Microbiota composition and diversity of multiple body sites vary according to reproductive performance in a seabird.

The microbiota is suggested to be a fundamental contributor to host reproduction and survival, but associations between microbiota and fitness are rare, especially for wild animals. Here, we tested the association between microbiota and two proxies of breeding performance in multiple body sites of the black-legged kittiwake, a seabird species. First we found that, in females, nonbreeders (i.e., birds that did not lay eggs) hosted different microbiota composition to that of breeders in neck and flank feathers, in the choanae, in the outer-bill and in the cloacae, but not in preen feathers and tracheae. These differences in microbiota might reflect variations in age or individual quality between breeders and nonbreeders. Second, we found that better female breeders (i.e., with higher body condition, earlier laying date, heavier eggs, larger clutch, and higher hatching success) had lower abundance of several Corynebacteriaceae in cloaca than poorer female breeders, suggesting that these bacteria might be pathogenic. Third, in females, better breeders had different microbiota composition and lower microbiota diversity in feathers, especially in preen feathers. They had also reduced dispersion in microbiota composition across body sites. These results might suggest that good breeding females are able to control their feather microbiota-potentially through preen secretions-more tightly than poor breeding females. We did not find strong evidence for an association between reproductive outcome and microbiota in males. Our results are consistent with the hypothesis that natural variation in the microbiota is associated with differences in host fitness in wild animals, but the causal relationships remain to be investigated.

Sex and hatching order modulate the association between MHC-II diversity and fitness in early-life stages of a wild seabird.

Genes of the major histocompatibility complex (MHC) play a pivotal role in parasite resistance, and their allelic diversity has been associated with fitness variations in several taxa. However, studies report inconsistencies in the direction of this association, with either positive, quadratic or no association being described. These discrepancies may arise because the fitness costs and benefits of MHC diversity differ among individuals depending on their exposure and immune responses to parasites. Here, we investigated in black-legged kittiwake (Rissa tridactyla) chicks whether associations between MHC class-II diversity and fitness vary with sex and hatching order. MHC-II diversity was positively associated with growth and tick clearance in female chicks, but not in male chicks. Our data also revealed a positive association between MHC-II diversity and survival in second-hatched female chicks (two eggs being the typical clutch size). These findings may result from condition-dependent parasite infections differentially impacting sexes in relation to hatching order. We thus suggest that it may be important to account for individual heterogeneities in traits that potentially exert selective pressures on MHC diversity in order to properly predict MHC-fitness associations.

Red coloration varies with dietary carotenoid access and nutritional condition in kittiwakes.

Carotenoid-based ornaments are common signaling features in animals. Although the mechanisms that link color-based signals to individual condition is key to understanding the evolution and function of these ornaments, they are most often poorly known. Several hypotheses have been posited. They include: (i) the role of foraging abilities on carotenoid acquisition and thereby carotenoid-based ornaments, and (ii) the role of internal processes linked to individual quality on the allocation and conversion of carotenoids in integuments. Here, we tested the influence of dietary carotenoid access versus internal process on gape coloration in black-legged kittiwakes (Rissa tridactyla). This seabird displays a vibrant red gape, whose coloration varies with individual quality in males and is due to the deposition of red ketocarotenoids, such as astaxanthin. We decreased hydroxycarotenoid and ketocarotenoid levels in plasma, but increased efficiency in internal processes linked to nutritional condition, by supplementing breeding males with capelin, a natural energy-rich fish prey. We found that, despite having lower carotenoid levels in plasma, supplemented birds developed redder coloration than control birds, but only in the year when dietary levels of astaxanthin in the natural diet were low. In contrast, in the astaxanthin-rich year, supplemented males had a less-red gape than unsupplemented birds. These results suggest that inter-individual differences in internal processes may be sufficient to maintain the honesty of gape coloration under conditions of low dietary astaxanthin levels. Nonetheless, when inter-individual variations in dietary astaxanthin levels are elevated (such as in the crustacean-rich year), carotenoid access seems a more limiting factor to the expression of gape coloration than internal processes. Therefore, our study revealed a complex mechanism of gape color production in kittiwakes, and suggests that the main factor maintaining the condition dependency of this ornaments may vary with environmental conditions and diet composition.

Coping with change in predation risk across space and time through complementary behavioral responses.

BACKGROUND: Our picture of behavioral management of risk by prey remains fragmentary. This partly stems from a lack of studies jointly analyzing different behavioral responses developed by prey, such as habitat use and fine-scale behavior, although they are expected to complement each other. We took advantage of a simple system on the Kerguelen archipelago, made of a prey species, European rabbit Oryctolagus cuniculus, a predator, feral cat Felis catus, and a mosaic of closed and open foraging patches, allowing reliable assessment of spatio-temporal change in predation risk. We investigated the way such a change triggered individual prey decisions on where, when and how to perform routine activities. RESULTS: Rabbit presence and behavior were recorded both day and night in patches with similar foraging characteristics, but contrasted in terms of openness. Cats, individually recognizable, were more active at night and in closed patches, in line with their expected higher hunting success in those conditions. Accordingly, rabbits avoided using closed patches at night and increased their vigilance if they did. Both day and night, rabbits increased their use of closed patches as compared to open patches in windy conditions, thereby probably reducing the thermoregulatory costs expected under such harsh environmental conditions. CONCLUSIONS: Overall, our data map the landscape of fear in this study system and indicate that prey habitat use and vigilance complement each other. Solely focusing on one or the other tactic may lead to erroneous conclusions regarding the way predation risk triggers prey decisions. Finally, future studies should investigate inter-individual variability in the relative use of these different types of complementary behavioral responses to perceived risk, along with the determinants and outcomes of such tactics.

Between-gender differences in vigilance do not necessarily lead to differences in foraging-vigilance tradeoffs.

When prey are time limited in their access to food, any trade-off involving time should ultimately affect their intake rate. In many herbivores, males and females experience different ecological pressures affecting their survival and reproduction because of differences in morphology, physiology and energy/nutrient requirements. If males and females have different vigilance strategies that affect their intake rates differently, they will suffer different foraging costs. This is particularly relevant in sexually monomorphic herbivores, where the two sexes have similar basal energy/nutrient requirements and risk of predation. We investigated how gender, reproductive status, age, group size, predation risk, and food biomass affected vigilance, intake rate, and their trade-off in a monomorphic species, the plains zebra (Equus quagga). Males were more vigilant than females, and lactating females were less vigilant than other females; the levels of vigilance were low (ca. 10 % of feeding time). The effects on time spent feeding, bite rates and intake rates were small and statistically not significant. Reproductive status did not affect the strength of the relationship between vigilance and intake rate, but intake rates increased with group size and, for adult females, were higher in tall grass. While gender and reproductive status were major drivers of vigilance, and group size and food biomass of the rate of food intake, males and females adjust their bite rates and food intake with vigilance in similar ways. Our results support the hypothesis that in monomorphic animals, males and females seem to make similar trade-offs (i.e. adjustments) between vigilance and intake rate.

Analyzing the proximity to cover in a landscape of fear: a new approach applied to fine-scale habitat use by rabbits facing feral cat predation on Kerguelen archipelago.

Although proximity to cover has been routinely considered as an explanatory variable in studies investigating prey behavioral adjustments to predation pressure, the way it shapes risk perception still remains equivocal. This paradox arises from both the ambivalent nature of cover as potentially both obstructive and protective, making its impact on risk perception complex and context-dependent, and from the choice of the proxy used to measure proximity to cover in the field, which leads to an incomplete picture of the landscape of fear experienced by the prey. Here, we study a simple predator-prey-habitat system, i.e., rabbits Oryctolagus cuniculus facing feral cat Felis catus predation on Kerguelen archipelago. We assess how cover shapes risk perception in prey and develop an easily implementable field method to improve the estimation of proximity to cover. In contrast to protocols considering the "distance to nearest cover", we focus on the overall "area to cover". We show that fine-scale habitat use by rabbits is clearly related to our measure, in accordance with our hypothesis of higher risk in patches with smaller area to cover in this predator-prey-habitat system. In contrast, classical measures of proximity to cover are not retained in the best predictive models of habitat use. The use of this new approach, together with a more in-depth consideration of contrasting properties of cover, could help to better understand the role of this complex yet decisive parameter for predator-prey ecology.

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.

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.

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.

Age-related differences in the cloacal microbiota of a wild bird species.

BACKGROUND: Gastrointestinal bacteria play a central role in the health of animals. The bacteria that individuals acquire as they age may therefore have profound consequences for their future fitness. However, changes in microbial community structure with host age remain poorly understood. We characterised the cloacal bacteria assemblages of chicks and adults in a natural population of black-legged kittiwakes (Rissa tridactyla), using molecular methods. RESULTS: We show that the kittiwake cloaca hosts a diverse assemblage of bacteria. A greater number of total bacterial OTUs (operational taxonomic units) were identified in chicks than adults, and chicks appeared to host a greater number of OTUs that were only isolated from single individuals. In contrast, the number of bacteria identified per individual was higher in adults than chicks, while older chicks hosted more OTUs than younger chicks. Finally, chicks and adults shared only seven OTUs, resulting in pronounced differences in microbial assemblages. This result is surprising given that adults regurgitate food to chicks and share the same nesting environment. CONCLUSIONS: Our findings suggest that chick gastrointestinal tracts are colonised by many transient species and that bacterial assemblages gradually transition to a more stable adult state. Phenotypic differences between chicks and adults may lead to these strong differences in bacterial communities. These data provide the framework for future studies targeting the causes and consequences of variation in bacterial assemblages in wild birds.

Human disturbances, habitat characteristics and social environment generate sex-specific responses in vigilance of Mediterranean mouflon.

In prey species, vigilance is an important part of the decision making process related to predation risk effects. Therefore, understanding the mechanisms shaping vigilance behavior provides relevant insights on factors influencing individual fitness. We investigated the role of extrinsic and intrinsic factors on vigilance behavior in Mediterranean mouflon (Ovis gmelini musimon×Ovis sp.) in a study site spatially and temporally contrasted in human pressures. Both sexes were less vigilant in the wildlife reserve compared to surrounding unprotected areas, except for males during the hunting period. During this period, males tended to be less strictly restricted to the reserve than females what might lead to a pervasive effect of hunting within the protected area, resulting in an increase in male vigilance. It might also be a rutting effect that did not occur in unprotected areas because males vigilance was already maximal in response to human disturbances. In both sexes, yearlings were less vigilant than adults, probably because they traded off vigilance for learning and energy acquisition and/or because they relied on adult experience present in the group. Similarly, non-reproductive females benefited of the vigilance effort provided by reproductive females when belonging to the same group. However, in the absence of reproductive females, non-reproductive females were as vigilant as reproductive females. Increasing group size was only found to reduce vigilance in females (up to 17.5%), not in males. We also showed sex-specific responses to habitat characteristics. Females increased their vigilance when habitat visibility decreased (up to 13.8%) whereas males increased their vigilance when feeding on low quality sites, i.e., when concomitant increase in chewing time can be devoted to vigilance with limited costs. Our global approach was able to disentangle the sex-specific sources of variation in mouflon vigilance and stressed the importance of reserves in managing and conserving wild sheep populations.

Reciprocal modulation of internal and external factors determines individual movements.

Movement is fundamental to individual and population dynamics, as it allows individuals to meet their basic requirements. Although movement patterns reflect interactions between internal and external factors, only few studies have examined the effects of these factors on movement simultaneously, and they generally focused on particular biological contexts (e.g. dispersal, foraging). However, the relative importance of these factors in driving individual routine movements might reflect a species' potential flexibility to cope with landscape changes and therefore buffer their potential impact on fitness. We used data from GPS collars on Scandinavian brown bears to investigate the relative role of these factors, as well as an additional factor (period of the year) on routine movements at two spatial scales (hourly and daily relocations). As expected, internal factors played a major role in driving movement, compared to external factors at both scales, but its relative importance was greater at a finer scale. In particular, the interaction between reproductive status and period of the year was one of the most influential variables, females being constrained by the movement capacity of their cubs in the first periods of the year. The effect of human disturbance on movement was also greater for females with cubs than for lone females. This study showed how reciprocal modulation of internal and external factors is shaping space use of brown bears. We stress that these factors should be studied simultaneously to avoid the risk of obtaining context-dependent inferences. Moreover, the study of their relative contribution is also highly relevant in the context of multiple-use landscapes, as human activities generally affect the landscape more than they affect the internal states of an individual. Species or individuals with important internal constraints should be less responsive to changes in their environment as they have less freedom from internal constraints and should thus be more sensitive to human alteration of the landscape, as shown for females with cubs in this study.

Investigating differences in vigilance tactic use within and between the sexes in eastern grey kangaroos.

Aggregation is thought to enhance an animal's security through effective predator detection and the dilution of risk. A decline in individual vigilance as group size increases is commonly reported in the literature and called the group size effect. However, to date, most of the research has only been directed toward examining whether this effect occurs at the population level. Few studies have explored the specific contributions of predator detection and risk dilution and the basis of individual differences in the use of vigilance tactics. We tested whether male and female (non-reproductive or with young) eastern grey kangaroos (Macropus giganteus) adopted different vigilance tactics when in mixed-sex groups and varied in their reliance on predator detection and/or risk dilution as group size changed. This species exhibits pronounced sexual dimorphism with females being much smaller than males, making them differentially vulnerable toward predators. We combined field observations with vigilance models describing the effects of detection and dilution on scanning rates as group size increased. We found that females with and without juveniles relied on predator detection and risk dilution, but the latter adjusted their vigilance to the proportion of females with juveniles within their group. Two models appeared to equally support the data for males suggesting that males, similarly to females, relied on predator detection and risk dilution but may also have adjusted their vigilance according to the proportion of mothers within their group. Differential vulnerability may cause sex differences in vigilance tactic use in this species. The presence of males within a group that do not, or only partially, contribute to predator detection and are less at risk may cause additional security costs to females. Our results call for reexamination of the classical view of the safety advantages of grouping to provide a more detailed functional interpretation of gregariousness.

Detecting predators and locating competitors while foraging: an experimental study of a medium-sized herbivore in an African savanna.

Vigilance allows individuals to escape from predators, but it also reduces time for other activities which determine fitness, in particular resource acquisition. The principles determining how prey trade time between the detection of predators and food acquisition are not fully understood, particularly in herbivores because of many potential confounding factors (such as group size), and the ability of these animals to be vigilant while handling food. We designed a fertilization experiment to manipulate the quality of resources, and compared awareness (distinguishing apprehensive foraging and vigilance) of wild impalas (Aepyceros melampus) foraging on patches of different grass height and quality in a wilderness area with a full community of predators. While handling food, these animals can allocate time to other functions. The impalas were aware of their environment less often when on good food patches and when the grass was short. The animals spent more time in apprehensive foraging when grass was tall, and no other variable affected apprehensive behavior. The probability of exhibiting a vigilance posture decreased with group size. The interaction between grass height and patch enrichment also affected the time spent in vigilance, suggesting that resource quality was the main driver when visibility is good, and the risk of predation the main driver when the risk is high. We discuss various possible mechanisms underlying the perception of predation risk: foraging strategy, opportunities for scrounging, and inter-individual interference. Overall, this experiment shows that improving patch quality modifies the trade-off between vigilance and foraging in favor of feeding, but vigilance remains ultimately driven by the visibility of predators by foragers within their feeding patches.