Behavioral Ecology Advance Access originally published online on January 8, 2007
Behavioral Ecology 2007 18(2):420-426; doi:10.1093/beheco/arl100
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Is hatching asynchrony beneficial for the brood?
siBehavioural Ecology Group, Department of Systematic Zoology and Ecology, Eötvös Loránd University, H-1117, Pázmány Péter sétány 1/C, Budapest, Hungary
Address correspondence to E. Szöllsi. E-mail: sz_eszter{at}ludens.elte.hu.
Received 21 August 2006; revised 28 November 2006; accepted 29 November 2006.
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ABSTRACT |
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Many hypotheses have been proposed to explain why female birds start to incubate before clutch completion (IBCC). Some of those suggest that the resulting hatching asynchrony (HA) is adaptive because it increases the size hierarchy among offspring and in turn reduces nestling competition and energy demands during the peak feeding period. Others argue that IBCC is a good strategy in unpredictable environments. When food conditions deteriorate, the large size hierarchy quickly results in the death of the last hatched nestlings, allowing the remaining ones to survive and fledge in better condition. In comparison, under favorable conditions, all nestlings can fledge independent of hatching order. To test these hypotheses, we performed a brood size manipulation experiment (as a simulation of good and bad years) in collared flycatchers Ficedula albicollis and examined the effect of size hierarchy on offspring and brood performance. We found that chicks with an initial size disadvantage experienced reduced body mass growth and had shorter feathers at fledging in both reduced and enlarged broods. In enlarged broods, they also fledged with a smaller skeletal size. Although broods on average or parents could possibly still benefit from HA when food is scarce, this was not seen in the current study. Parental survival was not related to the size hierarchy in the broods, and the average body mass growth of the nestlings was slower in broods with a high initial size variance. We therefore conclude that HA and the resulting size hierarchy are probably detrimental for the growth of nestlings in both good and bad years, at least in species where nestling mortality does not occur early in life.
Key words: collared flycatcher, fledging size, food supply, maternal effects, nestling growth, size hierarchy.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Females in many bird species start to incubate their eggs before clutch completion (IBCC). This results in hatching asynchrony (HA) and in turn a pronounced size hierarchy among nestlings. Many hypotheses have been proposed to explain the adaptive function of this phenomenon (reviewed in Nilsson 1993
; Stenning 1996). A large group of the explanations suggests that it is the established size hierarchy that increases the fitness of the parents and at least some of the offspring. The brood-reduction hypothesis (Lack 1954), for example, predicts that HA is advantageous in unpredictable environments. When food is abundant, all nestlings can fledge independent of hatching order. However, in cases of food shortage, older nestlings outcompete their younger siblings and, consequently, younger ones might quickly starve to death. By sacrificing the smallest nestlings, the rest of the brood can survive and fledge in better condition. This confers benefits both to the surviving young and the parents because fledglings in better condition might survive better (Pettifor et al. 2001) and therefore increase the fitness of their parents more than fledglings in poorer condition.
The sibling rivalry reduction hypothesis (Hahn 1981) predicts that in broods with an established size hierarchy among nestlings, sibling competition and thus energy expenditure of the nestlings are reduced. This results in faster growth or better body condition than in synchronous broods. Furthermore, the pronounced age hierarchy among siblings may reduce the peak energetic costs of the parents when feeding their young because nestlings reach their maximum growth rate and thus the highest food demand at different times (peak load reduction hypothesis: Hussell 1972).
Another group of the hypotheses argues that HA is only a by-product of IBCC, which is adaptive for reasons other than establishing sibling size asymmetry. If there is heavy nest predation or food resources are strongly declining during the chick-rearing period, IBCC can shorten the average time offspring spend in the nest (i.e., the combined length of the egg and nestling phase). Thus, females can reduce the risk of predation on their broods and prevent starvation at least of those nestlings which hatch and thus fledge earlier (hurry-up hypothesis: Hussell 1972; nest-failure hypothesis: Clark and Wilson 1981). According to the egg-viability hypothesis (Arnold et al. 1987; Veiga 1992), females start to incubate before completing their clutches in order to protect the hatchability of their eggs because the viability of unincubated eggs may decline with time.
When looking specifically at the effects of HA on the last hatched nestlings, it is often found that the size handicap with which these nestlings start their life results in disadvantages when competing for food (Ostreiher 1997; Pettifor et al. 2001). Thus, they might fledge with a smaller weight (Cotton et al. 1999; Clotfelter et al. 2000) and experience a lower survival probability later in life (Oddie 2000). Therefore in species where size asymmetry among siblings is only a by-product of earlier onset of incubation, we might expect the parents to compensate for the detrimental effects of HA. Indeed, in several species with asynchronous hatching, females lay larger eggs at the end of the laying sequence (Howe 1976; Hillström 1999; Rutkowska and Cicho
2005) or invest more testosterone into the last eggs to increase the rate of development (Schwabl 1996; Eising et al. 2001) and the competitive ability of the last hatched chicks (Schwabl 1993; Lipar and Ketterson 2000).
In our study species, the collared flycatcher Ficedula albicollis, previous studies have found successful compensation in terms of egg size for the detrimental effects of HA (Rosivall et al. 2005). However, egg volume increased with laying order only in years with a warm prelaying period, whereas in colder years, there was no such relationship (Hargitai et al. 2005). Because ambient temperature affects the availability of insect prey in general (Taylor 1963; Bryant 1975), and prelaying temperature was positively correlated with the food abundance during the nestling period in the study population (Spearman rank correlation: N = 6, R = 0.89, P = 0.019), we refer to warm and cold years as good and bad quality years, respectively.
Two explanations arise for the difference in the egg size pattern between good and bad years. First, females follow different strategies when they allocate nutrients into the eggs. This is because the adaptive value of size hierarchy differs between good and bad years with sibling size asymmetry being detrimental in good years but advantageous or neutral in bad years. Second, although compensation for HA would be beneficial independent of year type, because of energetic constraints during egg laying (i.e., less food is available) females are simply not able to lay larger eggs at the end of the laying sequence in poor years. To test the first hypothesis, we altered the rearing conditions of the chicks by conducting a brood size manipulation experiment and measuring the effects of size hierarchy on nestling growth, fledging size, and parental survival. Earlier studies have shown that though parents are to some extent able to adjust their provisioning rate according to the altered demand of their brood, which results in a change in workload, brood size manipulations can successfully alter the feeding rate to individual nestlings (for collared flycatchers see: Török and Tóth 1990; for other bird species see: e.g., Cronmiller and Thompson 1980; Nur 1984; Martins and Wright 1993) and change the level of nestling competition (Neuenschwander et al. 2003). Thus, enlarged and reduced broods have already been used to simulate years with bad and good food supply, respectively, for example, by Merilä (1996) and Råberg et al. (2005).
If the strategy of the females differs between good and bad quality years (first hypothesis), we would expect that HA and the resulting size hierarchy are either advantageous or have no effect on the fitness of the parents rearing enlarged broods (i.e., females did not compensate for HA in poor years [Hargitai et al. 2005]; see Table 1). The benefits could arise through the reduced peak load of the parents or decreased nestling competition (see above) that might have an important role under severe conditions. On the other hand, we expect that HA has negative effects on parental fitness in reduced broods, as in previous studies HA was compensated for in good years (Hargitai et al. 2005; Rosivall et al. 2005). In cases of good food supply, maximum parental workload may not be an issue, and females may prefer to decrease the detrimental effects of HA on the growth of the last hatched young (Rosivall et al. 2005). However, HA is expected to have negative effects on both enlarged and reduced broods if the lack of maternal compensation in poor years is only due to energetic constraints imposed on females during egg laying (second hypothesis; Table 1).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study species and field methods
The study was conducted in an artificial nest-box plot in the Pilis Mountains, Hungary (47°43'N, 19°01'E) in 2004. The study plot is part of a continuous, unmanaged, oak-dominated woodland, a protected area of Duna-Ipoly National Park. The collared flycatcher is a small hole-nesting, long-distance migratory passerine. Its breeding season starts in the middle of April, and females usually lay 5–7 eggs. The incubation period is about 12–13 days; nestlings hatch in a range from 12 to 44 h (mean ± standard error [SE] = 27.08 ± 1.32; Rosivall et al. 2005
) and fledge 14–15 days after hatching.
Altogether, we studied 48 broods with the most common brood size being of 6 or 7 nestlings. Because the offspring of subadult and adult males might grow at a different rate (Hegyi et al. 2006), we only studied broods of adult males. One brood that was predated on day 4 was excluded from the analyses as were those broods that were secondary broods of polygynous males or reared by only one parent. The remaining 43 nests were retained for the analyses. To exclude the possible confounding seasonal effects on nestling growth, the nests were selected so that the first egg was laid within an 8-day interval, and pairs of enlarged and reduced broods with the same hatching date were created. The original brood size of the brood pairs was the same in all but one case (in this case, the difference was one chick between the 2 broods). We partially cross-fostered broods 2 days after hatching so that 4 chicks were moved from nest A to nest B and 2 chicks were moved from nest B to nest A. As a result, we had enlarged (+2 chicks) and reduced (–2 chicks) broods consisting of approximately equal numbers of their own and foster chicks that were selected randomly with respect to their size.
Each nestling was weighed on the day of swapping and marked individually by clipping tufts of down on its head and back. Body mass of the nestlings was measured from day 2 (day 0 = hatching date of the first chick) and the length of the third outer primary from day 8 (to the nearest 0.1 g and 0.5 mm, respectively) and on every second day until day 14. On day 14, tarsus length was also measured (to the nearest 0.1 mm).
Data analysis
We analyzed nestling growth and fledging size data both at the individual and brood levels in order to estimate the effect of HA and brood size manipulation on both the individual nestlings and the parental fitness.
In a data set collected in a previous study (for field methods, see Rosivall et al. 2005), it was found that the extent of HA in a brood was correlated with the coefficient of variation (CV) of the 2-day body mass when controlled for year (using general linear model (GLM): F = 18.84, degrees of freedom [df] = 1,38, P < 0.001). Similarly, the hatching time of an individual nestling (i.e., the time elapsed between the first hatching in the given brood and the hatching of the chick in question) was correlated with the corrected deviation (CD) of nestling body mass from the brood mean (CD = (a – 
)/, where = mean body mass of the brood on day 2, a = the 2-day body mass of the chick in question; using GLM: F = 468.36, df = 1,212, P < 0.001). Therefore, in the present study, we did not directly measure HA but used CV ("size variation" later on) and CD ("relative size" later on) to estimate the effect of HA on nestling performance at the brood and individual level, respectively.
In the individual-level analyses, we used general linear mixed models including manipulation category (i.e., enlarged or reduced) as a factor, relative size as a covariate, and the interaction of these terms. Original and rearing broods were also included as random factors. Dependent variables were wing feather length (the length of the third outer primary), body mass and tarsus length on day 14, and wing feather growth rate. The growth of the primaries was linear so we calculated the slope of a linear regression for each nestling to describe feather growth rate (Nilsson and Svensson 1996) between day 8 and day 12. Body mass growth was analyzed by entering the body mass data between day 2 and day 12 into the model as a dependent variable while using age as a repeated measure variable. The interaction of explanatory variables with age indicates an effect on nestling growth. The covariance structure of the model was selected on the basis of the Akaike information criterion values (Burnham and Anderson 1998).
In the brood-level analyses, we used general linear models including the brood means of nestling size and feather growth rate as dependent variables, manipulation category as a factor, size variation as a covariate, and the interaction of these terms. When analyzing body mass growth, we entered the brood means of body mass between day 2 and day 12 into the model as dependent variable and used age as a repeated measure variable. Similar analyses were performed for the mean value of the 2 largest chicks in the broods in order to estimate the effect of the explanatory variables specifically on the nestlings with a competitive advantage. The 2 largest chicks were the chicks that weighed the most on day 2.
After the analyses of our initial models, we performed a stepwise backward deletion of nonsignificant terms. All analyses were performed using the Mixed Procedure of SAS 8.02 (SAS Institute, Cary, NC).
Two broods were predated after day 12, 6 nestlings had already fledged before the final measurements were taken, and some measurements were occasionally missing, therefore sample sizes varied among analyses. Nestlings that died (6 out of 162 and 2 out of 110 in enlarged and reduced broods, respectively) were excluded from the analyses. Brood means were calculated for the rest of the chicks in the brood.
The 2 manipulation categories did not differ in terms of the size difference between the largest and smallest chicks in the broods on day 2 (t41 = –0.69, P = 0.496). The average difference was 1.44 ± 0.13 and 1.30 ± 0.02 g (mean ± SE in enlarged and reduced broods, respectively), which corresponds to a hatching span of 30.65 and 29.22 h, respectively (the HA estimate is based on data from our earlier study on HA in this species [Rosivall et al. 2005]; equation of the linear regression HA = 16.04 + 10.16 x mass2dmax – min, where mass2dmax – min is the mass difference between the heaviest and the lightest chick at 2 days of age).
We also analyzed the effect of manipulation and the estimated HA on the survival of the parents. Because of the high site fidelity of breeding individuals (Könczey et al. 1992), we considered those individuals that were recaptured in 2 years after the experiment as survivors, whereas nonrecaptured birds as nonsurvivors. Survival was analyzed using generalized linear models with binomial error and logit link including manipulation category as a factor, size variation as a covariate, and the interaction of these terms. Because the dispersion parameter was larger than 1.0, we tested the significance of the parameters with an F-test (Crawley 1993); d-scale option was used in SAS 8.2.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Growth and fledging size of individual nestlings
To investigate the possible fitness consequences of nestling size hierarchy under different rearing conditions, we analyzed the effects of relative size of nestlings and brood size manipulation on body mass and feather growth rate and fledging sizes of the nestlings. The overall effects of these 2 variables and the interaction term were significant for all growth and fledging size parameters (Tables 2 and 3). Separate analyses of enlarged and reduced broods showed that initially smaller nestlings experienced slower body mass growth and smaller wing feather length at fledging in both manipulation categories (all P < 0.001; Figures 1a and 2b) with the disadvantage being larger in enlarged broods. However, feather growth rate, as well as the tarsus length and body mass of fledglings, was affected only in enlarged broods (enlarged broods: all P < 0.006, reduced broods: all P > 0.548; Figure 2a,c).
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Average performance of the broods and survival of the parents
With respect to parental fitness, brood performance may have a more important role than that of the individual nestlings. Therefore, we performed similar analyses as above to evaluate the effects of estimated HA on average nestling growth and fledgling size. We also analyzed how brood size manipulation and the magnitude of HA affected the survival of the parents.
Brood enlargement had an overall negative effect on body mass and feather growth rate and also on all measures of fledgling size (all P < 0.019). However, estimated hatching span of the brood affected only the average mass growth so that a higher initial size variation resulted in slower body mass growth (Figure 1b, Table 4). Neither initial size variation of the brood (for females P = 0.908, for males P = 0.110) nor brood size manipulation (for females P = 0.259, for males P = 0.105) affected survival of the parents.
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Average growth and fledging size of the initially heaviest chicks
According to some of the hypotheses proposed to explain the function of HA, it is also possible that the size hierarchy in the broods is beneficial only for nestlings with a competitive advantage. Therefore, we aimed to examine the effect of HA on nestlings with a higher rank in the size hierarchy.
We found that body mass and wing feathers of the 2 largest chicks grew slower in enlarged broods than in reduced broods (for feather growth rate: F = 19.55, df = 1,41, P < 0.001; for body mass growth: see Table 4), whereas brood size manipulation had no effect on the fledging sizes of these nestlings (all P > 0.402). The estimated HA did not affect any of the growth and fledging size parameters (all P > 0.246).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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HA and the consequently established size hierarchy in the broods may have a pronounced effect on nestling growth (Cotton et al. 1999
; Clotfelter et al. 2000) and survival (Forbes et al. 1997; Krebs 1999; Viñuela 2000). Therefore, it is not surprising that many hypotheses have been proposed to explain why females start the IBCC that leads to HA in the broods. These hypotheses can be divided into 2 groups according to whether the established size hierarchy is considered to be adaptive or not (for reviews see Nilsson 1993; Stenning 1996).
We investigated the adaptive value of size hierarchy in collared flycatchers F. albicollis by measuring nestling performance and parental survival. Earlier studies on this species have found maternal compensation for HA in terms of egg size in good quality years (Hargitai et al. 2005; Rosivall et al. 2005) but not in poor years. Therefore, we assumed that the size hierarchy may have different effects on parental and offspring fitness depending on environmental conditions, so that the size hierarchy is adaptive or neutral in bad years but detrimental in good years.
However, in our brood size manipulation experiment, nestlings with a relatively smaller size early in life suffered from reduced performance in both treatment groups. They gained body mass more slowly and had shorter wing feathers before fledging. The negative effects of small initial size were even more pronounced in enlarged broods where even feather growth rate and fledgling size (body mass and tarsus length) were correlated with relative size on day 2. Despite these negative effects on individual nestlings, it is still possible that size hierarchy has beneficial effects at the brood level or for the parents. However, this study showed that average body mass growth of the brood was negatively affected by the initial size variation, and even nestlings with a competitive advantage did not benefit from HA.
We conclude that our results on nestling growth and fledgling size in the 2 treatment categories do not support the predictions of the sibling rivalry reduction hypothesis (Hahn 1981). This hypothesis assumes that in broods with an established size hierarchy, siblings experience less severe competition and can therefore allocate saved energy into their maintenance. As a result, they should experience a better growth rate or fledge in better condition than those in synchronous broods. We have to note that unlike in our species, reduction in sibling rivalry may have important consequences on the growth and survival prospects of the offspring in species with direct aggression among the nestlings (Mock and Ploger 1987; Hébert and McNeil 1999; Viñuela 1999).
The peak load reduction hypothesis (Hussell 1972) also predicts either the nestlings or the parents to benefit from a size hierarchy. This is because in situations of food shortage (poor years or enlarged broods), parents could more easily meet the requirements of their progeny if nestlings reach their maximum energy demand at different times. Thus, at least in the enlarged broods, nestlings in more asynchronous broods should have grown faster (because they should receive enough food during their rapid growing period) or parents should have had higher survival probability (because they could save time for foraging for themselves in the most demanding phase of chick rearing) than those in synchronous broods. However, parents did not benefit from the increased size variation in the broods because parental survival was independent of the estimated HA under both conditions (for similar results, see Stoleson and Beissinger 1997).
The brood-reduction hypothesis (Lack 1954) is probably not applicable in collared flycatchers because this hypothesis assumes that parents cannot predict the environment in which they will rear their offspring. In this case, we should have found similar investments into the eggs independent of the quality of the year. Furthermore, in this study nestling mortality was very low (altogether 6 out of 162 and 2 out of 110 nestlings died in enlarged and reduced broods, respectively) suggesting that direct aggression is weak between nestlings, disabling efficient brood reduction.
So we conclude that pronounced nestling size hierarchy is not beneficial in the collared flycatcher, and parents would benefit from a compensatory investment into the last laid eggs. Our results do show that this compensatory investment would be even more beneficial in poor years than it was found to be in good years. This is because asynchronous broods suffered more in enlarged than in reduced broods. That female collared flycatchers did not lay larger final eggs in cold years (Hargitai et al. 2005) suggests that they were not able to invest preferentially into those eggs. This was probably because of their poor energetic conditions due to ambient temperatures affecting both the size of insect populations and the activity of flying insects (Taylor 1963; Bryant 1975), thus the food availability to the parents.
Our results on the growth of the nestlings are in concordance with previous findings. In the marsh tit Parus palustris and the collared flycatcher, mass growth was found to be depressed in the last hatched nestlings as a consequence of HA (Nilsson and Svensson 1996; Nilsson and Gårdmark 2001; Rosivall et al. 2005). On the other hand, the disadvantage of those chicks did not manifest in low feather growth rates (Zach 1982; Nilsson and Svensson 1996). In the great tit Parus major, parents were found to preferentially feed already fledged young if these and their siblings in the nests were begging simultaneously (Lemel 1989). This suggested that the priority of feather growth to mass growth reflects the importance of synchronized fledging, which in turn may have effects on the survival prospects of the nestlings. Not surprisingly, we got similar results in experimentally simulated "good quality years," that is nestlings experiencing relatively smaller size early in life showed slower mass but not slower feather growth rates. However, small chicks in enlarged broods were not able to keep up with their siblings even in feather growth. In this manipulation category, small nestlings also experienced reduced mass growth and smaller size at fledging.
In summary, after our experimental manipulations, nestlings experiencing relatively smaller size early in life performed worse, especially in poor environmental conditions. In addition, neither the nestlings with a competitive advantage nor the parents benefited from large size variation in the brood. We therefore conclude that IBCC and HA are not beneficial for nestlings in the context of the resulting size hierarchy and suggest that females would benefit from compensating for HA irrespective of the quality of the current year.
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ACKNOWLEDGEMENTS |
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The comments of T.G.G. Groothuis, G. Hegyi, J.-Å. Nilsson, M.E. Hauber, and the anonymous referees considerably improved the manuscript. We are indebted to R. Hargitai, G. Hegyi, and M. Herényi for their help during the fieldwork and to D. Campbell for the linguistic revision. The study was supported by FKFP 0021/2002 to the Biology PhD school of Eötvös Loránd University, the Hungarian State Eötvös Fellowship to B.R., the Hungarian Scientific Research Fund (OTKA grant No. T049650) to J.T., Erd
k a Közjóért Alapítvány, and the Pilis Park Forestry. The present study complies with the current laws of Hungary. |
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