consequences of each dispersal strategy should
be calculated as the precise number of within-and extrapair young produced by
each male through DNA paternity studies. However, the LRS values of each
dispersal strategy in this study is probably a realistic measure
(Richardson et al., 2000),
since microsatellite DNA fingerprinting has revealed that only breeding males
on low- and on high-quality territories gain extrapair paternity (helpers,
floaters, and budders never sire offspring through extrapair fertilizations),
and the degree of cuckoldry is equal for breeding males on low- and
high-quality territories.
Territorial inheritance: helping and budding as alternative
strategies
In cooperatively breeding species in which breeding is constrained, one
possible route to becoming a breeder is to remain at home as a helper. It is
argued that the act of helping is the route to dominant status over the
acquisition of the natal or a nearby territory in future years
(Balshine-Earn et al., 1998;
Koenig et al., 1992;
Lindström,
1986; Reyer, 1984;
Stacey and Ligon, 1987;
Woolfenden and Fitzpatrick,
1984; Zack, 1990;
Zahavi, 1976). By enhancing
the reproductive success of the breeders, helpers increase the size of the
family unit. Larger groups outcompete smaller ones at territorial boundaries,
through which they expand the size of the natal territory. This, in turn,
increases the likelihood that the former helper will be able to bud off a
portion of the enlarged parental territory for itself. However, it is unknown
whether the acquisition of a territory is linked to helping per se or to a
passive effect of delayed dispersal alone
(Blackwell and Bacon, 1993;
Emlen, 1994,
1995). Indeed, in several
species helping and budding go together: budders are former helpers
(Stacey and Koenig, 1990;
Koenig et al., 1992), but not
in the Seychelles warbler. None of the warbler helpers became budders
(n = 14). One reason that keeps helpers from becoming budders could
be differences between individual males such that each male adopts the
strategy that maximizes his fitness. Young males that ultimately adopted the
budding strategy show higher levels of aggressive behavior compared to similar
aged males that ultimately adopted the helping strategy
(Komdeur and Edelaar, in
press). This could be related to (fighting) quality necessary for
budding. Alternatively, and perhaps in interaction with the former
explanation, males might find themselves in different competitive
environments. For example, a helping male might forgo the otherwise high
fitness related budding strategy when several budders are already present near
the natal territory and local competition over the future vacancy is expected
to be high. Recently, Poiani
(1994) came up with an
alternative model to explain the nonhelping behavior as a strategy to increase
direct fitness. Nonhelpers take advantage of group defense (without paying the
cost of helping to raise potential competitors), through which the future
probability of becoming a breeder is increased (because of lack of
intergenerational competition for breeding status). In the Seychelles warbler,
nonhelping males that remained on their natal territories assisted their
parents significantly more with territory defense than helping males
(Komdeur and Edelaar, in
press). It is known for some species that extra individuals (e.g.,
their own offspring) remain within the breeders' territory but do not help
(Caffrey, 1992;
Sydeman, 1991;
Veltman, 1989; see also
Curry, 1988;
Poiani, 1994). Also in
Seychelles warblers, most young males remaining on their natal territory which
had a chance to help because their parents had produced younger offspring, did
not help (Cousin and Aride: 83.8%, n = 68). In addition, none of the
budders had been helpers before (n = 53).
The simultaneous presence of helping and nonhelping males in the Seychelles
warbler and the absence of switching between the two strategies enabled us to
investigate why helpers help. If future fitness effects of helping are taken
into account, nonhelping should be selected for in male warblers, even among
close relatives, because nonhelping males have higher longevity than helping
males, and nonhelping males become budders, through which they gain higher
fitness benefits than helping males by inheriting the breeding spot (both a
mate and a territory), while helping males never inherit a breeding spot. A
budder never obtained a high-quality breeding spot by evicting a breeder from
his territory (Komdeur and Edelaar, in
press). Instead, this was achieved either through expanding the
budded territory into a high-quality territory at the expense of neighboring
territories (observed on Aride when the high-quality habitat could still
support more territories after saturation) or through inheritance of either
the natal or an adjacent territory (observed on Cousin and Aride when no more
new territories could be established in the high-quality habitat). However,
experimental studies under natural conditions to test the inheritance
hypothesis for helping and Poiani's hypothesis for nonhelping have yet to be
performed (Balshine-Earn et al.,
1998; Emlen, 1991,
1995).
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ACKNOWLEDGEMENTS |
|---|
We thank Mark Elgar (Melbourne University, Australia), Serge Daan, Rudi Drent, and Christiaan Both (Groningen University, The Netherlands), and two anonymous referees for their constructive criticism of an early draft of the manuscript, and Jaap van der Meer (Netherlands Institute for Sea Research, The Netherlands) for statistical advice. We are also grateful to Michael Rands (BirdLife International, UK), who arranged permission to work on Cousin Island and to transfer warblers, and to James Cadbury and the late Christopher Cadbury, who generously provided support and agreed to have warblers on Aride Island. We thank the staff on the islands of Cousin and Aride for helping with logistics of the project. The study was supported by grants from BirdLife International, the Danish Natural Science Research Council (9401137), and the Netherlands Foundation for the Advancement of Tropical Research (WOTRO; W84-368).
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