Salivary corticosterone reflects plasmatic levels in a wild seabird.

Wild animals have been increasingly exposed to a wide range of stressors, mainly due to the intensification of human activities and habitat modifications. Consequently, new tools in order to assess the physiological and health status of wild animals have been developed. In particular, glucocorticoids have received a special attention. Primarily metabolic hormones, they are also used to evaluate the stress level of organisms. While historically measured in blood samples, new less-invasive methods have been recently developed to measure glucocorticoids in matrices such as faeces, hairs/feathers, or saliva. To date, measurements in saliva are still in their infancy despite the numerous advantages of the matrix: non-invasive, reflects the biologically active portion of glucocorticoids, allows to measure both baseline and stress-induced levels. In addition, most studies using saliva have been performed on domestic and captive animals, and recent development in wild animals have focused on mammals. Here, we show, for the first time, that saliva could also be reliably used in free-ranging birds, as glucocorticoid levels in saliva strongly correlated with plasma levels. This promising result opens new avenues for a non-invasive sampling method to assess health status of wild birds in conservation biology and ecology.

Parental age does not influence offspring telomeres during early life in common gulls (Larus canus).

Parental age can affect offspring telomere length through heritable and epigenetic-like effects, but at what stage during development these effects are established is not well known. To address this, we conducted a cross-fostering experiment in common gulls (Larus canus) that enabled us distinguish between pre- and post-natal parental age effects on offspring telomere length. Whole clutches were exchanged after clutch completion within and between parental age classes (young and old) and blood samples were collected from chicks at hatching and during the fastest growth phase (11 days later) to measure telomeres. Neither the ages of the natal nor the foster parents predicted the telomere length or the change in telomere lengths of their chicks. Telomere length (TL) was repeatable within chicks, but increased across development (repeatability = 0.55, intraclass correlation coefficient within sampling events 0.934). Telomere length and the change in telomere length were not predicted by post-natal growth rate. Taken together, these findings suggest that in common gulls, telomere length during early life is not influenced by parental age or growth rate, which may indicate that protective mechanisms buffer telomeres from external conditions during development in this relatively long-lived species.

Linking pollution and cancer in aquatic environments: A review.

Due to the interconnectedness of aquatic ecosystems through the highly effective marine and atmospheric transport routes, all aquatic ecosystems are potentially vulnerable to pollution. Whilst links between pollution and increased mortality of wild animals have now been firmly established, the next steps should be to focus on specific physiological pathways and pathologies that link pollution to wildlife health deterioration. One of the pollution-induced pathologies that should be at the centre of attention in ecological and evolutionary research is cancer, as anthropogenic contamination has resulted in a rapid increase of oncogenic substances in natural habitats. Whilst wildlife cancer research is an emerging research topic, systematic reviews of the many case studies published over the recent decades are scarce. This research direction would (1) provide a better understanding of the physiological mechanisms connecting anthropogenic pollution to oncogenic processes in non-model organisms (reducing the current bias towards human and lab-animal studies in cancer research), and (2) allow us to better predict the vulnerability of different wild populations to oncogenic contamination. This article combines the information available within the scientific literature about cancer occurrences in aquatic and semi-aquatic species. For the first aim, we use available knowledge from aquatic species to suggest physiological mechanisms that link pollution and cancer, including main metabolic detoxification pathways, oxidative damage effects, infections, and changes to the microbiome. For the second aim, we determine which types of aquatic animals are more vulnerable to pollution-induced cancer, which types of pollution are mainly associated with cancer in aquatic ecosystems, and which types of cancer pollution causes. We also discuss the role of migration in exposing aquatic and semi-aquatic animals to different oncogenic pollutants. Finally, we suggest novel research avenues, including experimental approaches, analysis of the effects of pollutant cocktails and long-term chronic exposure to lower levels of pollutants, and the use of already published databases of gene expression levels in animals from differently polluted habitats.

Variation in the Markers of Nutritional and Oxidative State in a Long-Lived Seabird: Associations with Age and Longevity.

Age-related declines in life-history traits have been widely observed in free-living animals. Several theories link senescence to oxidative stress. The aim of this study was to measure several widely used markers of oxidative and nutritional state in a long-lived seabird, the common gull (Larus canus), in order to assess the suitability of these markers for describing deterioration in physiological condition associated with chronological age and survival. Associations with longevity and individual consistency of these parameters over the years (repeatability) were also assessed. Senescence in fitness parameters was observed during the study period: in females, laying date and clutch mass were related to bird age in a curvilinear manner, with middle-aged birds breeding earlier and laying heavier eggs. The only parameter associated with aging processes was glutathione concentration in erythrocytes, which was lower in female birds with longer life spans. Of indexes of nutritional state, plasma triglyceride concentration showed a between-individual increase with age, suggesting selective mortality of birds with low levels. Additionally, total plasma protein levels of individual males increased with age. The mostly negative results of this study hint that the commonly used parameters of physiological condition and oxidative state used in this study do not adequately reflect an individual's long-term health condition. Alternatively, it is possible that in common gulls, senescence occurs in reproductive mechanisms but not in mechanisms responsible for maintaining an organism's redox balance, consistent with the idea that different aspects of an organism's physiological condition age at different rates. Significant interannual repeatability was detected in three plasma constituents-carotenoids, uric acid, and total protein-all of which can possibly be linked to variation in dietary habits.

Dexamethasone inhibits corticosterone deposition in feathers of greenfinches.

Corticosterone (CORT) content of feathers is a potent source of information about activation of hypothalamus-pituitary-adrenal (HPA) axis during feather growth, which is used for assessment of well-being and stress history of individuals and populations in avian studies. However, little is known about factors affecting deposition of CORT into feathers and how feather CORT covaries with other markers of stress imposed upon individuals during feather growth. We addressed these questions by measuring CORT levels in feathers of wild-caught greenfinches (Carduelis chloris) brought into captivity. One tail feather was removed from all the birds upon arrival to the laboratory and the CORT levels of replacement feathers, grown in captivity were recorded. The birds were subjected to treatments of immune activation (by injection of phytohaemagglutinin) and synthetic glucocorticoid (dexamethasone, DEX) administration. Only DEX injection affected feather CORT levels. DEX-injected birds deposited on average 37% less of CORT in their feathers than saline-injected birds. Despite significant effects of DEX and immune activation treatments on differential leukocyte counts, we did not find any correlations between CORT and leukocyte hemoconcentrations or heterophil/lymphocyte ratios (a haematological index of stress), measured at three stages of feather growth. Our findings provide novel evidence that feather CORT levels are sensitive to manipulation of hormonal balance of birds, thereby supporting the diagnostic value of feather CORT measurements. However, we did not find any evidence about covariation between feather CORT and other markers of stress perceived during the period of feather growth. This calls for further research on information content of feather CORT, preferably in experiments manipulating more diverse array of psychological, immunological and abiotic stressors.

Antioxidant protection, immune function and growth of nestling great tits Parus major in relation to within-brood hierarchy.

Differences in competitive abilities of siblings in birds can be caused by a combination of hatching asynchrony and intra-clutch variation in egg quality. However, very little is known how within-brood hierarchies affect the allocation of resources between different functions of the body. We examined the effects of within-brood hierarchy on growth of morphological parameters, blood plasma antioxidant protection and immune function of free-living great tit Parus major nestlings. To assure that competitive hierarchies occur, we experimentally delayed the start of incubation of the last two eggs in the clutch. At pre-fledging stage (day 13 post-hatch), late-hatched nestlings were smaller in body mass and wing length when compared to early-hatched nestlings, but no differences between siblings were found in tarsus length, plasma antioxidant potential, uric acid concentration, residual antioxidant potential (from regression with uric acid), hematocrit and response to phytohaemagglutinin injection. In early-hatched nestlings, the antioxidant potential and residual antioxidant potential measured in the middle of nestling period (day 6 post-hatch) were negatively related to body mass growth at early nestling stage, indicating that fast initial growth could reduce antioxidant properties of blood plasma.

Carotenoid coloration in greenfinches is individually consistent irrespective of foraging ability.

Carotenoid-based plumage coloration of birds has been hypothesized to honestly reflect individual quality, either because carotenoids are difficult to acquire via food or because of a trade-off in allocation of carotenoids between maintenance and signaling functions. We tested whether differential foraging ability is a necessary precondition for maintaining individual differences in carotenoid-based plumage coloration in male greenfinches (Carduelis chloris). Wild-caught birds were brought into captivity, where half of them were supplemented with carotenoids while the other half was maintained on a carotenoid-poor diet. Color of the yellow parts of tail feathers, grown under natural conditions, was compared with that of the replacement feathers, grown in captivity. Carotenoid supplementation increased feather chroma (saturation). Color of wild-grown feathers significantly correlated with the color of lab-grown feathers. This result demonstrates the existence of a significant component of variation in carotenoid coloration, which reflects physiological qualities or genetic differences among individuals independent of foraging ability. Among both experimental groups, plasma carotenoid concentration during feather growth strongly correlated with chroma of the feathers grown in captivity. This indicates that carotenoid-based plumage coloration can reveal circulating carotenoid levels over a very wide range of concentrations, suggesting the ample signaling potential of such a mechanism.

Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches.

Reactive oxygen and nitrogen species produced by metabolism and immune defenses can cause extensive damage to biomolecules. To counteract this damage, organisms rely on exogenous and endogenous antioxidants, although their relative importance in maintaining redox balance is unclear. We supplemented captive greenfinches with dietary antioxidants--carotenoids and vitamin E--and injected them with an inflammatory agent, phytohemagglutinin. Compared to controls, immune-challenged birds circulated more lipid peroxidation products but also increased total plasma antioxidativity. Carotenoid (but not vitamin E) supplementation generally reduced lipid peroxidation, but this did not compensate for the effects of immune activation. Levels of an endogenous antioxidant--uric acid--strongly contributed to plasma antioxidativity. We found no evidence that dietary antioxidants are immunostimulatory. These results demonstrate the antioxidant function of carotenoids in birds and show that simultaneous assessment of oxidative stress-driven damage, antioxidant barrier, and individual antioxidants is critical for explaining the potential costs of immune system activation.

Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches.

Costs accompanying immune challenges are believed to play an important role in life-history trade-offs and warranting the honesty of signal traits. We performed an experiment in captive greenfinches (Carduelis chloris L.) in order to test whether and how humoral immune challenge with non-pathogenic antigen [sheep red blood cells (SRBC)] affects parameters of individual condition including intensity of coccidian infection, estimates of total antioxidant protection, plasma carotenoids and ability to mount a cell-mediated immune response. We also asked whether the potential costs of immune challenge can be alleviated by dietary carotenoid supplementation. None of the treatments affected intensity of coccidiosis. Humoral immune challenge suppressed the cell-mediated response to phytohemagglutinin (PHA), suggesting a trade-off between the uses of different arms of the immune system. Immune challenge reduced body-mass gain, but only among the carotenoid-depleted birds, indicating that certain somatic costs associated with immune system activation can be alleviated by carotenoids. No evidence for oxidative stress-induced immunopathological damages could be found because immune activation did not affect total antioxidant protection or carotenoid levels. Carotenoid supplementation inclined birds to fattening, indicating that lutein interfered with lipid metabolism. Altogether, our results support the hypotheses of biological importance of carotenoids and exemplify the overwhelming complexity of their integrated ecophysiological functions.

Animal allure and health linked by plant pigments.

Darwin introduced the idea that ornamental secondary sexual traits have evolved in response to female preferences for showy males. Among such traits, yellow and red carotenoid-based ornaments have been considered as particularly good candidates for explaining why and how females would benefit from mating with showy partners. Because carotenoids can be used for promotion of both health and appearance, colourful male ornaments should honestly reveal the vigour of the bearers. Two recent experiments with birds now show how allocation of bodily carotenoids to sexual signalling is traded off against the use of carotenoids for boosting immune function.

Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence.

Hypotheses of parasite-mediated sexual selection (PMSS) propose that elaborate male ornaments have evolved due to female preferences. Females would benefit from mating with more ornamental males if males' ornamentation signals their health status and ability to provide parasite resistance genes for the offspring. Carotenoid-based plumage coloration of birds has been hypothesised to honestly reflect an individual's health status due to trade-off in allocation of carotenoids between maintenance and signalling functions. The prediction of this hypothesis, namely that individuals with brighter plumage are able to mount stronger immune responses against novel antigens and reveal generally better health state, was tested in captive male greenfinches (Carduelis chloris). Greenfinches with brighter yellow breast feathers showed stronger humoral immune response against novel antigen (SRBC) while no relationship between plumage coloration and an estimate of cell-mediated immune responsiveness (PHA response) was detected. Elaborately ornamental individuals had better general health state as indicated by the negative correlations between plumage brightness and heterophil haemoconcentration. Consistent with the concept of PMSS, these results suggest that carotenoid-based plumage coloration in greenfinches honestly signals immunocompetence and health status.