Parental investment and its sensitivity to corticosterone is linked to melanin-based coloration in barn owls

Behavioral and physiological responses to unpredictable changes in environmental conditions are, in part, mediated by glucocorticoids (corticosterone in birds). In polymorphic species, individuals of the same sex and age display different heritable melanin-based color morphs, associated with physiological and reproductive parameters and possibly alternative strategies to cope with variation in environmental conditions. We examined whether the role of corticosterone in resolving the trade-off between self-maintenance and reproductive activities covaries with the size of melanin-based spots displayed on the ventral body side of male barn owls. Administration of corticosterone to simulate physiological stress in males revealed pronounced changes in their food-provisioning rates to nestlings compared to control males. Corticosterone-treated males with small eumelanic spots reduced nestling provisioning rates as compared to controls, and also to a greater degree than did corticosterone-treated males with large spots. Large-spotted males generally exhibited lower parental provisioning and appear insensitive to exogenous corticosterone suggesting that the size of the black spots on the breast feathers predicts the ability to cope with stressful situations. The reduced provisioning rate of corticosterone-treated males caused a temporary reduction in nestling growth rates but, did not affect fledgling success. This suggests that moderately elevated corticosterone levels are not inhibitory to current reproduction but rather trigger behavioral responses to maximize lifetime reproductive success.     

The colour of fitness: plumage coloration and lifetime reproductive success in the tawny owl

We studied variation in plumage colour and life history in a population of tawny owls (Strix aluco) in southern Finland, using 26 years of data on individually marked male and female owls. Colour was scored on a semi-continuous scale from pale grey to reddish brown. Colour scoring was repeatable and showed a bimodal distribution (grey and brown morph) in both sexes. During the study period, colour composition was stable in the study population in both sexes. The sexes did not mate assortatively with respect to their colour. Colour was a highly heritable trait and was under selection. Grey-coloured male and female owls had a higher lifetime production of fledglings, and grey-coloured male (but not female) owls produced more recruits during their lifetime than brown individuals. Selection on colour was mediated through viability selection and not through fecundity selection. Our results reveal remarkably strong selection on a genetically determined phenotypic trait.     

Survival and reproductive rate of mites in relation to resistance of their barn swallow hosts

Parasite resistance may act via a number of different mechanisms that regulate or control the survival and the reproductive rate of parasites. Observations and experiments were used to test for effects of host resistance on parasite survival and rate of reproduction. Natural levels of infestation of barn swallow Hirundo rustica nests by the tropical fowl mite Ornithonyssus bursa were positively related to brood size, inversely related to the length of the outermost tail feathers of male nest owners (a secondary sexual character) and affected by time of reproduction by the host. A mite inoculation experiment, in which 50 adult mites were introduced into nests during the laying period of the host, was used to test for differential survival and reproduction of mites as a function of host resistance. The relationship between survival and reproduction of parasites, male tail length and host resistance was investigated. There was a negative relationship between mite numbers per nest after fledging of nestlings and male tail length. This relationship was mainly caused by a reduction in the number of mites in the first and second nymph stage with increasing tail length of male hosts, implying a reduction in rate of reproduction of mites. The proportion of mites that had recently fed was inversely related to tail length of male hosts. The proportion of nymph stages was positively related to the proportion of mites that had recently had a blood meal. Parasite resistance of barn swallows to the tropical fowl mite thus appeared to act through increased mortality rate of adult and nymph stages of mites, and through reduced reproductive rates of mites on resistant hosts. This is the first study demonstating a direct relationship between fitness components of a parasite and the expression of a secondary sexual character of a host. Received: 11 January 2000 / Accepted: 22 March 2000     

Seasonal variation in hormonal responses of timber rattlesnakes (<Emphasis Type="Italic">Crotalus horridus</Emphasis>) to reproductive and environmental stressors

Data addressing adrenocortical modulation across taxonomic groups are limited, especially with regard to how female reproductive condition influences the sensitivity of the hypothalamus–pituitary–adrenal axis. We investigated seasonal and reproductive variation in basal and stress-induced hormone profiles in a population of free-ranging timber rattlesnakes (Crotalus horridus) in north-central Pennsylvania during spring (i.e., May), summer (i.e., July), and early fall (i.e., September). Baseline corticosterone concentrations varied seasonally and were significantly lower during the summer sampling period in July. We observed a significant negative relationship between baseline corticosterone and testosterone in male snakes, while baseline corticosterone and estradiol tended to be positively correlated in females. Treatment of snakes with 1 h of capture stress significantly increased corticosterone across all seasons. However, there was a significant interaction between corticosterone responses to capture stress and season, suggesting that adrenocortical function is modulated seasonally. Because elevated corticosterone may be associated with reproduction, we asked whether hormonal stress responses vary with female reproductive condition. Although sample sizes are low, reproductive snakes had significantly higher baseline and stress-induced corticosterone concentrations than non-reproductive or post-parturient females. Further, despite similar baseline corticosterone concentrations between non-reproductive and post-parturient rattlesnakes, post-parturient females responded to capture stress with a significantly higher increase in corticosterone. Collectively, these data suggest that the sensitivity of the hypothalamus–pituitary–adrenal axis varies both seasonally and with changing reproductive states.     

Corticosterone secretion induced by chronic isolation in neonatal rats is sexually dimorphic and accompanied by elevated ACTH

Rat pups repeatedly subjected to brief periods of isolation during the stress hyporesponsive period (SHRP) exhibit varied neuroendocrine and behavioral changes as neonates and as adults. For example, neonatal rats exhibit increased circulating corticosterone after 1-h isolation on postnatal day 9 (P9) only if they were isolated daily from P2 to P8 [McCormick, C.M., Kehoe, P., Kovacs, S., 1998. Corticosterone release in response to repeated, short episodes of neonatal isolation: evidence of sensitization. Int. J. Dev. Neurosci. 16, 175-185]. It is not known if the increase in adrenocortical response on P9 following repeated isolation is mediated by increased pituitary ACTH secretion. The present study examined the responsivity of the hypothalamic-pituitary-adrenal (HPA) axis during the SHRP following brief, repeated isolation or acute pharmacological manipulation. Removal from the nest for 1 h daily on P4-8 increased circulating corticosterone after 1-h isolation on P9 by approximately twofold. Neither unhandled nor handled controls showed a corticosterone response to 1-h isolation on P9. The increased corticosterone was sexually dimorphic, with only females showing the sensitization response. Other findings suggest that the hormonal response is centrally mediated; chronically isolated pups of both sexes exhibit increased plasma ACTH following 1-h isolation on P9. While we could not detect an increase in Fos immunoreactivity (IR) on P9 in the hypothalamic paraventricular nucleus (PVN) of chronically isolated pups, acute pharmacological activation of serotonin 2A/2C receptors produced robust activation of ACTH and corticosterone secretion as well as expression of Fos in the PVN on P9. We conclude that chronic isolation stress limited to the SHRP stimulates the neonatal HPA axis, and that the adrenal response is sexually dimorphic. In addition, PVN neurons can express Fos IR on P9 in response to a very potent activation of the HPA axis.     

Stress, behaviour and reproductive performance in female cattle and pigs

Female farm animals are exposed to a great variety of environmental and management related stressors. As a consequence, their reproductive and maternal abilities may be compromised through mechanisms acting on the hypothalamic, pituitary, ovarian and uterine function. Responses to short- and long-term stressors may differ as short-term stressors often fail to affect reproduction or even may have stimulatory effects. Thus, the stress response induces diverse neuroendocrine reactions that can either increase or decrease the probability of an animal reproducing depending on the specific situation. The aim of the present review is to summarise the current knowledge on the stress concept and its implications on behaviour and reproductive performance in cows and female pigs as phenomena reported in laboratory animals are unable to explain all effects encountered in domesticated farm animals.     

Corticosterone manipulation reveals differences in hierarchical organization of multidimensional reproductive trade-offs in r-strategist and K-strategist females

Life history trade-offs are often hierarchical with decisions at one level affecting lower level trade-offs. We investigated trade-off structure in female side-blotched lizards (Uta stansburiana), which exhibit two evolved strategies: yellow-throated females are K-strategists and orange-throated are r-strategists. Corticosterone treatment was predicted to differentially organize these females' reproductive decisions. Corticosterone-treated yellow females suppressed reproduction but survived well, and augmented egg mass without decreasing clutch size. Conversely, corticosterone enhanced mortality and reproductive rates in orange females, and increased egg mass only after lengthy exposure. Corticosterone did not affect post-laying condition, suggesting that corticosterone increased egg mass through enhanced energy acquisition (income breeding). Corticosterone enhanced survival of lightweight females, but decreased survival of heavy females, introducing a foraging vs. predation trade-off. We conclude that rather than being a direct, functional relationship, observed trade-offs between offspring size and number represent evolved differences in hierarchical organization of multidimensional trade-offs, particularly in response to stress.     

Structural coloration and sexual selection in the barn swallow Hirundo rustica

Structural coloration has been hypothesized to play a role insexual selection, and we tested whether this was the case ina field study of the barn swallow Hirundo rustica. The dorsaliridescent plumage of barn swallows has a strong reflectancein the ultraviolet (UV) region, with adult males on averagereflecting 8-9% more than adult females, as revealed by a 2-yearstudy in southwestern Spain. The correlation between structural coloration (described by the reflectance in the UV part of thespectrum, UV chroma and blue chroma) and three other secondarysexual characters significantly associated with male matingsuccess (tail length, tail asymmetry, and red facial coloration)was weak and generally nonsignificant. Nor was there a significantrelationship between color parameters and body condition. Wetested for an association between structural coloration of the dorsal plumage and sexual selection in a number of independenttests. Arrival date of males was not significantly relatedto color; there was no significant relationship between colorationand probability of survival or age; mated males did not havestronger reflectance than unmated males; and the duration ofthe premating period was not significantly related to color.Reproductive success was not significantly correlated withplumage coloration in males, nor was the feeding rate of offspringby brightly colored males higher than that of males with lessbright plumage. Given that sample sizes were large, and the power of statistical tests high, we conclude that current sexualselection on the coloration of the dorsal plumage in the barnswallow is, at best, weak.     

Human disturbance alters endocrine and immune responses in the Galapagos marine iguana (Amblyrhynchus cristatus)

Anthropogenic disturbance is a relevant and widespread facilitator of environmental change and there is clear evidence that it impacts natural populations. While population-level responses to major anthropogenic changes have been well studied, individual physiological responses to mild disturbance can be equally critical to the long-term survival of a species, yet they remain largely unexamined. The current study investigated the impact of seemingly low-level anthropogenic disturbance (ecotourism) on stress responsiveness and specific fitness-related immune measures in different breeding stages of the marine iguana (Amblyrhynchus cristatus). Specifically, we found stress-induced elevations in plasma corticosterone among tourist-exposed populations relative to undisturbed populations. We also found changes in multiple immunological responses associated with stress-related effects of human disturbance, including bacterial killing ability, cutaneous wound healing, and hemolytic complement activity, and the responses varied according to reproductive state. By identifying health-related consequences of human disturbance, this study provides critical insight into the conservation of a well-known species that has a very distinct ecology. The study also broadens the foundation of knowledge needed to understand the global significance of various levels of human disturbance.     

Sensitivity to spectral interaural intensity difference cues in space-specific neurons of the barn owl

Barn owls use interaural intensity differences to localize sounds in the vertical plane. At a given elevation the magnitude of the interaural intensity difference cue varies with frequency, creating an interaural intensity difference spectrum of cues which is characteristic of that direction. To test whether space-specific cells are sensitive to spectral interaural intensity difference cues, pure-tone interaural intensity difference tuning curves were taken at multiple different frequencies for single neurons in the external nucleus of the inferior colliculus. For a given neuron, the interaural intensity differences eliciting the maximum response (the best interaural intensity differences) changed with the frequency of the stimulus by an average maximal difference of 9.4±6.2 dB. The resulting spectral patterns of these neurally preferred interaural intensity differences exhibited a high degree of similarity to the acoustic interaural intensity difference spectra characteristic of restricted regions in space. Compared to stimuli whose interaural intensity difference spectra matched the preferred spectra, stimuli with inverted spectra elicited a smaller response, showing that space-specific neurons are sensitive to the shape of the spectrum. The underlying mechanism is an inhibition for frequency-specific interaural intensity differences which differ from the preferred spectral pattern. Collectively, these data show that space-specific neurons are sensitive to spectral interaural intensity difference cues and support the idea that behaving barn owls use such cues to precisely localize sounds.Abbreviations ABI average binaural intensity - HRTF head-related transfer function - ICx external nucleus of the inferior colliculus - IID interaural intensity difference - ITD interaural time difference - OT optic tectum - RMS root mean square - VLVp nucleus ventralis lemnisci laterale, pars posterior     

Regulation of stress response is heritable and functionally linked to melanin‐based coloration

Sexual selection theory posits that ornaments can signal the genetic quality of an individual. Eumelanin‐based coloration is such an ornament and can signal the ability to cope with a physiological stress response because the melanocortin system regulates eumelanogenesis as well as physiological stress responses. In the present article, we experimentally investigated whether the stronger stress sensitivity of light than dark eumelanic individuals stems from differential regulation of stress hormones. Our study shows that darker eumelanic barn owl nestlings have a lower corticosterone release after a stressful event, an association, which was also inherited from the mother (but not the father) to the offspring. Additionally, nestlings sired by darker eumelanic mothers more quickly reduced experimentally elevated corticosterone levels. This provides a solution as to how ornamented individuals can be more resistant to various sources of stress than drab conspecifics. Our study suggests that eumelanin‐based coloration can be a sexually selected signal of resistance to stressful events.     

Electric signalling and reproductive behaviour in a mormyrid fish, the bulldog Marcusenius macrolepidotus (South African form)

Bulldog fish (Marcusenius macrolepidotus) generate short (<1 ms) electric-organ discharges (EODs), separated by much longer and highly variable interdischarge intervals (IDIs). We observed overt behaviour and electrical activity during reproductive behaviour in a male and in a female bulldog, and identified IDI patterns with putative signal functions. In contrast to Pollimyrus adspersus and Pollimyrus isidori, in which an elaborate and extended courtship precedes spawning proper, our fish started spawning almost immediately when we allowed the female to enter the males territory. The male did not construct a nest, and neither parent provided parental care. The male showed very little aggression towards the intruding female. Fish spawned in bouts near the males hiding place, and eggs were scattered by the females vigorous tail flips as she left the spawning site, only to return shortly thereafter. During spawning bouts, both fish generated highly stereotyped IDI patterns: the male generated a series of IDIs gradually decreasing from about 200 ms to about 55 ms that was abruptly terminated by a long IDI. The female generated a series of relatively regular IDIs (about 54 ms) that was followed by a marked increase in IDI duration (the probable time of spawning). Finally, a sharp decrease in IDIs to about 20 ms accompanied the females sudden escape from the spawning site. In between spawning bouts, both fish generated series of very short IDIs (high discharge rate, HD) that alternated abruptly with very low-rate inter-HD activity (especially in the male). IDIs as short as 9 ms (male) or 11 ms (female) occurred during HD displays. No visible aggression, in fact very little overt behaviour, occurred during these HD displays in both fish. Agonistic interactions between male and female, outside a reproductive context, were similar to those previously described in male pairs, including overt behavioural patterns such as parallel swimming, antiparallel display and attack, as well as HD displays. When not interacting, fish did not generate HD displays. We suggest the HD display is a communication signal in both reproductive and agonistic contexts.     

Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration

Local adaptation is a major mechanism underlying the maintenance of phenotypic variation in spatially heterogeneous environments. In the barn owl (Tyto alba), dark and pale reddish-pheomelanic individuals are adapted to conditions prevailing in northern and southern Europe, respectively. Using a long-term dataset from Central Europe, we report results consistent with the hypothesis that the different pheomelanic phenotypes are adapted to specific local conditions in females, but not in males. Compared to whitish females, reddish females bred in sites surrounded by more arable fields and less forests. Colour-dependent habitat choice was apparently beneficial. First, whitish females produced more fledglings when breeding in wooded areas, whereas reddish females when breeding in sites with more arable fields. Second, cross-fostering experiments showed that female nestlings grew wings more rapidly when both their foster and biological mothers were of similar colour. The latter result suggests that mothers should particularly produce daughters in environments that best match their own coloration. Accordingly, whiter females produced fewer daughters in territories with more arable fields. In conclusion, females displaying alternative melanic phenotypes bred in habitats providing them with the highest fitness benefits. Although small in magnitude, matching habitat selection and local adaptation may help maintain variation in pheomelanin coloration in the barn owl.     

To breed or not to breed: Physiological correlates of reproductive status in a facultatively biennial iguanid

It is unusual for seasonal breeders to frequently skip opportunities for reproduction. We investigated the relationship between physiological state and reproductive decision-making in Galápagos marine iguanas (Amblyrhynchus cristatus), a species in which females typically reproduce biennially, although the proportion of breeding individuals varies significantly across years. Nearly all adult-sized females initiated follicular development prior to the lekking period, but 38% of females resorbed all developing follicles 5-15 days before the start of copulations. Receptive and non-receptive females differed in reproductive hormones during the mate choice period. Testosterone peaked in receptive females immediately prior to copulation, indicating that testosterone or its derivative estradiol likely mediates female receptivity in Galápagos marine iguanas. Non-receptive females showed significant peaks in both testosterone and progesterone during follicular atresia, suggesting that these hormones may be involved in inhibiting vitellogenesis. Two to three weeks prior to the period of reproductive decision-making (and the onset of follicular atresia in non-receptive females) receptive females were in higher body condition, were developing larger follicles, and had lower levels of both baseline and stress-induced corticosterone. Reproduction is extremely costly in this long-lived species, and increases the likelihood of mortality in the year following breeding; females could therefore gain significant benefits from being attuned to indicators of reproductive success. We suggest that corticosterone may modulate reproductive decisions by altering individual sensitivity to both internal and external cues of the likelihood of successful reproduction.     

Spatial variation in the temporal change of male and female melanic ornamentation in the barn owl

Because the magnitude of selection can vary between sexes and in space and time, sexually antagonistic selection is difficult to demonstrate. In a Swiss population of barn owls (Tyto alba), a heritable eumelanic colour trait (size of black spots on ventral feathers) was positively selected with respect to yearling survival only in females. It remains unclear whether the absence of negative selection in males is typical in this species. To tackle this issue indirectly, we measured the size of black spots in 1733 skin specimens collected by museums from 1816 to 2001 in seven European countries and in the Middle-East. The temporal change in spot size was sex- and country-specific. In males, spots became smaller particularly in three countries (Middle-East, Italy and Switzerland). In females, the size of spots increased significantly in two countries (UK and Spain) and decreased in two others (Germany and Switzerland). Because migration and phenotypic plasticity cannot explain these results, selection is the most likely cause. The weaker temporal change in spot size in females than males may be because of the combined effect of strong genetic correlation between the sexes and stronger negative selection in males than positive selection in females. We thus suggest that in the barn owl, spot size (or genetically correlated traits) is sexually antagonistically selected and that its pattern of selection may account for the maintenance of its variation and sexual dimorphism.     

Isolation and characterization of 21 microsatellite markers in the barn owl (Tyto alba)

We report 21 new polymorphic microsatellite markers in the European barn owl (Tyto alba). The polymorphism of the reported markers was evaluated in a population situated in western Switzerland and in another from Tenerife, Canary Islands. The number of alleles per locus varies between two and 31, and expected heterozygosity per population ranges from 0.16 to 0.95. All loci are in Hardy-Weinberg equilibrium and no linkage disequilibrium was detected. Two loci exhibit a null allele in the Tenerife population.     

Sensitivity to interaural time difference and representation of azimuth in central nucleus of inferior colliculus in the barn owl

Standard electrophysiology and virtual auditory stimuli were used to investigate the influence of interaural time difference on the azimuthal tuning of neurons in the core and the lateral shell of the central nucleus of the inferior colliculus of the barn owl. The responses of the neurons to virtual azimuthal stimuli depended in a periodic way on azimuth. Fixation of the interaural time difference, while leaving all other spatial cues unchanged, caused a loss of periodicity and a broadening of azimuthal tuning. This effect was studied in more detail in neurons of the core. The azimuthal range tested and the frequency selectivity of the neurons were additional parameters influencing the changes induced by fixating the interaural time difference. The addition of an interaural time difference to the virtual stimuli resulted in a shift of the tuning curves that correlated with the interaural time difference added. In this condition, tuning strength did not change. These results suggest that interaural time difference is an important determinant of azimuthal tuning in all neurons of the core and lateral shell of the central nucleus of the inferior colliculus, and is the only determinant in many of the neurons from the core.