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.

Stigma associated with parental depression or cancer: Impact on spouse and offspring's cortisol levels and socioemotional functioning.

Stress associated with caring for a mentally ill spouse can adversely affect the health status of caregivers and their children. Adding to the stress of caregiving is the stigma often placed against spouses and children of people with mental illness. Contrary to mental illness, many physical disorders such as cancer may be less stigmatized (expect pulmonary cancer). In this study, we measured externalized and internalized stigma, as well as psychological (depressive symptoms and stressful life events) and physiological (basal salivary cortisol levels) markers of stress in 115 spouses and 154 children of parents suffering from major depressive disorder, cancer, or no illness (control group). The results show that spouses and children from families with parental depression present significantly more externalized stigma than spouses and children from families with parental cancer or no illness, although we find no group differences on internalized stigma. The analysis did not show a significant group difference either for spouses or their children on depressive symptomatology, although spouses from the parental depression group reported greater work/family stress. Finally, we found that although for both spouses children the awakening cortisol response was greater on weekdays than on weekend days, salivary cortisol levels did not differ between groups. Bayes factor calculated on the null result for cortisol levels was greater than 100, providing strong evidence for the null hypothesis H0. Altogether, these results suggest an impact of stigma toward mental health disorder on psychological markers of stress but no impact of stigma on physiological markers of stress. We suggest that these results may be due to the characteristics of the families who participated in the present study.

Plumage microbiota covaries with the major histocompatibility complex in blue petrels.

To increase fitness, a wide range of vertebrates preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC) or that have high MHC diversity. Although MHC often can be assessed through olfactory cues, the mechanism by which MHC genes influence odour remains largely unclear. MHC class IIB molecules, which enable recognition and elimination of extracellular bacteria, have been suggested to influence odour indirectly by shaping odour-producing microbiota, i.e. bacterial communities. However, there is little evidence of the predicted covariation between an animal's MHC genotype and its bacterial communities in scent-producing body surfaces. Here, using high-throughput sequencing, we tested the covariation between MHC class IIB genotypes and feather microbiota in the blue petrel (Halobaena caerulea), a seabird with highly developed olfaction that has been suggested to rely on oduor cues during an MHC-based mate choice. First, we show that individuals with similar MHC class IIB profiles also have similar bacterial assemblages in their feathers. Then, we show that individuals with high MHC diversity have less diverse feather microbiota and also a reduced abundance of a bacterium of the genus Arsenophonus, a genus in which some species are symbionts of avian ectoparasites. Our results, showing that feather microbiota covary with MHC, are consistent with the hypothesis that individual MHC genotype may shape the semiochemical-producing microbiota in birds.

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.

Pigeon odor varies with experimental exposure to trace metal pollution.

Trace metals are chemical pollutants that have well-known noxious effects on wildlife and that are current major environmental issues in urban habitats. Previous studies have demonstrated their negative (e.g. lead) or positive (e.g. zinc) effects on body condition, immunity and reproductive success. Because of their effects on condition, trace metals are likely to influence the production of condition-dependent ornaments. The last decade has revealed that bird odors, like mammal odors, can convey information on individual quality and might be used as secondary sexual ornaments. Here, we used solid-phase microextraction headspace sampling with gas chromatography-mass spectrometry to investigate whether plumage scent varied with experimental supplementation in lead and/or zinc in feral pigeons. Zinc supplementation (alone or in combination with lead) changed the proportion of several volatiles, including an increase in the proportion of hydroxy-esters. The production of these esters, that most likely originate from preen gland secretions, may be costly and might thus be reduced by stress induced by zinc deficiency. Although lead is known to negatively impact pigeon condition, it did not statistically affect feather scent, despite most of the volatiles that increased with zinc exposure tended to be decreased in lead-supplemented pigeons. Further studies should evaluate the functions of plumage volatiles to predict how trace metals can impact bird fitness.

Odour-based discrimination of similarity at the major histocompatibility complex in birds.

Many animals are known to preferentially mate with partners that are dissimilar at the major histocompatibility complex (MHC) in order to maximize the antigen binding repertoire (or disease resistance) in their offspring. Although several mammals, fish or lizards use odour cues to assess MHC similarity with potential partners, the ability of birds to assess MHC similarity using olfactory cues has not yet been explored. Here we used a behavioural binary choice test and high-throughput-sequencing of MHC class IIB to determine whether blue petrels can discriminate MHC similarity based on odour cues alone. Blue petrels are seabirds with particularly good sense of smell, they have a reciprocal mate choice and are known to preferentially mate with MHC-dissimilar partners. Incubating males preferentially approached the odour of the more MHC-dissimilar female, whereas incubating females showed opposite preferences. Given their mating pattern, females were, however, expected to show preference for the odour of the more MHC-dissimilar male. Further studies are needed to determine whether, as in women and female mice, the preference varies with the reproductive cycle in blue petrel females. Our results provide the first evidence that birds can use odour cues only to assess MHC dissimilarity.

Blue petrels recognize the odor of their egg.

Most studies on avian olfactory communication have focused on mate choice, and the importance of olfaction in subsequent nesting stages has been poorly explored. In particular, the role of olfactory cues in egg recognition has received little attention, despite eggs potentially being spread with parental odorous secretions known to elicit individual discrimination. Here, we used behavioral choice tests to determine whether female blue petrels (Halobaena caerulea) can discriminate the odor of their own egg from the odor of a conspecific egg. Females preferentially approached the odor of their own egg, suggesting that blue petrels can recognize their own egg using odor cues. This finding raises the question of the adaptive value of this mechanism, and may inspire further research on odor-based egg discrimination in species suffering brood parasitism.

Feather bacterial load shapes the trade-off between preening and immunity in pigeons.

BACKGROUND: Complex communities of bacteria inhabit the feathers of all birds. Under normal conditions, individuals maintain a healthy state by defending themselves against these potential invaders by preening. The immune system is only triggered when bacteria gain access into the body. Preening is, however, costly and may trade-off with investment in the immune system. To shed light on how birds balance the trade-off between immunity and preen secretions when facing high or low feather bacterial load, we experimentally manipulated feather bacteria load of feral pigeons (Columba livia), and investigated the effects on immune defenses. RESULTS: Birds facing high feather bacterial load had lower immune response to PHA skin-swelling test (a measure of induced pro-inflammatory capacity) than controls, while birds facing low feather bacterial load had higher blood bacterial killing ability (a measure of the capacity to eliminate bacterial pathogens) than controls. No other components of the immune system (i.e., hemagglutination and hemolysis capacity of plasma, primary and secondary responses to KLH and quantity of blood parasites) were found to be affected by feather bacterial load. CONCLUSION: Pigeons had previously been shown to adjust preening to feather bacterial load. The decrease in the energetically costly inflammatory response of birds experiencing high bacterial load suggests a trade-off between investment in preen secretion and immunity and reinforces the idea that feather microbiota may have a strong impact on the ecology and evolution of the avian host.

Molecular characterization of Babesia and Cytauxzoon species in wild South-African meerkats.

Piroplasms, including Babesia, Cytauxzoon and Theileria species, frequently infect domestic and wild mammals. At present, there is no information on the occurrence and molecular identity of these tick-borne blood parasites in the meerkat, one of South Africa's most endearing wildlife celebrities. Meerkats live in territorial groups, which may occur on ranchland in close proximity to humans, pets and livestock. Blood collected from 46 healthy meerkats living in the South-African Kalahari desert was screened by microscopy and molecular methods, using PCR and DNA sequencing of 18S rRNA and ITS1 genes. We found that meerkats were infected by 2 species: one species related to Babesia sp. and one species related to Cytauxzoon sp. Ninety one percent of the meerkats were infected by the Cytauxzoon and/or the Babesia species. Co-infection occurred in 46% of meerkats. The pathogenicity and vectors of these two piroplasm species remains to be determined.

Uropygial gland size and composition varies according to experimentally modified microbiome in Great tits.

BACKGROUND: Parasites exert important selective pressures on host life history traits. In birds, feathers are inhabited by numerous microorganisms, some of them being able to degrade feathers or lead to infections. Preening feathers with secretions of the uropygial gland has been found to act as an antimicrobial defence mechanism, expected to regulate feather microbial communities and thus limit feather abrasion and infections. Here, we used an experimental approach to test whether Great tits (Parus major) modify their investment in the uropygial gland in response to differences in environmental microorganisms. RESULTS: We found that males, but not females, modified the size of their gland when exposed to higher bacterial densities on feathers. We also identified 16 wax esters in the uropygial gland secretions. The relative abundance of some of these esters changed in males and females, while the relative abundance of others changed only in females when exposed to greater bacterial loads on feathers. CONCLUSION: Birds live in a bacterial world composed of commensal and pathogenic microorganisms. This study provides the first experimental evidence for modifications of investment in the defensive trait that is the uropygial gland in response to environmental microorganisms in a wild bird.

Gastrointestinal parasites in relation to host traits and group factors in wild meerkats Suricata suricatta.

Meerkats are one of the most endearing of South African's wildlife celebrities and one of the most highly studied social mammals. However, although parasites are widely recognized as important regulatory factors in animal population, basic knowledge on meerkats' parasites is lacking. Here 100 fresh fecal samples of wild meerkats were examined for the presence of endoparasitic infection. Endoparasitic taxa identified by the presence of eggs or oocysts included Toxocara suricattae, Oxynema suricattae, Pseudandrya suricattae, Cystoisospora sp. and Eimeria sp. Non-specific diagnoses were made for parasites in the Order Strongylida, Order Spirurida and coccidian based on the morphology and size of the eggs and oocysts. The prevalence of infection with T. suricattae and the strongylate species increased with age, while prevalence of coccidia and intensity of infection by the strongylate species increased with decreasing group size, suggesting that stress associated with living in smaller group may increase susceptibility to parasitism. Moreover, parasite communities were more similar between individuals from the same group than between individuals from different groups, suggesting an important role of the environment in parasite infestation. We did not detect any differences between males and females. This study represents the first detailed report of gastrointestinal parasites in wild meerkats, and is a key starting point for future studies on the effect of endoparasite load in the life history of this species.

Spatial distribution of selenium-mercury in Arctic seabirds.

Mercury (Hg) is a metallic trace element toxic for humans and wildlife that can originate from natural and anthropic sources. Hg spatial gradients have been found in seabirds from the Arctic and other oceans, suggesting contrasting toxicity risks across regions. Selenium (Se) plays a protective role against Hg toxicity, but its spatial distribution has been much less investigated than that of Hg. From 2015 to 2017, we measured spatial co-exposure of Hg and Se in blood samples of two seabird species, the Brünnich's guillemot (Uria lomvia) and the black-legged kittiwake (Rissa tridactyla) from 17 colonies in the Arctic and subarctic regions, and we calculated their molar ratios (Se:Hg), as a measure of Hg sequestration by Se and, therefore, of Hg exposure risk. We also evaluated concentration differences between species and ocean basins (Pacific-Arctic and Atlantic-Arctic), and examined the influence of trophic ecology on Hg and Se concentrations using nitrogen and carbon stable isotopes. In the Atlantic-Arctic ocean, we found a negative west-to-east gradient of Hg and Se for guillemots, and a positive west-to-east gradient of Se for kittiwakes, suggesting that these species are better protected from Hg toxicity in the European Arctic. Differences in Se gradients between species suggest that they do not follow environmental Se spatial variations. This, together with the absence of a general pattern for isotopes influence on trace element concentrations, could be due to foraging ecology differences between species. In both oceans, the two species showed similar Hg concentrations, but guillemots showed lower Se concentrations and Se:Hg than kittiwakes, suggesting a higher Hg toxicity risk in guillemots. Within species, neither Hg, nor Se or Se:Hg differed between both oceans. Our study highlights the importance of considering Se together with Hg, along with different species and regions, when evaluating Hg toxic effects on marine predators in international monitoring programs.

Odour-based kin discrimination in the cooperatively breeding meerkat.

Kin recognition is a useful ability for animals, facilitating cooperation among relatives and avoidance of excessive kin competition or inbreeding. In meerkats, Suricata suricatta, encounters between unfamiliar kin are relatively frequent, and kin recognition by phenotype matching is expected to avoid inbreeding with close relatives. Here, we investigate whether female meerkats are able to discriminate the scent of unfamiliar kin from unfamiliar non-kin. Dominant females were presented with anal gland secretion from unfamiliar individuals that varied in their relatedness. Our result indicates that females spent more time investigating the scent of related than unrelated unfamiliar individuals, suggesting that females may use a phenotype matching mechanism (or recognition alleles) to discriminate the odour of their kin from the odour of their non-kin. Our study provides a key starting point for further investigations into the use of kin recognition for inbreeding avoidance in the widely studied meerkat.

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.

Semiochemical compounds of preen secretion reflect genetic make-up in a seabird species.

Several vertebrates choose their mate according to genetic heterozygosity and relatedness, and use odour cues to assess their conspecifics' genetic make-up. In birds, although several species (including the black-legged kittiwake) exhibit non-random mating according to genetic traits, the cues used to assess genetic characteristics remain unknown. The importance of olfaction in birds' social behaviour is gaining attention among researchers, and it has been suggested that, as in other vertebrates, bird body scent may convey information about genetic traits. Here, we combined gas chromatography data and genetic analyses at microsatellite loci to test whether semiochemical messages in preen secretion of kittiwakes carried information about genetic heterozygosity and relatedness. Semiochemical profile was correlated with heterozygosity in males and females, while semiochemical distance was correlated with genetic distance only in male-male dyads. Our study is the first to demonstrate a link between odour and genetics in birds, which sets the stage for the existence of sophisticated odour-based mechanisms of mate choice also in birds.

'Doctor, I am so stressed out!' A descriptive study of biological, psychological, and socioemotional markers of stress in individuals who self-identify as being 'very stressed out' or 'zen'.

Surveys report that about three-quarters of visits to general practitioners in America are for stress-related complaints. Animal and human studies have consistently demonstrated that exposure to acute and/or chronic stress leads to the activation of the autonomic nervous system (ANS) and/or hypothalamic-pituitary-adrenal (HPA) axis, and to the production of catecholamines and glucocorticoids. Yet, many studies performed in humans do not report significant associations between subjective feelings of stress and increases in these stress biomarkers. Consequently, it is not clear whether the stress-related complaints of individuals are associated with significant increases in these stress biomarkers. In the present study, we measured whether individuals who self-identify as being 'very stressed out' or 'zen' present differences in psychological (depression and anxiety symptoms), biological (basal and reactive levels of glucocorticoids and alpha-amylase) and socioemotional (emotion regulation, mind wandering, personality, resilience and positive mental health) factors associated with stress. Salivary levels of cortisol and alpha-amylase were obtained in the home environment and in reaction to the Trier Social Stress Test in 123 adults aged between 19 and 55 years. All participants completed questionnaires assessing the psychological and socioemotional factors described above. The results showed that groups significantly differed on almost all psychological and socioemotional factors, although we found no significant group differences on biological markers of stress (cortisol or alpha-amylase). These results suggest that when people complain of being 'very stressed out', what they may really be alluding to is an experience of psychological distress that is related to poor emotion regulation capacities. It is thus possible that the construct of stress used by people to discuss their internal state of 'stress' is quite different than the construct of stress measured in animal and human laboratories using biomarkers of 'stress'.

Integument coloration signals reproductive success, heterozygosity, and antioxidant levels in chick-rearing black-legged kittiwakes.

Carotenoid pigments are important for immunity and as antioxidants, and carotenoid-based colors are believed to provide honest signals of individual quality. Other colorless but more efficient antioxidants such as vitamins A and E may protect carotenoids from bleaching. Carotenoid-based colors have thus recently been suggested to reflect the concentration of such colorless antioxidants, but this has rarely been tested. Furthermore, although evidence is accruing for multiple genetic criteria for mate choice, carotenoid-based colors have rarely been shown to reflect both phenotypic and genetic quality. In this study, we investigated whether gape, tongue, eye-ring, and bill coloration of chick-rearing black-legged kittiwakes Rissa tridactyla reflected circulating levels of carotenoids and vitamins A and E. We further investigated whether integument coloration reflected phenotypic (body condition and fledging success) and genetic quality (heterozygosity). We found that the coloration of fleshy integuments was correlated with carotenoid and vitamin A levels and fledging success but only in males. Furthermore, the coloration of tongue and eye-ring was correlated with heterozygosity in both males and females. Integument colors might therefore be reliable signals of individual quality used by birds to adjust their parental care during the chick-rearing period.

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.

Early childhood adversity and HPA axis activity in adulthood:The importance of considering minimal age at exposure.

Early adversity (EA) modulates stress hormone secretion in mixed directions. The Accumulation Model suggests that the number of EA predicts patterns of cortisol dysregulations, while the Life Cycle Model of Stress highlights the importance of considering the timing at which EA began, given that brain regions sensitive to stress hormones follow distinct developmental trajectories. We aimed to test these two models in 85 healthy men and women, aged 21-40 years old who reported having been exposed to EA during childhood. Participants were grouped based on the number of EA events to which they were exposed during their lifespan (Accumulation Model) and the age of first exposure to EA (Life Cycle Model). Diurnal and stress-induced reactive cortisol secretion were measured in all participants. Results showed that although the number of EA was not associated with patterns of basal or reactive cortisol secretion, adults first exposed to EA between the ages of 3 and 7 - an important time window for amygdala development - showed greater cortisol awakening response and lower cortisol reactivity relative to those first exposed to EA before 3 or after 7. These results provide support for the Life Cycle Model of Stress and highlight the importance of considering minimal age at exposure to EA when assessing the effects of early adversity on patterns of cortisol secretion.