Nicola Saino

Immunocompetence of nestling barn swallows in relation to brood size and parental effort

1. Intra-brood competition and parental feeding effort are considered important determinants of survival of offspring in altricial bird species because they affect accumulation of fat reserves by nestlings. However, the causal relationship between rearing conditions and post-fledging survival might also be mediated by other mechanisms ; for example, the amount and quality of food provided by parents to each nestling might affect development of immune system organs and functions and, hence, the ability of offspring to cope with parasites and pathogens. 2. The hypothesis that parental feeding effort, food quality and brood size affect immunocompetence of nestlings was tested for the first time in the barn swallow, Hirundo rustica, Linnaeus. 3. The intensity of T-lymphocyte cell-mediated immune responsiveness was evaluated after intradermal inoculation of a lectin (phytohaemagglutinin) in a large sample of nestlings from unmanipulated broods and broods whose size had been manipulated immediately after hatching. 4. In unmanipulated broods, immune response, body mass and body condition were correlated negatively with brood size and positively with the rate of parental feeding to each offspring. Nestlings in enlarged broods had smaller immune response and body mass, and received less food per capita than those in reduced broods. 5. Broods artificially provisioned with a food rich in proteins showed larger immune response, but not larger body mass, as compared to unprovisioned controls. 6. We conclude that T-lymphocyte cell-mediated immune response as well as body mass is influenced by the level of parental investment and brood size, perhaps via its effect on competition for food. Since T-lymphocytes are fundamental components of avian immunity, and parasites are known to affect survival of their avian hosts, our results suggest a new pathway through which rearing conditions might influence offspring survival.

Climate warming, ecological mismatch at arrival and population decline in migratory birds

Climate is changing at a fast pace, causing widespread, profound consequences for living organisms. Failure to adjust the timing of life-cycle events to climate may jeopardize populations by causing ecological mismatches to the life cycle of other species and abiotic factors. Population declines of some migratory birds breeding in Europe have been suggested to depend on their inability to adjust migration phenology so as to keep track of advancement of spring events at their breeding grounds. In fact, several migrants have advanced their spring arrival date, but whether such advancement has been sufficient to compensate for temporal shift in spring phenophases or, conversely, birds have become ecologically mismatched, is still an unanswered question, with very few exceptions. We used a novel approach based on accumulated winter and spring temperatures (degree-days) as a proxy for timing of spring biological events to test if the progress of spring at arrival to the breeding areas by 117 European migratory bird species has changed over the past five decades. Migrants, and particularly those wintering in sub-Saharan Africa, now arrive at higher degree-days and may have therefore accumulated a ‘thermal delay’, thus possibly becoming increasingly mismatched to spring phenology. Species with greater ‘thermal delay’ have shown larger population decline, and this evidence was not confounded by concomitant ecological factors or by phylogenetic effects. These findings provide general support to the largely untested hypotheses that migratory birds are becoming ecologically mismatched and that failure to respond to climate change can have severe negative impacts on their populations. The novel approach we adopted can be extended to the analysis of ecological consequences of phenological response to climate change by other taxa.

Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings

The yolk of bird eggs contains maternal carotenoids that may act as antioxidants thus influencing offspring performance and survival. However, to our knowledge, this hypothesis has not been subjected to experimental tests and the function of transmission of carotenoids to the egg is largely unknown. We directly manipulated the concentration of the main carotenoid (lutein) in the eggs of barn swallows (Hirundo rustica) and analysed the effect of experimental manipulation on growth of nestlings and two fundamental components of their acquired immunity. Nestlings hatched from lutein–inoculated eggs had larger T–cell–mediated immune response compared with those of two control groups. T–cell–mediated immune response predicted nestling survival until fledging. However, lutein inoculation did not affect antibody response to an immunogen, body mass, tarsus length or plumage development. Nestling body mass and plumage development declined with egg laying order, but the effects of lutein inoculation were independent of egg laying order for all traits. Our results show that maternal yolk carotenoids can have a major effect in promoting a fundamental component of immunity that predicts offspring survival and suggests that adaptive early maternal effects can be mediated by transmission of antioxidants to eggs.

Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks

Eggs of vertebrates contain steroid hormones of maternal origin that may influence offspring performance. Recently, it has been shown that glucocorticoids, which are the main hormones mediating the stress response in vertebrates, are transmitted from the mother to the egg in birds. In addition, mothers with experimentally elevated corticosterone levels lay eggs with larger concentrations of the hormone, which produce slow growing offspring with high activity of the hypothalamo-adrenal axis under acute stress. However, the effects and function of transfer of maternal corticosterone to the eggs are largely unknown. In the present study, we injected corticosterone in freshly laid eggs of yellow-legged gulls (Larus michahellis), thus increasing the concentration of the hormone within its natural range of variation, and analyzed the effect of manipulation on behavioral, morphological, and immune traits of the offspring in the wild. Eggs injected with corticosterone had similar hatching success to controls, but hatched later. Mass loss during incubation was greater for corticosterone-treated eggs, except for the last laid ones. Corticosterone injection reduced rate and loudness of late embryonic vocalizations and the intensity of chick begging display. Tonic immobility response, reflecting innate fearfulness, was unaffected by hormone treatment. Elevated egg corticosterone concentrations depressed T-cell-mediated immunity but had no detectable effects on humoral immune response to a novel antigen, viability at day 10, or growth. Present results suggest that egg corticosterone can affect the behavior and immunity of offspring in birds and disclose a mechanism mediating early maternal effects whereby stress experienced by females may negatively translate to offspring phenotypic quality.

Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation

Carotenoids are critical to embryonic development, immunity and protection from oxidative stress. Transmission of carotenoids to the eggs may affect development and maturation of immunity in offspring, but carotenoids may be available to females in limiting amounts. Females may thus transfer carotenoids to the eggs differentially in relation to the reproductive value of the offspring as affected by sexual ornamentation of their father. In this study of maternal allocation of carotenoids to the eggs in the barn swallow (Hirundo rustica), females whose immune system had been experimentally challenged with an antigen had smaller lutein concentrations in their eggs than controls. We manipulated the size of a secondary sexual character (tail length) of males, and analysed the effect of manipulation on allocation of lutein to eggs by their vaccinated mates. Contrary to our prediction based on parental allocation theory, mates of tail–shortened males had a larger lutein concentration in their eggs compared with those of control and tail–elongated males. According to previous studies, offspring of short–tailed males have larger exposure and/or susceptibility to parasites. A larger lutein concentration in the eggs of females mated to males with experimentally reduced ornaments may thus reflect adaptive maternal strategies to enhance offspring viability.

AN EXPERIMENTAL STUDY OF PATERNITY AND TAIL ORNAMENTATION IN THE BARN SWALLOW (HIRUNDO RUSTICA)

Previous studies of the socially monogamous barn swallow (Hirundo rustica) have shown that males that most frequently engage in extrapair copulations and whose partners are least involved in copulations with extrapair males are those with long tail ornaments. In this study, through the use of three highly polymorphic microsatellite markers, we analyze the relationships between length of tail ornaments of male barn swallows and proportion of nestlings fathered in own broods, number of offspring fathered in broods of other pairs, and total number of offspring fathered, using both a correlational and an experimental approach. Consistent with our predictions, we show that males with either naturally long or experimentally elongated tails have higher paternity (proportion of biological offspring in own broods), and they produce more biological offspring during the whole breeding season than males with naturally short or experimentally shortened tails. Males with naturally long tails also had more offspring in extrapair broods than short‐tailed males, but the effect of tail manipulation on the number of offspring fathered in extrapair broods, although being in the predicted direction, was not statistically significant. Cuckolded males that did not fertilize extrapair females had smaller postmanipulation tail length than cuckolders. We conclude that there is a causal, positive relationship between male tail length and paternity. Since female barn swallows have extensive control over copulation partners and heritability of tail length is high, this study shows that female choice is a component of selection for larger male ornaments. Benefits from extrapair fertilizations to females may arise because they acquire “good” genes for sexual attractiveness or high viability for their offspring.

Ecological conditions during winter affect sexual selection and breeding in a migratory bird.

Populations of migratory birds have undergone marked declines, although the causes and mechanisms remain unknown. Because environmental effects on population dynamics are mediated by the effects of ecological factors on individuals, understanding changes in individual phenotypes in response to ecological conditions is key to understanding population trends. We show that breeding individuals of a declining population of trans–Saharan migratory barn swallows, Hirundo rustica, were affected by environmental conditions, as estimated from the normalized difference vegetation index (NDVI), reflecting primary production, in their winter quarters. The breeding dates of the same individuals in consecutive breeding seasons were advanced and clutch sizes were larger after winters with high NDVI in the winter quarters. Feather moult was also affected by winter conditions, with consequences for male sexual attractiveness. Length of tail ornament was positively correlated with NDVI during the previous winter, and males with large tail ornaments reproduced earlier and had larger clutches. The mean annual breeding date of the population was earlier and breeding success was increased after favourable winters, but this result was mainly determined by a single winter with very low NDVI. Thus, ecological conditions in Africa influence individual performance and productivity in a barn swallow population.

Paternity and multiple signaling: effects of a secondary sexual character and song on paternity in the barn swallow.

Multiple signals may evolve because they provide independent information on the condition of a signaler. Females should pay attention to male characters relative to their reliability as signals of male attractiveness or quality. Since behavioral traits are flexible and, therefore, subject to strong environmental influences, females should weigh stable morphological signals higher in their choice of mates for genetic benefits than flexible behavioral traits, for example, by paying particular attention to phenotypically plastic traits when produced in combination with an exaggerated morphological signal. Consistent with this prediction, female barn swallows Hirundo rustica, which are known to prefer males with the longest tail feathers (a secondary sexual character), also preferred males with extreme expressions of a behavioral trait (song rate), as determined from patterns of paternity assessed by microsatellites. However, a statistical interaction between tail length and song rate implied that song rate was relatively unimportant for males with a short tail but more important for longtailed males. Since song rate is a flexible behavioral trait, females appear to have responded to this flexibility by devaluing the importance of song rate in assessment of unattractive sires.

Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings

Parasites can have a profound effect on biology and evolution of the hosts, which are expected to have evolved physiological and developmental mechanisms that allow them to minimise the costs imposed by parasites. In this study we analyse the effects of a dipteran ectoparasite on barn swallow (Hirundo rustica) nestling biology including rate of somatic growth, plasma protein concentration, blood cell sedimentation rate, hematocrit, concentration of leukocytes in peripheral blood, and T-lymphocyte cell-mediated immunocompetence. In a natural population, intensity of parasite infestation was positively correlated with growth of feathers. Nestlings in heavily infested nests may decide to allocate more resources to feather growth thus fledging early. To test this hypothesis, the detrimental effects of parasites on nestlings, and the existence of trade-offs between competing growth processes, we inoculated some nests with additional flies. Nestlings exposed to increased infestation had larger rate of feather growth but were in poorer condition than unmanipulated controls. Parasite inoculation resulted in larger concentrations of eosinophils and lymphocytes. Among siblings of broods inoculated with parasites, those that had the largest rate of feather growth had the lowest rate of increase in tarsus length and body mass. We conclude that louse flies depress barn swallow nestling condition and influence their immune profile. However, they also enhance growth of a morphological character that may allow nestlings to reduce the impact of parasites. Nestlings apparently experience a trade-off between the competing demands for growing feathers and other somatic characters.

Seasonal Changes in Immune Response and Parasite Impact on Hosts

Seasonal changes in the impact of parasites on hosts should result in seasonal changes in immune function. Since both ectoparasites and endoparasites time their reproduction to that of their hosts, we can predict that hosts have been selected to show an annual peak in their ability to raise an immune response during the reproductive season. We found large seasonal changes in immune function between the breeding and the nonbreeding season for a sample of temperate bird species. These changes amounted to a decrease in spleen mass from the breeding to the nonbreeding season by on average 18% across 71 species and a seasonal decrease in T‐cell‐mediated immunity by on average 33% across 13 species. These seasonal changes in immune function differed significantly among species. The condition dependence of immune function also differed between the breeding and the nonbreeding season, with individuals in prime condition particularly having greater immune responses during breeding. Analyses of ecological factors associated with interspecific differences in seasonal change of immune function revealed that hole‐nesting species had a larger increase in immune function during the breeding season than did open nesters. Since hole nesters suffer greater reduction in breeding success because of virulent parasites than do open nesters, this seasonal change in immune function is suggested to have arisen as a response to the increased virulence of parasites attacking hole‐nesting birds.