Gary R. Bortolotti

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.

Facultative sex ratio manipulation in American kestrels

SummaryFor animals that are sexually dimorphic in size, the larger sex is expected to be more costly to raise to independence. Manipulating offspring sex ratios may thus be one means by which parents can fine-tune their reproductive effort to resource availability. Parents in poor physical condition or during poor food years should produce more of the cheaper (smaller) sex. We examined the sex ratios of 259 broods of American kestrels (Falco sparverius) between 1988 and 1990 in relation to food abundance (small mammals) and various attributes to the parents. The proportion of males at hatching increased as the food supply declined, and both male and female parents in poor physical condition were more likely to have male-biased broods than those in good condition. The mortality of eggs and young did not appear to be responsible for the biased sex ratios. The sex ratio was independent of the laying date; however, it was correlated with female body size. Small females produced more sons, perhaps because small size is more detrimental for females than males.

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.

Influence of Sibling Competition on Nestling Sex Ratios of Sexually Dimorphic Birds

Theoretically, the ratio of male to female offspring should equal the inverse ratio of the cost of their rearing. For birds exhibiting brood reduction, the cost of raising offspring sexually dimorphic in size may not be independent of the sex composition of the brood if males and females are not equally affected by sibling competition or are not equally effective at competing with a sibling of the opposite sex. Parents may thus manipulate the sex ratio of their brood to achieve an optimal combination of the sexes and to maximize their fitness. By examining the effects of sex, growth, and hatching asynchrony on the relative size of sibling bald eagles, I show that the probability of brood reduction is not equal among broods of different sex composition. The hatching sequence of male first and female second was predicted to have the greatest chance of experiencing nestling mortality. This type of brood is rare in bald eagles because there is a sex-dependent hatching sequence whereby the first egg in mixed-sex clutches is predominantly female (93%). In contrast, golden eagle broods of female first and male second appear to be the combination most likely to result in brood reduction. Golden eagles do not adjust their prenatal sex ratio, but there is a postnatal sex bias in favor of females caused by brood reduction in years of poor food availability.

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.

Are avian hematocrits indicative of condition ? American kestrels as a model

Diseased animals or those in poor condition are known to have reduced hematocrits. Many investigators have assumed that hematocrit levels thus reflect condition and disease status of an animal. This study tested these assumptions by examining the relation between hematocrits of American kestrels (Falco sparverius) during several stages of the breeding season, and condition, prey abundance, and blood parasite load. We also examined the potential effects of a number of intrinsic and extrinsic influences on hematocrit. Hematocrits did not differ between the sexes, or between the pre-laying and incubation periods. Among females, hematocrit did not vary with the date of sampling, breeding chronology, prey abundance, condition, age, or molt, although hematocrit increased with ambient temperature during incubation. Hematocrit of males was not related to breeding chronology, prey abundance, condition, age, or molt. During incubation, male hematocrit increased with the date of sampling and ambient temperature. Hematocrits of both sexes declined with the time of day that the sample was taken, and increased with the level of infection of the blood parasite Haemoproteus. The use of hematocrits to assess the health and condition of clinically normal kestrels is therefore questionable, and given the positive association with parasite loads, may even lead to erroneous conclusions.

Sexual Dichromatism in Birds Independent of Diet, Parasites and Androgens

Sexual selection may explain why male animals are typically more colourful than females. Females may choose brightly coloured males for mating because colour is a reliable signal of a male’s genetic resistance to parasites, or that he can bear the cost of the immunosuppressant effects of androgens. Bright yellows, oranges and reds are the product of carotenoid pigments, which are known to have significant health benefits. Therefore, bright colours may be indicative of a bird’s quality because it shows access to a superior diet or superior foraging ability. We maintained populations of American kestrels and loggerhead shrikes in captivity that were largely free of parasites and fed a uniform diet. Male kestrels were more brightly coloured than females in the colour of their ceres, lores and legs, and there were pronounced age- and gender-specific patterns to concentrations of carotenoids in their plasma. Even though shrikes do not show any carotenoid-based colouration, the sexes had pronounced differences in plasma carotenoids. Carotenoids in kestrels were unrelated to androgen levels, but the correlation between carotenoids and plasma proteins suggest colour may be a condition-dependent trait. These results suggest that neglected physiological processes may regulate carotenoids, and hence some colour variation need not be explained by parasites, androgens or diet.

EFFECTS OF HEMATOZOAN PARASITES ON CONDITION AND RETURN RATES OF AMERICAN KESTRELS

Abstract We evaluated the relationship between blood parasites and body condition of American Kestrels (Falco sparverius) during the breeding season. Females that were infected with at least one species of parasite were in poorer condition than those without parasites during incubation but not prior to egg laying. We suggest that the relationship between parasitism and condition was masked before laying because of large increases in body mass of females during egg formation. Reduced condition of males during incubation also was associated with higher intensity of infections by Haemoproteus in one of two years. The negative association between condition and intensity of infection suggests that blood parasites impose costs on kestrels owing to competition for nutrients or allocation of energy by hosts to immune function or tissue repair. Alternatively, kestrels in poor condition may be more likely to have relapses of chronic infections, or they may be less able to control new infections because of resource limitations. In contrast to results during incubation, during the prelaying period the prevalence of parasites tended to be higher, and in one year infections were more intense, among males in good condition. One possible explanation for these results is that body condition of males during courtship is an important determinant of the quality of mate they are able to obtain, and males may be accumulating body reserves at the expense of decreased immune function. Return rates of female kestrels to the study area declined as the intensity of their Haemoproteus infections increased, suggesting that blood parasitism is associated with reduced survival or increased dispersal probability.

Food Supply and Hatching Spans of Birds: Energy Constraints or Facultative Manipulation

Clutches of altricial birds generally hatch over a period of hours or days. Numerous hypotheses have been generated to explain hatching asynchrony, but most experiments have focused on the nestling stage to determine some post—hatch benefit such as increased reproductive success. We concentrated on proximate causes in the prelaying period, which have largely been ignored. In northern Saskatchewan, we censused prey species (small mammals) in early spring and measured the asynchrony of 273 clutches of the American Kestrel (Falco sparverius) over 4 yr. Hatching asynchrony was quantified in two ways: time for all the eggs within a clutch to hatch and mass hierarchies among nestlings. In good food years, the hatchling spans of clutches were more synchronous than in poor years. Similarly, parents on good territories or females in good physical condition had more synchronous broods than parents under food stress. In an experiment, we supplemented food to kestrels during the prelaying period. Parents that were supplemented laid larger eggs and hatched those eggs more synchronously, but control pairs were more successful at raising young to the fledging stage. Synchronous hatching when food is abundant is consistent with the hypothesis of facultative manipulation of hatching spans in relation to nestling food supply, but not with the energy constraint hypothesis.

Carotenoid discrimination by the avian embryo: a lesson from wild birds

The concentrations (microg/g wet yolk) of total carotenoids in eggs of the common moorhen (Gallinula chloropus), American coot (Fulica americana) and lesser black-backed gull (Larus fuscus), collected in the wild, were 47.5, 131.0 and 71.6, respectively. In contrast to data for eggs of the domestic chicken, beta-carotene was a significant component in the yolks of these three wild species, forming 25-29% by wt. of the total carotenoids present. The concentration of total carotenoids in the livers of the newly-hatched chicks was 5-10 times higher than in the other tissues and beta-carotene was again a major component, forming 37-58% of the hepatic carotenoids. In the newly-hatched gull, the proportions of both lutein and zeaxanthin were very low in the liver but high in the heart and muscle when compared with the yolk. By contrast canthaxanthin, echinenone and beta-carotene were very minor constituents of heart and muscle when compared with their proportions in the yolk of the gull. The proportions of lutein and zeaxanthin in the liver of the newly-hatched coot and moorhen were also far lower than in the yolk whereas the liver was relatively enriched with beta-cryptoxanthin, beta-carotene and (in the moorhen) echinenone. The results indicate that avian embryos discriminate between different carotenoids during their distribution from the yolk to the various tissues.