Frédéric Angelier

Stress Response and the Value of Reproduction : Are Birds Prudent Parents?

In vertebrates, stressors such as starvation or predator attacks stimulate the rapid elevation of circulating glucocorticoid hormones, triggering physiological and behavioral responses that aid immediate survival but simultaneously inhibit reproduction. This stress response has been proposed to serve as a physiological mediator of life‐history trade‐offs: when the value of current reproduction is high relative to the value of future reproduction and survival, a mitigated stress response is expected to enable successful breeding and maximize fitness. Using phylogenetic comparative analyses, we investigated baseline and peak stress‐induced plasma corticosterone levels during parental care in 64 bird species. We found that (1) species with a higher value of the current brood relative to future breeding mounted weaker corticosterone responses during acute stress, and (2) females in species with more female‐biased parental care had weaker corticosterone responses. These results support the brood value hypothesis, suggesting that the stress response evolves as an adaptive basis for life‐history strategies. Further, we found that (3) baseline corticosterone correlated positively with brood value and negatively with body mass, and (4) peak corticosterone was greater in species breeding at higher latitudes. The latter findings suggest that circulating corticosterone concentrations might be matched to the anticipated demands and risks during nesting.

Corticosterone and Foraging Behavior in a Pelagic Seabird

Because endocrine mechanisms are thought to mediate behavioral responses to changes in the environment, examining these mechanisms is essential for understanding how long‐lived seabirds adjust their foraging decisions to contrasting environmental conditions in order to maximize their fitness. In this context, the hormone corticosterone (CORT) deserves specific attention because of its major connections with locomotor activities. We examined for the first time the relationships between individual CORT levels and measurements of foraging success and behavior using satellite tracking and blood sampling from wandering albatrosses (Diomedea exulans) before (pretrip CORT levels) and after (posttrip CORT levels) foraging trips during the incubation period. Plasma CORT levels decreased after a foraging trip, and the level of posttrip CORT was negatively correlated with individual foraging success, calculated as total mass gain over a foraging trip. Pretrip CORT levels were not linked to time spent at sea but were positively correlated with daily distance traveled and maximum range at sea. In this study, we were able to highlight the sensitivity of CORT levels to variation in energy intake, and we showed for the first time that individual CORT levels can be explained by variation in foraging success. Relationships between pretrip CORT levels and daily distance traveled and maximum range were independent of pretrip body mass, suggesting that slight elevations in pretrip CORT levels might facilitate locomotor activity. However, because both foraging behavior and pretrip CORT levels could be affected by individual quality, future experimental studies including manipulation of CORT levels are needed to test whether CORT can mediate foraging decisions according to foraging conditions.

Hormonal correlates of individual quality in a long-lived bird: a test of the ‘corticosterone–fitness hypothesis’

Measuring individual quality in vertebrates is difficult. Focusing on allostasis mechanisms may be useful because they are functionally involved in the ability of an individual to survive and reproduce in its environment. Thus, a rise in stress hormones levels (corticosterone) occurs when an organism has to cope with challenging environmental conditions. This has recently led to the proposal of the ‘cort–fitness hypothesis’, which suggests that elevated baseline corticosterone levels should be found in individuals of poor quality that have difficulty coping with their environment. We tested this hypothesis by comparing an integrative measure of individual quality to baseline corticosterone in black-browed albatrosses (Thalassarche melanophrys). We found that individual baseline corticosterone levels were related to individual quality and highly repeatable from one breeding season to the next. Importantly, this relationship was found in males, but not in females. Therefore, we suggest that the relationship between quality and baseline corticosterone levels may depend on the environmental and energetic constraints that individuals have to cope with.

Importance of the glucocorticoid stress response in a changing world: Theory, hypotheses and perspectives

In this perspective paper, we emphasize the importance that integrative mechanisms, and especially the GC (glucocorticoid) stress response, can play in the ability of vertebrates to cope with ongoing global change. The GC stress response is an essential mediator of allostasis (i.e., the responses of an organism to a perturbation) that aims at maintaining stability (homeostasis) despite changing conditions. The GC stress response is a complex mechanism that depends on several physiological components and aims at promoting immediate survival at the expense of other life-history components (e.g., reproduction) when a labile perturbation factor (LPF) occurs. Importantly, this mechanism is somewhat flexible and its degree of activation can be adjusted to the fitness costs and benefits that result from the GC stress response. Therefore, this GC stress response mediates life-history decisions and is involved in the regulation of important life-history trade-offs. By inducing abrupt and rapid changes in the regime of LPFs, we believe that global change can affect the efficiency of the GC stress response to maintain homeostasis and to appropriately regulate these trades-offs. This dysfunction may result in an important mismatch between new LPFs and the associated GC stress response and, thus, in the inability of vertebrates to cope with a changing world. In that context, it is essential to better understand how the GC stress response can be adjusted to new LPFs through micro-evolution, phenotypic plasticity and phenotypic flexibility (habituation and sensitization). This paper sets up a theoretical framework, hypotheses and new perspectives that will allow testing and better understanding how the GC stress response can help or constrain individuals, populations and species to adjust to ongoing global change.

Corticosterone and time-activity budget: An experiment with Black-legged kittiwakes

In vertebrates, the well established increase in plasma corticosterone in response to food shortage is thought to mediate adjustments of foraging behavior and energy allocation to environmental conditions. However, investigating the functional role of corticosterone is often constrained by the difficulty to track time-activity budget of free-ranging animals. To examine how an experimental increase in corticosterone affects the activity budget of male Black-legged kittiwakes (Rissa tridactyla), we used miniaturized activity loggers to record flying/foraging, presence on the sea surface and nest attendance. To investigate how corticosterone affects allocation processes between self-foraging and foraging devoted to the brood, we monitored body mass change of males from capture (day 0) to recapture (day 3). Among control birds, males in poor condition at day 0 spent significantly more time flying/foraging and less time attending the nest site than did males in good condition. Corticosterone treatment affected time spent flying/foraging in interaction with body condition at day 0: corticosterone-implanted males in good condition spent more time flying/foraging than control ones; this was not observed in poor condition males. In control birds, change in body mass was negatively correlated with body condition at day 0. This was reinforced by corticosterone treatment and, on average, corticosterone-implanted males gained much more mass than controls. These results suggest that in Black-legged kittiwakes, body condition and corticosterone levels can interact to mediate foraging decisions and possibly energy allocation: when facing stressful environmental conditions, birds in good body condition may afford to increase the time spent foraging probably to maintain brood provisioning, whereas poor body condition birds seemed rather to redirect available energy from reproduction to self-maintenance.

To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird

Mercury, a ubiquitous toxic element, is known to alter expression of sex steroids and to impair reproduction across vertebrates but the mechanisms underlying these effects are not clearly identified. We examined whether contamination by mercury predicts the probability to skip reproduction in black-legged kittiwakes (Rissa tridactyla) from Svalbard. We also manipulated the endocrine system to investigate the mechanism underlying this relationship. During the pre-laying period, we injected exogenous GnRH (gonadotropin-releasing hormone) to test the ability of the pituitary to release luteinizing hormone (LH, a key hormone for the release of sex steroids and hence breeding) in relation to mercury burden. Birds that skipped reproduction had significantly higher mercury concentration in blood than breeders. Endocrine profiles of these birds also varied based on breeding status (breeders versus non-breeders), mercury contamination and sex. Specifically, in skippers (birds that did not breed), baseline LH decreased with increasing mercury concentration in males, whereas it increased in females. GnRH-induced LH levels increased with increasing mercury concentration in both sexes. These results suggest that mercury contamination may disrupt GnRH input to the pituitary. Thus, high mercury concentration could affect the ability of long-lived birds to modulate their reproductive effort (skipping or breeding) according to ongoing environmental changes in the Arctic, thereby impacting population dynamics.

Does stress response predict return rate in a migratory bird species? A study of American redstarts and their non-breeding habitat

In vertebrates, the adrenocortical stress response activates an emergency life-history stage, which is thought to promote survival by helping individuals escape life-threatening situations. Although the adrenocortical stress response promotes many behavioural and physiological changes, it remains unclear whether this stress response actually translates into higher survival in wild vertebrates. We measured the adrenocortical stress response of non-breeding American redstarts (Setophaga ruticilla), a migratory bird that wintered in habitats of either high (mangroves) or low suitability (scrubs), and subsequently monitored their return rate during the following non-breeding seasons. The intensity of the adrenocortical stress response was consistent within individuals across the non-breeding season and was positively correlated with return rates in redstarts that wintered in scrubs, but not in redstarts that wintered in mangroves. Thus, in a context-dependent manner, the ability of an individual to physiologically react to stress determines its ability of returning to its non-breeding territory the following winters. For an individual, the ability to mount an important adrenocortical stress response probably benefits to survival. However, this beneficial effect probably depends on an individuals environment and phenotypic characteristics because these two variables are likely to affect its probability of being confronted with life-threatening stressors during its annual life cycle.

Corticosterone and foraging behavior in a diving seabird: the Adélie penguin, Pygoscelis adeliae.

Because hormones mediate physiological or behavioral responses to intrinsic or extrinsic stimuli, they can help us understand how animals adapt their foraging decisions to energetic demands of reproduction. Thus, the hormone corticosterone deserves specific attention because of its influence on metabolism, food intake and locomotor activities. We examined the relationships between baseline corticosterone levels and foraging behavior or mass gain at sea in a diving seabird, the Adélie penguin, Pygoscelis adeliae. Data were obtained from free-ranging penguins during the brooding period (Adélie Land, Antarctica) by using satellite transmitters and time-depth-recorders. The birds were weighed and blood sampled before and after a foraging trip (pre-trip and post-trip corticosterone levels, respectively). Penguins with elevated pre-trip corticosterone levels spent less time at sea and stayed closer to the colony than penguins with low pre-trip corticosterone levels. These short trips were associated with a higher foraging effort in terms of diving activity and a lower mass gain at sea than long trips. According to previous studies conducted on seabird species, these results suggest that penguins with elevated pre-trip corticosterone levels might maximize the rate of energy delivery to the chicks at the expense of their body reserves. Moreover, in all birds, corticosterone levels were lower post-foraging than pre-foraging. This decrease could result from either the restoration of body reserves during the foraging trip or from a break in activity at the end of the foraging trip. This study demonstrates for the first time in a diving predator the close relationships linking foraging behavior and baseline corticosterone levels. We suggest that slight elevations in pre-trip corticosterone levels could play a major role in breeding effort by facilitating foraging activity in breeding seabirds.

Long-term survival effect of corticosterone manipulation in Black-legged kittiwakes

The secretion of corticosterone in response to stress is thought to be an adaptive mechanism, which promotes immediate survival at the expense of current reproduction. However, at the individual level, the hypothesis of a corticosterone-related survival appears to be complex. In this study, we tested this hypothesis by combining for the first time an experimental manipulation of corticosterone levels and capture-mark-recapture (CMR) models. To do so, we increased corticosterone levels of chick-rearing Black-legged kittiwakes (Rissa tridactyla) via subcutaneous implants. Then, we monitored the long-term survival of kittiwakes over the 2 consecutive years. Corticosterone-implanted birds showed a significantly lower apparent annual survival than sham-implanted ones (46.9% vs 77.8%). This result is supported by the well-known deleterious effects of elevated corticosterone levels on cognitive and immune functions. Alternately and in the light of recent studies, our experimental manipulation may have down-regulated the endogenous secretion of corticosterone through a prolonged negative feedback. If so, the corticosterone-implanted kittiwakes may have failed to trigger an appropriate stress response during subsequent life-threatening perturbations, hence being unable to adjust their behavior and physiology toward immediate survival. This study highlights the complex long-term consequences of corticosterone manipulation on fitness in free-living vertebrates.

Telomere length, non‐breeding habitat and return rate in male American redstarts

Summary 1. Telomeres are long repetitive noncoding sequences of DNA located at the ends of chromosomes. Recently, the study of telomere dynamics has been increasingly used to investigate ecological questions. However, little is currently known about the relationships that link environmental conditions, telomere dynamics and fitness in wild vertebrates. 2. Using a small migratory bird (American redstart, Setophaga ruticilla), we investigated how telomere dynamics can be affected by non-breeding habitat quality and to what extent telomere length can predict the return rate of males. 3. We show that telomeres shorten in most individuals over a 1-year period and, importantly, that telomeres of individuals wintering in a low-quality habitat shorten more than those of individuals wintering in a high-quality habitat. 4. In addition, we found that longer telomeres are associated with a higher return rate than shorter telomeres, although the relationship between return rate and telomere length did not depend on habitat quality. 5. Our study suggests that telomere dynamics are affected by environmental conditions and are related to indices of fitness in a migratory bird species.