Toward understanding the endocrine regulation of diverse facultative migration strategies.

Migration is an important event in the annual cycle of many animals that facilitates the use of resources that vary across space and time. It can occur with regular and predictable timing, as in obligate migration, or with much greater flexibility, as in facultative migration. Most research aimed at understanding the endocrine mechanisms regulating the transition to a migratory stage has focused on obligate migration, whereas less is known about facultative forms of migration. One challenge for research into the endocrine regulation of facultative migration is that facultative migrations encompass a diverse array of migratory movements. Here, we present a framework to describe and conceptualize variation in facultative migrations that focuses on conditions at departure. Within the context of this framework, we review potential endocrine mechanisms involved in the initiation of facultative migrations in vertebrates. We first focus on glucocorticoids, which have been the subject of most research on the topic. We then examine other potential hormones and neurohormones that have received less attention, but are exciting candidates to consider. We conclude by highlighting areas where future research is particularly needed.

Perspectives on environmental heterogeneity and seasonal modulation of stress response in neotropical birds.

Corticosterone (CORT), the main glucocorticoid in birds, regulates physiological and behavioral traits linked to predictable and unpredictable environmental fluctuations (i.e., stressors). Baseline and stress-induced CORT concentrations are known to fluctuate seasonally, linked to life history stages (LHS) such as breeding, molt, and wintering stage. These variations have been relatively well described in North American birds, but poorly addressed in neotropical species. To fill this gap, we explored how baseline and stress-induced CORT variation by LHS was affected by seasonality and environmental heterogeneity (i.e., frequency of unpredictable events such as droughts, flashfloods, etc) within the Neotropics using two approaches. First, we reviewed all currently available data about CORT concentrations for neotropical bird species. Second, we performed an in-depth analysis comparing the CORT responses of the two most common species of the Zonotrichia genus from North and South America (Z. leucophrys and Z. capensis, respectively) and their subspecies to seasonality and environmental heterogeneity. These species have been analyzed with the same methodology, allowing for an in-depth comparison of CORT variations. Despite scant data on neotropical bird species, we observed overlap between molt and breeding, and lower fluctuations of CORT among LHS. These patterns would be considered atypical compared to those described for North temperate species. Further, we found no significant associations between environmental heterogeneity and the stress-responses. In Zonotrichia we observed a positive association between baseline and stress-induced concentrations of CORT and latitude. We also observed differences by LHS. Both baseline and stress-induced CORT concentrations were higher during breeding and lower during molt. In addition, for both species, the overall pattern of seasonal modulation of stress response was heavily influenced by the migration strategy, with long-distance migrants showing significantly higher stress-induced CORT levels. Our results highlight the need for more data collection in the Neotropics. Comparative data would shed further light on the sensitivity of the adrenocortical response to stress under different scenarios of environmental seasonality and unpredictability.

Feather mercury concentrations in omnivorous and granivorous terrestrial songbirds in Southeast Michigan.

Sublethal exposure to methylmercury (MeHg) can have consequences for the reproductive, neurological, and physiological health of birds. Songbirds, regardless of trophic position, are often exposed to mercury (Hg) and may be at risk for health effects - especially if they inhabit a place that is subject to high Hg atmospheric deposition and/or have local conditions that are prone to methylation. This study investigates Hg concentrations in terrestrial songbirds of Southeast Michigan, where historical and present-day anthropogenic emissions of heavy metals are elevated. We collected tail feather samples from 223 songbirds across four different species during summer and fall of 2018 and 2019. The mean (±SE) Hg concentration across all samples was 103 ± 3.43 ng/g of dry feather weight. Mercury concentration varied significantly among species, and by age and site in some species, but not by sex. Mean concentrations were nearly seven times higher in two omnivore species, American robin (Turdus migratorius) and European starling (Sturnus vulgaris), than in the two granivore species, American goldfinch (Spinus tristus) and house sparrow (Passer domesticus). Juveniles had higher feather Hg concentrations than adults in all species except American goldfinches - which feed their young primarily seeds, further supporting a role of diet in exposure. We also found a negative correlation between Hg concentration and body condition in American robins, but further research is needed to verify this relationship. While our sample concentrations do not exceed the threshold for sublethal effects, our findings provide insight into the patterns of Hg concentrations in terrestrial songbirds, which may help in understanding Hg exposure pathways, bioaccumulation and risks in terrestrial species.

Stress in paradise: effects of elevated corticosterone on immunity and avian malaria resilience in a Hawaiian passerine.

Vertebrates confronted with challenging environments often experience an increase in circulating glucocorticoids, which result in morphological, physiological and behavioral changes that promote survival. However, chronically elevated glucocorticoids can suppress immunity, which may increase susceptibility to disease. Since the introduction of avian malaria to Hawaii a century ago, low-elevation populations of Hawaii Amakihi (Chlorodrepanis virens) have undergone strong selection by avian malaria and evolved increased resilience (the ability to recover from infection), while populations at high elevation with few vectors have not undergone selection and remain susceptible. We investigated how experimentally elevated corticosterone affects the ability of high- and low-elevation male Amakihi to cope with avian malaria by measuring innate immunity, hematocrit and malaria parasitemia. Corticosterone implants resulted in a decrease in hematocrit in high- and low-elevation birds but no changes to circulating natural antibodies or leukocytes. Overall, leukocyte count was higher in low- than in high-elevation birds. Malaria infections were detected in a subset of low-elevation birds. Infected individuals with corticosterone implants experienced a significant increase in circulating malaria parasites while untreated infected birds did not. Our results suggest that Amakihi innate immunity measured by natural antibodies and leukocytes is not sensitive to changes in corticosterone, and that high circulating corticosterone may reduce the ability of Amakihi to cope with infection via its effects on hematocrit and malaria parasite load. Understanding how glucocorticoids influence a host's ability to cope with introduced diseases provides new insight into the conservation of animals threatened by novel pathogens.

The effects of food limitation on behavior, corticosterone, and the use of social information in the red crossbill (Loxia curvirostra).

Meeting metabolic demands through foraging is a basic animal need that drives the evolution of foraging adaptations. The use of social information is one adaptation that could improve foraging success and fitness if it helps animals locate food when conditions are challenging. It is unknown if food limitation-or the glucocorticoid hormones that are often released when food is limited-can influence the extent to which animals use social information or their ability to learn novel foraging techniques. We explored the effects of limited access to food on activity levels, corticosterone secretion, and social information use in red crossbills, a highly social songbird species adapted to cope with high degrees of resource unpredictability. Using an observer/demonstrator paradigm, food limited or well fed observers were allowed to watch demonstrators solve a novel feeding puzzle before being allowed to attempt the puzzle themselves across repeated trials. Our findings suggest that food limitation transiently increased activity levels but did not result in long-term elevations of corticosterone and did not increase the speed at which red crossbills utilized social information to solve the novel foraging task. However, food limitation may have increased the value of using socially acquired information, as foraging technique performance improved faster in food limited birds relative to controls. Social learning was further demonstrated by the red crossbills in this study when naïve observers overwhelmingly learned a socially-demonstrated task over an undemonstrated task when tested on a two-task foraging board.

Recovery of hematocrit and fat deposits varies by cage size in food-restricted captive red crossbills (Loxia curvirostra).

Hematocrit-or the percent volume of red blood cells in whole blood-is thought to fluctuate adaptively in response to changing oxygen demands that occur during different life activities and in different environments. Because red blood cells are made from materials that can be limiting, however, it is thought that hematocrit may also reflect general body condition and access to resources. We tested the effect of hydration state, resource restriction (i.e., time available to forage), and activity (i.e., different cage sizes) on hematocrit in captive red crossbills (Loxia curvirostra). We found no evidence that a mild dehydration protocol impacts hematocrit and only weak support that mild food restriction impacts hematocrit. Food restriction did, however, reduce fat deposits and fat loss was more significant in birds that were also sampled for hematocrit. Furthermore, food-restricted birds housed in flight aviaries recovered hematocrit but not fat stores following repeated blood sampling, whereas birds housed in small cages lost additional hematocrit but mitigated fat loss following successive bleeds. Together these results suggest that different flight demands may determine response to blood loss during food restriction, potentially revealing a trade-off between fat storage and red blood cell development. Our results also demonstrate the need for scientists to carefully record hematocrit data and the time course across which multiple tubes of blood are collected to avoid confounding real patterns with variation generated by sampling protocol.

Patterns of annual and seasonal immune investment in a temporal reproductive opportunist.

Historically, investigations of how organismal investments in immunity fluctuate in response to environmental and physiological changes have focused on seasonally breeding organisms that confine reproduction to seasons with relatively unchallenging environmental conditions and abundant resources. The red crossbill, Loxia curvirostra, is a songbird that can breed opportunistically if conifer seeds are abundant, on both short, cold, and long, warm days, providing an ideal system to investigate environmental and reproductive effects on immunity. In this study, we measured inter- and intra-annual variation in complement, natural antibodies, PIT54 and leucocytes in crossbills across four summers (2010-2013) and multiple seasons within 1 year (summer 2011-spring 2012). Overall, we observed substantial changes in crossbill immune investment among summers, with interannual variation driven largely by food resources, while variation across multiple seasons within a single cone year was less pronounced and lacked a dominant predictor of immune investment. However, we found weak evidence that physiological processes (e.g. reproductive condition, moult) or abiotic factors (e.g. temperature, precipitation) affect immune investment. Collectively, this study suggests that a reproductively flexible organism may be able to invest in both reproduction and survival-related processes, potentially by exploiting rich patches with abundant resources. More broadly, these results emphasize the need for more longitudinal studies of trade-offs associated with immune investment.

Innate immunity and environmental correlates of Haemoproteus prevalence and intensity in an opportunistic breeder.

While parasite infection can have substantial fitness consequences in organisms, the predictors of parasite prevalence and intensity are often complex and vary depending on the host species. Here, we examined correlates of Haemoproteus (a common malaria parasite) prevalence and intensity in an opportunistically breeding songbird, the red crossbill (Loxia curvirostra). Specifically, we quantified Haemoproteus prevalence and intensity in crossbills caught in the Grand Teton National Park from 2010 to 2013. We found that parasite prevalence varies seasonally and across years, with the highest number of infected individuals occurring in the summer, although there was variation across summers sampled, and that prevalence was positively related to annual mean cone crop sizes (a measure of crossbill food abundance) and daily ambient temperature (a correlate of vector abundance). Parasite intensity was significantly and positively related to one measure of innate immunity, leucocyte counts per blood volume. Finally, neither crossbill age, ecomorph, nor sex had significant effects on parasite infection intensity; however, parasite prevalence did significantly vary among ecomorph and age classes. These results support the interpretation that a combination of physiological (specifically immune activity) and environmental factors affects parasite prevalence and infection intensity in this opportunistically breeding avian species.

Understanding variation in migratory movements: A mechanistic approach.

Spatial and temporal fluctuations in resource availability have led to the evolution of varied migration patterns. In order to appropriately time movements in relation to resources, environmental cues are used to provide proximate information for timing and the endocrine system serves to integrate these external cues and behavioral and physiological responses. Yet, the regulatory mechanisms underlying migratory timing have rarely been compared across a broad range of migratory patterns. First, we offer an updated nomenclature of migration using a mechanistic perspective to clarify terminology describing migratory types in relation to ecology, behavior and endocrinology. We divide migratory patterns into three types: obligate, nomadic, and fugitive. Obligate migration is characterized by regular and directed annual movements between locations, most commonly for breeding and overwintering, where resources are predictable and sufficient. Nomadic migrations occur less predictably than do obligate migrations as animals make use of potentially rich but ephemeral resources that occur unpredictably in space or time. Fugitive migrations move animals away from an area in response to severe disruption of environmental conditions and occur as part of an emergency life history stage. We also consider partially migratory populations, which include a mix of sedentary and migratory individuals; the movement patterns of partial migrants are expected to fall into one of the three types above. For these various forms of migration, we review our understanding of the environmental cues and endocrine mechanisms that underlie the expression of a migratory state. Several common hormonal mechanisms exist across the varied migratory forms, but there are also important areas where further investigations are needed in order to gain broad insight into the origin of movements and the diversity of migratory patterns. We propose that taking a comparative approach across the migratory types that considers endocrine mechanisms will advance a new understanding of migration biology.

Social information changes stress hormone receptor expression in the songbird brain.

Social information is used by many vertebrate taxa to inform decision-making, including resource-mediated movements, yet the mechanisms whereby social information is integrated physiologically to affect such decisions remain unknown. Social information is known to influence the physiological response to food reduction in captive songbirds. Red crossbills (Loxia curvirostra) that were food reduced for several days showed significant elevations in circulating corticosterone (a "stress" hormone often responsive to food limitation) only if their neighbors were similarly food restricted. Physiological responses to glucocorticoid hormones are enacted through two receptors that may be expressed differentially in target tissues. Therefore, we investigated the influence of social information on the expression of the mineralocorticoid receptor (MR) and glucocorticoid receptor (GR) mRNA in captive red crossbill brains. Although the role of MR and GR in the response to social information may be highly complex, we specifically predicted social information from food-restricted individuals would reduce MR and GR expression in two brain regions known to regulate hypothalamic-pituitary-adrenal (HPA) activity - given that reduced receptor expression may lessen the efficacy of negative feedback and release inhibitory tone on the HPA. Our results support these predictions - offering one potential mechanism whereby social cues could increase or sustain HPA-activity during stress. The data further suggest different mechanisms by which metabolic stress versus social information influence HPA activity and behavioral outcomes.

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.

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

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.

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.

Environmental regulation of annual schedules in opportunistically-breeding songbirds: adaptive specializations or variations on a theme of white-crowned sparrow?

How birds use environmental cues to time breeding, migration and molt has been the subject of intensive study for nearly 90 years. Most work has focused on seasonal breeders; opportunistic breeders have been presumed to differ fundamentally from seasonal taxa in ways that facilitate coping with unpredictable environments. Understanding patterns and mechanisms of opportunists' responses to environmental cues can reveal the extent to which different environments require specialized adaptations of cue response systems. In this review we will present our perspective on how patterns and mechanisms of environmental cue response of three groups of opportunists--zebra finches, crossbills and Darwin's finches--compare with seasonal breeders. Long-standing predictions regarding tonic activity of the hypothalamic gonadotropin-releasing hormone system have been confirmed in at least some opportunists. However, opportunists resemble seasonal breeders in some surprising ways, illustrating basic similarity among taxa facing very different timing challenges. For instance, many opportunists completely regress the gonads outside breeding times, rely on initial predictive cues (both photic and non-photic) to regulate timing and rate of reproductive development, and in some cases even appear to display internal changes in responsiveness to environmental cues (i.e., cycles of reproductive refractoriness and sensitivity). Although advantages of unrestricted temporal flexibility are intuitively clear for animals coping with unpredictable habitats, the available data on these opportunists indicate that in all but the most extremely capricious situations the advantages of flexibility may be at least partly outweighed by contrasting advantages of following a reliable temporal schedule.