Julio Blas

Stress response during development predicts fitness in a wild, long lived vertebrate

Short-term elevation of circulating glucocorticosteroids (GCs) in vertebrates facilitates the adoption of a distinct emergency life history state, which allows individuals to cope with perturbations and recover homeostasis at the expense of temporarily suppressing nonessential activities. Although GC responses are viewed as a major evolutionary mechanism to maximize fitness through stress management, phenotypic variability exists within animal populations, and it remains unclear whether interindividual differences in stress physiology can explain variance in unequivocal components of fitness. We show that the magnitude of the adrenocortical response to a standardized perturbation during development is negatively related to survival and recruitment in a wild population of long lived birds. Our results provide empirical evidence for a link between stress response, not exposure to stressors, and fitness in a vertebrate under natural conditions. Recent studies suggest that variability in the adrenocortical response to stress may be maintained if high and low GC responders represent alternative coping strategies, with differential adaptive value depending on environmental conditions. Increased fitness among low GC responders, having a proactive personality, is predicted under elevated population density and availability of food resources, conditions that characterize our study population.

Testosterone increases bioavailability of carotenoids: Insights into the honesty of sexual signaling

Androgens and carotenoids play a fundamental role in the expression of secondary sex traits in animals that communicate information on individual quality. In birds, androgens regulate song, aggression, and a variety of sexual ornaments and displays, whereas carotenoids are responsible for the red, yellow, and orange colors of the integument. Parallel, but independent, research lines suggest that the evolutionary stability of each signaling system stems from tradeoffs with immune function: androgens can be immunosuppressive, and carotenoids diverted to coloration prevent their use as immunostimulants. Despite strong similarities in the patterns of sex, age and seasonal variation, social function, and proximate control, there has been little success at integrating potential links between the two signaling systems. These parallel patterns led us to hypothesize that testosterone increases the bioavailability of circulating carotenoids. To test this hypothesis, we manipulated testosterone levels of red-legged partridges Alectoris rufa while monitoring carotenoids, color, and immune function. Testosterone treatment increased the concentration of carotenoids in plasma and liver by >20%. Plasma carotenoids were in turn responsible for individual differences in coloration and immune response. Our results provide experimental evidence for a link between testosterone levels and immunoenhancing carotenoids that (i) reconciles conflicting evidence for the immunosuppressive nature of androgens, (ii) provides physiological grounds for a connection between two of the main signaling systems in animals, (iii) explains how these signaling systems can be evolutionary stable and honest, and (iv) may explain the high prevalence of sexual dimorphism in carotenoid-based coloration in animals.

CAUSES AND CONSEQUENCES OF TERRITORY CHANGE AND BREEDING DISPERSAL DISTANCE IN THE BLACK KITE

Factors affecting individual variation in between-year territory change and dispersal distance were measured in a long-term study of Black Kites (Milvus migrans) living in an area of ∼100000 ha in and around Donana National Park in southern Spain. Adult birds (N = 210) and fledglings (N = 3061) were individually marked, and breeding birds were monitored annually during 1989–1996 to detect banded individuals. Of these 3271 birds, 652 breeding birds were resighted, and 164 of them were sexed through copulatory behavior. Nests were checked annually to monitor breeding performance. Frequencies of return between years were 83.1% for breeding males and 89.5% for breeding females. Frequencies of territory change were 25.6% and 32.8%, respectively. Females >8 yr old rarely changed territories. Dispersing birds departed significantly more from low-quality territories (evaluated through breeding success variables). Breeding failure and mate loss (divorce or death) favored breeding dispersion, both in males and fema...

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.

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

SUMMARY 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 birds 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.

Individual improvements and selective mortality shape lifelong migratory performance

Billions of organisms, from bacteria to humans, migrate each year and research on their migration biology is expanding rapidly through ever more sophisticated remote sensing technologies. However, little is known about how migratory performance develops through life for any organism. To date, age variation has been almost systematically simplified into a dichotomous comparison between recently born juveniles at their first migration versus adults of unknown age. These comparisons have regularly highlighted better migratory performance by adults compared with juveniles, but it is unknown whether such variation is gradual or abrupt and whether it is driven by improvements within the individual, by selective mortality of poor performers, or both. Here we exploit the opportunity offered by long-term monitoring of individuals through Global Positioning System (GPS) satellite tracking to combine within-individual and cross-sectional data on 364 migration episodes from 92 individuals of a raptorial bird, aged 1–27 years old. We show that the development of migratory behaviour follows a consistent trajectory, more gradual and prolonged than previously appreciated, and that this is promoted by both individual improvements and selective mortality, mainly operating in early life and during the pre-breeding migration. Individuals of different age used different travelling tactics and varied in their ability to exploit tailwinds or to cope with wind drift. All individuals seemed aligned along a race with their contemporary peers, whose outcome was largely determined by the ability to depart early, affecting their subsequent recruitment, reproduction and survival. Understanding how climate change and human action can affect the migration of younger animals may be the key to managing and forecasting the declines of many threatened migrants.

Cell-mediated immune activation rapidly decreases plasma carotenoids but does not affect oxidative stress in red-legged partridges (Alectoris rufa).

SUMMARY In animals yellow-orange-red sexual traits pigmented by carotenoids have been suggested to act as signals of current health. Because carotenoids have important physiological functions, individuals might trade-off allocating these pigments to self-maintenance versus coloration. Carotenoids may act as scavengers of free radicals that are released during an immune response. Here, we experimentally assessed whether a local cell-mediated immune response affects circulating carotenoids, antioxidant status, oxidative damage and the expression of a carotenoid-based trait. Male red-legged partridges (Alectoris rufa) were subcutaneously injected with phytohaemagglutinin (PHA) or with phosphate buffer solution (controls). The effect of the treatment on circulating carotenoids, total plasma antioxidant status (TAS), lipid oxidative damage in erythrocytes (TBARS) and ornamentation was assessed. Immune challenge induced a 13% decrease in circulating carotenoids within 24 h. However, this treatment did not affect TAS, TBARS or coloration. Coloration, circulating carotenoids and cell-mediated immune response were positively correlated, but these were not related to TAS or TBARS. Carotenoids were only weakly related to TAS after controlling for the effect of uric acid levels. These results suggest that carotenoid-based ornaments may honestly indicate immunocompetence but probably not antioxidant capacity in this species, and that carotenoids might be relatively weak antioxidants in the plasma. Furthermore, even a relatively harmless and locally elicited immune challenge had important effects on circulating carotenoids, but this effect did not appear to be associated with oxidative stress. Alternative mechanisms linking carotenoids to immunity (not necessarily relying on the use of these pigments as antioxidants) should be considered in future studies on birds.

Condition and androgen levels: are condition-dependent and testosterone-mediated traits two sides of the same coin?

The immunocompetence handicap hypothesis posits that androgen-mediated signals honestly indicate the responsiveness of the immune system because of the immunosuppressive effect of androgens. However, androgen levels may also be related to nutritional status, and differences in body condition could be a more parsimonious explanation for variation in the expression of the signal. We maintained captive male red-legged partridges, Alectoris rufa, under regulated food shortage until they reached 85% of their initial body mass. Controls were provided with food ad libitum. After food shortage, experimental birds had lower androgen and higher corticosterone levels than controls. The condition dependence in androgen levels suggests that androgen-mediated signals could be indicating general nutritional state rather than immune function specifically. We propose that androgen-dependent signals may act as indicators of body condition or indicators of immune system quality, depending on the nutritional status of the individual.

Raptor Nest Decorations Are a Reliable Threat Against Conspecifics

Black kite nest decorations are honest signals of individual and territory quality. Individual quality is often signaled by phenotypic flags, such as bright plumage patches in birds. Extended phenotype signals can similarly show quality, but in these cases the signals are external to the individual, often taking the form of objects scavenged from the environment. Through multiple manipulative experiments, we showed that objects used for nest decoration by a territorial raptor, the black kite (Milvus migrans), act as reliable threats to conspecifics, revealing the viability, territory quality, and conflict dominance of the signaler. Our results suggest that animal-built structures may serve as signaling devices much more frequently than currently recognized.

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.