Double brooding and offspring desertion in the barn owl (Tyto alba)

Many bird species produce two annual broods during a single breeding season. However, not all individuals reproduce twice in the same year suggesting that double brooding is condition-dependent. In contrast to most raptors and owls, the barn owl Tyto alba produces two annual clutches in most worldwide distributed populations. Nevertheless, the determinants of double brooding are still poorly studied. We performed such a study in a Swiss barn owl population monitored between 1990 and 2014. The annual frequency of double brooding varied from 0 to 14% for males and 0 to 59% for females. The likelihood of double brooding was higher when individuals initiated their first clutch early rather than late in the season and when males had few rather than many offspring at the first nest. Despite the reproductive benefits of double brooding (single- and double-brooded individuals produced 3.97 +/- 0.11 and 7.07 +/- 0.24 fledglings, respectively), double brooding appears to be traded off against offspring quality because at the first nest double-brooded males produced poorer quality offspring than single-brooded males. This might explain why females desert their first mate to produce a second brood with another male without jeopardizing reproductive success at the first nest. Furthermore, the reproductive cycle being very long in the barn owl (120 d from start of laying to offspring independence), selection may have favoured behaviours that accelerate the initiation of a second annual brood. Accordingly, half of the double-brooded females abandoned their young offspring to look for a new partner in order to initiate the second breeding attempt, 9.48 d earlier than when producing the second brood with the same partner. We conclude that male and female barn owls adopt different reproductive strategies. Females have more opportunities to reproduce twice in a single season than males because mothers are not strictly required during the entire rearing period in contrast to fathers. A high proportion of male floaters may also encourage females to desert their first brood to re-nest with a new male who is free of parental care duties

Agricultural land use and human presence around breeding sites increase stress-hormone levels and decrease body mass in barn owl nestlings.

Human activities can have a suite of positive and negative effects on animals and thus can affect various life history parameters. Human presence and agricultural practice can be perceived as stressors to which animals react with the secretion of glucocorticoids. The acute short-term secretion of glucocorticoids is considered beneficial and helps an animal to redirect energy and behaviour to cope with a critical situation. However, a long-term increase of glucocorticoids can impair e.g. growth and immune functions. We investigated how nestling barn owls (Tyto alba) are affected by the surrounding landscape and by human activities around their nest sites. We studied these effects on two response levels: (a) the physiological level of the hypothalamus-pituitary-adrenal axis, represented by baseline concentrations of corticosterone and the concentration attained by a standardized stressor; (b) fitness parameters: growth of the nestlings and breeding performance. Nestlings growing up in intensively cultivated areas showed increased baseline corticosterone levels late in the season and had an increased corticosterone release after a stressful event, while their body mass was decreased. Nestlings experiencing frequent anthropogenic disturbance had elevated baseline corticosterone levels, an increased corticosterone stress response and a lower body mass. Finally, breeding performance was better in structurally more diverse landscapes. In conclusion, anthropogenic disturbance affects offspring quality rather than quantity, whereas agricultural practices affect both life history traits

Effect of the MC1R gene on sexual dimorphism in melanin-based colorations.

Variants of the melanocortin-1 receptor (MC1R) gene result in abrupt, naturally selected colour morphs. These genetic variants may differentially affect sexual dimorphism if one morph is naturally selected in the two sexes but another morph is naturally or sexually selected only in one of the two sexes (e.g. to confer camouflage in reproductive females or confer mating advantage in males). Therefore, the balance between natural and sexual selections can differ between MC1R variants, as suggest studies showing interspecific correlations between sexual dimorphism and the rate of nonsynonymous vs. synonymous amino acid substitutions at the MC1R. Surprisingly, how MC1R is related to within-species sexual dimorphism, and thereby to sex-specific selection, has not yet been investigated. We tackled this issue in the barn owl (Tyto alba), a species showing pronounced variation in the degree of reddish pheomelanin-based coloration and in the number and size of black feather spots. We found that a valine (V)-to-isoleucine (I) substitution at position 126 explains up to 30% of the variation in the three melanin-based colour traits and in feather melanin content. Interestingly, MC1R genotypes also differed in the degree of sexual colour dimorphism, with individuals homozygous for the II MC1R variant being 2 times redder and 2.5 times less sexually dimorphic than homozygous individuals for the VV MC1R variant. These findings support that MC1R interacts with the expression of sexual dimorphism and suggest that a gene with major phenotypic effects and weakly influenced by variation in body condition can participate in sex-specific selection processes

Social huddling and physiological thermoregulation are related to melanism in the nocturnal barn owl.

Endothermic animals vary in their physiological ability to maintain a constant body temperature. Since melanin-based coloration is related to thermoregulation and energy homeostasis, we predict that dark and pale melanic individuals adopt different behaviours to regulate their body temperature. Young animals are particularly sensitive to a decrease in ambient temperature because their physiological system is not yet mature and growth may be traded-off against thermoregulation. To reduce energy loss, offspring huddle during periods of cold weather. We investigated in nestling barn owls (Tyto alba) whether body temperature, oxygen consumption and huddling were associated with melanin-based coloration. Isolated owlets displaying more black feather spots had a lower body temperature and consumed more oxygen than those with fewer black spots. This suggests that highly melanic individuals display a different thermoregulation strategy. This interpretation is also supported by the finding that, at relatively low ambient temperature, owlets displaying more black spots huddled more rapidly and more often than those displaying fewer spots. Assuming that spot number is associated with the ability to thermoregulate not only in Swiss barn owls but also in other Tytonidae, our results could explain geographic variation in the degree of melanism. Indeed, in the northern hemisphere, barn owls and allies are less spotted polewards than close to the equator, and in the northern American continent, barn owls are also less spotted in colder regions. If melanic spots themselves helped thermoregulation, we would have expected the opposite results. We therefore suggest that some melanogenic genes pleiotropically regulate thermoregulatory processes

Duration of female parental care and their survival in the little auk Alle alle - are these two traits linked?

Desertion of offspring before its independence by one of the parents is observed in a number of avian species with bi-parental care but reasons for this strategy are not fully understood. This behaviour is particularly intriguing in species where bi-parental care is crucial to raise the brood successfully. Here, we focus on the little auk, Alle alle, a small seabird with intensive bi-parental care, where the female deserts the brood at the end of the chick rearing period. The little auk example is interesting as most hypotheses to explain desertion of the brood by females (e.g. “re-mating hypothesis”, “body condition hypothesis”) have been rejected for this species. Here, we analysed a possible relationship between the duration of female parental care over the chick and her chances to survive to the next breeding season. We performed the study in two breeding colonies on Spitsbergen with different foraging conditions – more favourable in Hornsund and less favourable in Magdalenefjorden. We predicted that in Hornsund females would stay for shorter periods of time with the brood and would have higher survival rates in comparison with birds from Magdalenefjorden. We found that indeed in less favourable conditions of Magdalenefjorden, females stay longer with the brood than in the more favourable conditions of Hornsund. Moreover, female survival was negatively affected by the length of stay in the brood. Nevertheless, duration of female parental care over the chick was not related to their parental efforts, earlier in the chick rearing period, and survival of males and females was similar. Thus, although females brood desertion and winter survival are linked, the relationship is not straightforward

Circulating testosterone and feather-gene expression of receptors and metabolic enzymes in relation to melanin-based colouration in the barn owl.

Knowledge of how and why secondary sexual characters are associated with sex hormones is important to understand their signalling function. Such a link can occur if i) testosterone participates in the elaboration of sex-traits, ii) the display of an ornament triggers behavioural response in conspecifics that induce a rise in testosterone, or iii) genes implicated in the elaboration of a sex-trait pleiotropically regulate testosterone physiology. To evaluate the origin of the co-variation between melanism and testosterone, we measured this hormone and the expression of enzymes involved in its metabolism in feathers of barn owl (Tyto alba) nestlings at the time of melanogenesis and in adults outside the period of melanogenesis. Male nestlings displaying smaller black feather spots had higher levels of circulating testosterone, potentially suggesting that testosterone could block the production of eumelanin pigments, or that genes involved in the production of small spots pleiotropically regulate testosterone production. In contrast, the enzyme 5α-reductase, that metabolizes testosterone to DHT, was more expressed in feathers of reddish-brown than light-reddish nestlings. This is consistent with the hypothesis that testosterone might be involved in the expression of reddish-brown pheomelanic pigments. In breeding adults, male barn owls displaying smaller black spots had higher levels of circulating testosterone, whereas in females the opposite result was detected during the rearing period, but not during incubation. The observed sex- and age-specific co-variations between black spottiness and testosterone in nestling and adult barn owls may not result from testosterone-dependent melanogenesis, but from melanogenic genes pleiotropically regulating testosterone, or from colour-specific life history strategies that influence testosterone levels

Baseline and stress-induced corticosterone levels are heritable and genetically correlated in a barn owl population.

The hypothalamic-pituitary-adrenal (HPA) axis is responsible for the regulation of corticosterone, a hormone that is essential in the mediation of energy allocation and physiological stress. As a continuous source of challenge and stress for organisms, the environment has promoted the evolution of physiological adaptations and led to a great variation in corticosterone profiles within or among individuals, populations and species. In order to evolve via natural selection, corticosterone levels do not only depend on the strength of selection exerted on them, but also on the extent to which the regulation of corticosterone is heritable. Nevertheless, the heritability of corticosterone profiles in wild populations is still poorly understood. In this study, we estimated the heritability of baseline and stress-induced corticosterone levels in barn owl (Tyto alba) nestlings from 8 years of data, using a multivariate animal model based on a behavioural pedigree. We found that baseline and stress-induced corticosterone levels are strongly genetically correlated (r = 0.68-0.80) and that the heritability of stress-induced corticosterone levels (h <sup>2</sup> = 0.24-0.33) was moderate and similar to the heritability of baseline corticosterone levels (h <sup>2</sup> = 0.19-0.30). These findings suggest that the regulation of stress-induced corticosterone and baseline levels evolves at a similar pace when selection acts with the same intensity on both traits and that contrary to previous studies, the evolution of baseline and stress-induced level is interdependent in barn owls, as they may be strongly genetically correlated

Nocturnal, diurnal and bimodal patterns of locomotion, sibling interactions and sleep in nestling Barn Owls

Temporal variation in physical activity is mainly determined by the day-night cycle. While this may be true for diurnal species whose vision at night is often poor, the situation might be more complex in nocturnal animals as many such species can see both in the dark and in the daylight. We examined in Barn Owl (Tyto alba) nestlings whether temporal variation of behavioural activities and sleep is shaped by parental feeding visits occurring during the first part of the night and the extent to which they also occur during daylight hours. We measured several behaviours in 280 individuals from 90 broods recorded in 4 years. Parental feeding visits progressively declined in frequency from the beginning to the end of the night, and a number of offspring behaviours followed the same pattern of activity (feeding, vocalization and self-preening). Surprisingly, nestlings were awake not only at sunset, but also at sunrise. Several behaviours (locomotion, wing flapping and sibling interactions, such as pecking and allopreening among nestlings) showed peaks of activity at sunset and sunrise, suggesting that they were performed for other reasons than to interact with parents. Allopreening was performed more often during the day than at night. We conclude that although adult Barn Owls are nocturnal, nestlings display a complex temporal pattern of activity that is governed not only by feeding but also by other unknown factors

Differential fitness effects of moonlight on plumage colour morphs in barn owls.

The Moon cycle exposes nocturnal life to variation in environmental light. However, whether moonlight shapes the fitness of nocturnal species with distinct colour variants remains unknown. Combining data from long-term monitoring, high-resolution global positioning system tracking and experiments using prey, we show that barn owls (Tyto alba) with distinct plumage colourations are differently affected by moonlight. The reddest owls are less successful at hunting and providing food to their offspring during moonlit nights, which associates with lower body mass and lower survival of the youngest nestlings and with female mates starting to lay eggs at low moonlight levels. Although moonlight should make white owls more conspicuous to prey, it either positively affects or does not affect the hunting and fitness of the whitest owls. We experimentally show that, under full-moon conditions, white plumage triggers longer freezing times in prey, which should facilitate prey catchability. We propose that the barn owl's white plumage, a rare trait among nocturnal predators, exploits the known aversion of rodents to bright light, explaining why, counterintuitively, moonlight has a lesser impact on the whitest owls. Our study provides evidence for the long-suspected influence of the Moon on the evolution of colouration in nocturnal species, highlighting the importance of colour in nocturnal ecosystems