Corticosterone implants produce stress-hyporesponsive birds.

In birds, the use of corticosterone (Cort) implants is a frequent tool aimed at simulating systemic elevations of this hormone and studying effects on biological traits (e.g. physiology, morphology, behavior). This manipulation may alter adrenocortical function, potentially changing both baseline (CortBAS) and stress-induced (CortSTRESS) plasma Cort levels. However, implant effects on the latter trait are rarely measured, disregarding downstream consequences of potentially altered stress responses. Here, we analyzed the effects of Cort implants on both CortBAS and CortSTRESS in nestling and adult European white storks, Ciconia ciconia In addition, we performed a review of 50 studies using Cort implants in birds during the last two decades to contextualize stork results, assess researchers' patterns of use and infer current study biases. High and low doses of Cort implants resulted in a decrease of both CortBAS (31-71% below controls) and CortSTRESS (63-79% below controls) in storks. Our literature review revealed that CortBAS generally increases (72% of experiments) whereas CortSTRESS decreases (78% of experiments) following implant treatment in birds. Our results challenge and expand the prevailing assumption that Cort implants increase circulating CortBAS levels because: (i) CortBAS levels show a quadratic association with implant dose across bird species, and decreased levels may occur at both high and low implant doses, and (ii) Cort implants also decrease CortSTRESS levels, thus producing stress-hyporesponsive phenotypes. It is time to work towards a better understanding of the effects of Cort implants on adrenocortical function, before addressing downstream links to variation in other biological traits.

Lifetime variation in feather corticosterone levels in a long-lived raptor.

In long-lived animals, the challenges that threaten individual homeostasis, and the way they are dealt with, are expected to vary in an age-related manner, encompassing the progressive selection of superior phenotypes and the acquisition and improvement of key skills (e.g. foraging, breeding and fighting abilities). Since exposure to homeostatic challenges typically elevates circulating glucocorticoid (GC) levels in vertebrates (modulating the behavioural and physiological responses that mediate allostasis), we may expect concomitant age-related changes in these hormones. Here, we investigated whether the level of corticosterone (the main avian GC) deposited in feathers during regular moult reflected the expected lifelong progression of energetic challenges in a long-lived raptor, the black kite (Milvus migrans). Feather corticosterone values were highest in the youngest birds, gradually declined to reach minimum levels in prime age, 7- to 11-year-old birds, and then increased again slightly among the oldest, senescent birds (≥12 years old). This pattern mirrored the age-related changes in reproductive success and survival rates previously reported for this population, suggesting that feather corticosterone levels captured the most vulnerable and challenging periods experienced by these birds as they proceeded through life. Moreover, feather corticosterone levels were negatively related to body size, suggesting that larger birds either experienced fewer homeostatic challenges, or were better able to cope with them. Feather corticosterone measures thus provided a valuable snapshot of how allostatic loads vary along the life of individuals, supporting the idea of a tight, long-term link between cumulative physiological responses to ecological challenges and demographic performance.

Experimental relationships between levels of corticosterone in plasma and feathers in a free-living bird.

Integrated measures of corticosterone (CORT), such as from feathers (CORTf), have intuitive appeal because they incorporate both the duration and amplitude of glucocorticoid secretion. An association between CORTf and plasma CORT has never been shown in wild birds, and it is unclear as to when and whether these measures should be correlated, given that they are fundamentally different yet related measures of physiology. We hypothesized that CORTf should correlate with instantaneous measurements of plasma CORT when the latter reflect sustained changes in the activity of the hypothalamic-pituitary-adrenal (HPA) axis. To test this, we experimentally manipulated levels of plasma CORT in wild nestling tree swallows (Tachycineta bicolor) using 5 day time-release CORT pellets, and measured plasma CORT and growth parameters before, during and at the end of hormone manipulation (days 7, 9 and 11 post-hatch, respectively). CORTf and plasma CORT were significantly positively related only when the latter was at its highest and most variable among individuals (day 9). A similar relationship was expected at day 11, but plasma CORT had returned to near-original levels. Nestlings with higher CORTf were smaller, lighter and less likely to fledge, but we did not detect seasonal effects on CORTf. Our results clearly demonstrate that CORTf from free-living birds can reflect plasma CORT, but correlations may not always be expected, especially if elevations in plasma CORT are relatively modest and of short duration. Our work suggests that CORTf is best used to study the activity of the HPA axis over relatively long time frames and can be used effectively to advance avian ecology.

Feather corticosterone of a nestling seabird reveals consequences of sex-specific parental investment.

Offspring of long-lived species should face costs of parental trade-offs that vary with overall energetic demands encountered by parents during breeding. If sex differences exist in how parents make the trade-off, sex-specific differences may exist in the contribution of each parent to those costs. Adaptations of offspring facing such costs are not well understood, but the hormone corticosterone probably plays a role. We manipulated breeding effort in Cory's shearwaters (Calonectris diomedea) to increase costs to offspring and used an integrated measure of corticosterone from chick feathers to investigate how experimental variation in parental investment influences offspring physiology. Average foraging trip duration and foraging efficiency (FE) of breeding pairs were not related to chick corticosterone, but sex biases in FE were. Adult male investment was more strongly related to chick corticosterone than was female investment. Importantly, we show for the first time suppression of adrenocortical activity in nestling Procellariiform seabirds, and explain how our results indicate an adaptive mechanism invoked by chicks facing increased costs of parental trade-offs.

Selection on individuals of introduced species starts before the actual introduction.

Biological invasion is a global problem with large negative impacts on ecosystems and human societies. When a species is introduced, individuals will first have to pass through the invasion stages of uptake and transport, before actual introduction in a non-native range. Selection is predicted to act during these earliest stages of biological invasion, potentially influencing the invasiveness and/or impact of introduced populations. Despite this potential impact of pre-introduction selection, empirical tests are virtually lacking. To test the hypothesis of pre-introduction selection, we followed the fate of individuals during capture, initial acclimation, and captivity in two bird species with several invasive populations originating from the international trade in wild-caught pets (the weavers Ploceus melanocephalus and Euplectes afer). We confirm that pre-introduction selection acts on a wide range of physiological, morphological, behavioral, and demographic traits (incl. sex, age, size of body/brain/bill, bill shape, body mass, corticosterone levels, and escape behavior); these are all traits which likely affect invasion success. Our study thus comprehensively demonstrates the existence of hitherto ignored selection acting before the actual introduction into non-native ranges. This could ultimately change the composition and functioning of introduced populations, and therefore warrants greater attention. More knowledge on pre-introduction selection also might provide novel targets for the management of invasive species, if pre-introduction filters can be adjusted to change the quality and/or quantity of individuals passing through such that invasion probability and/or impacts are reduced.

Differences in adrenocortical responses between urban and rural burrowing owls: poorly-known underlying mechanisms and their implications for conservation.

The hypothalamus-pituitary-adrenal/interrenal (HPA) axis of vertebrates integrates external information and orchestrates responses to cope with energy-demanding and stressful events through changes in circulating glucocorticoid levels. Urbanization exposes animals to a wide variety of ever-changing stimuli caused by human activities that may affect local wildlife populations. Here, we empirically tested the hypothesis that urban and rural owls (Athene cunicularia) show different adrenocortical responses to stress, with urban individuals showing a reduced HPA-axis response compared to rural counterparts to cope with the high levels of human disturbance typical of urban areas. We applied a standard capture-restraint protocol to measure baseline levels and stress-induced corticosterone (CORT) responses. Urban and rural owls showed similar circulating baseline CORT levels. However, maximum CORT levels were attained earlier and were of lower magnitude in urban compared to rural owls, which showed a more pronounced and long-lasting response. Variability in CORT responses was also greater in rural owls and contained the narrower variability displayed by urban ones. These results suggest that only individuals expressing low-HPA-axis responses can thrive in cities, a pattern potentially mediated by three alternative and non-exclusive hypotheses: phenotypic plasticity, natural selection and matching habitat choice. Due to their different conservation implications, we recommend further research to properly understand wildlife responses to humans in an increasingly urbanized world.

Adrenocortical response to stress and thyroid hormone status in free-living nestling white storks (Ciconia ciconia) exposed to heavy metal and arsenic contamination.

BACKGROUND/OBJECTIVE: Endocrine parameters have proven useful in the detection of early or low-level responses to pollutants. Although most of the studies on endocrine modulation have been focused on processes involving gonadal steroids, contaminants may target other parts of the endocrine system as well. In this study we examined the adrenocortical stress response and thyroid hormone status in free-living nestling white storks (Ciconia ciconia) in relation to heavy metals (zinc, lead, copper, cadmium) and arsenic levels in blood. METHODS: Fieldwork was conducted in an area polluted by the Aznalcóllar mine accident (southwestern Spain) and in a reference site. We used a standardized capture, handling, and restraint protocol to determine both baseline and maximum plasma corticosterone. Circulating levels of thyroxine (T4) and triiodothyronine (T3) were also measured. RESULTS: No effects of metals or As were found on baseline corticosterone, but maximum levels of corticosterone were positively related to Pb in both locations. This relationship was stronger in single nestlings than in birds from multiple-chick broods, which suggests a greater impact of Pb on more stressed individuals. Metal pollution did not affect plasma T4 or T3 levels, although thyroid status differed with location. CONCLUSIONS: Because a compromised hypothalamus-pituitary-adrenal (HPA) function can have far-reaching consequences in terms of altered behavioral and metabolic processes necessary for survival, our results suggest that birds exposed to sublethal Pb levels may be at risk through an altered adrenocortical stress response, and further support the idea that HPA axis-related end points might be useful indicators of metal exposure and potential toxicity in wild animals.

Effects of Ontogeny, Diel Rhythms, and Environmental Variation on the Adrenocortical Physiology of Semialtricial Black Kites (Milvus migrans).

We examined whether hypothalamic-pituitary-adrenal axis activity in the nestlings of a semialtricial raptor, the black kite (Milvus migrans), varied with advancing age, throughout the day, and in response to a number of socioecological factors presumed to affect allostatic load. Both baseline corticosterone (CORT) titers and maximum CORT levels during 30 min of handling and restraint augmented across all sampled ages, suggesting that nestlings' energetic demands and capacity to respond to perturbations increase progressively throughout development. CORT secretion also peaked in the early morning, reached minimum levels in the central hours of the day, and increased again before dusk, suggesting a possible role of CORT in the regulation of activity-inactivity patterns. Finally, nestlings raised in a year of low marsh inundation, implying lower food availability and heightened allostatic loads, exhibited higher adrenocortical responsiveness to stress than nestlings raised in years of intermediate or high flooding. The nondetectable effect of other socioecological variables, such as territory quality, temperature, or brood order, suggests that parents may be able to buffer their nestlings from adverse environmental conditions or that the effect of such factors may have been obscured by selective mortality operating before sampling. We propose that future studies increase the simultaneous use of complementary techniques (fecal sampling, feather analysis) to reach firmer and more comprehensive conclusions, especially for planning the management and conservation of sensitive species.

Large-scale spatial variation in feather corticosterone in invasive house sparrows (Passer domesticus) in Mexico is related to climate.

Ecologists frequently use physiological tools to understand how organisms cope with their surroundings but rarely at macroecological scales. This study describes spatial variation in corticosterone (CORT) levels in feathers of invasive house sparrows (Passer domesticus) across their range in Mexico and evaluates CORT-climate relationships with a focus on temperature and precipitation. Samples were collected from 49 sites across Mexico. Feather CORT (CORTf) was measured using methanol-based extraction and radioimmunoassay. Relationships between CORTf and spatial and climate variables were examined using simple linear regressions. Ordination was used on climate data, CORTf was plotted against the resulting axes, and univariate regression trees were used to identify important predictors of CORTf. Universal kriging interpolation was used to illustrate spatial variation in CORTf across Mexico. Correlations with ordination axes showed that high CORTf was associated with low precipitation during the rainy season and low dry season temperatures. Specifically, CORTf was negatively related to May precipitation and January and July minimum temperatures, and positively related to April deuterium excess and June minimum temperatures. CORTf was higher in second-year birds compared to after-hatch years and after-second years. House sparrows had higher CORTf levels in the hot, dry, north-central region of Mexico, and CORTf was negatively related to temperature and precipitation. House sparrows molt primarily from August-September but climate conditions throughout the year were important predictors of CORTf, suggesting that conditions outside of molt can carry over to influence energetics during feather growth. These data suggest that dry conditions are challenging for house sparrows in Mexico, supporting previous work showing that precipitation is an important predictor of broad-scale CORT variation. This work highlights the utility of CORTf for evaluating the influence of physiology on current avian range limits; furthermore, these data may allow us to predict future changes in species distributions.

Links between fear of humans, stress and survival support a non-random distribution of birds among urban and rural habitats.

Urban endocrine ecology aims to understand how organisms cope with new sources of stress and maintain allostatic load to thrive in an increasingly urbanized world. Recent research efforts have yielded controversial results based on short-term measures of stress, without exploring its fitness effects. We measured feather corticosterone (CORTf, reflecting the duration and amplitude of glucocorticoid secretion over several weeks) and subsequent annual survival in urban and rural burrowing owls. This species shows high individual consistency in fear of humans (i.e., flight initiation distance, FID), allowing us to hypothesize that individuals distribute among habitats according to their tolerance to human disturbance. FIDs were shorter in urban than in rural birds, but CORTf levels did not differ, nor were correlated to FIDs. Survival was twice as high in urban as in rural birds and links with CORTf varied between habitats: while a quadratic relationship supports stabilizing selection in urban birds, high predation rates may have masked CORTf-survival relationship in rural ones. These results evidence that urban life does not constitute an additional source of stress for urban individuals, as shown by their near identical CORTf values compared with rural conspecifics supporting the non-random distribution of individuals among habitats according to their behavioural phenotypes.

Assessing costs of carrying geolocators using feather corticosterone in two species of aerial insectivore.

Despite benefits of using light-sensitive geolocators to track animal movements and describe patterns of migratory connectivity, concerns have been raised about negative effects of these devices, particularly in small species of aerial insectivore. Geolocators may act as handicaps that increase energetic expenditure, which could explain reported effects of geolocators on survival. We tested this 'Energetic Expenditure Hypothesis' in 12 populations of tree swallows (Tachycineta bicolor) and barn swallows (Hirundo rustica) from North America and Europe, using measurements of corticosterone from feathers (CORTf) grown after deployment of geolocators as a measure of physiology relevant to energetics. Contrary to predictions, neither among- (both species) nor within-individual (tree swallows only) levels of CORTf differed with respect to instrumentation. Thus, to the extent that CORTf reflects energetic expenditure, geolocators apparently were not a strong handicap for birds that returned post-deployment. While this physiological evidence suggests that information about migration obtained from returning geolocator-equipped swallows is unbiased with regard to levels of stress, we cannot discount the possibility that corticosterone played a role in reported effects of geolocators on survival in birds, and suggest that future studies relate corticosterone to antecedent factors, such as reproductive history, and to downstream fitness costs.

Developmental toxicity of in ovo exposure to polychlorinated biphenyls: II. Effects of maternal or paternal exposure on second-generation nestling american kestrels.

The development of second-generation nestling American kestrels (Falco sparverius) was altered by in ovo exposure of only one parent to polychlorinated biphenyls (PCBs). Polychlorinated biphenyls appear to alter nestling development through both maternally and paternally mediated effects. In 1998, F0 parent kestrels consumed approximately 5 to 7 microg total PCBs/g bird/d (Aroclors 1248:1254: 1260) for approximately 100 d prior to eggs hatching; these eggs, containing total PCB concentrations of 34.1 microg/g, produced 13 F1 offspring, which were then paired in 1999 with unexposed kestrels to examine developmental effects of maternal or paternal in ovo PCB exposure. Using a toxicokinetics model, eggs from the maternally exposed group had predicted PCB levels of 0.03 to 0.34 microg/g, with enriched higher chlorinated congeners. Polychlorinated biphenyl concentrations in eggs of all generations have recently been found in eggs and nestlings of free-ranging eagles. Consistent with the first generation, maternally exposed F2 females generally were larger, had altered growth rates, and delayed maximal growth and fledging compared with control females. Maternally exposed F2 males were heavier but had shorter bones, grew more quickly and earlier, and fledged 2 d later than control males. In the maternally exposed group, concentrations of plasma triiodothyronine were elevated in F2 females but suppressed in F2 males. Paternally exposed F2 hatchlings of both sexes were comparable in size to controls with the exception of having longer tarsi bones, but subsequently showed slower, delayed growth (both sexes) and fledging (females) and lower thyroxine concentrations (males). The alterations in thyroid hormones in the F2 generation are discussed in light of the enrichment of higher chlorinated PCB congeners and hydroxylated PCB congeners. The developmental changes in the kestrel nestlings are likely a function of several possible mechanisms involving maternal PCB deposition, parental behavior, and neurobehavioral and endocrine-thyroid function in nestlings.

Tracking stress: localisation, deposition and stability of corticosterone in feathers.

How animals cope with stressors is an important determinant of their well being and fitness. Understanding what environmental perturbations are perceived as stressors, and quantifying how they are responded to, how often they occur and the negative consequences of exposure to glucocorticoids, has been problematic and limited to short-term physiological measures. By contrast, the quantification of corticosterone (CORT) in feathers represents a long-term, integrated measure of hypothalamic-pituitary-adrenal activity. In the present study, we show that by understanding how the hormone is deposited in feathers, in combination with specific sampling protocols, one can identify localised patterns of CORT deposition that reveal different temporal patterns of a bird's response to stressors. CORT in feathers appears to be stable over time, is resistant to heat exposure and is useful in determining both the overall exposure of the bird to the hormone over days or weeks, as well as identifying discrete, punctuated, stressful events. Variation in feather CORT can also be examined among individuals of a population at one point in time, as well as over years by using museum specimens. The ability to track stress over time allows for new questions to be asked about the health and ecology of birds and their environment.

Physiological stress levels predict survival probabilities in wild rabbits.

Among vertebrates, short-term elevations of glucocorticoid hormones (corticosterone or cortisol) facilitate a suite of physiological and behavioral changes aimed at overcoming environmental perturbations or other stressful events. However, chronically elevated glucocorticoids can have deleterious physiological consequences, and it is still unclear as to what constitutes an adaptive physiological response to long-term stress. In this study, we experimentally exposed European wild rabbits Oryctolagus cuniculus to a source of long-term stress (simulated through a 2- to 4-week period of captivity) and tested whether glucocorticoid physiology predicted two major components of rabbit fitness: body condition and survival probability. Following exposure to long-term stress, moderately elevated serum corticosterone and fecal glucocorticoid metabolites levels in the wild rabbits were negatively associated with body condition, but positively associated with subsequent survival upon release. Our results suggest that the cost of maintaining elevated corticosterone levels in terms of decreased body condition is balanced by the increased chance of survival upon release.

Age-related variation in the adrenocortical response to stress in nestling white storks (Ciconia ciconia) supports the developmental hypothesis.

The post-natal development of the adrenocortical response to stress was investigated in European white storks. Sixty wild nestlings aged 24-59 days old were subjected to a standardized capture and restraint protocol, and the time-course pattern of the response to stress was assessed through determination of circulating corticosterone in blood samples collected at five fixed times during the 45-min period following capture. The time course of the response was best fit to a third-order function of handling time, and showed a strong effect of age. Although age did not affect baseline titers and all birds showed a positive post-capture increase in circulating corticosterone, age had a positive effect on the relative increase from baseline titer, the recorded time to reach maximum level, and the acute concentration after 10 min following capture and restraint. While young nestlings displayed very little response to capture, the response near fledging resembled the typical adrenocortical pattern widely reported in fully developed birds. Our results concur with those found in altricial and semi-altricial species, and suggest that non-precocial birds follow a similar mode of development of the hypothalamic-pituitary-adrenal (HPA) axis. The fact that HPA sensitivity to stress is functional suggests that young storks gradually develop emergency responses of adaptive value and are able to overcome acute perturbations in spite of their parental dependence, at least during the last two-thirds of post-natal development. According to the Developmental Hypothesis, such gradual changes would allow nestlings to respond to perturbations as a function of the specific behavioral and physiological abilities of their age. The potential sources of stress that nestlings have to face during development (i.e., weather conditions, dietary restrictions, and social competition) are discussed according to developmental changes in behavioral and physiological abilities.

Biomarker responses in nesting, common eiders in the Canadian arctic in relation to tissue cadmium, mercury and selenium concentrations.

Populations of many North American sea ducks are declining. Biomarkers may offer valuable insights regarding the health and fitness of sea ducks in relation to contaminant burdens. In this study we examined body condition, immune function, corticosterone stress response, liver glycogen levels and vitamin A status in relation to tissue concentrations of mercury, selenium and cadmium in female common eiders during the nesting period. The study was conducted in the eastern Canadian arctic during July, 2000. Hepatic mercury, selenium and renal cadmium concentrations ranged 1.5-9.8, 6.5-47.5 and 74-389 microg/g, dry wt, respectively. Mercury concentrations were negatively related to dissection body mass, heart mass and fat mass. Cadmium concentrations were negatively related to mass at capture and dissection mass after controlling for the mercury concentration-dissection mass relationship. Cell-mediated immunity was assessed by the skin swelling reaction to an injection of phytohemagglutinin-P, and was unrelated to metal concentrations. After adjusting the corticosterone concentration to account for the time between capture and sampling, there was a negative relationship between the residual corticosterone concentration and selenium. Liver glycogen concentrations were not significantly related to metal concentrations. Mercury concentrations were positively related to those of hepatic retinol and retinyl palmitate and the ratio of the retinol to retinyl palmitate in liver. They were negatively related to the ratio of plasma to liver retinol. Our findings do not indicate that exposure to metals may have adversely affected the health of these birds. They do, however, suggest that more research is required to elucidate mechanisms by which exposure to these metals could impact body condition.