HATCHING ASYNCHRONY IN ALTRICIAL BIRDS

1. The review aims to provide a simple conceptual framework on which to place recent studies of hatching asynchrony in altricial birds and to assess the evidence used in support of specific hypotheses. 2. Hatching asynchrony arises bsecause parents start incubation before laying is complete, but the precision of parental control is largely unknown. 3. Hypothesses concerning the functional significance of hatching asynchrony fall into four broad types. Hatching asynchrony might: (i) arise because of selection on the timing of events during the nesting period; (ii) facilitate the adaptive reduction in brood size; (iii) increase the energetic efficiency of raising the brood, or (iv) result from environmental or phylogenetic constraints. 4. The incubation pattern could function to minimize the losses of eggs, nestlings or adults to predators (or climatic sources of mortality), particularly in species which cannot actively defend their nest. The best evidence comes from comparative studies of hatching asynchrony. Early incubation might also be favoured if the food supply declines sharply through the breeding season, although the evidence is weak and indirect, or if there is a risk of brood parasitism. In species in which only the female incubates, early incubation could ‘force’ the male to invest more in the nestlings, but this idea remains to be tested. Males may be constrained by the risk of cuckoldry to delay incubation until laying is complete. 5. Hatching asynchrony could be adaptive by enabling the efficient reduction of brood size if food proves short after hatching (primarily because of a shortage of food in the environment or possibly because of a large proportion of ‘expensive’ nestlings in the brood in species which are sexually dimorphic). Observational evidence is often consistent with this hypothesis but few experimental studies provide adequate tests. Brood reduction could be adaptive in species (primarily eagles and pelecaniformes) which lay an extra egg to act as insurance against hatching failure, and again hatching asynchrony might facilitate brood reduction, although there are few experimental tests on such species. Hatching asynchrony might also enable sex ratio manipulation through selective brood reduction, although there is as yet no clear supportive evidence. 6. Ins species in which young have a marked peak in energy demand during the period of parental care, hatching asynchrony can reduce the peak demand of the brood, which might allow the parents to raise more healthy young. In many species such savings are likely to be small or absent. There is some behavioural evidence that hatching asynchrony can reduce fighting amongst nestlings and therefore lead to the more efficient use of energy by the brood. In general this effect seems small and the only energetic study found no difference in the energy requirements of synchronous and asynchronous broods. Other possible energetic advantages to hatching asynchrony have not been tested. 7. Environmental conditions during laying can influence both egg size and laying interval in aerial insectivores, and might directly influence incubation in this and other groups. Thus some variation in hatching asynchrony and the relative size of siblings is probably non-adaptive. The variability of incubation pattern within and across species suggests that hatching asynchrony is not under strong phylogenetic constraint. 8. The hypotheses about the adaptive significance of hatching asynchrony are complementary rather than mutually exclusive: within a species, several selective pressures could influence the optimal incubation pattern, and the relative importance of selective pressures will differ among species. Furthermore one should expect that the incubation pattern and parent–offspring interactions will be coadapted to maximize brood productivity.     

Hatching Asynchrony Decreases the Magnitude of Parental Care in Domesticated Zebra Finches: Empirical Support for the Peak Load Reduction Hypothesis

Parent–offspring conflict over the supply of parental care results in offspring attempting to exert control using begging behaviours and parents attempting to exert control by manipulating brood sizes and hatching patterns. The peak load reduction hypothesis proposes that parents can exert control via hatching asynchrony, as the level of competition amongst siblings is determined by their age differences and not by their growth rates. Theoretically, this benefits the parents by reducing both the peak load of the offspring's demand and their overall demand for food and benefits the offspring by reducing the amplification of their competition. However, the peak load reduction hypothesis has only received mixed support. Here, we describe an experiment where we manipulated the hatching patterns of domesticated zebra finch Taeniopygia guttata broods and quantified patterns of nestling begging and parental feeding effort. There was no difference in the begging intensity of nestlings raised in asynchronous or experimentally synchronous broods, yet parental feeding effort was lower when provisioning asynchronous broods and particularly so when levels of nestling begging were low. Further, both parents acted in unison, as there was no evidence of parentally biased favouritism in relation to hatching pattern. Therefore, our study provided empirical support for the prediction that hatching asynchrony reduces the feeding effort of parents, thereby providing empirical support for the peak load reduction hypothesis.     

Asynchronous hatching in the laughing gull: Cutting losses and reducing rivalry

The adaptive significance of hatching asynchrony was investigated in the laughing gull (Larus atricilla). Staggered hatching of the brood is frequently correlated with reduced survival in the later-hatching chicks, and the phenomenon has therefore been the subject of speculation about adaptive function. The relative timing of hatching within the brood was experimentally manipulated in order to compare the effects of synchrony versus asynchrony on parental reproductive success. The average number of young fledging per nest was significantly higher in the asynchronous group. Staggered hatching of the brood is hypothesized to be a parental strategy offering the option of brood reduction under conditions of food shortage. The possibility is discussed that asynchronous hatching benefits parents independently by reducing sibling rivalry over parental investment and minimizing wasteful competition.     

Egg temperature and initial brood patch area determine hatching asynchrony in Magellanic penguin Spheniscus magellanicus

In birds, the adaptive significance of hatching asynchrony has been under debate for many years and the parental effects on hatching asynchrony have been largely assumed but not often tested. Some authors suggest that hatching asynchrony depends on the incubation onset and many factors have been shown to influence hatching asynchrony in different species. Our objective was to analyze the exact timing of the onset of incubation and if this affects hatching asynchrony; and, in addition, which other factors (brood patch development, incubation position, adult body condition, intra‐clutch egg dimorphism, laying date and year) affect hatching asynchrony in Magellanic penguins Spheniscus magellanicus. We first estimated the eggshell temperature at which embryo development starts, with a non‐destructive and novel method. We then recorded individual egg temperatures in 61 nests during incubation, and related them, and other breeding parameters, to hatching asynchrony. We also observed incubation positions in 307 nests. We found a significant positive relationship between hatching asynchrony and the temperature that the first‐laid egg experienced during egg laying and between hatching asynchrony and the initial brood patch area. We also found a negative relationship between hatching asynchrony and the difference in temperature between second and first‐laid eggs within a clutch, measured after the egg‐laying period was finished. We ruled out position of the eggs during incubation, adult body condition, egg volume, laying date, and study year as factors influencing hatching asynchrony. The egg temperature during laying and the difference in temperature between eggs of a clutch are determinants of hatching asynchrony in Magellanic penguins.     

Asynchronous hatching provides females with a means for increasing male care but incurs a cost by reducing offspring fitness

In species with biparental care, sexual conflict occurs because the benefit of care depends on the total amount of care provided by the two parents while the cost of care depends on each parent's own contribution. Asynchronous hatching may play a role in mediating the resolution of this conflict over parental care. The sexual conflict hypothesis for the evolution of asynchronous hatching suggests that females adjust hatching patterns in order to increase male parental effort relative to female effort. We tested this hypothesis in the burying beetle Nicrophorus vespilloides by setting up experimental broods with three different hatching patterns: synchronous, asynchronous and highly asynchronous broods. As predicted, we found that males provided care for longer in asynchronous broods whereas the opposite was true of females. However, we did not find any benefit to females of reducing their duration of care in terms of increased lifespan or reduced mass loss during breeding. We found substantial negative effects of hatching asynchrony on offspring fitness as larval mass was lower and fewer larvae survived to dispersal in highly asynchronous broods compared to synchronous or asynchronous broods. Our results suggest that, even though females can increase male parental effort by hatching their broods more asynchronously, females pay a substantial cost from doing so in terms of reducing offspring growth and survival. Thus, females should be under selection to produce a hatching pattern that provides the best possible trade‐off between the benefits of increased male parental effort and the costs due to reduced offspring fitness.     

Parental versus offspring control on food division within the brood: the role of hatching asynchrony

Using an individual-based simulation model we study how different mechanisms of food division among multiple offspring influence nestling number and quality, as well as parental effort. We consider the combination of different scenarios of food availability (feeding conditions), hatching asynchrony and food division. If parents have full control on how to divide food among offspring, asynchronous broods have higher breeding performance than synchronous ones in a wide range of feeding conditions, giving theoretical support to empirically proved benefits of hatching asynchrony. If parents accept the outcome of sibling competition there is a threshold in feeding conditions below which asynchronous broods produced more fledglings and the reverse was true above the threshold. Interestingly, parents relying on the outcome of nestling competition do not necessarily differ in breeding performance from those which have full control over food allocation. Our study combines hatching asynchrony, provisioning behaviour of parents, jostling behaviour of nestlings and feeding conditions as a network of interacting processes of enormous interest to fully understand the parent–offspring conflict.     

Overproduction in the Lesser Black‐backed Gull – can marginal chicks overcome the initial handicap of hatching asynchrony?

In response to unpredictability of both food availability and core offspring failure, parents of many avian species initially produce more offspring than they commonly rear (overproduction). When parental investment is insufficient to raise the whole brood the handicap of hatching last means ‘marginal’ chicks are less likely to survive if brood reduction occurs. Conversely, if marginal offspring are required as replacements for failed ‘core’ chicks, or parental investment is sufficient to rear the whole brood, the handicap imposed on marginal chicks must be reversible if overproduction is to be a viable strategy. I investigated the ability of marginal offspring to overcome the handicap imposed by hatching asynchrony using a combination of a field experiment, designed to manipulate both the amount of total competition and the relative competitive ability of chicks within a brood, and data on the growth and survival of unmanipulated, three‐chick broods from three consecutive years. The results indicate that, even when resources are abundant, marginal offspring do not begin to overcome the competitive handicap imposed by hatching asynchrony until the period of growth when energetic requirements reach their peak, and subsequent survival to fledging is almost assured. This is apparently a consequence of parents controlling allocation of early parental investment, so that any brood reduction ‘decisions’ can be left as late as possible. Marginal chicks initially channel resources into maintaining mass, relative to skeletal size, as a buffer against starvation. However this also means competitiveness is reduced, so if conditions are poor marginal chicks are rapidly out‐competed, lose condition and die. Conversely, when food availability is good marginal offspring devote more resources to skeletal growth and quickly close the gap on their core siblings, meaning the handicap is reversible. The benefits of overproduction and hatching asynchrony as reproductive strategies to maximise success in Lesser Black‐backed Gulls are discussed in relation to the reproductive alternatives.     

Incubation prior to clutch completion accelerates embryonic development and so hatch date for eggs laid earlier in a clutch in the great tit Parus major

The ability of parents to respond to changes in food supply within a season will have a large effect on fitness through the number and quality of chicks fledged. Great tits, Parus major, attempt to synchronise their production of chicks with a seasonal food peak, but when food supply fails, hatching asynchrony of chicks provides a mechanism by which some young can be fledged because more developed chicks outcompete their less developed siblings for the reduced parental food supply. We tested whether female great tits can potentially control the degree of hatching asynchrony by using incubation before clutch completion, so that early laid eggs develop faster and hatch sooner. The temperature of an artificial egg placed in 29 nests during the laying period was measured with data loggers, and nocturnal incubation of eggs similar to incubation post clutch completion was recorded in all nests. We then demonstrated that eggs removed from the nest for 72 hour periods prior to clutch completion hatched later than eggs remaining in the nest for the entirety of the laying period. Our results show that variable pre clutch completion incubation (which was mostly nocturnal) can lead to faster embryo development and earlier hatching, so potentially providing a mechanism for adaptive female control of degree of hatching asynchrony.     

Family dynamics through time: brood reduction followed by parental compensation with aggression and favouritism

Parental food allocation in birds has long been a focal point for life history and parent–offspring conflict theories. In asynchronously hatching species, parents are thought to either adjust brood size through death of marginal offspring (brood reduction), or feed the disadvantaged chicks to reduce the competitive hierarchy (parental compensation). Here, we show that parent American coots (Fulica americana) practice both strategies by switching from brood reduction to compensation across time. Late‐hatching chicks suffer higher mortality only for the first few days after hatching. Later, parents begin to exhibit parental aggression towards older chicks and each parent favours a single chick, both of which are typically the youngest of the surviving offspring. The late‐hatched survivors can equal or exceed their older siblings in size prior to independence. A mixed allocation strategy allows parents to compensate for the costs of competitive hierarchies while gaining the benefits of hatching asynchrony.     

Are brood sex ratios adaptive?—The effect of experimentally altered brood sex ratio on nestling growth,mortality and recruitment

Brood sex ratios (BSRs) have often been found to be nonrandom in respect of parental and environmental quality, and many hypotheses suggest that nonrandom sex ratios can be adaptive. To specifically test the adaptive value of biased BSRs, it is crucial to disentangle the consequences of BSR and maternal effects. In multiparous species, this requires cross-fostering experiments where foster parents rear offspring originating from multiple broods, and where the interactive effect of original and manipulated BSR on fitness components is tested. To our knowledge, our study on collared flycatchers (Ficedula albicollis) is the first that meets these requirements. In this species, where BSRs had previously been shown to be related to parental characteristics, we altered the original BSR of the parents shortly after hatching by cross-fostering nestlings among trios of broods and examined the effects on growth, mortality and recruitment of the nestlings. We found that original and experimental BSR, as well as the interaction of the two, were unrelated to the fitness components considered. Nestling growth was related only to background variables, namely brood size and hatching rank. Nestling mortality was related only to hatching asynchrony. Our results therefore do not support that the observed BSRs are adaptive in our study population. However, we cannot exclude the possibility of direct effects of experimentally altered BSRs on parental fitness, which should be evaluated in the future. In addition, studies similar to ours are required on various species to get a clearer picture of the adaptive value of nonrandom BSRs.     

The Function of Embryonic Vocalization in the Little Tern (Sterna albifrons)

Various functional explanations can be proposed for the evolution of bird embryonic vocalizations during the pre-hatching period, namely: 1. To elicit switching of parents from incubation to parental behaviour typical of the chick period; 2. To allow thermoregulation of embryos by soliciting parents to incubate; or 3. To establish parent—offspring individual recognition. In this paper, we present the results of field experiments designed to test hypotheses 1 and 3 in the colonial, ground-nesting little tern. Parents that had their hatching eggs cross-fostered with foreign eggs at the same hatching stage exhibited a parental behaviour similar to unmanipulated controls. Parents that incubated foreign eggs up to a stage in which embryos were not yet vocalizing, and were challenged with their own hatching eggs that had been incubated in foster nests, performed less efficient parental cares than unmanipulated control pairs and pairs that had cross-fostered hatching eggs. The results do not support the hypothesis of early individual recognition and suggest that embryonic vocalizations in little terns have the function of promoting switching of parents from incubation to accepting and feeding hatchlings. Similar to other tern and gull species, the duration of incubation period in the little tern varies markedly among pairs and years. In these species, embryonic vocalizations can be adaptive since they provide parents a cue to switch at a proper time from incubation to parental cares typical of the chick period.     

Experimentally delayed hatching triggers a magnified stress response in a long-lived bird

In birds, the timing of breeding is a key life-history trait with crucial fitness consequences. We predicted that parents may value a brood less if it hatched later than expected, thereby decreasing their parental effort. In addition, breeding effort would be further modulated by the age-specific decline of future breeding opportunities. We experimentally investigated whether snow petrels, Pagodroma nivea, were less committed to care for a chick that hatched later than expected. The timing of hatching was manipulated by swapping eggs between early and late known-age pairs (7-44 years old), and investigations on hormonal and behavioral adjustments were conducted. As a hormonal gauge of parental commitment to the brood, we measured the corticosterone stress response of guarding adults. Indeed, an acute stress response mediates energy allocation towards survival at the expense of current reproduction and is magnified when the current brood value is low, as it is expected to be in young and/or delayed parents. As predicted, egg desertion and the magnitude of the stress response was stronger in delayed pairs compared to control ones. However, the treatment did not decrease the length of the guarding period, chick condition and chick survival. In addition, old parents resisted stress better (lower stress-induced corticosterone levels) than young ones. Our study provides evidence that snow petrels, as prudent parents, may value a brood less if it hatched later than expected. Thus, in long-lived birds, the responsiveness to stressors appeared to be adjusted according to the individual prospect of future breeding opportunities (age) and to the current brood value (timing of breeding).     

FISHER'S SEX RATIO THEORY MAY EXPLAIN HATCHING PATTERNS IN BIRDS

I present the hypothesis that asynchronous hatching is a means of ensuring an equal degree of parental investment in the progeny of each sex in altricial species of birds that are sexually dimorphic in size. In a comparative analysis of bird species of Africa and the Western Palearctic, I find a positive relationship between hatching asynchrony and sexual size dimorphism, in support of the hypothesis. The relation is significant for species in which males are larger than females, and in species in which females are larger than males. In addition, it holds even if allometric effects of body size are controlled for. No such relationship is found in species with self-feeding young. Alternative hypotheses to explain asynchronous hatching in altricial birds are discussed. The results of the comparative study are also consistent with some of these hypotheses. For instance, asynchronous hatching may be a mechanism used by parents of dimorphic species to deal with unpredictable primary sex ratios; it may be a way of avoiding simultaneous peak food demands by the young; or it may be a way of advancing the time of hatching so that the division of labor between the parents is optimized.     

Brood reduction and brood division in coots

The probability of starvation of chicks increases through hatching order in broods of the coot, Fulica atra. After hatching chicks accompany, and are fed by, parents as they swim around the territory. The time that chicks are able to spend outside the nest increases rapidly with age, so that the earlier hatching chicks gain a feeding advantage over the later. Starvation of chicks occurs within 4–5 days of hatching. Even after this initial mortality there persist large differences in the parental feeding rates of individual chicks within a brood. These do not correlate with age and do not seem to be the result of sibling competition. Instead, the parents regulate which chicks accompany them on foraging trips and therefore actively maintain feeding differences within the brood. Chicks cannot counter this parental regulation and the least fed of the brood grow more slowly in spite of an increased self-feeding effort. The possible functions of this parental behaviour are discussed.     

Hatching asynchrony as a bet-hedging strategy – an offspring diversity hypothesis

Many birds begin to incubate before their clutch is full, which results in the chicks hatching at different times. I propose that hatching asynchrony could serve as an adaptive parental strategy to produce phenotypic variation in the offspring through asymmetric sibling competition. Producing diverse offspring that follow variable life history strategies might be a risk-spreading strategy in spatially and temporally variable environments.     

Influence of hatching asynchrony and within-brood parental investment on size, condition, and immunocompetence in nestling red-billed choughs

Studies of hatching asynchrony have rarely assessed the effect of parental investment strategies on the development of intra-brood hierarchies using indicators of nestling quality. The influence of hatching asynchrony and other variables related to parental investment on immunocompetence was evaluated measuring T-cell mediated immune response in broods of red-billed choughs ( Pyrrhocorax pyrrhocorax ), a large long-living passerine with a pronounced sexual size dimorphism. The results showed that T-cell mediated immune response depends on parental effects as shown by the differences between broods on hatching asynchrony. Male nestlings were both heavier and larger than female nestlings, but there was no effect of hatching order on these traits, nor on sex differences in immunocompetence. Differential investment strategy in relation to laying order did not favour older offspring or either of the sexes. Successful reproduction in this species might be so unpredictable and infrequent that strategies of parental investment in the brood could have evolved to attempt to maximize the survival of all nestlings by avoiding within-brood hierachies of size, body condition, and immunocompetence.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 675–684.     

Proximate causes and fitness consequences of hatching failure in lesser kestrels Falco naumanni

Hatching failure is a pervasive phenomenon in birds, but factors affecting hatchability remain poorly understood. We studied proximate causes and fitness consequences of hatching failure in a long‐monitored population of the colonial lesser kestrel Falco naumanni. We investigated whether hatchability was related to clutch characteristics, parental traits, and social or environmental features. Hatching failure represents a cost for the parents in terms of immediate fitness, since it reduced both their number of young fledged and recruits in the breeding population, even when controlling for clutch size. Hatching failure showed a non‐linear relationship with clutch size, clutches of four eggs showing higher levels of hatching success than larger or smaller clutches. Hatchability could therefore play a role in the evolution of optimal clutch size in this species, at least constraining the maximum number of eggs the parents can afford to incubate. Contrary to most studies, the mean volume of the clutch and the individual egg volume were negatively related to hatching failure, indicating that large eggs have thermoregulatory and/or nutritional advantages. Mean daily maximum temperature during incubation affected hatching success negatively, but only for females in poor condition. This result seems to indicate that females are reluctant to jeopardize their own condition, but instead sacrifice incubation effort by paying the costs of a lower hatching success in circumstances of high temperatures. There was no evidence that hatching failure was related to the intrinsic properties of individuals or genetic similarity between the parents as indicated by low repeatabilities of: (1) males that bred with different females, (2) females that bred with different males, and (3) pairs breeding together in different years. Neither colony size nor subpopulation size affected hatchability. All these findings show how hatching failure is simultaneously influenced by several factors acting in a complex way, which could in part explain the apparently conflicting conclusions of empirical or even experimental studies carried out to date.     

The separate effects of egg size and parental quality on the development of ornamental plumage coloration

The fitness‐related consequences of egg size, independent of the influences of parental quality, are poorly understood in altricial birds. Not only can egg size and parental quality influence growth and survival, but each could influence the development of condition‐dependent plumage coloration in offspring. The Eastern Bluebird Sialia sialis is an altricial, multi‐brooded, cavity‐nesting passerine in which juveniles display dichromatic UV‐blue plumage. Previous research suggests that plumage coloration acts as a signal of individual quality among juvenile and adult Eastern Bluebirds. Here, we separate the effects of egg size and parental quality (defined by egg size laid) on nestling growth and plumage ornamentation by exchanging clutches of large eggs with clutches of small eggs. Nestlings were significantly larger immediately post‐hatching when hatched from a large egg, but to maintain a larger size, nestlings needed to have hatched from a large egg and to have been reared by high‐quality parents. Nestlings were brighter when reared by high‐quality parents and this relationship was strongest later in the breeding season. Nestlings exhibited greater UV chroma if hatched early in the season, but UV chroma was not significantly affected by egg size or parental quality. These findings demonstrate varying influences of both egg size and parental quality on offspring growth and plumage ornamentation but suggest that quality of post‐hatching investment is more influential than pre‐hatching investment.     

Individual variation in baseline and stress-induced corticosterone and prolactin levels predicts parental effort by nesting mourning doves

Endocrine systems have an important mechanistic role in structuring life-history trade-offs. During breeding, individual variation in prolactin (PRL) and corticosterone (CORT) levels affects behavioral and physiological processes that drive trade-offs between reproduction and self-maintenance. We examined patterns in baseline (BL) and stress induced (SI; level following a standard capture-restraint protocol) levels of PRL and CORT for breeding mourning doves (Zenaida macroura). We determined whether the relationship of adult condition and parental effort to hormone levels in wild birds was consistent with life-history predictions. Both BL PRL and BL CORT level in adults were positively related to nestling weight at early nestling ages, consistent with the prediction of a positive relationship of hormone levels to current parental effort of adults and associated increased energy demand. Results are consistent with the two hormones acting together at baseline levels to limit negative effects of CORT on reproduction while maintaining beneficial effects such as increased foraging for nestling feeding. Our data did not support predictions that SI responses would vary in response to nestling or adult condition. The magnitude of CORT response in the parents to our capture-restraint protocol was negatively correlated with subsequent parental effort. Average nestling weights for adults with the highest SI CORT response were on average 10–15% lighter than expected for their age in follow-up visits after the stress event. Our results demonstrated a relationship between individual hormone levels and within population variation in parental effort and suggested that hormonal control plays an important role in structuring reproductive decisions for mourning doves.