Chronic stress in infancy fails to affect body size and immune response of adult female blue‐footed boobies or their offspring

Experiments on birds, fish and mammals have shown that adverse conditions during infancy can produce diverse long‐term and delayed deficits during adulthood, prejudicing both the individual and its offspring. Natural selection should prepare animals to cope with adversity of the type, magnitude and timing that commonly occur in their natural habitat, but very little is known about such evolved developmental buffering against natural ‘poor starts’ in life. In two‐chick broods of the blue‐footed booby Sula nebouxii, the junior (younger) chick usually experiences aggressive subordination, reduced nutrition and growth and elevated circulating corticosterone. To test whether this poor start produces long‐term, delayed or intergenerational deficits in body size, body condition or cell‐mediated immune response, we measured 3–8 yr old female breeders banded as chicks, and their infant offspring. Results failed to support our predictions. Compared to former seniors and former singletons (solitary nestlings), former juniors showed no deficit in cell‐mediated immune response at any age. They showed an 8.04% deficit in body condition at age 4–6 yr but this deficit disappeared completely by age 7–8 yr. Furthermore, their offspring showed no deficits in body size, body condition or immune response. Junior chicks are affected by their poor start, but their developmental resilience, also confirmed by studies of post‐fledging survivorship, recruitment, natal dispersal, aggressive nest defense and reproduction, is evidence of evolved developmental buffering against predictable adversity during infancy.     

Costs of growing up as a subordinate sibling are passed to the next generation in blue‐footed boobies

As stresses in early development may generate costs in adult life, sibling competition and conflict in infancy are expected to diminish the reproductive value of surviving low‐status members of broods and litters. We analysed delayed costs to blue‐footed booby fledglings, Sula nebouxii, of junior status in the brood, which involves aggressive subordination, food deprivation and elevated corticosterone, but little or no deficit in size at fledging. In ten cohorts observed for up to 16 years, juniors showed no deficit in breeding success at any age, independent of lifespan, including in a sample of sibling pairs. Among females, juniors actually outreproduced seniors across the 16‐year span. However, offspring produced by juniors in the first 3 years of life were less likely to recruit into the breeding population than offspring of seniors. Since junior fledglings survive, recruit and compete as well as seniors (shown earlier), and breed as successfully as seniors across the lifespan, it appears the delayed cost of subordination is passed to offspring, and only to those few offspring produced in the first 3 years of life. These correlational results indicate that systematic competition‐related differences in developmental conditions of infant siblings can alter their reproductive value by affecting the viability of their eventual offspring.     

Natural 'poor start' does not increase mortality over the lifetime

Poor nutrition and other challenges during infancy can impose delayed costs, and it has been proposed that expression of costs during adulthood should involve increased mortality rather than reduced reproduction. Demonstrations of delayed costs come mostly from experimental manipulations of the diet and hormones of captive infants of short-lived species, and we know very little about how natural poor starts in life affect wild animals over their lifetimes. In the blue-footed booby, sibling conflict obliges younger brood members to grow up suffering aggressive subordination, food deprivation and elevated stress hormone, but surviving fledglings showed no deficit in reproduction over the first 5-10 years. A study of 7927 individuals from two-fledgling and singleton broods from 20 cohorts found no significant evidence of a higher rate of mortality nor a lower rate of recruitment in younger fledglings than in elder fledglings or singletons at any age over the 20 year lifespan. Development of boobies may be buffered against the three challenges of subordination. Experimental challenges to neonates that result in delayed costs have usually been more severe, more prolonged and more abruptly suspended, and it is unclear which natural situations they mimic.     

Buffered development: resilience after aggressive subordination in infancy

Do aggressive dominance and subordination in vertebrate broods and litters affect development? We examined 1,167 fledglings from two-chick broods of the blue-footed booby (Sula nebouxii), a species in which the first-hatched chick dominates with violent attacks throughout the nestling period and subordinates suffer lower fledging success, but if both broodmates survive, they grow to the same size. There was little evidence that dominant fledglings were more likely to recruit into the breeding population than were subordinate fledglings, and there was no evidence that dominant and subordinate recruits differed in their age, date, brood size, or nest success at first reproduction or in their summed brood sizes or total nest success over the first 5 yr or first 10 yr of life. Compared with dominants, subordinate fledglings were less prejudiced by late hatching and established clutches earlier over the first 10 yr, and subordinate recruits had 33% larger broods over the first 5 yr. However, in broods where both chicks fledged, accumulated reproductive success for chicks up to age 5 yr was similar for dominants and subordinates. Exercising dominance throughout infancy apparently does not fortify a chick for the future and may incur a long-term cost, and suffering violent subordination throughout infancy has little or no prejudicial effect and may even steel a chick for adult life.     

Effects of testosterone on growth, plumage pigmentation, and mortality in Black-headed Gull chicks

In the Black-headed Gull Larus ridibundus, sibling chicks defend small territories against conspecifics with testosterone-dependent aggressive behaviour. The energetic requirements for the performance of this behaviour may trade off against the energetic requirements for growth. There are indications that testosterone suppresses growth in birds and, therefore, regulate this trade-off. In this study, the effect of testosterone on growth and plumage pigmentation of Black-headed Gull chicks was analysed. Young chicks in small groups were treated for ten days with testosterone or sham treated. Testosterone-treated birds showed decreased growth rate (daily increase in body mass, head-bill length and tarsus-length) and a marked decrease in juvenile pigmentation of the plumage (tail-bar, back, and secondary coverts). Field measurements revealed a negative correlation between nest density, which correlates positively with aggressive behaviour of adults, and plumage coloration. Furthermore, these measurements showed an increase in mortality of chicks that had low levels of pigmentation early in life. The data suggest that chicks face a testosterone-regulated trade-off between growth and territory defence.     

Nest Defence of Nesting Chinstrap Penguins (Pygoscelis antarctica) against Intruders

We tested some predictions of parental investment theory by studying the aggressive behaviour of colonial nesting chinstrap penguins (Pygoscelis antarctica) against human intruders into their nesting territories. We tested for differences in the aggressive behaviour of penguins according to offspring age (eggs vs. chicks), offspring number, nest location in the colonies (central vs. peripheral) and sex. Offspring age was the main factor influencing nest defence, although nest location and sex were also important. Chicks were defended more strongly than eggs, in accordance with changes in the reproductive value of offspring, and this increase in aggressiveness was not related to revisitation of the same individuals. The level of aggression of penguins breeding in central sites was higher than that of peripheral birds, a difference that could be due to the lower residual reproductive value of central-nesting, probably older, birds. The stronger aggressiveness of males could be due to a combination of factors related to sexual selection and life-history traits. Offspring number did not affect the level of nest defence.     

Causal and functional correlates of brood amalgamation in the chinstrap penguin<Emphasis Type="Italic"> Pygoscelis antarctica</Emphasis>: parental decision and adult aggressiveness

Despite the high number of species in which crèching behaviour has been analysed, the factors determining brood desertion and chick aggregations remain relatively poorly understood. We analysed crèching behaviour of chinstrap penguins (Pygoscelis antarctica) to test whether: (1) timing of chick aggregations was mainly determined by the growth stage of chicks or by adult physiological constraints; (2) the crèche acts as a protective mechanism against predation or as a defence against conspecific adult aggressiveness. Our results show that chick desertion was not related to chick growth rate and was driven primarily by a parental decision, determined by adult physical constraints imposed by moulting needs and the short breeding season in Antarctica. With respect to the functional meaning of brood amalgamations, our results suggest that they are originated by the aggressive behaviour of adults, although the forces driving them could depend greatly on ecological conditions and vary among species and populations. Finally, because brood amalgamations can be determined by adult aggressiveness contrasting with the origin and typical definition of the term "crèche" (which implies the nursery concept), we propose the use of the term "brood amalgamation" for the penguin "crèches".     

Maternal yolk androgens stimulate territorial behaviour in black-headed gull chicks

Avian eggs contain substantial amounts of maternal androgens. The concentrations of these yolk androgens are affected by the maternal environment, such as the level of social competition, parasite exposure or food conditions. Since yolk androgens have been shown to affect a wide array of offspring traits, they may adjust the chicks to the expected post-hatching environment, but experimental evidence is still scarce. We investigate in colonial breeding black-headed gulls whether high concentrations of yolk androgens, such as those found in environments with high numbers of social interactions, facilitate aggressiveness and territorial behaviour of the chicks. Black-headed gulls are highly suitable for this, as the semi-precocial chicks defend the natal territory and food against intruders. We manipulated yolk androgen concentrations and investigated their role in both within-nest and between-nest aggression. We found that chicks hatching from androgen-treated eggs defended the natal territory more often than their nest mates from control eggs, without increasing sibling aggression. This suggests that variation in yolk androgen concentrations in relation to the social environment of the mother may indeed allow adjustment of the offspring''s behaviour to the expected frequency of territorial interactions with conspecifics post-hatching.     

Growth strategies of passerine birds are related to brood parasitism by the brown-headed cowbird (Molothrus ater)

Sibling competition was proposed as an important selective agent in the evolution of growth and development. Brood parasitism by the brown-headed cowbird (Molothrus ater) intensifies sibling competition in the nests of its hosts by increasing host chick mortality and exposing them to a genetically unrelated nestmate. Intranest sibling competition for resources supplied by parents is size dependent. Thus, it should select for high development rates and short nestling periods, which would alleviate negative impacts of brood parasitic chicks on host young. I tested these predictions on 134 North American passerines by comparative analyses. After controlling for covariates and phylogeny, I showed that high parasitism rate was associated with higher nestling growth rate, lower mass at fledging, and shorter nestling periods. These effects were most pronounced in species in which sibling competition is most intense (i.e., weighing over about 30 g). When species were categorized as nonhosts versus old hosts (parasitized for thousands of years) versus new hosts (parasitized the last 100-200 years), there was a clear effect of this parasitism category on growth strategies. Nestling growth rate was the most evolutionarily flexible trait, followed by mass at fledging and nestling period duration. Adjustments during incubation (incubation period length, egg volume) were less pronounced and generally disappeared after controlling for phylogeny. I show that sibling competition caused by brood parasites can have strong effects on the evolution of host growth strategies and that the evolution of developmental traits can take place very rapidly. Human alteration of habitats causing spread of brood parasites to new areas thus cascades into affecting the evolution of life-history traits in host species.     

Woodpigeons nesting in association with hobby falcons: advantages and choice rules

Many bird species nest in close association with other bolder and more aggressive birds which provide protection against nest predators. The woodpigeons, Columba palumbus, that nest in poplar plantations in Northern Italy are found almost exclusively clumped around hobby, Falco subbuteo, nests. Woodpigeons settle in the area and build their nests after the hobby has started nesting. We carried out experiments with dummy nests and observations on woodpigeon nests. Dummy woodpigeon nests placed near a hobby's nest suffered less depredation by hooded crows, Corvus corone cornix, than those placed far from it. A logistic regression analysis showed that three variables, hobby nesting stage, distance from the hobby's nest and the hobby's aggressiveness, influenced the probability of nest predation. The degree of protection varied during the hobby's nesting period and was highest when chicks were in the nest. The hobby's aggressiveness against intruders varied both between and within individuals during different nesting phases. The predation rate of dummy nests associated with the falcon was negatively correlated with the aggressiveness score of the hobby during the 6 days of dummy nest exposure. Observations on real nests showed that woodpigeons selected hobbies that had a high fledging success, and a more vigorous defensive behaviour. Clues that would allow woodpigeons to choose the best protector may be early nesting by the hobby and its aggressiveness. Hobbies preyed on adult woodpigeons, but the risk incurred by the woodpigeons was low compared with the very high risk of nest predation in this area. Copyright 1999 The Association for the Study of Animal Behaviour.     

Early life predictors of the development of aggressive behaviour in the domestic pig

Individuals show stable differences in their aggressive responses towards unfamiliar conspecifics. We investigated the extent to which variables present during early life could be identified that were correlated with these later individual differences in aggressive behaviour. The behaviour and growth of 125 domestic pigs, Sus scrofa, from 16 litters, were studied from birth until 18 days after weaning, when they were tested on two occasions in resident-intruder tests to measure their aggressiveness. Aggressiveness was affected by litter, although not by sex. A number of early life correlates of later resident-intruder aggressiveness were found at the litter level. Pigs became more aggressive if they had been born into larger litters. Pigs in these aggressive litters were more active in the 8-h period immediately after birth, perhaps taking longer to achieve satiety at the udder. They were also in poorer condition 2 days after birth. Aggressive pigs also engaged in more pushing with littermates over the whole preweaning period. The best correlates of aggressiveness appear to be a number of correlated variables relating to low nutrition, either prenatally or in the early postnatal period. The results are consistent with the concept that early environmental conditions can programme behavioural responses for later life.     

Maternal effects as drivers of sibling competition in a parent–offspring conflict context? An experimental test

Maternal effects occur when the mother's phenotype influences her offspring's phenotype. In birds, differential allocation in egg yolk components can allow mothers to compensate for the competitive disadvantage of junior chicks. We hypothesize that the parent–older chick conflict peaks at intermediate conditions: parents benefit from the younger chick(s) survival, but its death benefits the older chick in terms of growth and survival. We thus expect maternal compensation to follow a bell‐shaped pattern in relation to environmental conditions. We studied a black‐legged kittiwake (Rissa tridactyla) population where previous results revealed increased allocation of yolk testosterone in younger as compared to older chicks in intermediate conditions, in line with our theoretical framework. We therefore predicted a maternally induced increase in aggressiveness, growth, and survival for younger chicks born in intermediate environmental conditions. Controlling for parental effects and chick sex, we manipulated food availability before egg laying to create a situation with intermediate (Unfed group) and good (Fed group) environmental conditions. Within each feeding treatment, we further created experimental broods where the natural hatching order was reversed to maximize our chances to observe an effect of feeding treatment on the younger chicks' aggressiveness. As predicted, we found that chick aggressiveness was higher in younger chicks born from the Unfed group (i.e., in intermediate environmental conditions), but only when they were put in a senior position, in reversed broods. Predictions on growth and survival were not confirmed. Mothers thus seem to favor the competitiveness of their younger chick in intermediate conditions via egg yolk components, but our study also suggests that hatching asynchrony need to be small for maternal compensation to be efficient. We emphasize the need for further studies investigating other chick behaviors (e.g., begging) and focusing on the relative role of different yolk components in shaping parent–offspring conflict over sibling competition.     

Individual differences in aggressiveness of adelie penguins

The number of pecks per minute given by individual Adelie penguins to an artificial model is used as a measure of aggressiveness. Penguins without eggs or chicks are less aggressive than thoes with eggs or chicks. Aggressiveness increases after egg-laying, and reaches a peak at about chick hatching. Prior to egg-laying, males are more aggressive towards the model than females, but after egg-laying there is no difference between them (on average). Most penguins with above average aggressiveness are located at territories in the centre of a colony, whereas those with below average aggressiveness tend to occur at the periphery. Penguins with high aggressiveness also have a higher breeding success than less aggressive ones.     

High juvenile annual survival probabilities in Southern Rockhopper Penguins Eudyptes chrysocome are independent of individual fledging traits

Juvenile survival is an important demographic parameter. Southern Rockhopper Penguins Eudyptes chrysocome have undergone a dramatic population decline in the past century across their distribution, but the demographic processes are poorly understood. To estimate juvenile annual survival probabilities, Rockhopper Penguin chicks from two cohorts on New Island, Falkland Islands, were marked with transponders and recorded in subsequent years using an automated gateway. We first estimated annual survival and detection probabilities using a Cormack‐Jolly‐Seber (CJS) model, and found that both probabilities were extremely high (81% in the first and 98% in the second, third and fourth years of life), even in comparison with adult birds. Because detection probability after 3 years was effectively 1, and our sample size (n = 114) was too small to explore the effects of individual traits on survival in a CJS model, we assessed whether sex, cohort, body mass and laying sequence affected whether juveniles returned to the colony during their first 3 years of life using a simple generalized linear model that assumed perfect detection. Juveniles from the first cohort and males showed a higher return probability than juveniles from the second cohort and females. There was no clear effect of fledging body mass on return rate, probably related to the favourable environmental conditions during the study period. The laying sequence did not markedly affect the return probability of chicks, indicating that, once fledged, first‐laid A‐chicks have the same probability to return as second‐laid B‐chicks despite a much larger initial maternal investment in B‐eggs in this species. This study demonstrates extraordinarily high juvenile survival probabilities and will help to understand the recent changes in the population dynamics of the Falkland Islands Southern Rockhopper Penguins.     

Possible roles for corticosterone and critical size in the fledging of nestling pied flycatchers

Our study was designed to see whether corticosterone (B) rises abruptly in the blood of nestling pied flycatchers (Ficedula hypoleuca) at the time they fledge, as reported recently for kestrels, and if so, why. We measured the growth and blood levels of B and selected nutrients of nestlings in broods of five, seven, and nine chicks during 1998 and 1999. In half of the broods, we clipped selected wing and tail feathers of both parents with the intention of making it more difficult for them to provide their chicks with food. We collected blood samples when the chicks were six to 10 d old (period of rapid growth) and 15 d of age or older (0-5 d before fledging). B increased substantially several days before the chicks left the nest and then declined somewhat. We found no differences in rates of growth or blood levels of B, nutrients, and hematocrit as a function of either brood size or parental handicapping. Nestlings within a day of fledging appear to have been food deprived in 1998; their glucose was significantly reduced, and B, free fatty acids, and glycerol were significantly elevated compared to levels in chicks 1-4 d younger. Such changes did not occur in 1999. Blood levels of B were significantly correlated with brood size near the day of fledging, but not earlier, in both years of the study. It was possible to predict the day on which chicks would leave the nest, using their wing length when 12 d old. These results suggest that high blood levels of B associated with food restriction and sibling competition induce chicks to fledge, provided they have reached a critical size, and that the importance of fasting, sibling competition, and B may vary from year to year.     

Yolk testosterone reduces oxidative damages during postnatal development

Conditions experienced during early life can influence the development of an organism and several physiological traits, even in adulthood. An important factor is the level of oxidative stress experienced during early life. In birds, extra-genomic egg substances, such as the testosterone hormone, may exert a widespread influence over the offspring phenotype. Interestingly, testosterone can also upregulate the bioavailability of certain antioxidants but simultaneously increases the susceptibility to oxidative stress in adulthood. However, little is known about the effects of maternally derived yolk testosterone on oxidative stress in developing birds. Here, we investigated the role of yolk testosterone on oxidative stress of yellow-legged gull chicks during their early development by experimentally increasing yolk testosterone levels. Levels of antioxidants, reactive oxygen species and lipid oxidative damage were determined in plasma during nestlings'' growth. Our results revealed that, contrary to control chicks, birds hatched from testosterone-treated eggs did not show an increase in the levels of oxidative damage during postnatal development. Moreover, the same birds showed a transient increase in plasma antioxidant levels. Our results suggest that yolk testosterone may shape the oxidative stress-resistance phenotype of the chicks during early development owing to an increase in antioxidant defences and repair processes.     

Food availability modulates the effects of maternal antibodies on growth and immunity in young feral pigeons

It is now widely acknowledged that mothers can transfer their own immune experience to their progeny through the allocation of specific maternal antibodies (hereafter referred as MatAb) that can shape offspring phenotype and affect their fitness. However, the importance of environmental variability in modulating the effects of MatAb on offspring traits is still elusive. Using an experimental approach, we investigated how food availability interacted with MatAb to solve the trade‐off between humoral immunity and growth in young feral pigeons Columba livia. Results show that the inhibitory effect of MatAb on the humoral response of chicks was detected regardless of the food treatment. In addition, body mass growth was higher in chicks receiving lower amounts of maternal antibodies but only in chicks of the ad libitum food treatment. This contradicts previous studies and suggests that the transfer of MatAb could entail some costs for chicks and reduce their growth. Taken together these results reinforce the idea that the maternal antibodies play a central role in shaping offspring life‐history traits but that their adaptive value is highly dependent on the environmental context in which they are transmitted by the mother.     

Early life maternal sociality predicts juvenile sociality in blue monkeys

Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.     

Benefits and costs of increased levels of corticosterone in seabird chicks

Seabird chicks respond to food shortages by increasing corticosterone (cort) secretion, which is probably associated with fitness benefits and costs. To examine this, we experimentally increased levels of circulating cort in captive black-legged kittiwake chicks fed ad libitum. We found that cort-implanted chicks begged more frequently and were more aggressive compared to controls. These behavioral modifications must be beneficial to chicks as they facilitate acquisition of food from the parents and might trigger brood reduction and reduced competition for food. Cort-implanted chicks also increased food intake; however, their growth rates were similar to controls. To examine the costs of chronically increased circulating levels of cort, we removed cort implants and, after a 10-day recovery period, tested cognitive abilities of young kittiwakes. We found that the ability of kittiwakes to associate a visual cue with the presence of food in a choice situation was compromised by the experimental elevation of cort during development. To examine the long-term costs of increased levels of cort, 8 months later we tested the performance of the same individuals in a spatial task requiring them to make a detour around a barrier in order to escape from an enclosure. Individuals treated with cort during development took significantly more time to solve this task compared to controls. The results of this study suggest that the adrenocortical response of a developing bird to environmental stressors is associated with both benefits (increased food intake, foraging behavior, and aggression) and costs (low growth efficiency and compromised cognitive abilities later in life). This provides an evolutionary framework for relating juvenile physiological traits to fitness of birds in subsequent life-history stages.     

Density But Not Kinship Regulates the Growth and Developmental Traits of Chinese Tiger Frog （Hoplobatrachus chinensis） Tadpoles

Kinship and density are believed to affect important ecological processes such as intraspecific competition, predation, growth, development, cannibalism, habitat selection and mate choice, In this work, we used Chinese tiger frog Hoplobatrachus chinensis tadpoles as an experimental model to investigate the effects of kinship and density on growth and development of this species over a 73 day period. The results showed that density can affect the growth and developmental traits （survival rate, larval period, size at the limb bud protrusion/metamorphic climax and body mass at different life stages） of H. chinensis tadpoles, while kinship does not. Tadpoles took longer to develop and potential metamorphosis was greater in high density groups of both sibling and non-siblings. The interaction of kinship and density did not significantly influenced growth traits of H. chinensis tadpoles during the experimental period. For coefficient variations of each growth trait, no differences were detected between sibling and non-sibling groups. These findings provide valuable information on the basic ecology of H. chinensis which will be helpful in future studies of other anuran species.