Behavioral Ecology Vol. 14 No. 2: 157-164
© 2003 International Society for Behavioral Ecology
Facultative control of offspring sex in the cooperatively breeding bell miner, Manorina melanophrys
a Department of Zoology, La Trobe University, Victoria 3086, Australia b School of Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia c Laboratoire d'Ecologie, Ecole Normale Superieure, 46 rue d'Ulm, 75230 Paris Cedex 05, France d Department of Conservation, 59 Marine Parade, Napier, New Zealand e Department of Genetics and Human Variation, La Trobe University, Victoria 3086, Australia f Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada
Address correspondence to J. Ewen, who is now at the Laboratoire d'Ecologie Evolutive Parasitaire, CNRS UMR 7103, Université Pierre et Marie Curie, Bat A 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France. E-mail: john.ewen{at}snv.jussieu.fr.
Received 21 September 2001; revised 30 May 2002; accepted 7 June 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The ability to alter primary sex ratios has the potential to increase a breeding individual's fitness. This is certainly true in those cooperative breeders where one sex is both philopatric and helps raise future offspring of its parents. We examined the primary sex ratio variation in the cooperatively breeding bell miner (Manorina melanophrys) in southeastern Australia over six breeding seasons. Male offspring are the philopatric and helping sex in this system and can increase the reproductive output of their parents. Bell miners aggressively defend their territory from all interspecific competitors and by doing so allow food resources to dramatically increase. The increase in phytophagous Psyllidae insects (which secrete a carbohydrate-rich coating that constitutes the major component of bell miner diet) leads to a decrease in tree health, often culminating in death of the tree. Bell miners then move as groups to new areas with low psyllid abundance, and the cycle repeats. Using this predictable temporal variation in food availability, we aimed to determine whether female breeders adjusted the sex ratio of broods to produce more of the philopatric sex when food resources were high and more of the dispersing sex when food resources were low. Our results provide clear evidence for such facultative control of sex ratio by female bell miners. Newly founded colonies are characterized by low food availability and a female-biased primary sex ratio, whereas colonies more than 1 year old have an increased food availability and a male-biased primary sex ratio. We suggest treating forces associated with resource enhancement and competition as opposing sides of a single general principle and suggest that it is necessary to view both the costs and benefits of philopatric individuals within a variable environment.
Key words: bell miners, cooperative breeding, facultative control, Manorina melanophrys, primary sex ratio.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Understanding the potential fitness benefits available to individuals through altering the relative numbers of sons and daughters has long challenged theoretical biologists (Charnov, 1982
; Darwin, 1871; Fisher, 1930; Trivers and Willard, 1973). Numerous hypotheses and models have been made to predict when sons and daughters should be produced at parity and when the production of one sex is favored (for review of major hypotheses, see Frank, 1990). Despite the proliferation of ideas, there has, until recently, been little in the way of empirical support for sex ratio fluctuations in any vertebrate group (Emlen, 1997). Birds are a prime example of a group favored for testing evolutionary theory. However, due to difficulties in sexing individuals, birds were not thought to bias primary sex ratios as recently as 15 years ago (Clutton-Brock, 1986). This view has certainly changed, largely as a result of the advent of molecular sexing techniques (Griffiths et al., 1996), which have revealed numerous examples of sex ratio modification (e.g., Heinsohn et al., 1997; Komdeur et al., 1997; Sheldon et al., 1999). Such evidence has resulted in a renewed focus on adaptive sex ratio variation, particularly in birds, and a reassessment of theoretical predictions.
The subject of adaptive sex ratios in cooperatively breeding species has been one of the more controversial areas of research in this field. This is largely due to the numerous factors hypothesized to affect sex ratio and the difficulty associated with disentangling these factors (Koenig et al., 2001). The majority of models build on the premise that parents should invest equally in both sexes, so that when sons and daughters provide the same genetic return from a given unit of investment, the resulting sex ratio of the population will be at parity (Fisher, 1930). Any deviations from this 50:50 ratio will then tend to be drawn back to parity through frequency-dependent selection (Charnov, 1982). Equal investment will result in biased sex ratios in any situation where the genetic returns from producing sons and daughters differ. For example, biases are predicted when members of one sex provide help to their parents in controlling critical resources (local resource enhancement; Emlen, 1997) or more specifically when one sex repays part of the cost of their production by providing help in future reproductive efforts of their mother (repayment models in various forms; Emlen et al., 1986; Koenig and Walters, 1999; Lessells and Avery, 1987; Pen and Weissing, 2000). Biases toward the dispersing sex in cooperatively breeding species have also been predicted when there is increased sex-specific competition for mates (local mate competition; Hamilton, 1967) or other limiting local resources (local resource competition; Clark, 1978).
Early investigation of sex ratios in birds focused on the number of sons and daughters produced at the population level. Population-level analyses provided strong support for sex ratios in birds to be optimized, or constrained, at parity (see early review in Clutton-Brock 1986). Even in cooperative breeding systems where models have predicted biases (see above), population biases are not clearly evident (see, e.g., Gowaty and Lennartz, 1985; Koenig and Walters, 1999; Ligon and Ligon, 1990; but see Clarke et al., 2002). However, recent discussion has highlighted the difficulty in predicting the expected population biases in cooperative systems (Koenig and Walters, 1999). In the past few years, there has been a clear switch to investigation of primary sex ratio bias at the individual breeder level. Facultative control of offspring sex ratios by individual breeding females has long been predicted (e.g., Trivers and Willard, 1973). However, empirical support has been a long time in coming; for example, Williams (1979) concluded there was no evidence for any theory of adaptive sex ratio variation. However, he did expect selection would favor females who could "rear that combination of sons and daughters that has a total optimum expenditure that approximates her own personal optimum" (Williams, 1979: 569). These predictions are now gaining support due mostly to the ease of molecular sexing, with numerous studies showing clear facultative control of primary sex ratio by breeding female birds (see recent meta-analysis of sex ratio skews in birds; West and Sheldon, 2002). This trend may continue as more researchers switch their focus from population-wide estimates of sex ratio bias to individual variation by breeding females.
Facultative control in cooperative breeding birds has been recorded in few species (including red-cockaded woodpeckers, Picoides borealis: Gowarty and Lennartz, 1985; green woodhoopoe, Phoeniculus purpureus: Ligon and Ligon, 1990; eclectus parrots, Eclectus roratus: Heinsohn et al., 1997; but with the strongest evidence provided by the Seychelles warbler, Acrocephalus sechellensis: Komdeur, 1996; Komdeur et al., 1997, and the kookaburra, Dacelo novaeguineae: Legge et al., 2001). These results have largely been interpreted within models for local resource enhancement and competition. Although these models make clear and opposing predictions, they are certainly not mutually exclusive and must be considered together to better understand observed sex ratio biases.
In this study we investigated the ability of cooperatively breeding bell miners (Manorina melanophrys) to facultatively control the sex ratio of their offspring. Previous analysis of a reduced data set has already presented evidence indicating, at the population level, that adult sex ratios are heavily biased toward males (64.4%), and, among groups of helpers, 96 ± 1.9% of helpers were male (Clarke et al., 2002). This male bias was partially reflected in the primary sex ratio, with 55.6% of all nestlings produced being male (Clarke et al., 2002). This was interpreted as consistent with the repayment models of sex allocation, as males are the philopatric sex, provide aid in raising subsequent broods, and their presence increases the reproductive success of the breeding pair (Clarke, 1989; Clarke et al., 2002). The possibility of facultative control of sex ratio by individual breeding females was not considered in these previous analyses.
We had two aims. First, we aimed to determine whether females altered the sex of their offspring in response to habitat quality. Bell miners have a complex relationship with infestations of phytophagous insects (Psyllidae, see Methods), which provides a unique opportunity to measure temporal variation in habitat quality. According to the forces of local resource competition and enhancement, we predicted females would produce more of the dispersing sex when habitat quality is low (to avoid competition for limited local resources) and more of the philopatric sex when quality is high (competition for limited resources reduced and benefits of increased workforce can be realized). Second, we assessed whether the existing number of helpers a breeding pair had affects the subsequent choice of nestling sex. This was of interest because earlier research presented a nonsignificant trend for females with no helpers to produce more male-biased broods (Clarke et al., 2002), a pattern which may be expected under existing repayment models.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area and species
We studied nine bell miner colonies over six breeding seasons within the Coranderrk Reserve and adjacent Wurundjeri (local Aboriginal people) land in Healesville, Victoria, Australia (37°41' S, 145°31' E) between November 1992 and February 2000. Bell miners typically inhabit open eucalypt forest supporting a dense, shrubby understory suitable for nesting (Higgins et al., 2001
). Their diet consists predominantly of lerps, the carbohydrate coating secreted by psyllids, gleaned from the eucalypt foliage (Higgins et al., 2001). Adults are slightly dimorphic in size (males 7.3% heavier), but there is no significant size difference during the nestling stages of development (Clarke et al., 2002). Colonies are typically large (8–200 birds; Higgins et al., 2001) and are made up of several well defined subgroups (coteries) that function as discrete social and genetic units (Painter et al., 2000). A coterie comprises usually between one and three breeding pairs (Clarke, 1989) which share a contingent of nonbreeding, mostly male helpers (Clarke, 1989). Small colonies may consist of a single coterie. Breeding is protracted and can occur for up to 10 months of the year, with individual females being multibrooded (0.65 breeding attempts per month throughout the year; Clarke, 1988). Individuals generally pair for life (age of first breeding is about 15.4 months; Clarke, 1988), and molecular data suggest that these bonds are monogamous (Conrad et al., 1998). Previous data from Healesville reported the age of breeding females ranging from 9.1 to more than 90.5 months and from 14.1 to more than 82.1 months for breeding males (Poiani, 1993). However, another study reported a much shorter tenure for breeders in other study sites of 13.3 ± 5.84 months for breeding females and only 7.3 ± 5.93 months for breeding males (Clarke, 1988). Therefore, it is likely that in some cases the breeding females will be replaced within the coterie during the period they occupy a given territory. We used a combination of active nest searching and following identified females within entire colonies to find and sample 243 broods, comprising 437 nestlings or embryos from 129 different breeding females. An effort was made to mistnet and color band the majority of adults and color band all surviving nestlings older than 9 days. We took a small blood sample from all nestlings for genetic sexing (see below). Additionally, we examined unhatched eggs for evidence of embryo development, and, if present, collected tissue samples (see below). Broods were considered either complete, if all individuals within the brood were sexed, or partial, if an egg or nestling was known to have disappeared or where an individual was unable to be sexed.
Habitat quality
The presence of bell miner colonies is closely linked with psyllid infestation and eucalypt dieback (Clarke and Schedvin, 1998; Loyn et al., 1983). New areas of eucalypt forest are occupied when either an entire colony, or single coterie, move as a unit to a previously unoccupied site (Clarke and Fitz-Gerald, 1994; McCulloch and Noelker, 1974). Evidence suggests bell miners establishing new sites aggressively exclude almost all other bird species (Clarke, 1984; Clarke and Fitz-Gerald, 1994), thereby allowing psyllid numbers to increase (Clarke and Schedvin, 1998; Loyn et al., 1983) and providing additional food resources. Data from the current population shows that the relative numbers of lerps per leaf dramatically increase during occupancy of a given site, at least doubling within the first 2 years (Clarke and Schedvin, 1998). However, this increase in relative lerp density is not immediate; little clear increase is observed within the first year of occupancy (Clarke and Schedvin, 1998). Eventually this leads to a decrease in tree health (including significant tree death) through phytophagous insect loading and culminates with abandonment of colony sites by bell miners (Clarke and Schedvin, 1998).
To better understand the dynamics of bell miner colony tenure, we investigated bell miner persistence within given areas over a 12-year period from August 1989 to August 2000. Colony boundaries were mapped by M.F.C. between August and October of each year (apart from 1989, when they were mapped by G. Underwood, and 1990 and 1991, when they were not mapped). Given that the most cohesive group within the bell miner social system is the coterie, the coterie would provide the ideal level of analysis. Additionally, single coteries rather than entire colonies often move location (see above). Unfortunately, we do not have detailed information regarding coterie boundaries available for the present data. In an attempt to approach this level of analysis, we chose to overlay a 50 x 50 m grid, representing the mean coterie size estimated from home range data (Painter et al., 2000). The presence of bell miners within each cell was then recorded. For consistent measurement, a minimum of one-quarter of each cell had to be occupied before bell miners were recorded as present. We chose this method, plus a relatively large grid cell size, to minimize erroneous measurement of tenure due to error associated with the mapping of colony boundaries. These data were used to first investigate temporal patterns of bell miner presence throughout the study area and second to investigate bell miner tenure within each cell once it became occupied. Four tenure scores were recognized, with 1–3 representing individual years and 4 representing bell miner presence for 4 or more years. As such, our analysis follows patterns of tenure and sex ratio within given areas (grid cells), which approximate areas associated with coterie occupancy. Data on bell miner presence were arcsine-square root transformed to normalize the residuals of proportional data (Sokal and Rohlf, 1969).
Tree health was assessed, and psyllids were counted at different stages throughout the study (but not in every year and every colony) as a part of concurrent research (see Clarke and Schedvin, 1998; Weston, 1999) and for detailed investigation of tree health within two colonies (see below). We present these data in relation to the tenure scores described above to illustrate changes in tree health and psyllid number as the duration of bell miner presence within sites increased. Assessment of tree health followed a method developed by Grimes (1988). Four attributes were scored (crown size, crown density, presence of dead branches, and the abundance of epicormic growth) using a scale of 0–5 for each, with 0 representing the poorest score. Scores were summed to give an overall index of tree health out of 20. The number of trees assessed at each colony varied from 10 by Clarke and Schedvin (1998) to complete colony assessment in the present study (see below). Psyllid abundance was recorded by counting the number of lerps visible on 40 leaf surfaces on 10 trees at each sampling site using a high-powered telescope (see Clarke and Schedvin, 1998, for detailed methods). This provides only a relative measure of psyllid abundance and therefore gives qualitative information on temporal patterns in food availability. Where more than one site is available for a tenure score, separate results are presented to avoid problems with interobserver variability in both tree health assessment and psyllid counting.
Additionally, we focused on fine-scale quantification of habitat quality within two large colonies (likely to contain numerous coteries in each) in the 1998–1999 and 1999–2000 breeding seasons. A combination of tree health assessment and density of trees allowed us to directly assess habitat quality variation and its possible effects on primary sex ratio. The health of all 843 eucalypt canopy trees within the two colonies was assessed between February and March in each year using methods detailed above. Colony boundaries were mapped using a GPS unit (Garmin GPS 12). We calculated the density of trees by dividing the number of canopy trees by the area (calculated using ArcView GIS 3.0a; Environmental Systems Research Institute Inc.). This provided two closely linked measures of quality, mean tree health and density, for each colony in each year. To include these data into a statistical model (see below), we averaged both tree health and density for each colony (n = 2) in each year (n = 2); therefore our measures of both parameters are represented by four categorical values.
Breeding variables
In four breeding seasons (1993–1994, 1994–1995, 1995–1996, and 1998–1999) a total of 59 broods from 47 females were observed in detail during the nestling stage. A minimum of four nest watches of at least 1 h were conducted, with two nest watches between nestling ages 2–8 days and two nest watches between 9 days and fledging. We made observations from a portable hide positioned at least 6 m from the nest using a telescope. Parameters recorded are as detailed by Clarke et al. (2002), and we similarly calculated the mean Rabenold's (1985) index for each provisioning adult over the nesting cycle. Rabenold's (1985) index was used to differentiate helpers that made regular feeding trips throughout the nesting cycle (major helpers, 
0.3) from those birds that helped infrequently (minor helpers, < 0.3).
Sex identification
We collected blood samples (5–100 µl) from nestlings of any age by wing venipuncture (nestlings older than 6 days) or leg venipuncture (nestlings between 1 and 6 days old), using a 26-gauge needle, and stored samples in 1 ml of Queens lysis buffer (Suetin et al., 1991). Tissue samples from unhatched embryos were collected 2 days after the remaining eggs had hatched (hatching is synchronous in the bell miner) and stored in 100% ethanol. Two nests were deserted by bell miner females, and the embryos were similarly collected for molecular sexing. These desertions were associated with a movement of the entire colony to a new site and were unlikely to have resulted from disturbance by researchers. We used two molecular protocols to determine the sex of all sampled individuals. Both protocols always sexed known-sex birds correctly (deduced from breeding behavior and brood patches). Polymerase chain reaction amplification condition and thermal profiles for both methods are outlined in Clarke et al. (2002).
Statistical analysis
Both partial and complete broods were included in all analyses following the convention of Fiala (1980), who warned that limiting analysis to only complete broods may create a bias in favor of the sex with greater early survivorship. Justification for including partial broods also comes from an earlier investigation of this data set that highlighted no detectable bias in the mortality of male and female embryos or nestlings and showed that sex ratios of partial and complete broods were no different (Clarke et al., 2002).
To determine whether multiple broods by individual females could be treated as independent sampling units, we compared the mean variance in sex ratio over repeated broods by the same female to a distribution of mean variances attained through resampling multiple broods from the complete data set. Resampling without replacement was performed using SAS software (SAS Institute, 1993) on sex ratio data (proportion of males) with 10,000 iterations of 169 broods used to generate a distribution of independent mean variances. Our observed mean variance for the 169 broods from multibrooded females was compared to this distribution and the significance was taken as the proportion of resampled mean variances greater than that of our observed mean variance.
Investigations of how well putative explanatory terms explain variation in offspring sex ratio were analyzed using the SAS module Genmod with a logit link function and binomial errors. Stepwise sequential tests were used to manually assess and remove any nonsignificant explanatory variables and interaction terms until no further terms could be removed without reducing the model's explanatory powers (Wilson and Hardy, 2002). Models were initially checked for overdispersion and further checked by investigation of residual plots, where a lack of pattern indicates a well-specified model (Wilson and Hardy, 2002). Univariate terms were checked for multicollinearity and second-order interactions were included for closely related variables. Wald's test statistics (Krackow and Tkadlec, 2001) were chosen due to the reduced type 1 error associated with the large number of sample broods (model 1 n = 243, model 2 n = 109) and the low average brood size. Significance was assessed by comparing change in deviance, once a given term was removed from the model, to the chi-square with degrees of freedom equal to the difference in the number of terms in the two models (Crawley, 1993; McCullagh and Nelder, 1990). Sex ratio patterns were further investigated through computing the predicted proportion of males within broods from the linear predictor values. We assessed significance of differences between levels within such terms through investigation of planned orthogonal contrasts. We also ran a univariate logistic model to examine whether the number of major helpers present with a female is associated with the proportion of males within her broods.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Brood sex ratio was measured as the number of males in a brood over the total brood size (number of males plus number of females). There was no significant difference in the mean variance of sex ratio in repeated broods of individual females when compared to a distribution of mean variances attained by resampling multiple broods from randomly selected females (resampling test; 10,000 iterations, two-tailed p =.82). This result is expected given the small clutch size in bell miners and the constrained variance consequently available, and it supports our treatment of repeated broods from individual females as independent sampling units.
Territory quality
During the study individual cells were occupied on average for 2.27 ± 1.28 (SD) years. There was a significant decline in the proportion of Coranderrk Reserve and Warundjeri land occupied by bell miners over the 12-year period (R2 =.84, p <.001; Figure 1).
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pi = 0.501 -0.019(year), where pi is the proportion of cells occupied by bell miners, and the equation calculated with 1988 represented as year 0Mean tree health changed substantially when compared to the length of time that cells were occupied (tenure) by bell miners (Figure 2a). Tree health in a newly established colony was relatively good (17.8 ± 2.55). However, the longer bell miners inhabited cells, the less healthy of trees became, with eventual abandonment associated with very low tree-health scores (4 ± 1.23). Psyllid numbers reflected a different pattern with a loading in the first year of cell occupancy only half that of cells occupied for more than 1 year (Figure 2b).
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There was a significant positive relationship between the number of years bell miners had been present within a cell and the proportion of males in the brood (Table 1). This relationship was largely due to a female-biased brood sex ratio in the first year of cell occupancy, which was significantly different from the more male-biased brood sex ratios in all other years (
2 = 16.71, df = 3, p <.001; Figure 3). No seasonal trends were detected, nor was there any significant effect of year, female identity, or colony on proportion of males in the brood (Table 1). There was no evidence that the standardized residuals did not belong to a logistic distribution (Kolmogorov-Smirnov test; Z = 0.84, p >.1). Investigation of standardized residuals revealed no trends with respect to our fitted values, thus indicating a well-specified model (Figure 4a).
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When we considered the effects of tree health and density on the proportion of males within broods in our more detailed examination of two colonies over 2 years, a more complex pattern emerged. Under our selection criteria the minimal model retained three significant terms that together maintained the model's explanatory powers (change in deviance from the maximal model = 2.94, df = 2, p =.23; Table 2). The colony occupying the site with the lower density and less healthy trees (these measures are represented as the health x density interaction in our model) had a significantly higher proportion of males per brood. There was a close negative relationship (although not significant) between the proportion of males in broods and the year in which the study was conducted (Table 2). Additionally, as the interaction between health and density (our measure of territory quality) decreased, the proportion of males within broods increased (Table 2). Again, there was no evidence that the standardized residuals did not belong to a logistic distribution (Kolmogorov Smirnov test; Z = 0.61, p >.1). Investigation of our standardized residual plots initially highlighted a single outlier, and this brood was removed before model fitting. Replotting standardized residuals subsequently indicated a well-specified model (Figure 4b).
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Presence of major helpers
We found no evidence of a relationship between the number of major helpers a female had and the subsequent proportion of males in her broods (between 0 and 19, mean = 4.9 major helpers; Wald
2 = 0.41, df = 1, p =.53). Following Clarke et al. (2002), we reanalyzed this relationship with major helpers presented as a binary response with either 0 or 1 major helper. Again, we found that females with no major helpers produced proportions of males in their broods (mean proportion of brood male = 92.9 ± 7%, n = 7), which did not differ significantly from those females with one or more major helpers (mean proportion of brood male = 52.6 ± 5.5%, n = 52), although this pattern was much closer to significance (Wald 2 = 3.2, df = 1, p =.074). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We found clear evidence for facultative control of sex ratio between broods by female bell miners. Control was in response to predictable temporal changes in food availability, as represented in our models by associated habitat quality variables. Newly founded colonies inhabit sites with relatively good tree health and low psyllid loading (i.e., lower food availability). Our results indicated that the sex ratio was biased toward females at this stage. In all other years we found male-biased broods, and sites older than 1 year were characterized by worse tree health and increased psyllid loading (i.e., increased food availability). Our detailed analysis of tree health and density within two colonies supports this, with an increase in the proportion of males as tree health and density declined. Our methods have provided only relative density of psyllids in each tenure score, and our results are therefore restricted to showing general patterns. Future research would greatly benefit from developing a methodology that could provide accurate information regarding psyllid availability per bird in this system.
Male bell miners are the philopatric sex and remain in close proximity to their natal nest area, providing help to their mothers and other related individuals breeding nearby (Clarke, 1989; Clarke and Fitz-Gerald, 1994). In contrast, females are the dispersing sex and provide little aid (Clarke, 1989; Clarke and Heathcote, 1990). Our results are consistent with breeding females producing more of the dispersing sex when resources are limited (predicted mean proportion of males in broods for tenure score 1 was 0.36) and more of the philopatric sex when food availability increases (predicted mean proportion of males in broods for tenure scores 2–4 was 0.59).
Sex ratio biases resulting from variation in resource availability have been predicted under numerous models (Clark, 1978; Charnov, 1982). Two general principles are important here. The first, proposed by Clark (1978), reasons that sex-specific competition between siblings and their parents for limited local resources would lead to a primary sex ratio bias toward the dispersing sex (local resource competition). The second is the converse situation, which suggests that parents should overproduce the sex that increases their ability to control resources (Emlen, 1997), therefore leading to a primary sex ratio bias toward the philopatric sex (local resource enhancement). The latter has been further specified for cooperative breeding species to account for the benefits accrued by parents through aid received in provisioning subsequent broods from the philopatric sex (Emlen et al., 1986; Koenig and Walters, 1999; Lessells and Avery, 1987; Pen and Weissing, 2000). Both these models (local resource competition and local resource enhancement) should be viewed together within a single cost-benefit framework, and this is particularly true when considering potential for facultative control within a variable environment.
Facultative manipulation of offspring sex in response to resource availability has been shown in some raptor species, where females produce more of the less expensive sex during times of food shortage (e.g., American kestrels, Falco sparverius: Wiebe and Bortolotti, 1992; Eurasian kestrels, Falco tinnunculus: Korpimaki et al., 2000), and in a captive population of zebra finches, Taeniopygia guttata, which also produced the less expensive sex during times of experimentally reduced food availability (Kilner, 1998; but see Wilson and Hardy, 2002). However, in cooperatively breeding species, there has been only one other study presenting clear evidence for such control in response to resource availability. Komdeur (1996) showed that in Seychelles warblers, unassisted pairs on low-quality territories produced 77% sons, whereas unassisted pairs on high-quality territories produced only 13% sons (sons being the nonhelping and dispersing sex in this species). Moreover, breeding pairs that were transferred from low- to high-quality territories switched from the production of male to female eggs. These results are consistent with those presented for the bell miner and lend support for investigation of sex ratio biases in such systems on an individual breeder basis. Certainly such systems will continue to test sex ratio theory with at least one other detailed study finding no evidence of facultative control in a cooperatively breeding species in response to habitat quality or numerous other parameters predicted to influence sex ratio (acorn woodpecker, Melanerpes formicivorus: Koenig et al., 2001).
Although our study indicates a bias toward males when food resources are increased, this study provides no evidence for benefits of increased numbers of philopatric individuals. Males do provide help to subsequent breeding attempts and have been shown to increase the breeding pair's reproductive success (Clarke, 1989). Therefore, a bias may be expected under repayment models (see above; see also discussion in Clarke et al., 2002). Yet our analysis revealed no indication that females with few helpers produced more sons than those with many helpers. This indicates other factors may also influence a female's preferential allocation into sons. Provisioning nestlings is likely to be one of many beneficial roles philopatric males provide. Predator vigilance and territory defense are two additional roles commonly invoked (see summary in Stacey and Ligon, 1987). Territory defense may be a strong driving force in this particular system given the intensity of observed interspecific aggression (Clarke, 1984) and the increased food availability resulting from exclusion of all competing species (Loyn et al., 1983). Perhaps a general rule is "more males are better," and the limit becomes the resources available to sustain these numbers (i.e., a trade-off between local resource enhancement and local resource competition).
Bell miner systems differ from the typical negative relationship between density and local resource competition. Once established, colonies may continue to enhance food availability through efficient interspecific colony defense until negative affects on tree health cause the system to crash. As such, our rule of more males is better may place constraints on bias in offspring sex early in colony establishment (when food is limited). Once a founding colony has increased food availability to a level able to sustain increased density, they may switch to produce more philopatric individuals, in turn increasing the efficiency of colony defense. Given that in all years except the first year of occupancy are characterized by a male-biased primary sex ratio and that mean tenure or period of occupancy was > 2 years, this may help explain the population-wide male bias previously reported from this data set (Clarke et al., 2002). The previous conclusion that local resource enhancement leads to this bias is therefore maintained within the present interpretation. Additionally, such interpretation may also explain the large number of helpers often recorded (up to 28; Clarke, unpublished data). Certainly such high numbers of helpers are in excess of those needed to reduce the breeding females' investment in provisioning young (feeding rates asymptote after the third major helper in bell miners; Clarke et al., 2002). Our study attempts to treat forces associated with resource enhancement and competition as opposing sides of a single general principle-the costs and benefits associated with philopatric individuals within a variable environment. Such cost-benefit approaches have recently been advocated in sex ratio literature (West and Sheldon, 2002).
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ACKNOWLEDGEMENTS |
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We thank P. Martin, L. Robertson, F. Connor, S. Maxwell, K. Munro, E. Moysey, B. Gonzalez, B. Lees, R. Boulton, R. Clarke, and N. Schedvin for assistance in the field. We are grateful to Alan Wandin and the Wurundjeri people, and to the Zoological Board of Victoria for permission to work on their property, and for the support we received from their staff, especially from G. Underwood and P. Slinger. We also thank Y. C. Crozier, M. Carew, R. Johnson, and M. Goodisman for their support and help in the molecular aspects of the study and R. Clarke, Andrew Bourke, and two anonymous referees for their useful feedback on the manuscript. This research was supported by Natural Science and Engineering Research Council grants to R.J.R. and M.F.C. and Australian Research Council grants to M.F.C. and R.H.C. The study was conducted in accordance with a color-banding permit from the Australian Bird and Bat Banding Scheme, Animal Experimentation and Ethics permits from La Trobe University and the Zoological Parks and Gardens Board of Victoria, and research permits from the Department of Natural Resources and Environment.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Charnov EL, 1982. The theory of sex allocation. Princeton, New Jersey: Princeton University Press.
Clark AB, 1978. Sex ratio and local resource competition in a prosimian primate. Science 201:163-165.
Clarke MF, 1984. Co-operative breeding by the Australian bell miner Manorina melanophrys Latham: A test of kin selection theory. Behav Ecol Sociobiol 14:137-146.
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