Ádám Z. Lendvai

Stress Response and the Value of Reproduction : Are Birds Prudent Parents?

In vertebrates, stressors such as starvation or predator attacks stimulate the rapid elevation of circulating glucocorticoid hormones, triggering physiological and behavioral responses that aid immediate survival but simultaneously inhibit reproduction. This stress response has been proposed to serve as a physiological mediator of life‐history trade‐offs: when the value of current reproduction is high relative to the value of future reproduction and survival, a mitigated stress response is expected to enable successful breeding and maximize fitness. Using phylogenetic comparative analyses, we investigated baseline and peak stress‐induced plasma corticosterone levels during parental care in 64 bird species. We found that (1) species with a higher value of the current brood relative to future breeding mounted weaker corticosterone responses during acute stress, and (2) females in species with more female‐biased parental care had weaker corticosterone responses. These results support the brood value hypothesis, suggesting that the stress response evolves as an adaptive basis for life‐history strategies. Further, we found that (3) baseline corticosterone correlated positively with brood value and negatively with body mass, and (4) peak corticosterone was greater in species breeding at higher latitudes. The latter findings suggest that circulating corticosterone concentrations might be matched to the anticipated demands and risks during nesting.

Lean birds in the city: body size and condition of house sparrows along the urbanization gradient

1. Urbanized habitats differ from natural ones in several ecological features, including climate, food availability, strength of predation and competition. Although the effects of urbanization on avian community composition are well known, there is much less information about how individual birds are affected by these human-generated habitat differences. 2. In this study we investigated the relationships between the morphological characteristics and the degree of habitat urbanization in house sparrows, Passer domesticus (Linne 1758) . We collected data for more than 1000 non-breeding adult birds in Hungary between 1997 and 2006, from seven sites including farmlands, suburban areas and city centres. 3. We found that the body mass, tarsus length and body condition of free-living sparrows differed among the sites: birds in more urbanized habitats were consistently smaller and in worse condition than birds in more rural habitats. A composite measure of habitat urbanization (based on building density, road density and vegetation cover) explained over 75% of variance between sites in the studied traits, after we controlled for the effects of sex, year, season and time of capture. 4. The difference in body mass between rural and urban sparrows was significant when birds were kept in aviaries under identical conditions, with constant ad libitum food availability. It is therefore unlikely that the reduced body size and condition of urban sparrows are a consequence of reduced access to food for adults (e.g. due to strong competition), or their short-term responses to high food predictability (e.g. by strategic mass regulation). 5. We suggest that habitat differences in nestling development or adaptive divergence of sparrow populations due to distinct environmental conditions (such as differing predation pressure) may account for the differences along the urbanization gradient.

Predictions of avian Plasmodium expansion under climate change

Vector-borne diseases are particularly responsive to changing environmental conditions. Diurnal temperature variation has been identified as a particularly important factor for the development of malaria parasites within vectors. Here, we conducted a survey across France, screening populations of the house sparrow (Passer domesticus) for malaria (Plasmodium relictum). We investigated whether variation in remotely-sensed environmental variables accounted for the spatial variation observed in prevalence and parasitemia. While prevalence was highly correlated to diurnal temperature range and other measures of temperature variation, environmental conditions could not predict spatial variation in parasitemia. Based on our empirical data, we mapped malaria distribution under climate change scenarios and predicted that Plasmodium occurrence will spread to regions in northern France, and that prevalence levels are likely to increase in locations where transmission already occurs. Our findings, based on remote sensing tools coupled with empirical data suggest that climatic change will significantly alter transmission of malaria parasites.

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.

An investigation of mate choice based on manipulation of multiple ornaments in Kentish plovers

Many animals have multiple sexual ornaments, a fact variously explained as signalling of multiple attributes, or nonadaptive retention of now redundant, but previously informative, signals. Despite the widespread occurrence of multiple ornaments, and the theoretical interest in how they are maintained by selection, there have been few experimental studies of the phenomenon. We investigated the role of two ornaments, each plausibly signalling different male attributes, in attracting a new mate in the Kentish plover, Charadrius alexandrinus. Previously we have shown that male Kentish plovers vary in how long they take to acquire a new mate, and we hypothesized that this variation may relate to their attractiveness or parental ability. We created single males by removing their mate and clutch, and then manipulated both their badge size (a presumed signal of either their genetic quality or their dominance status and hence defensive abilities) and the length of their flank feathers (a presumed signal of their parental quality in incubation) in a 2×2 factorial design. We found no difference in remating times between manipulated and control males. Furthermore, neither body size nor body condition of males was related to their remating times, although males with enlarged badges spent less time fighting than control males. Taken together, our results suggest that female Kentish plovers do not use either badge size or the length of flank feathers as cues in their mate choice decisions. However, badge size may influence male–male competition.

Experimental Food Restriction Reveals Individual Differences in Corticosterone Reaction Norms with No Oxidative Costs

Highly plastic endocrine traits are thought to play a central role in allowing organisms to respond rapidly to environmental change. Yet, not all individuals display the same degree of plasticity in these traits, and the costs of this individual variation in plasticity are unknown. We studied individual differences in corticosterone levels under varying conditions to test whether there are consistent individual differences in (1) baseline corticosterone levels; (2) plasticity in the hormonal response to an ecologically relevant stressor (food restriction); and (3) whether individual differences in plasticity are related to fitness costs, as estimated by oxidative stress levels. We took 25 wild-caught house sparrows into captivity and assigned them to repeated food restricted and control treatments (60% and 110% of their daily food intake), such that each individual experienced both food restricted and control diets twice. We found significant individual variation in baseline corticosterone levels and stress responsiveness, even after controlling for changes in body mass. However, these individual differences in hormonal responsiveness were not related to measures of oxidative stress. These results have implications for how corticosterone levels may evolve in natural populations and raise questions about what we can conclude from phenotypic correlations between hormone levels and fitness measures.

Early developmental conditions affect stress response in juvenile but not in adult house sparrows (Passer domesticus)

The short- and long-term consequences of developmental conditions on fitness have received growing attention because the environmental conditions during early life may influence growth, condition at independence, recruitment, reproductive success or survival. We tested here, in a natural house sparrow population, if early conditions during nestling stage affected the stress response of the birds (i) shortly after fledging and (ii) next year, during their first breeding. We experimentally manipulated brood size to mimic different rearing conditions, creating reduced (-2 chicks) and enlarged broods (+2 chicks), while in a third group brood size was not manipulated. Nestling nutrition state decreased with post-manipulation brood sizes as indicated by lower body mass. Fledglings with higher body mass at the age of ten days showed lower stress response than birds that were leaner at the same age. Fledglings reared in large broods showed a higher response to stress protocol than chicks from small broods, and this effect was in significant interaction with the age of fledglings at capture. This interaction indicates that the effects of the brood size became gradually smaller as the fledglings grew older and were further from their nestling period. The effects of early conditions vanished by the next year: the stress response of adult first time breeders was unrelated to the brood size they fledged from. These results suggest that stress response may reflect the actual state of an individual, rather than its developmental history.

Do smart birds stress less? An interspecific relationship between brain size and corticosterone levels

Vertebrates respond to unpredictable noxious environmental stimuli by increasing secretion of glucocorticoids (CORT). Although this hormonal stress response is adaptive, high levels of CORT may induce significant costs if stressful situations are frequent. Thus, alternative coping mechanisms that help buffer individuals against environmental stressors may be selected for when the costs of CORT levels are elevated. By allowing individuals to identify, anticipate and cope with the stressful circumstances, cognition may enable stress-specific behavioural coping. Although there is evidence that behavioural responses allow animals to cope with stressful situations, it is unclear whether or not cognition reduces investment in the neuroendocrine stress response. Here, we report that in birds, species with larger brains relative to their body size show lower baseline and peak CORT levels than species with smaller brains. This relationship is consistent across life-history stages, and cannot be accounted for by differences in life history and geographical latitude. Because a large brain is a major feature of birds that base their lifetime in learning new things, our results support the hypothesis that enhanced cognition represents a general alternative to the neuroendocrine stress response.

Mercury exposure, stress and prolactin secretion in an Arctic seabird: an experimental study

Summary Life-history theory predicts that long-lived organisms should reduce parental effort under inclement environmental conditions in order to favour long-term survival. Seabirds are long-lived top predators often exposed to environmental endocrine disrupting chemicals such as mercury (Hg). Hg-contaminated birds show disrupted parental behaviour. Avian parental behaviour is governed by two key hormones in birds: corticosterone (CORT, a glucocorticoid hormone) and prolactin (PRL, a pituitary hormone involved in parental care). Any disruption of these hormones may alter the ability of an individual to adjust parental behaviour to environmental conditions. The first aim of this study was to describe the relationships between blood Hg concentrations, plasma PRL and reproductive performance in Arctic black-legged kittiwakes (Rissa tridactyla). We a found negative relationship between plasma initial PRL and blood Hg concentrations in males. Moreover, Hg concentration was negatively related to breeding success in chick-rearing males. Secondly, to study the effect of a chronic increase in CORT levels on the Hg–PRL relationship, we experimentally increased stress with CORT pellet implantation. We predicted that Hg and CORT would act synergistically on PRL and an increase in CORT concentration would steepen the Hg–PRL relationship. However, adding CORT did not steepen the Hg–PRL relationship. Hatching success was significantly lower in CORT-implanted males than in controls, and breeding success was not reduced in CORT-implanted male kittiwakes with high levels of blood Hg. Our results suggest that Hg may impair reproductive performance through a disruption of PRL secretion. Contrary to our prediction, Hg and CORT did not act synergistically and the underlying mechanisms associating CORT and Hg with PRL might be more complex than a single interaction between two factors.

Increased adrenal responsiveness and delayed hatching date in relation to polychlorinated biphenyl exposure in Arctic-breeding black-legged kittiwakes (Rissa tridactyla)

High levels of environmental contaminants such as polychlorinated biphenyls (PCBs), organochlorine pesticides (OCPs) and mercury (Hg) have been reported in some Arctic top predators such as seabirds. Chronic exposure to these contaminants might alter the response to environmental changes through interference with the regulation of corticosterone (CORT), a glucocorticoid stress hormone released by the hypothalamo-pituitary-adrenal (HPA) axis. Positive and negative relationships between CORT and environmental contaminants have been reported in polar seabirds. However, patterns appear inconclusive and it is difficult to attribute these relationships to a dysfunction of the HPA axis or to other confounding effects. In order to explore the relationships between the HPA axis activity and contaminants, we tested whether different aspects of the HPA axis of an Arctic seabird, the black-legged kittiwakes Rissa tridactyla, would be related to blood Hg, PCB and OCP concentrations. Male kittiwakes were caught during the incubation period in Svalbard and were subjected to different stress series: (1) a capture-restraint stress protocol, (2) an injection of dexamethasone (DEX) that enabled to test the efficacy of the HPA negative feedback and (3) an injection of adrenocorticotropic hormone (ACTH) that informed on the adrenal responsiveness. The HPA axis activity was unrelated to ΣOCPs and Hg. However, birds with high concentrations of ΣPCBs released more CORT after the ACTH injection. It is suggested that ΣPCBs may increase the number of ACTH-receptors on the adrenals. Additionally, hatching date was delayed in males with higher concentrations of ΣPCBs and ΣOCPs. This study gives new evidence that PCBs and adrenal activity may be related. Thus high PCB burden may make individuals more prone to other stressors such as ongoing climate change.