Aurélie Goutte

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.

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.

Demographic responses to mercury exposure in two closely related Antarctic top predators

Although toxic chemicals constitute a major threat for wildlife, their effects have been mainly assessed at the individual level and under laboratory conditions. Predicting population-level responses to pollutants in natural conditions is a major and ultimate task in ecological and ecotoxicological research. The present study aims to estimate the effect of mercury (Hg) levels on future apparent survival rates and breeding performances. We used a long-term data set (-10 years) and recently developed methodological tools on two closely related Antarctic top predators, the South Polar Skua Catharacta maccormicki from Adélie Land and the Brown Skua C. lonnbergi from the Kerguelen Archipelago. Adult survival rates and breeding probabilities were not affected by Hg levels, but breeding success in the following year decreased with increasing Hg levels. Although South Polar Skuas exhibited much lower Hg levels than Brown Skuas, they suffered from higher Hg-induced breeding failure. This species difference could be attributed to an interaction between Hg and other environmental perturbations, including climate change and a complex cocktail of pollutants. By including Hg-dependent demographic parameters in population models, we showed a weak population decline in response to increasing Hg levels. This demographic decline was more pronounced in South Polar Skuas than in Brown Skuas. Hence, Hg exposure differently affects closely related species. The wide range of environmental perturbations in Antarctic regions could exacerbate the demographic responses to Hg levels. In that respect, we urge future population modeling to take into account the coupled effects of climate change and anthropogenic pollution to estimate population projections.

Stress and the timing of breeding: Glucocorticoid-luteinizing hormones relationships in an arctic seabird

In birds, stressful environmental conditions delay the timing of breeding but the underlying mechanisms are poorly understood. The stress hormone corticosterone appears to be a good candidate for mediating the decision to breed and when to start egg-laying, via a possible inhibition of luteinizing hormone (LH) and sex-steroids production. We used luteinizing hormone releasing hormone (LHRH) challenge in pre-laying male and female Black-legged kittiwakes (Rissa tridactyla) to test whether LH and testosterone secretion were depressed by elevated corticosterone levels. Females bearing high baseline corticosterone levels showed reduced baseline LH levels and a low ability to release LH, following LHRH challenge. Further, females bearing low baseline LH levels and elevated baseline corticosterone levels were more likely to skip breeding. However, non-breeding females were physiologically primed for breeding, since they mounted high LHRH-induced LH release. Egg-laying date was advanced in good body condition females but was unaffected by hormones secretion. In males, corticosterone levels had no effect on LH and/or testosterone secretion and did not affect their decision to breed. Interestingly, males with high LHRH-induced testosterone release bred early. Our study highlights clear sex-differences in the HPG sensitivity to stress hormones in pre-laying kittiwakes. Because females have to store body reserves and to build up the clutch, they would be more sensitive to stress than males. Moreover, intrasexual competition could force male kittiwakes to acquire reproductive readiness earlier in the season than females and to better resist environmental perturbations. We suggest that high testosterone releasing ability would mediate behavioural adjustments such as courtship feeding, which would stimulate early egg-laying in females.

Demographic consequences of heavy metals and persistent organic pollutants in a vulnerable long-lived bird, the wandering albatross

Seabirds are top predators of the marine environment that accumulate contaminants over a long life-span. Chronic exposure to pollutants is thought to compromise survival rate and long-term reproductive outputs in these long-lived organisms, thus inducing population decline. However, the demographic consequences of contaminant exposure are largely theoretical because of the dearth of long-term datasets. This study aims to test whether adult survival rate, return to the colony and long-term breeding performance were related to blood mercury (Hg), cadmium (Cd) and persistent organic pollutants (POPs), by using a capture–mark–recapture dataset on the vulnerable wandering albatross Diomedea exulans. We did not find evidence for any effect of contaminants on adult survival probability. However, blood Hg and POPs negatively impacted long-term breeding probability, hatching and fledging probabilities. The proximate mechanisms underlying these deleterious effects are likely multifaceted, through physiological perturbations and interactions with reproductive costs. Using matrix population models, we projected a demographic decline in response to an increase in Hg or POPs concentrations. This decline in population growth rate could be exacerbated by other anthropogenic perturbations, such as climate change, disease and fishery bycatch. This study gives a new dimension to the overall picture of environmental threats to wildlife populations.

Persistent organic pollutants in benthic and pelagic organisms off Adélie Land, Antarctica

The concentrations of polychlorinated biphenyls (PCB), hexachlorobenzene (HCB), pentachlorobenzene (PeCB) and polybrominated diphenylethers (PBDE) were described in benthic and pelagic species collected off Adélie Land, Antarctica. Strong differences were observed among species, with reduced PeCB and HCB levels in benthic species, and elevated PCB levels in the Antarctic yellowbelly rockcod, the Antarctic sea urchin and the snow petrel. Lower-chlorinated congeners were predominant in krill; penta-PCBs in benthic organisms; hexa- and hepta-PCBs in seabirds and cryopelagic fish. This segregation may result from sedimentation process, specific accumulation and excretion, and/or biotransformation processes. The presence of PBDEs in Antarctic coastal organisms may originate from atmospheric transport and partly from a contamination by local sources. Although POP levels in Antarctic marine organisms were substantially lower than in Arctic and temperate organisms, very little is known about their toxic effects on these cold-adapted species, with high degree of endemism.

Experimentally reduced corticosterone release promotes early breeding in black-legged kittiwakes

SUMMARY Breeding at the right time is important for successful reproduction. In birds, stressful environmental conditions are known to delay the timing of breeding but the underlying mechanisms are poorly understood. The stress hormone corticosterone appears to be a good candidate for mediating egg-laying date according to early environmental conditions and physiological state. By experimentally reducing the release of corticosterone in black-legged kittiwakes during the pre-laying period, we tested whether egg-laying date was mechanistically linked to corticosterone levels. Male and female kittiwakes were implanted with a low dose of exogenous corticosterone to inhibit endogenous corticosterone production. According to our predictions, the experimental reduction of corticosterone release was paralleled by a significant advancement of egg laying in females (around 4 days earlier). In addition, females with experimentally reduced corticosterone release gained mass during the pre-laying period compared with controls. Ultimately, the advancement of egg laying in females with experimentally reduced corticosterone levels was associated with an enhanced breeding success. This effect was strongly sex specific. In corticosterone-treated male kittiwakes, egg-laying date and reproductive success were not affected, but breeding probability was lower than in controls. This corticosterone treatment did not influence immediate clutch size, or return rate and breeding decision the following year. Our results support the hypothesis that corticosterone secretion during the pre-laying period mediates the timing of breeding in this long-lived seabird, possibly through the dynamics of energy reserves.

Survival rate and breeding outputs in a high Arctic seabird exposed to legacy persistent organic pollutants and mercury

Chronic exposure to pollutants may represent a threat for wildlife. We tested whether adult survival rate, breeding probability and breeding success the year of sampling and the following year were affected by blood levels of mercury or persistent organic pollutants in Svalbard black-legged kittiwake Rissa tridactyla, by using capture-mark-recapture models over a five-year period. Survival rate was negatively linked to HCB levels in females, to chlordane mixture and oxychlordane, tended to decrease with increasing PCBs or DDE levels, but was unrelated to mercury. Breeding probability decreased with increasing mercury levels during the sampling year and with increasing CHL or HCB levels during the following year, especially in males observed as breeders. Surprisingly, the probability of raising two chicks increased with increasing HCB levels. Although levels of these legacy pollutants are expected to decline, they represent a potential threat for adult survival rate and breeding probability, possibly affecting kittiwake population dynamics.

Relationships between POPs and baseline corticosterone levels in black-legged kittiwakes (Rissa tridactyla) across their breeding cycle

Chronic exposure to persistent organic pollutants (POPs) in wildlife might alter the response to environmental changes through interference with the regulation of stress hormones. Here, we examined the relationship between blood concentrations of several POPs and baseline plasma corticosterone levels in the black-legged kittiwake (Rissa tridactyla) during three distinct periods in the breeding season. The concentrations of POPs and corticosterone increased, whereas body mass decreased progressively from the pre-laying period to the incubation and the chick rearing period. ∑PCB (polychlorinated biphenyls) correlated positively with the baseline corticosterone levels during the pre-laying period, which might suggest that PCBs affect the regulation of corticosterone. However, this relationship was not found during the incubation or the chick rearing period. Possible explanations are discussed with emphasis on how total stress/allostatic load is handled during different periods and conditions.

Age, sex, and breeding status shape a complex foraging pattern in an extremely long‐lived seabird

Evidence of age-dependent changes in foraging behavior of free-ranging individuals is scarce, especially at older stages. Using the isotopic niche as a proxy of the trophic niche during both the breeding (blood) and inter-nesting (feather) periods, we report here empirical evidence for age-, gender-, and breeding status-dependent foraging ecology and examine its potential consequences on subsequent reproduction and survival in an extremely long-lived species, the Wandering Albatross (Diomedea exulans). Immature Wandering Albatrosses of both sexes forage in the subtropics (delta13C) and feed at the same trophic position (delta15N) as the adults. In contrast to immature birds, adult females forage, on average, at more northern latitudes than males, with both sexes feeding in the subtropics during the internesting period, and males, not females, favoring subantarctic waters during incubation. In contrast to adult females, males show a unique pattern among birds and mammals of a continuous change with age in their main feeding habitat by foraging progressively farther south in colder waters during both the breeding and inter-nesting periods. In males, foraging at higher latitudes (lower feather delta13C values) is associated with a lower probability of breeding during the following years compared to other birds, but with no effect on their probability of surviving. Foraging in cold and windy waters may be linked to foraging impairment that might explain different life history trade-offs and lower investment in reproduction with age. This key point requires further longitudinal investigations and/or studies examining foraging success and the energy budget of birds feeding in different water masses.