Corticosterone release in very young siblicidal seabird chicks (Rissa tridactyla) is sensitive to environmental variability and responds rapidly and robustly to external challenges.

In birds, patterns of development of the adrenocortical response to stressors vary among individuals, types of stressors, and species. Since there are benefits and costs of exposure to elevated glucocorticoids, this variation is presumably a product of selection such that animals modulate glucocorticoid secretion in contexts where doing so increases their fitness. In this study, we evaluated hypothalamo-pituitary-adrenal (HPA) activity in first-hatched free-living seabird nestlings that engage in intense sibling competition and facultative siblicide (black-legged kittiwakes, Rissa tridactyla). We sampled 5 day old chicks (of the ∼45 day nestling period), a critical early age when food availability drives establishment of important parent-offspring and intra-brood dynamics. We experimentally supplemented parents with food ("supplemented") and measured chick baseline corticosterone secretion and capacity to rapidly increase corticosterone in response to an acute challenge (handling and 15 min of restraint in a bag). We also used topical administration of corticosterone to evaluate the ability of chicks to downregulate physiologically relevant corticosterone levels on a short time scale (minutes). We found that 5 day old chicks are not hypo-responsive but release corticosterone in proportion to the magnitude of the challenge, showing differences in baseline between parental feeding treatments (supplemented vs non-supplemented), moderate increases in response to handling, and a larger response to restraint (comparable to adults) that also differed between chicks from supplemented and control nests. Topical application of exogenous corticosterone increased circulating levels nearly to restraint-induced levels and induced downregulation of HPA responsiveness to the acute challenge of handling. Parental supplemental feeding did not affect absorbance/clearance or negative feedback. Thus, while endogenous secretion of corticosterone in young chicks is sensitive to environmental context, other aspects of the HPA function, such as rapid negative feedback and/or the ability to clear acute elevations in corticosterone, are not. We conclude that 5 day old kittiwake chicks are capable of robust adrenocortical responses to novel challenges, and are sensitive to parental food availability, which may be transduced behaviorally, nutritionally, or via maternal effects. Questions remain about the function of such rapid, large acute stress-induced increases in corticosterone in very young chicks.

Telomere length correlates with physiological and behavioural responses of a long-lived seabird to an ecologically relevant challenge.

Determinants of individual variation in reallocation of limited resources towards self-maintenance versus reproduction are not well known. We tested the hypothesis that individual heterogeneity in long-term 'somatic state' (i) explains variation in endocrine and behavioural responses to environmental challenges, and (ii) is associated with variation in strategies for allocating to self-maintenance versus reproduction. We used relative telomere length as an indicator of somatic state and experimentally generated an abrupt short-term reduction of food availability (withdrawal of food supplementation) for free-living seabirds (black-legged kittiwakes, Rissa tridactyla). Incubating male kittiwakes responded to withdrawal by increasing circulating corticosterone and losing more weight compared to continuously supplemented controls. Males with longer telomeres increased time in directed travel regardless of treatment, while experiencing smaller increases in corticosterone. Males with longer telomeres fledged more chicks in the control group and tended to be more likely to return regardless of treatment. This study supports the hypothesis that somatic state can explain variation in short-term physiological and behavioural responses to challenges, and longer-term consequences for fitness. Male kittiwakes with longer telomeres appear to have prioritized investment in self over investment in offspring under challenging conditions.

Effects of Prenatal Environment on Phenotype Are Revealed by Postnatal Challenges: Embryonic Hormone Exposure, Adrenocortical Function, and Food in Seabird Chicks.

The interaction between prenatal environments and postnatal environments is an important source of phenotypic variability. We examined the ability of prenatal steroid exposure and postnatal energy restriction to explain adrenocortical function and fledging age in captive seabird chicks. We proposed and tested two hypotheses: (1) the strength of prenatal effects is attenuated by challenging postnatal environments (postnatal override) and (2) the strength of prenatal effects increases with the severity of postnatal challenges (postnatal reveal). We reared common murre (Uria aalge) chicks and measured prenatal exposure to corticosterone (CORT) and testosterone (T) from allantoic waste. Adrenocortical function was assessed after 10 d of ad lib. feeding and then after 5 and 10 d on controlled diets. Postnatal override predicts that prenatal steroids will explain more phenotypic variation before implementation of energy restriction; postnatal reveal predicts that the contribution of prenatal steroids will increase with duration and severity of energy restriction. Energy restriction increased secretion of baseline CORT and the adrenocortical response to the standardized stressor of handling and restraint. The ability of prenatal steroids to explain baseline CORT increased with duration of energy restriction, and for day 20 free baseline CORT, there was a significant interaction between kilojoules per day and prenatal CORT levels; severity of restriction strengthened the relationship between prenatal hormone levels and postnatal hormone levels. Both maximum CORT at day 20 and fledging age were best explained by diet treatment and day 15 or day 20 baseline CORT, respectively. Overall, prenatal CORT increased fledging age and baseline secretion of CORT, while prenatal T decreased them. However, prenatal effects on adrenocortical function were apparent only under the energy restriction conditions. Thus, we found some support for the postnatal reveal hypothesis; our results suggest that some prenatal effects on phenotype may be more likely to manifest in challenging postnatal environments.

Differential reproductive responses to stress reveal the role of life-history strategies within a species.

Life-history strategies describe that 'slow'- in contrast to 'fast'-living species allocate resources cautiously towards reproduction to enhance survival. Recent evidence suggests that variation in strategies exists not only among species but also among populations of the same species. Here, we examined the effect of experimentally induced stress on resource allocation of breeding seabirds in two populations with contrasting life-history strategies: slow-living Pacific and fast-living Atlantic black-legged kittiwakes. We tested the hypothesis that reproductive responses in kittiwakes under stress reflect their life-history strategies. We predicted that in response to stress, Pacific kittiwakes reduce investment in reproduction compared with Atlantic kittiwakes. We exposed chick-rearing kittiwakes to a short-term (3-day) period of increased exogenous corticosterone (CORT), a hormone that is released during food shortages. We examined changes in baseline CORT levels, parental care and effects on offspring. We found that kittiwakes from the two populations invested differently in offspring when facing stress. In response to elevated CORT, Pacific kittiwakes reduced nest attendance and deserted offspring more readily than Atlantic kittiwakes. We observed lower chick growth, a higher stress response in offspring and lower reproductive success in response to CORT implantation in Pacific kittiwakes, whereas the opposite occurred in the Atlantic. Our findings support the hypothesis that life-history strategies predict short-term responses of individuals to stress within a species. We conclude that behaviour and physiology under stress are consistent with trade-off priorities as predicted by life-history theory. We encourage future studies to consider the pivotal role of life-history strategies when interpreting inter-population differences of animal responses to stressful environmental events.

mtDNA haplotypes differ in their probability of being eliminated by a mass die-off in an abundant seabird.

In this study, we take advantage of a natural experiment--a 2004 mass die-off of the Common Murre in Alaska to determine whether closely related mtDNA haplotypes differ in their probability of being eliminated during such a short term but a marked event removing hundreds of thousands of individuals. We sequenced complete mtDNA ND2 gene (1041 bp) for 168 Common Murres sampled from seven breeding colonies across Alaska before the 2004 die-off and 127 dead murres washed ashore during the die-off. We found little mtDNA variation and lack of geographical structuring among the seven Common Murre breeding colonies in Alaska. A comparison of the single-dominant mtDNA haplotype's frequency between live murres sampled on breeding colonies before the die-off (73.2%; 95% confidence interval 66.3-79.9%) and dead murres sampled during the die-off (59.1%; 95% confidence interval 50.4-67.4%; Fisher's exact P=0.01) showed that carriers of the dominant haplotype were significantly less likely to die than carriers of other haplotypes. At the same time, the ratio of non-synonymous to synonymous substitutions did not differ between live (10:35) and dead birds (18:34; Fisher's exact P=0.26), indicating that non-synonymous substitutions were as likely to be eliminated as synonymous substitutions. These results are consistent with the possibility of positive selection on the dominant mtDNA haplotype during the die-off.

Individual variation in plasma estradiol-17beta and androgen levels during egg formation in the European starling Sturnus vulgaris: implications for regulation of yolk steroids.

While it is clear that maternal transfer of steroids to egg yolk can have significant effects on offspring phenotype, an unresolved question is whether females can facultatively adjust yolk hormone levels independently of their own plasma levels or whether yolk steroid levels are simply a direct consequence of temporal variation in the female's hormonal status. In part, this is because we lack detailed information about the day-to-day pattern of changes in plasma hormone levels during the laying cycle for non-domesticated birds. Here, we describe changes in plasma estradiol-17beta (E2) and androgens, throughout laying in relation to specific stages of ovarian follicular development in the European starling (Sturnus vulgaris). Plasma E2 levels increased rapidly from the onset of rapid yolk development (RYD) to reach maximum levels in birds with a complete follicle hierarchy (> or = 4 yolky follicles). However, levels decreased linearly throughout the later stages of follicle development returning to pre-breeding values before the final yolky follicle was ovulated. In females with > or = 4 yolky follicles there was 10-fold variation in plasma E2 levels among individual females, but this was not related to plasma levels of the main yolk precursor vitellogenin or to the total mass of yolky follicles developing at the time of blood sampling. In contrast to E2, plasma androgen levels showed only a very gradual linear decline throughout the laying cycle from pre-RYD to clutch completion. Furthermore, androgen levels showed less individual variability: 4-fold variation among females with > or = 4 yolky follicles, although this was also independent of our measures of reproductive function. Data on inter- and intra-individual variation in female hormone levels are important to set-up a priori predictions for, and interpretation of, studies of yolk hormone levels.

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.

Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli).

Birds respond to short-term deterioration in foraging conditions by increasing their plasma level of corticosterone but the physiological effects of long-term deterioration in food supplies are not well known. In resident passerine birds that winter in temperate climates, such as the mountain chickadee (Poecile gambeli), the food supply may be limited and unpredictable over long periods of time. Whether the long-term limited and unpredictable food supply has an effect on (a) baseline levels of corticosterone and (b) the adrenocortical stress response to a standardized acute stress of handling and restraint in mountain chickadees was assessed. For a period of 94 days, one group of chickadees was maintained on limited and unpredictable food (food-restricted) and the other group was maintained on an ad libitum food supply. The food-restricted birds had significantly higher baseline levels of corticosterone than those maintained on ad libitum food. All birds responded to the acute stressor by an increasing secretion of corticosterone but there were no differences between the treatment groups in their stress response. There was a significant effect of sex on the stress response, with females reaching higher levels of corticosterone and responding at a faster rate than males. These results suggest that permanent resident birds wintering in harsh environments may have elevated levels of corticosterone on a long-term basis. Whereas other factors, such as day length and ambient temperature, may contribute to energetic hardship during the winter, the results showed that limited and unpredictable food alone can trigger significant changes in baseline levels of plasma corticosterone. The potential costs and benefits of long-term increased corticosterone levels in resident food-caching birds are discussed.

Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks.

Release of corticosterone in hungry kittiwake chicks facilitates begging and allows them to restore depleted energy reserves by increasing parental food provisioning. However, in order to avoid detrimental effects of chronic elevation of corticosterone, chicks might suppress adrenocortical activity in response to prolonged food shortages. In this study we examined temporal dynamics of corticosterone release in red-legged kittiwake (Rissa brevirostris) chicks exposed to prolonged restrictions in energy content and/or nutritional quality (low versus high lipid content) of their food. Starting at the age of 15 days, chicks were fed either high- or low-lipid fish at 40%, 65%, and 100% of ad libitum energy intake. Body mass measurements and baseline plasma samples were taken on a weekly basis after beginning of the treatment. After 3 weeks of treatment, chicks were exposed to a standardized acute handling and restraint stress protocol, where in addition to a baseline sample, three plasma samples were taken at intervals up to 50 min. We found that food-restricted chicks had lower body mass, chronically (during 2-3 weeks) elevated baseline and higher acute stress-induced levels of corticosterone compared to chicks fed ad libitum. Low lipid content of food further exacerbated these effects. An increase in baseline levels of corticosterone was observed within a week after energy requirements of food-restricted chicks exceeded their daily energy intake. A tendency for suppression of adrenocortical activity was observed in treatments fed low-lipid diets only at the end of the experiment. We suggest that nest-bound chicks, if food-stressed, might suffer deleterious effects of chronic elevation of corticosterone.

Metabolic and developmental responses of alcid chicks to experimental variation in food intake.

I tested whether the ability of chicks to suspend growth and developmental processes in response to food shortages is greater among alcids with food resources that fluctuate over short time periods than it is among close relatives with food that is continuously available. I examined changes in chick resting metabolic rate (RMR) in response to short-term food deprivation in horned and tufted puffins (intermittent food provisioning) and crested and parakeet auklets (continuous food provisioning). RMR was based on measurements of chick oxygen consumption rates (Vo2) under thermoneutral conditions. RMR of postabsorptive chicks scaled allometrically with body mass, and regression slopes were statistically indistinguishable among species. Mass-independent RMR of the same individuals decreased significantly after 48 h of food deprivation. The decrease in the mass-independent RMR was greater in puffins (46.8% in horned and 47.4% in tufted puffins) than in auklets (29.4% in crested and 23.7% in parakeet auklets). To test whether the observed decrease in RMR was due to less energy being allocated to growth, I examined developmental responses of horned and tufted puffins to experimental variation in rates of food intake. I found retarded growth rates in body mass, skeletal elements, and feathers in chicks experiencing low rates of food intake. The retardation of growth processes extended the developmental period. My findings suggest that developmental plasticity in juvenile alcids might be related to temporal variability of prey in oceanic environments.