Jamie M. Cornelius

Contributions of endocrinology to the migration life history of birds

Migration is a key life cycle stage in nearly 2000 species of birds and is a greatly appreciated phenomenon in both cultural and academic arenas. Despite a long research tradition concerning many aspects of migration, investigations of hormonal contributions to migratory physiology and behavior are more limited and represent a comparatively young research field. We review advances in our understanding of the hormonal mechanisms of migration with particular emphasis on the sub-stages of the migration life history: development, departure, flight and arrival. These sub-stages vary widely in their behavioral, ecological and physiological contexts and, as such, should be given appropriate individual consideration.

Physiological trade-offs in self-maintenance: plumage molt and stress physiology in birds

SUMMARY Trade-offs between self-maintenance processes can affect life-history evolution. Integument replacement and the stress response both promote self-maintenance and affect survival in vertebrates. Relationships between the two processes have been studied most extensively in birds, where hormonal stress suppression is down regulated during molt in seasonal species, suggesting a resource-based trade-off between the two processes. The only species found to differ are the rock dove and Eurasian tree sparrow, at least one of which performs a very slow molt that may reduce resource demands during feather growth, permitting investment in the stress response. To test for the presence of a molt–stress response trade-off, we measured hormonal stress responsiveness during and outside molt in two additional species with extended molts, red crossbills (Loxia curvirostra) and zebra finches (Taeniopygia guttata). We found that both species maintain hormonal stress responsiveness during molt. Further, a comparative analysis of all available species revealed a strong relationship between molt duration and degree of hormonal suppression. Though our results support trade-off hypotheses, these data can also be explained by alternative hypotheses that have not been formally addressed in the literature. We found a strong relationship between stress suppression and seasonality of breeding and evidence suggesting that the degree of suppression may be either locally adaptable or plastic and responsive to local environmental conditions. We hypothesize that environmental unpredictability favors extended molt duration, which in turn allows for maintenance of the hormonal stress response, and discuss implications of a possible trade-off for the evolution of molt schedules.

Natural selection and glucocorticoid physiology

Glucocorticoid hormones are considered potent modulators of trade‐offs between reproduction and survival. As such, selection should affect glucocorticoid physiology, although relatively little is known about how selection may act on glucocorticoid profiles. In general, the evolution of physiology is less studied and less well understood than morphological or life history traits. Here, we used a long‐term data set from a population of mountain white‐crowned sparrows to estimate natural selection on glucocorticoid profiles. Our study suggests that survival selection favours higher hormone concentrations for multiple components of glucocorticoid physiology (both baseline and stress‐induced glucocorticoid levels). Fecundity selection varies depending on the component of hypothalamic–pituitary–adrenal physiology; greater reproductive output was associated with higher baseline glucocorticoid levels, but lower stress‐induced glucocorticoid levels. Additionally, the selection gradient was greater for glucocorticoids than for a morphological trait (wing length). These results support the hypothesis that stress‐induced glucocorticoids increase survival over reproduction within a wild population (the CORT‐trade‐off hypothesis). Taken together, these results add to our knowledge of how selection operates on physiological traits and also provide an evolutionary and ecological perspective on several key open issues in the field of glucocorticoid physiology.

Physiological and behavioral responses of migrants to environmental cues

Migrant species express wide varieties of movement strategies that closely mirror patterns of resource distribution. Resources can vary predictably in space and time (e.g., seasonal peaks of productivity in temperate regions) or can be unpredictable in one or both dimensions. Evolution of migration strategies and the underlying physiological and behavioral mechanisms are therefore diverse, but similarities have been noted. To understand how migrants respond to environmental cues, we focus on species that represent extremes along a continuum between obligate versus facultative migratory behavior and address the physiological mechanisms regulating these movements. Obligate migrants, which travel on highly predictable schedules, generally rely on the annual change in daylength and circannual rhythms to initiate the vernal and, where known, the fall phases of migration. Facultative species may show similar seasonal preparations in cases where resources are temporally predictable, but appear to rely more heavily upon local supplementary cues in the environment to initiate migrations. In general, the physiological response mechanisms to environmental cues that coordinate migratory movements include perception of the environmental cue and transduction to neuroendocrine and endocrine systems. Clearly, there are huge gaps in our knowledge in this area, but published studies of each of the migratory types suggest striking parallels. Based on a comparison of the physiological aspects of the divergent migratory patterns, we emphasize that the migratory types are not completely distinct. Instead, the differences of migration patterns and responsiveness to cues reflect differences in the relative contributions of common physiological mechanisms that underly the control of movements. A more complete understanding of migratory physiology requires continued descriptive studies, particularly in a greater diversity of model systems, in addition to experimental methods that utilize innovative tracking technology as well as behavioral and physiological innovations to draw attention to different levels of organization. Comprehending the physiological mechanisms underlying migratory patterns will be vital for knowing how migrants respond to current environmental cues and anticipating their reactions to future conditions.

Under a neighbour's influence: public information affects stress hormones and behaviour of a songbird

Socially acquired information improves the accuracy and efficiency of environmental assessments and can increase fitness. Public information may be especially useful during unpredictable food conditions, or for species that depend on resources made less predictable by human disturbance. However, the physiological mechanisms by which direct foraging assessments and public information are integrated to affect behaviour remain largely unknown. We tested for potential effects of public information on the behavioural and hormonal response to food reduction by manipulating the social environment of captive red crossbills (Loxia curvirostra). Red crossbills are irruptive migrants that are considered sensitive to changes in food availability and use public information in decision making. Here, we show that public information can attenuate or intensify the release of glucocorticoids (i.e. stress hormones) during food shortage in red crossbills. The observed modulation of corticosterone may therefore be a physiological mechanism linking public information, direct environmental assessments and behavioural change. This mechanism would not only allow for public information to affect individual behaviour, but might also facilitate group decision making by bringing group members into more similar physiological states. The results further suggest that stressors affecting entire populations may be magnified in individual physiology through social interactions.

Evolution of environmental cue response mechanisms: adaptive variation in photorefractoriness.

Appropriate timing of transitions between annual cycle stages (reproduction, plumage molt, migration) is critical to fitness for birds living in temporally varying environments. Environmental cue response systems permit birds to orchestrate these transitions. This paper focuses on how photorefractoriness and one neuroendocrine correlate of it (GnRH system plasticity) have evolved to permit appropriate timing of the transition from breeding to plumage molt. Photorefractoriness is defined by two criteria. Criterion 1: photoinduced gonadal regression occurs without any decline in photoperiod. Criterion 2: photoinduced gonadal regression cannot be reversed by increased photoperiod, even continuous light. Through a comparative approach we show that: (1) Loss of Refractoriness Criterion 1 and of GnRH system down-regulation appear to represent adaptive specializations favoring highly temporally flexible or continuous breeding, (2) Refractoriness Criteria 1 and 2 are not always concordant, and Criterion 2 in particular is not well-correlated with degree of temporal reproductive flexibility, (3) occurrence of some cue response traits are better-explained by phylogenetic relationships among taxa than by current reproductive schedules (seasonal, flexible, opportunistic), (4) substantial temporal flexibility can be achieved in a variety of ways besides adaptive modifications of refractoriness, such as relaxation of long-day requirements for reproductive development, and enhancement of non-photic cue responsiveness. These comparisons also highlight fundamental similarities between some of the most opportunistic species and seasonal breeders, such as an autumn reproductive hiatus during molt. Even in the face of substantial environmental unpredictability, selection may often strongly favor regular scheduling of particularly critical life cycle stages such as plumage molt.

Assessing the role of reproduction and stress in the spring emergence of Haematozoan parasites in birds

A spring emergence of avian haemosporidian infections is nearly universal among temperate zone birds and is often described as a cost of reproductive effort. We take advantage of the opportunistic (i.e. aseasonal) breeding schedule of the red crossbill (Loxia curvirostra) to determine the relative contributions of season versus host physiology to the timing and intensity of Haemoproteus infections in the temperate zone. Despite breeding activity in both the winter and summer, Haemoproteus infections were highly seasonal – occurring largely from May through September – and measures of host physiology (i.e. reproductive condition and stress parameters) did not explain parasite prevalence. However, within the spring–summer peak, infection intensity (i.e. parasite density) was positively correlated with plasma levels of testosterone and free corticosterone and negatively correlated with corticosterone binding globulin capacity. These data are discussed in terms of the behavioral ecology of host and vector, and suggest that both seasonal increases in vector activity and relapse of latent (i.e. dormant) infections contribute to the spring emergence in birds. Relapse of latent infections does not appear to be induced by reproductive activity or increased allostatic (i.e. energy) load, but rather by a season-specific change in host or parasite physiology (e.g. melatonin or endogenous rhythms).

Coping with the extremes: stress physiology varies between winter and summer in breeding opportunists

Seasonal changes in stress steroid hormone secretions are thought to reflect investment in self-maintenance versus reproduction. The capricious conditions hypothesis (CCH) posits that reduced corticosterone (CORT) secretion during stress coincident with parental phases of breeding is necessary in harsh environments because a full response would otherwise trigger repeated nest abandonments. To test this hypothesis, we measured seasonal changes in stress physiology in free-living red crossbills (Loxia curvirostra), an opportunistically breeding songbird that regularly breeds in summer and winter. This species allows unique comparisons of breeding physiology under very different seasonal environmental conditions within locations. We found strong support for the CCH: red crossbills showed reduced CORT secretion only when in high reproductive condition in the winter, when compared with summer breeders and winter non-breeders. These data demonstrate that behavioural status and local environmental conditions interact to affect mechanisms underlying investment trade-offs, presumably in a way that maximizes lifetime reproductive success.

Haemoproteus infected birds have increased lifetime reproductive success

The impact of haematozoan infection on host fitness has received substantial attention since Hamilton and Zuk posited that parasites are important drivers of sexual selection. However, short-term studies testing the assumption that these parasites consistently reduce host fitness in the wild have produced contradictory results. To address this complex issue, we conducted a long-term study examining the relationship between naturally occurring infection with Haemoproteus and Plasmodium, and lifetime reproductive success and survival of Mountain White-crowned Sparrows. Specifically, we tested the hypothesis that birds infected with haematozoan parasites have reduced survival (as determined by overwinter return rates) and reproductive success. Contrary to expectation, there was no relationship between Haemoproteus and Plasmodium infection and reproduction or survival in males, nor was there a relationship between Plasmodium infection and reproduction in females. Interestingly, Haemoproteus-infected females had significantly higher overwinter return rates and these females fledged more than twice as many chicks during their lifetimes as did uninfected females. We discuss the impact of parasitic infections on host fitness in light of these findings and suggest that, in the case of less virulent pathogens, investment in excessive immune defence may decrease lifetime reproduction.

Song exposure during juvenile dispersal in Mountain White-crowned Sparrows

ABSTRACT The degree to which local song structure reflects the singers population of origin is a long-standing and contentious issue. Young songbirds that settle to breed outside their natal song-dialect area may learn to produce nonnatal dialect by hearing and memorizing these songs during juvenile dispersal. We quantified adult singing rates in a population of Mountain White-crowned Sparrows (Zonotrichia leucophrys oriantha) in the Sierra Nevada in 2 yr, and compared them with the arrival schedule of juveniles not hatched on the study area. Our results show that opportunities for juveniles to learn new (nonnatal) song types become highly limited during the premigratory dispersal phase, because adult singing rates are very low by the time nonlocal juveniles begin to arrive. Thus, if individuals learn nonnatal songs during dispersal, they must do so hearing relatively few repetitions of the unfamiliar dialect.