Behavioral Ecology Advance Access published online on January 18, 2008
Behavioral Ecology, doi:10.1093/beheco/arm149
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Strong but variable associations between social dominance and clutch sex ratio in a colonial corvid
Behavioural Biology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands
Address correspondence to H.M. Salomons. E-mail: h.m.salomons{at}rug.nl.
Received 16 February 2007; revised 22 November 2007; accepted 3 December 2007.
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ABSTRACT |
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We studied primary sex ratio of clutches in relation to social dominance for 6 years in a colony of free-living jackdaws, a small corvid. Social dominance was strongly associated with clutch sex ratio, with the difference in clutch sex ratio between the most and least dominant pairs being 30–40%. To our knowledge, this is the first demonstration of an association between social dominance and sex allocation in birds. However, the direction of this effect varied between years. Dominant jackdaws produced more sons during the first years of the study but fewer sons during the last years. Offspring sex was not related to laying order within a clutch, and the effect of social dominance on sex ratio was similar on eggs laid first, middle, or last. We investigated the effect of 2 factors (laying date and parental condition) that could have mediated the shift in the effect of social dominance on sex allocation in the course of the study. Laying date was positively associated with the proportion of males, but this effect was independent of social dominance. Maternal condition (residual mass over tarsus and egg volume) was related to social dominance but not to clutch sex ratio. Paternal condition (residual mass over tarsus) was not related to clutch sex ratio. We discuss how spatial or temporal variation in effects of variables such as social dominance on sex allocation can contribute to our understanding of the evolution of sex allocation in species with complex life histories.
Key words: body condition, corvidae, egg volume, resource holding potential, sex allocation.
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INTRODUCTION |
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Sex allocation theory predicts that parents should bias resource allocation toward the sex that yields the highest net fitness benefits (Trivers and Willard 1973
; Charnov 1982; Frank 1990). Parents can allocate resources differentially between sons and daughters in various ways. In birds, females may, for instance, vary the volume of their eggs and thereby the available resources depending on the sex of the embryo (Anderson et al. 1997; Magrath et al. 2003; Müller et al. 2005). Parents can also differentiate the amount (Nishiumi et al. 1996) or quality (Magrath et al. 2004) of food delivered to sons and daughters (Lessells et al. 1998). However, the most direct strategy to modify sex allocation is through adjustment of the primary sex ratio of offspring (Fisher 1930; Charnov 1982; Pike and Petrie 2003; Alonso-Alvarez 2006), and here, we focus on the latter variant of sex allocation in free-living jackdaws Corvus monedula.
Evidence for biased sex allocation in birds has accumulated in recent years (see Pike and Petrie 2003; Alonso-Alvarez 2006 for reviews). Most of these studies focus on specific life-history traits to explain observed differences in sex-biased resource allocation. For instance, in kestrels, offspring sex ratio (% males) was negatively related to laying date of the clutch (Dijkstra, Daan, et al. 1990). Other studies showed biased sex allocation in relation to maternal condition (Nager et al. 1999; Pike 2005), paternal quality, or attractiveness (Burley 1981; Svensson and Nilsson 1996; Pike and Petrie 2005b; Fawcett et al. 2007). In many species, the fitness prospects of offspring decline with laying order; thus, adjusting offspring sex would be particularly beneficial in the first eggs of a clutch. Indeed, such laying order-dependent biases in the level of sex ratio manipulation have been reported for many bird species (Weatherhead 1985; Dijkstra, Daan, et al. 1990; Albrecht 2000). Food availability has also been shown to affect sex allocation decisions in, for example, the kakapo Strigops habroptilus (Clout et al. 2002) and the Seychelles warbler Acrocephalus sechellensis (Komdeur 1996).
In social animals, groups are usually structured in the sense that when there is a conflict, some individuals are consistently more successful at obtaining resources than others (Allee 1952; Drews 1993). Thus, if resource access or condition is important in determining optimal sex allocation, it is to be expected that social dominance is often associated with sex allocation. This hypothesis has been extensively studied in mammals (Clutton-Brock and Iason 1986; Brown and Silk 2002; Sheldon and West 2004) but has been little studied in birds. Moreover, to our best knowledge, the avian studies that investigated this hypothesis found no support for dominance-dependent sex allocation: domestic fowl, Gallus gallus (Leonard and Weatherhead 1996; Müller et al. 2002), peafowl, Pavo cristatus (Pike and Petrie 2005a), and black-capped chickadees, Poecile atricapilla (Ramsay and Ratcliffe 2003). However, in collared flycatchers, Ficedula albicollis, there is indirect evidence for an effect of social dominance on sex allocation because males with a large forehead patch are more successful in competition over nest-boxes (Qvarnström 1997), and females mated to such males produce more sons (Ellegren et al. 1996). Similarly, in great tits, Parus major, the size of the breast stripe is correlated with social dominance (Lemel and Wallin 1993), and there was a positive trend in the relation between breast stripe size and clutch sex ratio (Kolliker et al. 1999). Furthermore, paternal tarsus length, another correlate of resource holding potential in this species (Garnett 1981), was also related to brood sex ratio variation in the same species (Kolliker et al. 1999; Yamaguchi et al. 2004). However, in house sparrows, Passer domesticus, there is an effect of badge size on social dominance (Møller 1987), but no relation was found between male badge size and the number of sons and daughters produced (Husby et al. 2006).
Social dominance plays a major role in the life of jackdaws (Lorenz 1931). Being dominant provides primary access to nesting opportunities and food (Röell 1978) and also affects breeding success (Henderson and Hart 1995; Verhulst and Salomons 2004). Jackdaws are moderately sexually size dimorphic at fledging, with males being 5–10% larger than females (Salomons HM, Dijkstra C, Verhulst S, unpublished data), indicating that higher costs are involved in producing male offspring. When one sex is more costly to produce than the other, this indicates that the relationship between parental investment and fitness benefits differs between sons and daughters. The details of these relationships have to be known to predict the optimal sex allocation in response to variation in resource access (Leimar 1996; Komdeur and Pen 2002), but the moderate sexual size dimorphism in itself increases the likelihood that the optimal sex allocation depends on parental resource access. We therefore investigated clutch sex ratio in relation to social dominance for 6 years in colonial jackdaws.
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METHODS |
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Study population
We studied free-living jackdaws in the colony at the Zoological Laboratory in Haren (The Netherlands), a semiurban environment. The data reported in this paper were collected in 6 years in the period from 1997 to 2005. Data on hatchling sex were not available for 1999, 2002, and 2003.
Nest-boxes were checked daily, starting in the first week of April, until the clutch was complete, and eggs were numbered with a felt tip pen. To determine from which egg a chick had hatched, clutches were moved to an incubator 1–2 days before the estimated hatching date (temperature 37.7 °C, humidity 75%). Clutches were exchanged for hard-boiled quail eggs, which were readily accepted and incubated by the jackdaws. Length and width of the eggs were measured to the nearest 0.1 mm, and egg volume (V, in cubic centimeter) was estimated using the formula: V = 
A2 L K/6, where A is width, L is length, and for jackdaws K = 0.00096 (Soler 1988). Eggs in the incubator were checked at least every 2 h during daytime (from dawn until dusk), and hatchlings were immediately placed in the nest and quail eggs were simultaneously removed. It is unlikely that using an incubator affected hatching success as the eggs were only in the incubator for the last 1–2 days of the total incubation period (±18 days) (Salomons et al. 2006). Before being placed in a nest, the hatchlings were weighed and a blood sample (10–20 µL) was taken by clipping the tip of a toenail for sexing and future DNA analysis. The clipping of a nail does not interfere with nestling growth. The clipped nail is identifiable by a blunt tip up to fledging, and we used this to identify the chicks within broods.
The survival of the chicks in the nest was checked every 5 days (hatch date of the first egg = day 1). At day 10, 20, and 30, the chicks were also weighed, and tarsus and wing lengths (day 20 and day 30) were measured. At day 30, shortly before fledging, the chicks were ringed.
Breeding birds were individually marked with color rings and a metal numbered ring. Birds were caught before the breeding season in a large baited cage or in their nest-box using trap doors before or during breeding. Early in the nestling period (day 5), a sample of adults was captured in 1998, and most breeding birds were captured at that stage in 2000, 2001, 2004, and 2005. Biometric characteristics (tarsus and wing length, mass) were measured, a small blood sample was taken for DNA using puncture of the brachial vein, and as a rule birds were released within 20 min after capture.
Sex determination
Sex was determined by polymerase chain reaction analysis of blood samples (Griffiths et al. 1998). The reliability of this method was confirmed using adult birds of known sex (N > 50). All unhatched eggs were checked for embryos (except for 1997). In total, 35 embryos were recovered, of which we were able to sex 32 (91%). Sex ratio among unhatched embryos was female biased (21 females and 11 males); however, this bias was not significant (binomial test: P = 0.1). In all sex ratio analyses, the hatchlings and unhatched embryos were pooled.
Dominance
Agonistic interactions were recorded during March and the first half of April in 1998, 2000, 2004, and 2005 until the first egg in the colony was laid. To stage conflicts, food was offered in small pits (internal diameter 10 cm) approximately 10 m from the nearest nest-box. For further details, see Verhulst and Salomons (2004).
The success in agonistic interactions of an individual bird was calculated using "David's score" (David 1987; Gammell et al. 2003). This equation takes both the proportion of interactions won and the proportion of individual birds supplanted into account (other methods to calculate rank from these data yielded almost identical results). Based on the success score, a rank number was assigned to each bird. For each year, we then scaled rank between 0 and 1 (most and least dominant male, respectively) because the number of birds in the hierarchy differed slightly between years.
Male jackdaws are dominant over females, and the females‘ success in conflicts is highly dependent on the rank and proximity of her partner (Lorenz 1931; Röell 1978; Wechsler 1988). Consequently, we cannot determine female rank independently and used the rank of the male to characterize the pair.
In 1997 and 2001, insufficient data on social status were collected to assign dominance ranks. Because the hierarchy within the colony was highly stable over several years (Röell 1978; Verhulst and Salomons 2004; Salomons et al. unpublished data), we used the dominance rank recorded in 1998 for 1997 and the dominance rank observed in 2000 for 2001. Note that insofar we erred in assigning dominance rank in this way, this makes statistical tests of the effect of dominance on sex ratio and other traits more conservative.
Statistical analysis
A number of individuals were sampled in multiple years, and different breeding attempts from the same individuals cannot be considered as independent samples. To avoid pseudoreplication, we analyzed the data with a repeated-measures hierarchical linear model, using the program MlwiN (version 2.02) (Rasbash et al. 2005). We used identity of the mother and breeding attempt (nested within mother) as random effects. Binary data (offspring sex) were transformed by the logit link function and analyzed, assuming a binomial error distribution on the individual level. Statistical significance of variables was assessed from the increase in deviance (
Dev) when the variable was removed from the model. The change in deviance is asymptotically distributed as chi square (
2) with corresponding change in degrees of freedom (df) (Snijders and Bosker 1999).
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RESULTS |
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Overall sex ratio for the 6 years combined did not deviate significantly from 50% (51.3% males, N = 489, and binomial test P > 0.05), and the clutch sex ratio distribution did not differ significantly from a random binomial distribution with Pmale = 0.5 (
2 = 32.4, df = 26, and P = 0.18). However, the overall sex ratio differed significantly between years (Figure 1; Dev = 16.35, df = 5, and P = 0.005). The subset of birds of which the dominance rank was known (68%) showed the same pattern, although due to the reduction in sample size, the difference between years did not quite reach significance (Figure 1; Dev = 8.55, df = 5, and P = 0.1).
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Social dominance was related to sex ratio (Figure 2), but the direction of this correlation varied significantly between years (Table 1). To explore the cause of the variation between years, it is useful to first identify in more detail which (groups of) years were similar to each other and which (groups of) years differed from each other. Based on the slope of the relation between dominance rank and sex ratio in the different years (Table 1), we created a model with either 2 year groups (group 1: 1997, 1998, 2000, and 2001; group 2: 2004 and 2005) or 3 year groups (group 1: 1997 and 1998; group 2: 2000 and 2001; group 3: 2004 and 2005). We tested these models against the original model (all years separate) using the Akaike information criterion. The model with 2 year groups emerged as the best fitting model (Figure 3 and Table 1); more complicated models did not yield a significant increase in the explained variation. This was further confirmed by the finding that within the 2 year groups the slopes did not differ significantly between years. In both year groups, the slope of the relation between social dominance and brood sex ratio was significantly different from 0 (group 1:
Dev = 4.508, df = 1, and P = 0.03; group 2: Dev = 4.830, df = 1, and P = 0.03). These results did not change; for example, the slopes are almost identical (Table 1, model D), when data from 1997 and 2001 (in which dominance was not measured directly) were removed from the analysis.
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In many avian species, chick survival probability decreases with laying order (Dijkstra, Bult, et al. 1990
; e.g., Badyaev et al. 2002), and this pattern is also evident in jackdaws (Gibbons 1987). When sex ratio adjustment is costly, it is to be expected that such adjustment is most pronounced in eggs early in the laying order because the potential benefits will be highest for eggs laid early in the clutch. Analyses of effects of laying order are complicated by variation in clutch size (should the third egg of a 3-egg clutch be compared with the third or the fifth egg of a 5-egg clutch?). We chose to assign eggs to 1 of 3 categories: first egg, last egg, and all "middle" eggs. The sex of a chick was independent of laying order (N = 489, Dev = 1.67, df = 2, and P = 0.43). More importantly, we found no interaction between social dominance and laying order in relation to offspring sex in either of the year groups (1997–2001, N = 247, Dev = 1.90, df = 2, and P = 0.39; 2004–2005, N = 85, Dev = 0.13, df = 2, and P = 0.94; Figure 4). Thus, we conclude that the effect of social dominance on sex ratio was equally strong in all eggs of a clutch.
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To investigate the cause of the change in slope from the first to the second year group, we first tested whether the change was present within individuals or, alternatively, could be explained by a change in colony composition over time. There are 9 individual females for which information on sex ratio and pair dominance rank was available for both year groups. Unfortunately, this subsample was too small to allow for a reliable analysis using (binomial) hierarchical linear models. Therefore, we calculated the expected change in clutch sex ratio, based on our regression model (Table 1, model C), for these individuals from the first year group to the second year group, taking into account the (generally small) changes in dominance rank, and plotted the expected change against the observed change in clutch sex ratio. If the change in slope between year groups (Figure 3) was due to changes in population composition, we would expect no correlation between predicted and observed change in sex ratio. In contrast, if the change in slope between year groups was due to some environmental effect on the whole colony, we would expect a correlation between observed and expected change in sex ratio with a slope of 1. The slope of the regression line was indeed very close to 1 (slope = 0.84; Figure 5), suggesting that the observed change in the relation between social dominance and clutch sex ratio over time also occurred within individuals, although it should be noted that, perhaps due to the small sample size, the relationship did not reach significance (r9 = 0.53, P = 0.1). Nevertheless, because the slope of the relationship between observed and expected change was approximately 1, we consider a temporal change in the environment as opposed to a change in the population composition, the most parsimonious explanation for the change in slope between year groups.
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Given that this change in the relationship between social dominance and sex ratio indeed occurred within individuals, this implies that there was another mediating factor affecting sex ratio, which interacted with social dominance and has changed over time. Based on the literature, we selected 2 factors that were repeatedly shown to be associated with clutch sex ratio, namely parental condition (Nager et al. 1999
; Pike 2005) and laying date (Dijkstra, Daan, et al. 1990; Arnold and Griffiths 2003). We used body mass (residual of regression of mass on tarsus [Dev = 62.1, P < 0.001]) as an index of parental condition and retained tarsus in the model as index of body size. Neither male residual mass nor female residual mass measured during the breeding season (when nestlings were 5 days old) was correlated with clutch sex ratio (Table 2). The same (lack of) result emerged when we tested the effects of residual mass measured before the breeding season (data available for 2004 and 2005 only; Table 2). For neither measurement was there a significant interaction with year or year group. As a second estimate of parental (maternal) condition, we used egg volume, which was previously shown to be correlated with female condition and subsequent reproductive success (Verhulst and Salomons 2004). There was no difference in the size of an egg containing a male or a female embryo (males: 10.52 cm3 [±0.08] and females: 10.65 cm3 [±0.08]; for statistics see Table 2), and clutch sex ratio was not correlated with mean clutch egg volume. Females high in social rank laid smaller eggs in all years of this study, and there was no significant interaction between social dominance and year group (Table 2).
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Sex ratio increased significantly with laying date (N = 489 chicks,
Dev = 4.0, df = 1, and P < 0.05). However, visual inspection of the regression results (Figure 6) showed that this effect was present in 1 year only (2000), whereas sex ratio was largely independent of laying date in the other years. This difference in the effect of laying date on sex ratio in 2000 compared with the other years combined was significant (N = 489 chicks, Dev = 7.0, df = 1, and P < 0.01). There was no correlation between social dominance and laying date and no significant interaction between social dominance and year group.
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DISCUSSION |
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Effects of social dominance on sex allocation have repeatedly been demonstrated in mammals, and we provide what is to our knowledge the first direct evidence for dominance-dependent sex allocation in birds. Social dominance (Henderson and Hart 1995
; Verhulst and Salomons 2004) and sex allocation (Arnold and Griffiths 2003) are both important components in the life history of jackdaws, and therefore, it was not unexpected that these were related. However, the effect was very strong when compared with most avian sex ratio studies (West and Sheldon 2002), with a sex ratio difference of 30–40% between the most and least dominant pairs (Figure 3). What was further surprising was that there was a dramatic shift in the effect of social dominance on sex allocation in the course of the study (Figure 3). In the first 4 years, social dominance was positively related to the proportion of sons, in agreement with the pattern generally found in mammals. However, in the last 2 years, the relationship was reversed, with high-ranked jackdaws producing more daughters and low ranking birds producing more sons. Thus, we conclude that social dominance has a strong effect on sex allocation in jackdaws but that the direction of this effect is variable.
Spatial or temporal variation in sex allocation in relation to a trait such as social dominance is difficult to detect. Nevertheless, there are other examples of studies showing spatial or temporal variation in sex allocation patterns. For example, significant interactions between year and ultraviolet coloration in relation to sex ratio variation have been reported for blue tits (Griffith et al. 2003; Korsten et al. 2006), and variation in sex allocation patterns between different populations have been reported for house finches (Badyaev et al. 2002) and red deer (Kruuk et al. 1999). Although explanations for these kinds of variations are mostly absent, and some authors themselves even suggest methodical instead of biological causes, such studies, nevertheless, illustrate that sex allocation can be a subtle process and also that data sets will need to cover a substantial amount of temporal and/or spatial variation to fully capture the sex allocation strategies employed.
To study the shift in the relation between social dominance and brood sex ratio between years more closely, we checked whether this effect was also found within individuals. Data from a subset of individuals that produced offspring in both year groups provided suggestive evidence that the relation between social dominance and sex ratio changed within individuals (Figure 5). Consequently, it is unlikely that our results were caused by a change in colony composition. This implies that there is at least one other factor that affects sex allocation and its relation to social dominance.
The main criterion that this unknown factor should fulfill is that it should be related to sex ratio and social dominance and that the relation with social dominance differed between the 2 year groups. We tested 2 candidates: laying date and parental condition. Laying date was recently shown to correlate with clutch sex ratio in jackdaws, with later clutches containing progressively fewer sons (Arnold and Griffiths 2003). Surprisingly, the jackdaws in our population showed the opposite pattern, with broods produced late in the season containing on average more sons, although this effect was largely due to 1 year (Figure 6). More important in the present context is that laying date was not related to social dominance in either year group or overall, and there was no interaction between social dominance and year group with respect to laying date. Thus, we conclude that the shift in effect of social dominance on clutch sex ratio was not mediated by effects of timing of breeding.
The second candidate was parental condition. Previously, it was shown in the same colony that social dominance negatively affected female condition during the breeding season of 1998 and 2000 (Verhulst and Salomons 2004). This was reflected in both a lower body condition (residual mass over tarsus) at day 5 of the chick stage and in the smaller size of the eggs laid by females that were paired to dominant males. Analyses of the larger data set now available confirmed these earlier findings but found no evidence for a significant interaction between social dominance and year group on maternal condition. Furthermore, when using residual body mass and egg volume as indices of female and male condition, we found no evidence for condition-dependent sex ratio in our study. We conclude, therefore, that the shift in effect of social dominance on clutch sex ratio was not mediated by (our measures of) parental condition.
An alternative explanation is that the relation between brood sex ratio and social dominance, and the observed shift in this relationship, is mediated by maternal hormones, which are in turn affected by environmental changes. Both testosterone and corticosterone make good candidates for such mediating effects. The relation between social dominance and testosterone has been shown to interact with the environment (i.e., population density and stability of the social hierarchy; Schwabl 1997; Rogovin et al. 2003), whereas corticosterone level is known to depend on stress and body condition (Kitaysky et al. 1999; Cyr and Romero 2007). Furthermore, broods produced by females with high levels of testosterone were found to be male biased in Japanese quail (Pike and Petrie 2005a), and experimentally increased maternal levels of testosterone resulted in an increase in brood sex ratio in the zebra finch and the spotless starling (Veiga et al. 2004; Rutkowska and Cichon 2006) but not in Japanese quail (Pike and Petrie 2006). Similarly, corticosterone has been shown to reduce brood sex ratio in peafowl and Japanese quail (Pike and Petrie 2005a, 2006). Unfortunately, we have not yet measured hormone levels in this study. The number of breeding pairs, however, has slightly decreased in recent years, suggesting that relevant environmental circumstances (e.g., breeding density) have changed. Indeed, there was a trend that the number of breeding pairs is correlated with the slope of the relation between social dominance and brood sex ratio (rs = 0.64, n = 6, and P = 0.054). We will gather more data on this because the sample size is at present too low to allow firm conclusions.
We attempted to understand the shift in effect of social dominance on clutch sex ratio from a mechanistic perspective (Hogan 2005) by investigating correlations of clutch sex ratio with factors known to affect sex allocation in other species. Alternatively, one could analyze how the fitness prospects depend on clutch sex ratio for birds with different social dominance, which could yield an understanding of the observed shift from a functional perspective (Cuthill 2005). However, life histories of birds and mammals are often very complex, making it difficult to derive predictions regarding the optimal sex ratio with confidence (Komdeur and Pen 2002; West et al. 2002). In this context, spatial or temporal variation in the effect of a trait on clutch sex ratio as found in this study may be an asset because it creates the opportunity to make multiple comparisons between predictions and observations within 1 study system. Furthermore, predictions regarding temporal or spatial differences in sex allocation within study systems are likely to be more accurate than predictions for single values because one can reasonably hope that inaccuracies in parameter values will affect all estimates in the same way (provided there are no strong interactions with these parameters). Nonetheless, the cause of the shift in the effect of social dominance on sex ratio in this study remains an open question at present, and the number of study years will probably have to increase before this can be resolved.
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FUNDING |
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H.M.S. and S.V. were supported by a Vici grant from the Netherlands Organisation for Scientific Research to S.V.
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ACKNOWLEDGEMENTS |
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Guido Meeuwissen and Ellis Mulder helped sexing the birds, Peter Visser measured dominance in 1998 and comments from 2 anonymous reviewers improved the manuscript. Work reported in this paper was carried out under licenses from the Ethical Committee for animal experiments of the University of Groningen (license numbers 2496, 2501, 2698, 4071).
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