Mathieu Giraudeau

Corticosterone and foraging behavior in a diving seabird: the Adélie penguin, Pygoscelis adeliae.

Because hormones mediate physiological or behavioral responses to intrinsic or extrinsic stimuli, they can help us understand how animals adapt their foraging decisions to energetic demands of reproduction. Thus, the hormone corticosterone deserves specific attention because of its influence on metabolism, food intake and locomotor activities. We examined the relationships between baseline corticosterone levels and foraging behavior or mass gain at sea in a diving seabird, the Adélie penguin, Pygoscelis adeliae. Data were obtained from free-ranging penguins during the brooding period (Adélie Land, Antarctica) by using satellite transmitters and time-depth-recorders. The birds were weighed and blood sampled before and after a foraging trip (pre-trip and post-trip corticosterone levels, respectively). Penguins with elevated pre-trip corticosterone levels spent less time at sea and stayed closer to the colony than penguins with low pre-trip corticosterone levels. These short trips were associated with a higher foraging effort in terms of diving activity and a lower mass gain at sea than long trips. According to previous studies conducted on seabird species, these results suggest that penguins with elevated pre-trip corticosterone levels might maximize the rate of energy delivery to the chicks at the expense of their body reserves. Moreover, in all birds, corticosterone levels were lower post-foraging than pre-foraging. This decrease could result from either the restoration of body reserves during the foraging trip or from a break in activity at the end of the foraging trip. This study demonstrates for the first time in a diving predator the close relationships linking foraging behavior and baseline corticosterone levels. We suggest that slight elevations in pre-trip corticosterone levels could play a major role in breeding effort by facilitating foraging activity in breeding seabirds.

Parasites in the city: degree of urbanization predicts poxvirus and coccidian infections in house finches (Haemorhous mexicanus).

Background Urbanization can strongly impact the physiology, behavior, and fitness of animals. Conditions in cities may also promote the transmission and success of animal parasites and pathogens. However, to date, no studies have examined variation in the prevalence or severity of several distinct pathogens/parasites along a gradient of urbanization in animals or if these infections increase physiological stress in urban populations. Methodology/Principal Findings Here, we measured the prevalence and severity of infection with intestinal coccidians (Isospora sp.) and the canarypox virus (Avipoxvirus) along an urban-to-rural gradient in wild male house finches (Haemorhous mexicanus). In addition, we quantified an important stress indicator in animals (oxidative stress) and several axes of urbanization, including human population density and land-use patterns within a 1 km radius of each trapping site. Prevalence of poxvirus infection and severity of coccidial infection were significantly associated with the degree of urbanization, with an increase of infection in more urban areas. The degrees of infection by the two parasites were not correlated along the urban-rural gradient. Finally, levels of oxidative damage in plasma were not associated with infection or with urbanization metrics. Conclusion/Significance These results indicate that the physical presence of humans in cities and the associated altered urban landscape characteristics are associated with increased infections with both a virus and a gastrointestinal parasite in this common songbird resident of North American cities. Though we failed to find elevations in urban- or parasite/pathogen-mediated oxidative stress, humans may facilitate infections in these birds via bird feeders (i.e. horizontal disease transmission due to unsanitary surfaces and/or elevations in host population densities) and/or via elevations in other forms of physiological stress (e.g. corticosterone, nutritional).

Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria

The preen gland is a holocrine sebaceous gland of the avian integument which produces an oily secretion that is spread on the plumage during preening. It has been suggested that birds may defend themselves against feather-degrading bacteria (FDB) and other potential pathogens using preen gland secretions. However, besides some in vitro studies, the in vivo bacterial inhibitory effects of the preen oil on the abundance of feather-associated bacterial species has not yet been studied in passerines. Here we tested the effect of gland removal on the abundance of FDB and other-cultivable bacterial loads (OCB) of male house sparrows (Passer domesticus). Our results did not support earlier results on in vitro antibacterial activity of preen oil against FDB since the absence of the preen gland did not significantly affect their loads related to the control birds. In contrast, we found that preen gland removal led to higher loads of OCB. This result suggests that the antimicrobial spectrum of the preen oil is broader than previously thought and that, by reducing the overall feather bacterial loads, the preen gland could help birds to protect themselves against a variety of potentially harmful bacteria.

Maternal investment of female mallards is influenced by male carotenoid-based coloration

The differential allocation hypothesis predicts that females modify their investment in a breeding attempt according to its reproductive value. One prediction of this hypothesis is that females will increase reproductive investment when mated to high-quality males. In birds, it was shown that females can modulate pre-hatch reproductive investment by manipulating egg and clutch sizes and/or the concentrations of egg internal compounds according to paternal attractiveness. However, the differential allocation of immune factors has seldom been considered, particularly with an experimental approach. The carotenoid-based ornaments can function as reliable signals of quality, indicating better immunity or ability to resist parasites. Thus, numerous studies show that females use the expression of carotenoid-based colour when choosing mates; but the influence of this paternal coloration on maternal investment decisions has seldom been considered and has only been experimentally studied with artificial manipulation of male coloration. Here, we used dietary carotenoid provisioning to manipulate male mallard (Anas platyrhynchos) bill coloration, a sexually selected trait, and followed female investment. We show that an increase of male bill coloration positively influenced egg mass and albumen lysozyme concentration. By contrast, yolk carotenoid concentration was not affected by paternal ornamentation. Maternal decisions highlighted in this study may influence chick survival and compel males to maintain carotenoid-based coloration from the mate-choice period until egg-laying has been finished.

Carotenoid-based plumage coloration reflects feather corticosterone levels in male house finches (Haemorhous mexicanus)

Indicator models of sexual selection predict that exaggerated traits communicate information about sender condition or quality to conspecific receivers. Environmental challenges have often been considered as one such condition that could be encoded in an ornamental trait, and there is now extensive evidence showing how different stressors (e.g., nutritional, parasitological, and environmental) impact sexual signal elaboration. One of the primary means of assessing stress is by quantifying glucocorticoid (corticosterone or cortisol (CORT)) levels. For many ornaments, CORT impairs trait expression; however, the evidence is limited and mixed for one of the classic honest signals in animals, ornamental carotenoid coloration. In a model species for studies of carotenoid ornamentation (the house finch, Haemorhous mexicanus), we examined the relationship between male plumage redness and feather CORT levels, which serve as an integrated measure of hormone concentration during feather growth. We measured CORT in both tail (melanin-containing) and breast (carotenoid-containing) feathers and found that CORT levels were not different between body regions, but they were negatively correlated with plumage hue, with redder birds having more CORT in feathers. Despite opposing traditional views on stress and ornamentation, our results actually corroborate three other studies showing positive relationships between carotenoid coloration and CORT levels. Though the molecular mechanisms underlying such a relationship are still unclear, our results suggest that CORT should not be considered as a simple indicator of individual quality but rather as a mediator of complex allocation decisions or signals of metabolic activity that could link up with more elaborate expression of ornamental traits.

Effects of carotenoid and vitamin E supplementation on oxidative stress and plumage coloration in house finches (Haemorhous mexicanus)

There has been much recent interest from both applied and basic scientists in the broad series of benefits that animals reap from acquiring high concentrations of dietary antioxidants, such as carotenoids and vitamins (e.g., vitamin E, or tocopherol). Most attention has been paid to separate effects of these compounds on, for example, coloration, health state, development, and vision, but because of possible interactions between these lipid-soluble molecules, we are in need of more studies that co-manipulate these substances and examine their possible synergistic impacts on animal physiology and phenotype. We capitalized on a model avian system (the house finch, Haemorhous mexicanus), where extensive information is available on the fitness roles of carotenoids, to test how variation in carotenoid and/or vitamin E concentrations in the diet impacts body accumulation of these compounds, factors related to oxidative damage (e.g., breast muscle and plasma oxidative-stress susceptibility, plasma nitric-oxide levels), and plumage color development. As in a previous study of ours on carotenoids and health in finches, we employed a 2×2 factorial experimental design on birds in both molting and non-molting conditions, to understand how seasonal shifts in carotenoid use (i.e., pigment incorporation into plumage) might alter the accumulation and roles of carotenoids and vitamins. As expected, lutein supplementation increased the level of circulating carotenoids in both experiments and the color of newly molted plumage. By contrast, vitamin E provisioning did not significantly affect plasma carotenoid levels or plumage coloration in either experiment. Interestingly, carotenoid provisioning decreased circulating vitamin E levels during molt, which suggests either molecular competition between carotenoids and tocopherol at the absorption/transport stages or that vitamin E serves as an antioxidant to offset harmful actions that carotenoids may have at very high concentrations. Finally, in both experiments, we found a reduction in breast-muscle oxidative damage for tocopherol-supplemented birds, which constitutes the first demonstration of a protective effect of vitamin E against oxidative stress in wild birds. Taken together, these findings provide an interesting contrast with our earlier work on season-specific physiological benefits of carotenoids in finches and point to complex associations between indicators of antioxidant and oxidative state in wild-caught animals.

Effect of preen oil on plumage bacteria: An experimental test with the mallard

Feathers are essential for avian thermoregulation, communication or flight and a reduction of plumage condition may alter these functions and reduce individual fitness. Recently, descriptive studies provided evidence that birds carry feather-degrading bacteria on their plumage that have the ability to degrade feathers rapidly under laboratory conditions. If such bacteria reduce avian fitness, natural selection should favour the evolution of anti-bacterial defences to limit the effects of these detrimental microorganisms. Preening behaviour and associated preen gland secretions have been proposed as the main factor used by birds to limit feather-degrading bacterial growth and some recent in vitro studies provided evidence that uropygial oil inhibited the growth of some keratinolytic strains in passerines. However, preen oil antimicrobial properties remained to be experimentally tested in vivo. We conducted an experiment with mallards (Anas platyrhynchos) onto which we fixed a removable mechanism that blocked access to the uropygial gland in a first group of mallards, whilst birds in a second group had the same removable mechanism but access to their gland and a third group of birds had normal access to their gland. We found no significant effect of our treatment on total and feather-degrading bacterial loads. Three hypotheses may explain the discrepancy between our results and previous in vitro studies. First, in vitro studies may have over-estimated the bactericidal properties of the preen oil. Second, preen gland deprivation may have affected only a small portion of the feather-degrading bacterial community. Third, ducks and passerine oils might have different bactericidal properties.

Physiological Correlates of Urbanization in a Desert Songbird

Rapid worldwide urbanization is creating novel environments to which animals must adapt, a topic of growing interest for biologists. Studies of how organisms are affected by cities historically centered on large-scale censusing of populations, but recent investigations have considered finer-scaled, urban-rural differences among individuals and species in their behavior, morphology, and physiology, specifically as they relate to urban stress. A number of factors (e.g., corticosterone (CORT)-related stress response) may contribute to the degree of stress experienced by animals living under urban versus natural conditions, but several physiological variables have yet to be considered together in a large-scale assessment. Here, in a widespread species of desert passerine (the house finch, Haemorhous mexicanus), we quantified variation in plasma oxidative stress, plasma concentrations of vitamins and carotenoids, and body-mass of males in three successive seasons (winter, spring, and late summer/early fall) along an urban-rural gradient in Phoenix, Arizona, USA. We found that degree of urbanization was: (1) negatively related to circulating vitamin A concentrations in winter, (2) positively correlated with body-mass during spring, and (3) negatively associated with plasma concentrations of two carotenoids: zeaxanthin (during breeding) and 3-hydroxy-echinenone (3HE) (during molting). The striking link between 3HE levels and urbanization is consistent with previous research showing that urban songbirds have lower carotenoid levels and faded plumage; our finding is the first to implicate specific effects on a metabolically derived carotenoid for coloration. The fact that we observed only season-specific links between urbanization and indicators of quality in finches suggests that (at least for these metrics) there are no strong, lasting urban pressures imposed on finch physiology over the year. Interestingly, we found that a metric of plasma oxidative stress (lipid peroxidation) was positively correlated with levels of two carotenoids (lutein during breeding and 3HE during molting), which is consistent with a prior study of ours showing that finches with redder plumage deposit higher levels of CORT in their feathers; taken together, our studies suggest complex associations between carotenoids and stress.

Song characteristics track bill morphology along a gradient of urbanization in house finches (Haemorhous mexicanus)

IntroductionUrbanization can considerably impact animal ecology, evolution, and behavior. Among the new conditions that animals experience in cities is anthropogenic noise, which can limit the sound space available for animals to communicate using acoustic signals. Some urban bird species increase their song frequencies so that they can be heard above low-frequency background city noise. However, the ability to make such song modifications may be constrained by several morphological factors, including bill gape, size, and shape, thereby limiting the degree to which certain species can vocally adapt to urban settings. We examined the relationship between song characteristics and bill morphology in a species (the house finch, Haemorhous mexicanus) where both vocal performance and bill size are known to differ between city and rural animals.ResultsWe found that bills were longer and narrower in more disturbed, urban areas. We observed an increase in minimum song frequency of urban birds, and we also found that the upper frequency limit of songs decreased in direct relation to bill morphology.ConclusionsThese findings are consistent with the hypothesis that birds with longer beaks and therefore longer vocal tracts sing songs with lower maximum frequencies because longer tubes have lower-frequency resonances. Thus, for the first time, we reveal dual constraints (one biotic, one abiotic) on the song frequency range of urban animals. Urban foraging pressures may additionally interact with the acoustic environment to shape bill traits and vocal performance.

Effect of Restricted Preen-Gland Access on Maternal Self Maintenance and Reproductive Investment in Mallards

Background As egg production and offspring care are costly, females should invest resources adaptively into their eggs to optimize current offspring quality and their own lifetime reproductive success. Parasite infections can influence maternal investment decisions due to their multiple negative physiological effects. The act of preening – applying oils with anti-microbial properties to feathers – is thought to be a means by which birds combat pathogens and parasites, but little is known of how preening during the reproductive period (and its expected disease-protecting effects) influences maternal investment decisions at the level of the egg. Methodology/Principal Findings Here, we experimentally prevented female mallards (Anas platyrhynchos) from accessing their preen gland during breeding and monitored female immunoresponsiveness (e.g., plasma lysozyme concentration) as well as some egg traits linked to offspring quality (e.g., egg mass, yolk carotenoid content, and albumen lysozyme levels). Females with no access to their preen gland showed an increase in plasma lysozyme level compared to control, normally preening females. In addition, preen-gland-restricted females laid significantly lighter eggs and deposited higher carotenoid concentrations in the yolk compared to control females. Albumen lysozyme activity did not differ significantly between eggs laid by females with or without preen gland access. Conclusion/Significance Our results establish a new link between an important avian self-maintenance behaviour and aspects of maternal health and reproduction. We suggest that higher yolk carotenoid levels in eggs laid by preen-gland-restricted females may serve to boost health of offspring that would hatch in a comparatively microbe-rich environment.