Maternal effect senescence via reduced DNA repair ability in the three-spined stickleback.

Maternal effect senescence, a decline in offspring viability with maternal age, has been documented across diverse animals, but its mechanisms remain largely unknown. Here, we test maternal effect senescence and explore its possible molecular mechanisms in a fish. We compared the levels of maternal mRNA transcripts of DNA repair genes and mtDNA copies in eggs and the levels of DNA damage in somatic and germline tissues between young and old female sticklebacks. We also tested, in an in vitro fertilization experiment, whether maternal age and sperm DNA damage level interactively influence the expression of DNA repair genes in early embryos. Old females transferred less mRNA transcripts of DNA repair genes into their eggs than did young females, but maternal age did not influence egg mtDNA density. Despite a higher level of oxidative DNA damage in the skeletal muscle, old females had a similar level of damage in the gonad to young females, suggesting the prioritization for germline maintenance during ageing. The embryos of both old and young mothers increased the expression of DNA repair genes in response to an increased level of oxidative DNA damage in sperm used for their fertilization. The offspring of old mothers showed higher rates of hatching, morphological deformity and post-hatching mortality and had smaller body size at maturity. These results suggest that maternal effect senescence may be mediated by reduced capacity of eggs to detect and repair DNA damages, especially prior to the embryonic genomic activation.

Covariation between glucocorticoid levels and receptor expression modulates embryo development and postnatal phenotypes in gulls.

The hypothalamic-pituitary-adrenocortical axis can translate, through glucocorticoid secretion, the prenatal environment to development to produce phenotypes that match prevailing environmental conditions. However, whether developmental plasticity is modulated by the interaction between circulating glucocorticoids and receptor expression remains unclear. Here, we tested whether covariation between plasma corticosterone (CORT) and glucocorticoid receptor gene (Nr3c1) expression in blood underlies embryonic developmental programming in yellow-legged gulls (Larus michahellis). We examined variations in circulating levels of CORT and the expression and DNA methylation patterns of Nr3c1 in response to two ecologically relevant prenatal factors: adult alarm calls (a cue of predator presence) and changes in prenatal light environment (a cue of competitive disadvantage). We then determined whether embryonic development and postnatal phenotypes were associated with CORT levels and Nr3c1 expression, and explored direct and indirect relationships between the prenatal environment, hormone-receptor covariation, and postnatal phenotypes. Prenatal exposure to alarm calls increased CORT levels and up-regulated Nr3c1 expression in gull chicks, while exposure to light cues reduced both hormone levels and receptor expression. Chicks prenatally exposed to alarm calls showed altered DNA methylation profiles in the Nr3c1 regulatory region, but patterns varied throughout the breeding season and between years. Moreover, our results suggest a negative relationship between DNA methylation and expression in Nr3c1 , at least at specific CpG sites. The interplay between circulating CORT and Nr3c1 expression affected embryo developmental timing and vocalizations, as well as hatchling mass and fitness-relevant behaviours. These findings provide a link between prenatal inputs, glucocorticoid function and phenotypic outcomes, suggesting that hormone-receptor interaction may underlie developmental programming in free-living animals.

Inputs of seabird guano alter microbial growth, community composition and the phytoplankton-bacterial interactions in a coastal system.

Seabird guano enters coastal waters providing bioavailable substrates for microbial plankton, but their role in marine ecosystem functioning remains poorly understood. Two concentrations of the water soluble fraction (WSF) of gull guano were added to different natural microbial communities collected in surface waters from the Ría de Vigo (NW Spain) in spring, summer, and winter. Samples were incubated with or without antibiotics (to block bacterial activity) to test whether gull guano stimulated phytoplankton and bacterial growth, caused changes in taxonomic composition, and altered phytoplankton-bacteria interactions. Alteromonadales, Sphingobacteriales, Verrucomicrobia and diatoms were generally stimulated by guano. Chlorophyll a (Chl a) concentration and bacterial abundance significantly increased after additions independently of the initial ambient nutrient concentrations. Our study demonstrates, for the first time, that the addition of guano altered the phytoplankton-bacteria interaction index from neutral (i.e. phytoplankton growth was not affected by bacterial activity) to positive (i.e. phytoplankton growth was stimulated by bacterial activity) in the low-nutrient environment occurring in spring. In contrast, when environmental nutrient concentrations were high, the interaction index changed from positive to neutral after guano additions, suggesting the presence of some secondary metabolite in the guano that is needed for phytoplankton growth, which would otherwise be supplied by bacteria.

Maternal testosterone affects offspring telomerase activity in a long-lived seabird.

Androgens are a group of steroid hormones that have long been proposed as a mechanism underpinning intergenerational plasticity. In birds, maternally allocated egg testosterone, one of the main androgens in vertebrates, affects a wide variety of offspring phenotypic traits but the mechanisms underlying this form of intergenerational plasticity are not yet well understood. Recent in vitro and animal model studies have shown that telomerase expression and activity are important targets of androgen signaling. The telomerase enzyme is known for its repair function on telomeres, the DNA-protein complexes at the ends of chromosomes that are involved in genomic integrity and cell aging. However, the role of maternal testosterone in influencing offspring telomerase levels in natural populations and its consequences on telomere length and potentially on offspring development is still unknown. Here, by experimentally modifying the level of egg testosterone in a natural population of yellow-legged gull (Larus michahellis), we show that chicks hatched from testosterone-treated eggs had higher average levels of telomerase and faster growth than controls during the first week of life. While testosterone-treated chicks also tended to have longer telomeres than controls at hatching this difference disappeared by day 6 of age. Overall, our results suggest that maternal testosterone may have a potential adaptive value by promoting offspring growth and presumably telomerase levels, as this enzyme plays other important physiological functions (e.g., stress resistance, cell signaling, or tissue genesis) besides telomere lengthening. Nonetheless, our knowledge of the potential adaptive function of telomerase in natural populations is scarce and so the potential pathways linking maternal hormones, offspring telomerase, and fitness should be further investigated.

Mitochondrial DNA content in eggs as a maternal effect.

The transmission of detrimental mutations in animal mitochondrial DNA (mtDNA) to the next generation is avoided by a high level of mtDNA content in mature oocytes. Thus, this maternal genetic material has the potential to mediate adaptive maternal effects if mothers change mtDNA level in oocytes in response to their environment or body condition. Here, we show that increased mtDNA abundance in mature oocytes was associated with fast somatic growth during early development but at the cost of increased mortality in three-spined sticklebacks. We also examined whether oocyte mtDNA and sperm DNA damage levels have interacting effects because they can determine the integrity of mitochondrial and nuclear genes in offspring. The level of oxidative DNA damage in sperm negatively affected fertility, but there was no interacting effect of oocyte mtDNA abundance and sperm DNA damage. Oocyte mtDNA level increased towards the end of the breeding season, and the females exposed to warmer temperatures during winter produced eggs with increased mtDNA copies. Our results suggest that oocyte mtDNA level can vary according to the expected energy demands for offspring during embryogenesis and early growth. Thus, mothers can affect offspring development and viability through the context-dependent effects of oocyte mtDNA abundance.

Relationships between male secondary sexual traits, physiological state and offspring viability in the three-spined stickleback.

BACKGROUND: Sexual signals produced by males play a central role in sexual selection, but the relationship between these traits and the quality of the bearer are often ambiguous. Secondary sexual traits may represent genetic quality of the bearer, resulting in positive relationships with physiological state, or may be costly to produce, showing trade-off with physiological state. A number of studies have explored the relationships between secondary sexual traits and other functional traits, but few have studied their fitness consequences. We studied the link between diverse physiological traits and both morphological and behavioural sexual traits and examined how their interplay influences offspring viability in the three-spined stickleback. RESULTS: Male sticklebacks showing nest building and courtship behaviour were smaller than those not investing in reproductive activities. There was no evidence that the expression of red nuptial colouration and the quality of courtship behaviour of males are positively related to their metabolic rates, swim ability, oxidative damage and mtDNA copy number. However, individuals showing larger red nuptial colour areas had higher levels of oxidative DNA damage in their sperm. Male courtship behaviour and aggressiveness, but not red colour area, were good predictors of offspring hatching and survival. CONCLUSIONS: Our results suggest that, in our study population at the southern edge of the species' distribution, sexual colouration of male sticklebacks was not a good indicator of their body state, but both courtship quality and aggressiveness during the courtship are reliable cues of their gamete quality, influencing the viability of their offspring. Thus, females that choose mates based on their courtship behaviour will have high fitness. In the study population, which represents a fast pace-of-life with high reproductive rate and short lifespan, sexual ornaments of males may not honestly signal their physiological and physical state because they invest at maximum in a single reproductive season despite high costs.

Egg corticosterone can stimulate telomerase activity and promote longer telomeres during embryo development.

It is often assumed that the transfer of maternal glucocorticoids (GCs; e.g., corticosterone or cortisol) to offspring is an inevitable cost associated with adverse or stressful conditions experienced by mothers. However, recent evidence indicates that maternal GCs may adaptively programme particular physiological and molecular pathways during development to enhance offspring fitness. In this context, an important mechanism through which maternal GCs may lastingly affect offspring phenotypic quality and survival is via effects on embryo telomerase activity and so on offspring postnatal telomere length. Here, using a field experimental design for which we manipulated the corticosterone content in yellow-legged gull (Larus michahellis) eggs, we show that embryos from corticosterone-injected eggs not only had a higher telomerase activity but also longer telomeres just after hatching. A complementary analysis further revealed that gull hatchlings with longer telomeres had a higher survival probability during the period when most of the chick mortality occurs. Given the important role that telomere length and its restoring mechanisms have on ageing trajectories and disease risk, our findings provide a new mechanistic link by which mothers may presumably shape offspring life-history trajectories and phenotype.

Smart mating: the cognitive ability of females influences their preference for male cognitive ability.

Cognitive abilities may be crucial for individuals to respond appropriately to their social and natural environment, thereby increasing fitness. However, the role of cognitive traits in sexual selection has received relatively little attention. Here, we studied 1) whether male secondary sexual traits (colour, courtship, and nest) reflect their cognitive ability, 2) whether females choose mates based on males' and their own cognitive abilities, and 3) how the interplay between secondary sexual traits and cognitive ability determines male attractiveness in the three-spined stickleback (Gasterosteus aculetaus). For this, we first evaluated the cognitive ability of sexually mature males and females in a detour-reaching task. Then, female preference was repeatedly assessed in a dichotomous-choice test, where the female was exposed to two males with contrasting performances (relatively good and bad) in the detour-reaching task. Female preference for better performing males was affected by the female's own cognitive ability. Females with relatively medium-low cognitive ability preferred males with high ability, whereas females with high ability showed no preference. We also found that males with higher cognitive abilities built more elaborated nests, but showed weaker red nuptial colouration. To our knowledge, this is among the first results that illustrate how cognitive traits of both sexes influence female mate preference, which has implications for the strength and direction of sexual selection.

Gut microbiome and telomere length in gull hatchlings.

In many animals, recent evidence indicates that the gut microbiome may be acquired during early development, with possible consequences on newborns' health. Thus, it has been hypothesized that a healthy microbiome protects telomeres and genomic integrity against cellular stress. However, the link between the early acquired microbiome and telomere dynamics has not hitherto been investigated. In birds, this link may also be potentially modulated by the transfer of maternal glucocorticoids, since these substances dysregulate microbiome composition during postnatal development. Here, we examined the effect of the interplay between the microbiome and stress hormones on the telomere length of yellow-legged gull hatchlings by using a field experiment in which we manipulated the corticosterone content in eggs. We found that the hatchling telomere length was related to microbiome composition, but this relationship was not affected by the corticosterone treatment. Hatchlings with a microbiome dominated by potential commensal bacteria (i.e. Catellicoccus and Cetobacterium) had larger telomeres, suggesting that an early establishment of the species-specific microbiome during development may have important consequences on offspring health and survival.

Telomerase activity can mediate the effects of growth on telomeres during post-natal development in a wild bird.

In wild animals, telomere attrition during early development has been linked with several fitness disadvantages throughout life. Telomerase enzyme can elongate telomeres, but it is generally assumed that its activity is suppressed in most somatic tissues upon birth. However, recent evidence suggests that this may not be the case for long-lived bird species. We have therefore investigated whether telomerase activity is maintained during the postnatal growth period in a wild yellow-legged gull (Larus michahellis) population. Our results indicate that telomerase activity is not negligible in the blood cells, but activity levels sharply decline from hatching to fledging following a similar pattern to the reduction observed in telomere length. Our results further suggest that the observed variation in telomere length may be the result of a negative effect of fast growth on telomerase activity, thus providing a new mechanism through which growth rates may affect telomere dynamics and potentially life-history trajectories.

Environment-induced changes in reproductive strategies and their transgenerational effects in the three-spined stickleback.

An organism may increase its fitness by changing its reproductive strategies in response to environmental cues, but the possible consequences of those changes for the next generation have rarely been explored. By using an experiment on the three-spined stickleback (Gasterosteus aculeatus), we studied how changes in the onset of breeding photoperiod (early versus late) affect reproductive strategies of males and females, and life histories of their offspring. We also explored whether telomeres are involved in the within- and transgenerational effects. In response to the late onset of breeding photoperiod, females reduced their investment in the early clutches, but males increased their investment in sexual signals. Costs of increased reproductive investment in terms of telomere loss were evident only in the late females. The environmentally induced changes in reproductive strategies affected offspring growth and survival. Most notably, offspring growth rate was the fastest when both parents experienced a delayed (i.e., late) breeding photoperiod, and survival rate was the highest when both parents experienced an advanced (i.e., early) breeding photoperiod. There was no evidence of transgenerational effects on offspring telomere length despite positive parents-offspring relationships in this trait. Our results highlight that environmental changes may impact more than one generation by altering reproductive strategies of seasonal breeders with consequences for offspring viability.

Gull chicks grow faster but lose telomeres when prenatal cues mismatch the real presence of sibling competitors.

During embryonic life, individuals should adjust their phenotype to the conditions that they will encounter after birth, including the social environment, if they have access to (social) cues that allow them to forecast future conditions. In birds, evidence indicates that embryos are sensitive to cues from clutch mates, but whether embryos adjust their development to cope with the expected level of sibling competition has not hitherto been investigated. To tackle this question, we performed a 'match versus mismatch' experimental design where we manipulated the presence of clutch mates (i.e. clutch size manipulation) and the real (postnatal) level of sibling competition (i.e. brood size manipulation) in the yellow-legged gull (Larus michahellis). We provide evidence that the prenatal cues of sibling presence induced developmental changes (such as epigenetic profiles) that had programming effects on chick begging behaviour and growth trajectories after hatching. While receiving mismatching information favoured chick begging and growth, this came at the cost of reduced antioxidant defences and a premature loss of telomeres. Our findings highlight the role of the prenatal social environment in developmental plasticity and suggest that telomere attrition may be an important physiological cost of phenotype-environment mismatch.

Attractive male sticklebacks carry more oxidative DNA damage in the soma and germline.

Trade-offs between the expression of sexual signals and the maintenance of somatic and germline tissues are expected when these depend upon the same resources. Despite the importance of sperm DNA integrity, its trade-off with sexual signalling has rarely been explored. We experimentally tested the trade-off between carotenoid-based sexual coloration and oxidative DNA damage in skeletal muscle, testis and sperm by manipulating reproductive schedule (early vs. late onset of breeding) in male three-spined sticklebacks. Oxidative DNA damage was measured as the amount of 8-hydroxy-2-deoxyguanosine in genomic DNA. Irrespective of the experimentally manipulated reproductive schedule, individuals investing more in red coloration showed higher levels of oxidative DNA damage in muscle, testis and sperm during the peak breeding season. Our results show that the expression of red coloration traded off against the level of oxidative DNA damage possibly due to the competing functions of carotenoids as colorants and antioxidants. Thus, female sticklebacks may risk fertility and viability of offspring by choosing redder, more deteriorated partners with decreased sperm DNA integrity. The evolution of sexual signal may be constrained by oxidative DNA damage in the soma and germline.

Reduced telomere length in embryos exposed to predator cues.

It is often assumed that embryos are isolated from external influences, but recent studies indicate that environmental stressors during prenatal stages can exert long-term negative effects on fitness. A potential mechanism by which predation risk may lastingly shape life-history traits and phenotypes is via effects on telomeres. However, whether prenatal exposure to environmental stressors, such as cues of predator presence, affects postnatal telomere length has not hitherto been investigated. Using an experimental design in which we modified the exposure of yellow-legged gull (Larus michahellis) embryos to social cues of predator presence (i.e. alarm calls), we show that prenatally exposed chicks had shorter telomeres after hatching. As young birds with shorter telomere lengths have reduced fledging success, reproductive success and lifespan, the reduced telomere length in the exposed chicks is likely to have long-term fitness consequences. Moreover, our results provide a mechanistic link through which predators may negatively affect population dynamics.

Bird embryos perceive vibratory cues of predation risk from clutch mates.

During development in fluctuating environments, phenotypes can be adjusted to the conditions that individuals will probably encounter later in life. As developing embryos have a limited capacity to fully capture environmental information, theory predicts that they should integrate relevant information from all reliable sources, including the social environment. In many oviparous species, embryos are able to perceive cues of predator presence in some circumstances, but whether this information is socially transmitted among clutch mates-promoting phenotypic adjustments in the whole clutch-is unknown. Here, using an experimental design for which we modified the exposure to some, but not all, embryos of the same clutch to cues of predator presence (that is, alarm calls), we show that exposed embryos of the yellow-legged gull (Larus michahellis) and their unexposed clutch mates showed similar developmental changes that were absent in embryos from control clutches. Compared with the control broods, both embryos that were exposed to alarm calls and their unexposed clutch mates showed altered prenatal and postnatal behaviours, higher levels of DNA methylation and stress hormones, and reduced growth and numbers of mitochondria (which may be indicative of the capacity for energy production of cells). These results strongly suggest that gull embryos are able to acquire relevant environmental information from their siblings. Together, our results highlight the importance of socially acquired information during the prenatal stage as a non-genetic mechanism promoting developmental plasticity.

Redox-regulation and life-history trade-offs: scavenging mitochondrial ROS improves growth in a wild bird.

It has been proposed that animals usually restrain their growth because fast growth leads to an increased production of mitochondrial reactive oxygen species (mtROS), which can damage mitochondrial DNA and promote mitochondrial dysfunction. Here, we explicitly test whether this occurs in a wild bird by supplementing chicks with a mitochondria-targeted ROS scavenger, mitoubiquinone (mitoQ), and examining growth rates and mtDNA damage. In the yellow-legged gull Larus michahellis, mitoQ supplementation increased the early growth rate of chicks but did not reduce mtDNA damage. The level of mtDNA damage was negatively correlated with chick mass, but this relationship was not affected by the mitoQ treatment. We also found that chick growth was positively correlated with both mtDNA copy number and the mitochondrial enzymatic activity of citrate synthase, suggesting a link between mitochondrial content and growth. Additionally, we found that MitoQ supplementation increased mitochondrial content (in males), altered the relationship between mtDNA copy number and damage, and downregulated some transcriptional pathways related to cell rejuvenation, suggesting that scavenging mtROS during development enhanced growth rates but at the expense of cellular turnover. Our study confirms the central role of mitochondria modulating life-history trade-offs during development by other mechanisms than mtROS-inflicted damage.

Carry-over effects of early thermal conditions on somatic and germline oxidative damages are mediated by compensatory growth in sticklebacks.

Most studies of climate change impacts focus on the effects of summer temperatures, which can immediately impact fitness of breeders, but winter temperatures are expected to have a greater impact on development and growth of animals with long-lasting consequences. Exposure to warmer temperatures can increase cellular oxidative damage in ectotherms. Yet, it is unknown whether thermal stress during early life has prolonged effects on oxidative status during adulthood. In an experiment using F1 fish originated from a wild three-spined stickleback population at the southern edge of its European distribution, we examined whether experimental thermal conditions experienced in winter had carry-over effects on oxidative status and telomere length, a marker of accumulated stress, in the soma and germline during adulthood. For this, oxidative DNA damage, enzymatic antioxidant activities and telomere length were measured three months after the termination of the temperature manipulation. In addition, we tested whether such delayed effects, if any, were due to individuals' compensatory growth after experiencing unfavourable growth conditions in winter. Warm acclimation during winter induced increased levels of oxidative DNA damage in muscle and sperm and increased enzymatic antioxidant defences in muscle during the breeding season. Telomere length of adult fish was not influenced by thermal conditions experienced during early life. Winter temperature manipulation influenced fish to alter the temporal pattern of growth trajectories across the juvenile and adult stages. Fish reared in warm winter conditions grew at a slower rate than the controls during the period of temperature manipulation then accelerated body mass gain to catch up during the breeding season. Faster somatic growth during the breeding season incurred a higher cost in terms of oxidative damage in the warm-treated individuals. For the first time, we experimentally show the long-lasting detrimental effects of thermal stress on and the positive link between catch-up growth and oxidative DNA damage in the soma and germline. Winter temperature increases due to climate change can reduce fertility and survival of fish by inducing catch-up growth. The detrimental effects of winter climate change may accumulate across generations through the pre-mutagenic DNA damage in the germline.

La mayoría de los estudios sobre los efectos del cambio climático se centran en los efectos de las temperaturas estivales, ya que estas pueden afectar de forma inmediata a la eficacia biológica de los individuos reproductores. No obstante, es esperable que las temperaturas invernales tengan un mayor impacto a largo plazo debido a sus efectos durante el desarrollo y el crecimiento temprano. Aunque la exposición a temperaturas más elevadas puede aumentar el daño oxidativo celular en ectotermos, todavía se desconoce si un estrés térmico durante el desarrollo temprano tiene efectos a largo plazo sobre el estado oxidativo en la edad adulta. En este experimento, en el que usamos la F1 procedente de una población de pez espinoso situada al borde sur de su distribución, examinamos los efectos a largo plazo de las condiciones térmicas invernales sobre los niveles de estrés oxidativo y longitud telomérica de la línea somática y germinal en la edad adulta. Además, evaluamos si tales efectos a largo plazo, si los hubo, se relacionaron con las tasa de crecimiento de los individuos. La aclimatación cálida durante el invierno indujo un aumento de los niveles de daño oxidativo en al ADN del músculo y los espermatozoides durante la estación reproductora, así como un aumento de las defensas antioxidantes enzimáticas en el músculo. La longitud telomérica adulta no se vio influenciada por las condiciones térmicas experimentadas durante el desarrollo temprano. La manipulación de la temperatura invernal alteró la trayectoria de crecimiento de los peces a lo largo de la fase juvenil y adulta. Los peces criados en condiciones invernales cálidas crecieron a un ritmo más lento que los controles durante el período de manipulación pero posteriormente mostraron una mayor tasa de crecimiento. Este crecimiento compensatorio se completó durante la temporada de reproducción. Este crecimiento compensatorio durante la temporada de reproducción tuvo un coste más elevado, en términos de daño oxidativo, en los individuos que experimentaron una condiciones invernales más cálidas. Por primera vez mostramos experimentalmente que el estrés termino temprano tiene efectos perjudiciales a largo plazo, y que existe una relación positiva entre la tasa de crecimiento compensatorio y los niveles de daño oxidativo en el ADN de las línea somática y germinal. El aumento de las temperaturas invernales debido al cambio climático podría reducir la fertilidad y la supervivencia de las poblaciones de peces al inducir cambios en las tasas de crecimiento. Además, los efectos perjudiciales del cambio climático invernal podrían ser trans-generacionales como consecuencia de la acumulación de daños pre-mutagénicos en el ADN de la línea germinal.

The use of European shag pellets as indicators of microplastic fibers in the marine environment.

Microplastic particles are abundant marine pollutants that are ingested by many seabirds. Some seabirds regurgitate non-digestible materials in the form of pellets and their analysis may be useful to study the abundance of plastic debris at the local scale. Here, we aimed to provide baseline data for the presence of microplastics in pellets regurgitated by European shags (Phalacrocorax aristotelis) (n = 41) in the Iberia peninsula (NW Spain). We found microplastic fibers in 63% of pellets, suggesting that this type of plastic pollution is prevalent in the study area. According to Fourier Transform Infrared spectrometry, nylon fibers were the most abundant, followed by polyester. We also found that the presence of microplastics was higher in pellets containing remains of benthic fishes. Our results suggest that shag pellets may be useful to monitor microplastic pollution in coastal waters.

Glucocorticoids modulate gastrointestinal microbiome in a wild bird.

It has recently been hypothesized that stress exposure (e.g. via glucocorticoid secretion) may dysregulate the bacterial gut microbiome, a crucial 'organ' in animal health. However, whether stress exposure (e.g. via glucocorticoid secretion) affects the bacterial gut microbiome of natural populations is unknown. We have experimentally altered the basal glucocorticoid level (corticosterone implants) in a wild avian species, the yellow-legged gull Larus michahellis, to assess its effects on the gastrointestinal microbiota. Our results suggest underrepresentation of several microbial taxa in the corticosterone-implanted birds. Importantly, such reduction included potentially pathogenic avian bacteria (e.g. Mycoplasma and Microvirga) and also some commensal taxa that may be beneficial for birds (e.g. Firmicutes). Our findings clearly demonstrate a close link between microbiome communities and glucocorticoid levels in natural populations. Furthermore, they suggest a beneficial effect of stress in reducing the risk of infection that should be explored in future studies.

Complex demographic heterogeneity from anthropogenic impacts in a coastal marine predator.

Environmental drivers, including anthropogenic impacts, affect vital rates of organisms. Nevertheless, the influence of these drivers may depend on the physical features of the habitat and how they affect life history strategies depending on individual covariates such as age and sex. Here, the long-term monitoring (1994-2014) of marked European Shags in eight colonies in two regions with different ecological features, such as foraging habitat, allowed us to test several biological hypotheses about how survival changes by age and sex in each region by means of multi-event capture-recapture modeling. Impacts included fishing practices and bycatch, invasive introduced carnivores and the severe Prestige oil spill. Adult survival was constant but, unexpectedly, it was different between sexes. This difference was opposite in each region. The impact of the oil spill on survival was important only for adults (especially for females) in one region and lasted a single year. Juvenile survival was time dependent but this variability was not synchronized between regions, suggesting a strong signal of regional environmental variability. Mortality due to bycatch was also different between sex, age and region. Interestingly the results showed that the size of the fishing fleet is not necessarily a good proxy for assessing the impact of bycatch mortality, which may be more dependent on the fishing grounds and the fishing gears employed in each season of the year. Anthropogenic impacts affected survival differently by age and sex, which was expected for a long-lived organism with sexual size dimorphism. Strikingly, these differences varied depending on the region, indicating that habitat heterogeneity is demographically important to how environmental variability (including anthropogenic impacts) and resilience influence population dynamics.