Thomas Merkling

An individual and a sex odor signature in kittiwakes? Study of the semiochemical composition of preen secretion and preen down feathers

The importance of olfaction in birds’ social behavior has long been denied. Avian chemical signaling has thus been relatively unexplored. The black-legged kittiwake provides a particularly appropriate model for investigating this topic. Kittiwakes preferentially mate with genetically dissimilar individuals, but the cues used to assess genetic characteristics remain unknown. As in other vertebrates, their body odors may carry individual and sexual signatures thus potentially reliably signaling individual genetic makeup. Here, we test whether body odors in preen gland secretion and preen down feathers in kittiwakes may provide a sex and an individual signature. Using gas chromatography and mass spectrometry, we found that male and female odors differ quantitatively, suggesting that scent may be one of the multiple cues used by birds to discriminate between sexes. We further detected an individual signature in the volatile and nonvolatile fractions of preen secretion and preen down feathers. These results suggest that kittiwake body odor may function as a signal associated with mate recognition. It further suggests that preen odor might broadcast the genetic makeup of individuals, and could be used in mate choice to assess the genetic compatibility of potential mates.

Preen secretions encode information on MHC similarity in certain sex-dyads in a monogamous seabird

Animals are known to select mates to maximize the genetic diversity of their offspring in order to achieve immunity against a broader range of pathogens. Although several bird species preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC), it remains unknown whether they can use olfactory cues to assess MHC similarity with potential partners. Here we combined gas chromatography data with genetic similarity indices based on MHC to test whether similarity in preen secretion chemicals correlated with MHC relatedness in the black-legged kittiwake (Rissa tridactyla), a species that preferentially mates with genetically dissimilar partners. We found that similarity in preen secretion chemicals was positively correlated with MHC relatedness in male-male and male-female dyads. This study provides the first evidence that preen secretion chemicals can encode information on MHC relatedness and suggests that odor-based mechanisms of MHC-related mate choice may occur in birds.

Is natural hatching asynchrony optimal? An experimental investigation of sibling competition patterns in a facultatively siblicidal seabird

In unpredictable environments, any tactic that enables avian parents to adjust brood size and, thus, energy expenditure to environmental conditions should be favoured. Hatching asynchrony (HA), which occurs whenever incubation commences before clutch completion, may comprise such a tactic. For instance, the sibling rivalry hypothesis states that the hierarchy among chicks, concomitant to HA, should both facilitate the adjustment of brood size to environmental conditions and reduce several components of sibling competition as compared to synchronous hatching, at both brood and individual levels. We thus predicted that brood aggression, begging and feeding rates should decrease and that older chick superiority should increase with HA increasing, leading to higher growth and survival rates. Accordingly, we investigated the effects of an experimental upward and downward manipulation of HA magnitude on behaviour, growth and survival of black-legged kittiwake (Rissa tridactyla) chicks. In line with the sibling rivalry hypothesis, synchronous hatching increased aggression and tended to increase feeding rates by parents at the brood level. Begging rates, however, increased with HA contrary to our expectations. At the individual level, as HA magnitude increased, the younger chick was attacked and begged proportionally more often, experienced a slower growth and a higher mortality than its sibling. Overall, the occurrence of energetic costs triggered by synchronous hatching both for parents and chicks, together with the lower growth rate and increased mortality of the younger chick in highly asynchronous broods suggest that natural HA magnitude may be optimal.

Carotenoids increase immunity and sex specifically affect color and redox homeostasis in a monochromatic seabird

Carotenoid-based integument coloration is extremely widespread in animals and commonly used as an honest signal of condition in sexual selection. Besides being used for color expression, carotenoids have antioxidant and immunomodulatory activity. Being a limited resource, carotenoid allocation to competing demands generates a trade-off. Recent studies, however, suggest that the antioxidant role of carotenoids might not be as important as previously thought. To shed light on the mechanism maintaining carotenoid-based signal honesty in the black-legged kittiwake (Rissa tridactyla), we supplemented males and females with dietary yellow xanthophylls (lutein and zeaxanthin) during the chick-rearing period, when male coloration may be a good indicator of future reproductive success. The supplementation affected plasma carotenoid levels similarly in males and females, i.e., it increased the levels of lutein but decreased the levels of total astaxanthin, one of the main pigments coloring integuments in this species. Supplemented adults and their chicks had stronger immune response than controls, suggesting that yellow xanthophylls enhance the innate immune system in kittiwakes. However, supplementation caused sex-specific effects on integument coloration and oxidative stress. Supplemented males had duller integuments, but similar oxidative damages compared to control males, while supplemented females had more colorful integuments, but higher oxidative damages than control females. Because the increase in lutein was associated with a decrease in other potential antioxidants (i.e., astaxanthin and vitamin A), the role of carotenoids as antioxidants in kittiwakes remains undetermined. Our results, however, indicate that the trade-off responses to carotenoid availability are sex-specific in kittiwakes.

Reproductive effort and oxidative stress: effects of offspring sex and number on the physiological state of a long‐lived bird

Summary 1.Individuals must trade-off between energetically costly activities to maximise their fitness. However, the underlying physiological mechanism remains elusive. Oxidative stress, the imbalance between reactive oxygen species production and antioxidant and/or repair activities, has been suggested to underlie life-history trade-offs: greater investment in reproduction supposedly generating higher oxidative damage, thus reducing lifespan. 2.While most studies used natural or experimental variation in offspring number to examine how reproduction affects oxidative stress, none studied the impact of offspring sex, although it could influence physiological costs and fitness, if the sexes differ in terms of energetic cost. 3.Here, we aim at further understanding how reproduction (in terms of offspring sex, experimentally manipulated, and number, not manipulated) influences oxidative stress in a wild seabird, where sons are energetically costlier than daughters. We did so by conducting a chick fostering experiment (to disentangle foster and produced sex-ratio) and using four oxidative stress markers plus baseline corticosterone. 4.First, the results suggest that individual physiological state before laying modulates upcoming reproductive effort. Individuals with higher pre-laying baseline corticosterone and lower antioxidant activity, estimated by their superoxide dismutase activity, subsequently invested more in reproduction, estimated by the cumulative number of days spent rearing chicks. Hence, it seems that only individuals that could afford to invest heavily in reproduction did so. 5.Then, we examined the effects of reproductive effort on individual physiological state at the end of the breeding season. Higher reproductive effort seemed to imply higher physiological costs. Oxidative stress, estimated by the ratio of oxidised over reduced glutathione, increased with more male-biased foster sex-ratio among mothers but not among fathers, whereas baseline corticosterone did so in both sexes. Similarly, lipid oxidative damage to red blood cells increased with increasing cumulative number of days spent rearing chicks. 6.Our study provides the first evidence that brood sex-ratio variation can affect oxidative balance, potentially in a sex-specific way, although more studies are needed to understand whether the observed physiological costs could lead to fitness costs. It also highlights the need to consider sex-ratio in future studies investigating the role of oxidative stress in life-history trade-offs. This article is protected by copyright. All rights reserved.

Carry-over effects of food supplementation on recruitment and breeding performance of long-lived seabirds

Supplementation of food to wild animals is extensively applied as a conservation tool to increase local production of young. However, in long-lived migratory animals, the carry-over effects of food supplementation early in life on the subsequent recruitment of individuals into natal populations and their lifetime reproductive success are largely unknown. We examine how experimental food supplementation early in life affects: (i) recruitment as breeders of kittiwakes Rissa tridactyla born in a colony on Middleton Island (Alaska) between 1996 and 2006 (n = 1629) that bred in the same colony through 2013 (n = 235); and (ii) breeding success of individuals that have completed their life cycle at the colony (n = 56). Birds were raised in nests that were either supplemented with food (Fed) or unsupplemented (Unfed). Fledging success was higher in Fed compared with Unfed nests. After accounting for hatching rank, growth and oceanic conditions at fledging, Fed fledglings had a lower probability of recruiting as breeders in the Middleton colony than Unfed birds. The per-nest contribution of breeders was still significantly higher for Fed nests because of their higher productivity. Lifetime reproductive success of a subset of kittiwakes that thus far had completed their life cycle was not affected by the food supplementation during development. Our results cast light on the carry-over effects of early food conditions on the vital rates of long-lived animals and support food supplementation as an effective conservation strategy for long-lived seabirds.

Effects of developmental conditions on growth, stress, and telomeres in black‐legged kittiwake chicks

Early‐life conditions can drive ageing patterns and life history strategies throughout the lifespan. Certain social, genetic and nutritional developmental conditions are more likely to produce high‐quality offspring: those with good likelihood of recruitment and productivity. Here, we call such conditions “favoured states” and explore their relationship with physiological variables during development in a long‐lived seabird, the black‐legged kittiwake (Rissa tridactyla). Two favoured states were experimentally generated by manipulation of food availability and brood size, while hatching order and sex were also explored as naturally generating favoured states. Thus, the favoured states we explored were high food availability, lower levels of sibling competition, hatching first and male sex. We tested the effects of favoured developmental conditions on growth, stress, telomere length (a molecular marker associated with lifespan) and nestling survival. Generation of favoured states through manipulation of both the nutritional and social environments furthered our understanding of their relative contributions to development and phenotype: increased food availability led to larger body size, reduced stress and higher antioxidant status, while lower sibling competition (social environment) led to lower telomere loss and longer telomere lengths in fledglings. Telomere length predicted nestling survival, and wing growth was also positively correlated with telomere length, supporting the idea that telomeres may indicate individual quality, mediated by favoured states.

Physiological and fitness correlates of experimentally altered hatching asynchrony magnitude in chicks of a wild seabird

Nest-bound chicks depend entirely on their parents for food, often leading to high sibling competition. Asynchronous hatching, resulting from the onset of incubation before clutch completion, facilitates the establishment of within-nest hierarchy, with younger chicks being subject to lower feeding and growth rates. Because social and nutritional stresses affect baseline stress hormone levels in birds, younger chicks are expected to have higher levels of corticosterone than their siblings. As previous studies showed that hatching asynchrony magnitude influences the course of sibling competition, it should also affect baseline corticosterone. We measured baseline corticosterone at age 5 days in nestling black-legged kittiwakes (Rissa tridactyla) in 3 types of experimental broods: synchronous, asynchronous, and highly asynchronous. Sexual dimorphism takes place during chick-rearing and might also influence baseline corticosterone, we thus included chick sex in our analyses and also monitored chick growth and survival. Baseline corticosterone did not differ among A-chicks, but was higher in B-chicks from highly asynchronous broods compared with the other brood types, in line with the presumed increase in nutritional stress. In asynchronous broods, A-chicks had higher baseline corticosterone than their siblings, contrary to our expectations. We interpret that result as a cost of dominance among A-chicks. In line with previous studies, mass gain was negatively correlated with baseline corticosterone levels. We found that baseline corticosterone predicted survival in a sex-specific way. Regardless of hatching rank, males with higher baseline corticosterone suffered higher mortality, suggesting that males were more sensitive to high level of stress, independently of its cause.