Comparison of the Phenotypic Flexibility of Muscle and Body Condition of Migrant and Resident White-Crowned Sparrows.

AbstractSeasonally breeding birds express variations of traits (phenotypic flexibility) throughout their life history stages that represent adaptations to environmental conditions. Changes of body condition during migration have been well studied, whereas alterations of skeletal and cardiac muscles, body mass, and fat scores have yet to be characterized throughout the spring or fall migratory stages. Additionally, we examined flexible patterns of muscle, body mass, and fat score in migrant white-crowned sparrows (Zonotrichia leucophrys gambelii) in comparison with those in a resident subspecies (Zonotrichia leucophrys nuttalli) during the stages they share to evaluate the influence of different life histories. Migrants showed hypertrophy of the pectoralis muscle fiber area on the wintering grounds in late prealternate molt, yet increased pectoralis muscle mass was not detected until birds readied for spring departure. While pectoralis profile and fat scores enlarged at predeparture in spring and fall, pectoralis, cardiac, and body masses were greater only in spring stages, suggesting seasonal differences for migratory preparation. Gastrocnemius mass showed little change throughout all stages, whereas gastrocnemius fiber area declined steadily but rebounded in fall on the wintering grounds, where migrants become more sedentary. In general, residents are heavier birds with larger leg structures, while migrants sport longer wings and greater heart mass. Phenotypic flexibility was most prominent among residents with peaks of pectoralis, gastrocnemius, and body masses during the winter stage, when local weather is most severe. Thus, the subspecies express specific patterns of phenotypic flexibility with peaks coinciding with the stages of heightened energy demands: the winter stage for residents and the spring stages for migrants.

Flexibility underlies differences in mitochondrial respiratory performance between migratory and non-migratory White-crowned Sparrows (Zonotrichia leucophrys).

Migration is one of the most energy-demanding behaviors observed in birds. Mitochondria are the primary source of energy used to support these long-distance movements, yet how mitochondria meet the energetic demands of migration is scarcely studied. We quantified changes in mitochondrial respiratory performance in the White-crowned Sparrow (Zonotrichia leucophrys), which has a migratory and non-migratory subspecies. We hypothesized that the long-distance migratory Gambel's subspecies (Z. l. gambelii) would show higher mitochondrial respiratory performance compared to the non-migratory Nuttall's subspecies (Z. l. nuttalli). We sampled Gambel's individuals during spring pre-migration, active fall migration, and a period with no migration or breeding (winter). We sampled Nuttall's individuals during periods coinciding with fall migration and the winter period of Gambel's annual cycle. Overall, Gambel's individuals had higher citrate synthase, a proxy for mitochondrial volume, than Nuttall's individuals. This was most pronounced prior to and during migration. We found that both OXPHOS capacity (state 3) and basal respiration (state 4) of mitochondria exhibit high seasonal flexibility within Gambel's individuals, with values highest during active migration. These values in Nuttall's individuals were most similar to Gambel's individuals in winter. Our observations indicate that seasonal changes in mitochondrial respiration play a vital role in migration energetics.

A chromosome-level genome assembly of a free-living white-crowned sparrow (Zonotrichia leucophrys gambelii).

The white-crowned sparrow, Zonotrichia leucophrys, is a passerine bird with a wide distribution and it is extensively adapted to environmental changes. It has historically acted as a model species in studies on avian ecology, physiology and behaviour. Here, we present a high-quality chromosome-level genome of Zonotrichia leucophrys using PacBio and OmniC sequencing data. Gene models were constructed by combining RNA-seq and Iso-seq data from liver, hypothalamus, and ovary. In total a 1,123,996,003 bp genome was generated, including 31 chromosomes assembled in complete scaffolds along with other, unplaced scaffolds. This high-quality genome assembly offers an important genomic resource for the research community using the white-crowned sparrow as a model for understanding avian genome biology and development, and provides a genomic basis for future studies, both fundamental and applied.

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.

Urbanization and maternal hormone transfer: Endocrine and morphological phenotypes across ontogenetic stages.

The phenotypes observed in urban and rural environments are often distinct; however, it remains unclear how these novel urban phenotypes arise. Hormone-mediated maternal effects likely play a key role in shaping developmental trajectories of offspring in different environments. Thus, we measured corticosterone (Cort) and testosterone (T) concentrations in eggs across the laying sequence in addition to Cort concentrations in nestling and adult female house wrens (Troglodytes aedon) at one urban and one rural site. We found that egg T concentrations were not different between birds from urban and rural sites. However, across all life stages (egg, nestling, and adult female), Cort concentrations were higher at the urban site. Additionally, urban nestling Cort concentrations, but not rural, correlated with fine-scale urban density scores. Furthermore, rural egg volume increased over the laying sequence, but urban egg volume leveled off mid-sequence, suggesting either that urban mothers are resource limited or that they are employing a different brood development strategy than rural mothers. Our study is one of the first to show that egg hormone concentrations differ in an urban environment with differences persisting in chick development and adult life stages. We suggest that maternal endocrine programing may shape offspring phenotypes in urban environments and are an overlooked yet important aspect underlying mechanisms of urban evolution.

Integrating orientation mechanisms, adrenocortical activity, and endurance flight in vagrancy behaviour.

Avian migratory processes are typically precisely oriented, yet vagrants are frequently recorded outside their normal range. Wind displaced vagrants often show corrective behaviour, and as an appropriate response is likely adaptive. We investigated the physiological response to vagrancy in passerines. Activation of the emergency life-history stage (ELHS), assessed by high baseline plasma corticosterone, is a potential mechanism to elicit compensatory behaviour in response to challenges resulting from navigational error, coupled with response to fuel load and flight. We compared circulating plasma corticosterone concentrations and body condition between three migratory groups in autumn: (1) wind displaced southwest (SW) vagrants and (2) long range southeast (SE) vagrants on the remote Faroe Islands, and (3) birds within the expected SW migratory route (controls) on the Falsterbo peninsula, Sweden. Vagrants were further grouped by those sampled immediately upon termination of over-water migratory flight and those already on the island. In all groups there was no indication of the activation of the ELHS in response to vagrancy. We found limited support for an increased rate of corticosterone elevation within our 3 min sample interval in a single species, but this was driven by an individual ELHS outlier. Fat scores were negatively correlated with circulating corticosterone; this relationship may suggest that ELHS activation depends upon an individual's energetic states. Interestingly, in individuals caught at the completion of an obligate long-distance flight, we found some evidence of corticosterone suppression. Although limited, data did support the induction of negative feedback mechanisms that suppress corticosterone during endurance exercise, even when fuel loads are low.

Gene expression of sex steroid metabolizing enzymes and receptors in the skeletal muscle of migrant and resident subspecies of white-crowned sparrow (Zonotrichia leucophrys).

Circulating sex steroid concentrations vary dramatically across the year in seasonally breeding animals. The ability of circulating sex steroids to effect muscle function can be modulated by changes in intracellular expression of steroid metabolizing enzymes (e.g., 5α-reductase type 2 and aromatase) and receptors. Together, these combined changes in plasma hormones, metabolizing enzymes and receptors allow for seasonally appropriate changes in skeletal muscle function. We tested the hypothesis that gene expression of sex steroid metabolizing enzymes and receptors would vary seasonally in skeletal muscle and these changes would differ between a migrant and resident life history strategy. We quantified annual changes in plasma testosterone and gene expression in pectoralis and gastrocnemius skeletal muscles using quantitative polymerase chain reaction (qPCR) in free-living migrant (Zonotrichia leucophrys gambelii) and resident (Z. l. nuttalli) subspecies of white-crowned sparrow during breeding, pre-basic molt, and wintering life history stages. Pectoralis muscle profile was largest in migrants during breeding, while residents maintained large muscle profiles year-round. Circulating testosterone peaked during breeding in both subspecies. Pectoralis muscle androgen receptor mRNA expression was lower in females of both subspecies during breeding. Estrogen receptor-α expression was higher in the pectoralis muscle, but not gastrocnemius, of residents throughout the annual cycle when compared to migrants. Pectoralis aromatase expression was higher in resident males compared to migrant males. No differences were observed for 5α-reductase 2. Between these two subspecies, patterns of plasma testosterone and androgen receptors appear to be conserved, however estrogen receptor gene expression appears to have diverged.

Uncovering the Sex-Specific Endocrine Responses to Reproduction and Parental Care.

Hormones mediate physiological and behavioral changes in adults as they transition into reproduction. In this study, we characterize the circulating levels of five key hormones involved in reproduction in rock doves (Columba livia): corticosterone, progesterone, estradiol, testosterone, and prolactin using univariate and multivariate approaches. We show similar patterns as previous studies in the overall patterns in circulating levels of these hormones, i.e., testosterone (males) and estradiol (females) high during nest-building or egg-laying, prolactin increasing at mid-incubation and peaking at hatching (both sexes), and elevated corticosterone levels in later incubation and early nestling development. In our investigation of hormone co-variation, we find a strong correlation between prolactin and corticosterone across sampling stages and similarities in earlier (early to mid-incubation) compared to later (late incubation to nestling d9) sampling stages in males and females. Finally, we utilized experimental manipulations to simulate nest loss or altered caregiving lengths to test whether external cues, internal timing, or a combination of these factors contributed most to hormone variation. Following nest loss, we found that both males and females responded to the external cue. Males generally responded quickly following nest loss by increasing circulating testosterone, but this response was muted when nest loss occurred early in reproduction. Similar treatment type, e.g., removal of eggs, clustered similarly in hormone space. These results suggest internal drivers limited male response early in reproduction to nest loss. In contrast, circulating levels of these hormones in females either did not change or decreased following nest manipulation suggesting responsiveness to external drivers, but unlike males, this result suggests that reproductive processes were decreasing.

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.

Seasonal differences in hypothalamic thyroid-stimulating hormone ß, gonadotropin-releasing hormone-I and deiodinase expression between migrant and resident subspecies of white-crowned sparrow (Zonotrichia leucophrys).

Across taxa, the seasonal transition between non-breeding and breeding states is controlled by localised thyroid hormone signalling in the deep brain via reciprocal switching of deiodinase enzyme expression from type 3 (DIO3) to type 2 (DIO2). This reciprocal switch is considered to be mediated by increasing thyroid-stimulating hormone ß (TSHß) release from the pars tuberalis, which occurs in response to a change in photoperiod. Although well characterised in a handful of model organisms in controlled laboratory settings, this pathway remains largely unexplored in free-living animals under natural environmental conditions. In this comparative gene expression study, we investigated hypothalamic thyroid hormone signalling in two seasonally breeding subspecies of white-crowned sparrow (Zonotrichia leucophrys), across the entirety of their annual cycles. The migratory Gambel's (Z. l. gambelii) and resident Nuttall's (Z. l. nuttalii) subspecies differ with respect to timing of reproduction, as well as life history stage and migratory strategies. Although DIO3 mRNA expression was elevated and DIO2 mRNA expression was reduced in the wintering period in both subspecies, DIO2 peaked in both subspecies prior to the onset of reproduction. However, there was differential timing between subspecies in peak DIO2 expression. Intriguingly, seasonal modulation of TSHß mRNA was only observed in migrants, where expression was elevated at the start of breeding, consistent with observations from other highly photoperiodic species. There was no correlation between TSHß, DIO2 and gonadotropin-releasing hormone-I mRNA or reproductive metrics in residents. Based on these observed differences, we discuss potential implications for our understanding of how changes in medial basal hypothalamic gene expression mediates initiation of seasonal reproduction.

Isolating the Role of Corticosterone in the Hypothalamic-Pituitary-Gonadal Transcriptomic Stress Response.

Investigation of the negative impacts of stress on reproduction has largely centered around the effects of the adrenal steroid hormone, corticosterone (CORT), and its influence on a system of tissues vital for reproduction-the hypothalamus of the brain, the pituitary gland, and the gonads (the HPG axis). Research on the action of CORT on the HPG axis has predominated the stress and reproductive biology literature, potentially overshadowing other influential mediators. To gain a more complete understanding of how elevated CORT affects transcriptomic activity of the HPG axis, we experimentally examined its role in male and female rock doves (Columba livia). We exogenously administrated CORT to mimic circulating levels during the stress response, specifically 30 min of restraint stress, an experimental paradigm known to increase circulating CORT in vertebrates. We examined all changes in transcription within each level of the HPG axis as compared to both restraint-stressed birds and vehicle-injected controls. We also investigated the differential transcriptomic response to CORT and restraint-stress in each sex. We report causal and sex-specific effects of CORT on the HPG transcriptomic stress response. Restraint stress caused 1567 genes to uniquely differentially express while elevated circulating CORT was responsible for the differential expression of 304 genes. Only 108 genes in females and 8 in males differentially expressed in subjects that underwent restraint stress and those who were given exogenous CORT. In response to elevated CORT and restraint-stress, both sexes shared the differential expression of 5 genes, KCNJ5, CISH, PTGER3, CEBPD, and ZBTB16, all located in the pituitary. The known functions of these genes suggest potential influence of elevated CORT on immune function and prolactin synthesis. Gene expression unique to each sex indicated that elevated CORT affected more gene transcription in females than males (78 genes versus 3 genes, respectively). To our knowledge, this is the first study to isolate the role of CORT in HPG genomic transcription during a stress response. We present an extensive and openly accessible view of the role corticosterone in the HPG transcriptomic stress response. Because the HPG system is well conserved across vertebrates, these data have the potential to inspire new therapeutic strategies for reproductive dysregulation in multiple vertebrate systems, including our own.

Relationships between avian malaria resilience and corticosterone, testosterone and prolactin in a Hawaiian songbird.

Glucocorticoids, androgens, and prolactin regulate metabolism and reproduction, but they also play critical roles in immunomodulation. Since the introduction of avian malaria to Hawaii a century ago, low elevation populations of the Hawaii Amakihi (Chlorodrepanis virens) that have experienced strong selection by avian malaria have evolved increased resilience (the ability to recover from infection), while high elevation populations that have undergone weak selection remain less resilient. We investigated how variation in malaria selection has affected corticosterone, testosterone, and prolactin hormone levels in Amakihi during the breeding season. We predicted that baseline corticosterone and testosterone (which have immunosuppressive functions) would be reduced in low elevation and malaria-infected birds, while stress-induced corticosterone and prolactin (which have immunostimulatory functions) would be greater in low elevation and malaria-infected birds. As predicted, prolactin was significantly higher in malaria-infected than uninfected females (although more robust sample sizes would help to confirm this relationship), while testosterone trended higher in malaria-infected than uninfected males and, surprisingly, neither baseline nor stress-induced CORT varied with malaria infection. Contrary to our predictions, stress-induced corticosterone was significantly lower in low than high elevation birds while testosterone in males and prolactin in females did not vary by elevation, suggesting that Amakihi hormone modulation across elevation is determined by variables other than disease selection (e.g., timing of breeding, energetic challenges). Our results shed new light on relationships between introduced disease and hormone modulation, and they raise new questions that could be explored in experimental settings.

Annual regulation of adrenocortical function in migrant and resident subspecies of white-crowned sparrow.

Corticosterone affects physiology and behavior both during normal daily processes but also in response to environmental challenges and is known to mediate life history trade-offs. Many studies have investigated patterns of corticosterone production at targeted times of year, while ignoring underlying annual profiles. We aimed to understand the annual regulation of hypothalamic-pituitary-adrenal (HPA) axis function of both migrant (Zonotrichia leucophrys gambelii; n = 926) and resident (Z. l. nutalli; n = 688) subspecies of white-crowned sparrow and how it is influenced by environmental conditions - wind, precipitation, and temperature. We predicted that more dramatic seasonal changes in baseline and stress-induced corticosterone would occur in migrants to precisely time the onset of breeding and cope with environmental extremes on their arctic breeding grounds, while changes in residents would be muted as they experience a more forgiving breeding schedule and comparatively benign environmental conditions in coastal California. During the course of a year, the harshest conditions were experienced the summer breeding grounds for migrants, at which point they had higher corticosterone levels compared to residents. For residents, the winter months coincided with harshest conditions at which point they had higher corticosterone levels than migrants. For both subspecies, corticosterone tended to rise as environmental conditions became colder and windier. We found that the annual maxima in stress-induced corticosterone occurred prior to egg lay for all birds except resident females. Migrants had much higher baseline and acute stress-induced corticosterone during breeding compared to residents; where in a harsher environment the timing of the onset of reproduction is more critical because the breeding season is shorter. Interestingly, molt was the only stage within the annual cycle in which subspecies differences were absent suggesting that a requisite reduction in corticosterone may have to be met for feather growth. These data suggest that modulation of the HPA axis is largely driven by environmental factors, social cues, and their potential interactions with a genetic program.

Acute restraint stress does not alter corticosteroid receptors or 11ß-hydroxysteroid dehydrogenase gene expression at hypothalamic-pituitary-adrenal axis regulatory sites in captive male white-crowned sparrows (Zonotrichia leucophrys gambelii).

Capture-restraint is often used to investigate the acute hypothalamic-pituitary-adrenal axis (HPA) response to stress in wild and captive animals through the production of glucocorticoids. Although this approach is useful for understanding changes in glucocorticoids, it overlooks potential changes in the complex regulatory systems associated with the glucocorticoid response, including genomic receptors, steroid metabolizing enzymes, carrier proteins, and downstream target proteins (e.g. gonadotropin-inhibitory hormone; GnIH). The present study in captive male white-crowned sparrows (Zonotrichia leucophrys) tests the hypothesis that corticosteroid receptors (mineralocorticoid - MR and glucocorticoid - GR), 11ß-hydroxysteroid dehydrogenase 1 (11ßHSD1) and 2 (11ßHSD2), corticosteroid binding globulin (CBG), and GnIH undergo rapid changes in expression to mediate the glucocorticoid response to acute stress. To determine dynamic changes in gene mRNA expression in the hippocampus, hypothalamus, pituitary gland, and liver, birds were sampled within 3 min of entering the room and after 10, 30, and 60 min of capture restraint stress in a cloth bag. Restraint stress handling increased CBG and decreased GnIH mRNA expression in the liver and hypothalamus, respectively. MR, GR, 11ßHSD1, and 11ßHSD2 mRNA expression in the brain, pituitary gland, and liver did not change. No correlations were found between gene expression and baseline or stress-induced plasma corticosterone levels. No rapid changes of MR, GR, 11ßHSD1, and 11ßHSD2 mRNA expression during a standardized acute restraint protocol suggests that tissue level sensitivity may remain constant during acute stressors. However, the observed rise in CBG mRNA expression could act to facilitate transport to target tissues or buffer the rise in circulating glucocorticoids. Further studies on tissue specific sensitivity are warranted.

Tissue-specific expression of 11ß-HSD and its effects on plasma corticosterone during the stress response.

The hypothalamic-pituitary-adrenal (HPA) axis is under complex regulatory control at multiple levels. Enzymatic regulation plays an important role in both circulating levels of glucocorticoids and target tissue exposure. Three key enzyme pathways are responsible for the immediate control of glucocorticoids. De novo synthesis of glucocorticoid from cholesterol involves a multistep enzymatic cascade. This cascade terminates with 11ß-hydroxylase, responsible for the final conversion of 11-deoxy precursors into active glucocorticoids. Additionally, 11ß-hydroxysteroid dehydrogenase type 1 (11ß-HSD1) controls regeneration of glucocorticoids from inactive metabolites, providing a secondary source of active glucocorticoids. Localized inactivation of glucocorticoids is under the control of Type 2 11ß-HSD (11ß-HSD2). The function of these enzymes is largely unexplored in wild species, particularly songbirds. Here, we investigated the contribution of both clearance and generation of glucocorticoids to regulation of the hormonal stress response via the use of pharmacological antagonists. Additionally, we mapped 11ß-HSD gene expression. We found 11ß-HSD1 primarily in liver, kidney and adrenal glands, although it was detectable across all tissue types. 11ß-HSD2 was predominately expressed in the adrenal glands and kidney with moderate gonadal and liver expression. Inhibition of glucocorticoid generation by metyrapone was found to decrease levels peripherally, while both peripheral and central administration of the 11ß-HSD2 inhibitor DETC resulted in elevated concentrations of corticosterone. These data suggest that during the stress response, peripheral antagonism of the 11ß-HSD system has a greater impact on circulating glucocorticoid levels than central control. Further studies should aim to elucidate the respective roles of the 11ß-HSD and 11ß-hydroxylase enzymes.

Ontogeny of the adrenocortical response in an extremely altricial bird.

Life history theory predicts that physiological and behavioral responsiveness to stress should be delayed in development until the benefits of heightened reactivity outweigh the costs of potentially chronic glucocorticoid levels. Birds often acquire stress-responsiveness at locomotor independence, however, both stress-responsiveness and locomotor ability are delayed in birds with altricial developmental strategies. Parrots (Psittacidae) are extremely altricial, but it is not known whether they also postpone physiological responsiveness to stress until locomotor independence. We quantified individual variation in baseline and stress-induced plasma corticosterone (CORT) concentrations, the main avian glucocorticoid, in wild green-rumped parrotlets (Forpus passerinus) of Venezuela at four stages of nestling development. Parrotlet neonates are very underdeveloped and compete for parental care among extreme sibling size hierarchies, a competitive scenario that might benefit from early hypothalamic-pituitary-adrenal (HPA) functionality. Nestlings that underwent a standardized restraint stress-treatment showed higher average CORT concentrations compared to baseline in all age groups sampled, and exhibited no evidence of age-related changes in the stress response. This is 2 weeks before locomotor independence and earlier than previously documented for altricial species. Results suggest that precocity of HPA function may be advantageous to growth and survivorship in extremely altricial birds.

Weathering the storm: Do arctic blizzards cause repeatable changes in stress physiology and body condition in breeding songbirds?

Severe weather events are increasing worldwide because of climate change. To cope with severe weather events, vertebrates rely on the stress response which is activated by the hypothalamic-pituitary adrenal (HPA) axis to adjust physiology and behavior. Previous studies have detailed changes in baseline concentrations of the stress hormone corticosterone during a single storm event, but little data exists on how stress physiology and body condition are adjusted as the storm progresses across multiple days. This represents a serious gap in our understanding of how birds respond physiologically over the duration of a storm. We documented arctic snowstorms that occurred over five consecutive years that were endured by Lapland longspurs (Calcarius lapponicus; 2012-2016) and in three consecutive years by white-crowned sparrows (Zonotrichia leucophrys gambelii; 2014-2016). Data were collected on storm-free days, during snowstorms ranging in length from 1 to 3 days, and the day immediately following a snowstorm. The specific aims were to understand how stress physiology, measured at baseline and in response to restraint handling, and body condition changed over multiple days of the storm, and if these responses were consistent across years. Snowstorms did not affect baseline corticosterone concentrations for either species except for female Lapland longspurs and male white-crowned sparrows in 2014. Lapland longspurs, regardless of sex, increased stress-induced (restraint handling) corticosterone in response to snowstorms in all years but 2013, which was characterized by unusually harsh conditions. Both sexes of White-crowned sparrows showed a significant increase in the stress-induced levels of corticosterone during snowstorms in one of the three years of the study. Stress-induced corticosterone concentrations were only different across each day of the storm in one year of the study for Lapland longspurs. Changes in fat and body mass were not uniform across years, but measurable increases in fat stores and body mass were detected in males of both species during the first day of a snowstorm with declines typically occurring by the second day. Our study showed that severe weather events often caused rapid increases in HPA axis activity and body condition, but these profiles are likely dependent upon ecological and environmental context within the breeding season.

Eavesdropping on the Arctic: Automated bioacoustics reveal dynamics in songbird breeding phenology.

Bioacoustic networks could vastly expand the coverage of wildlife monitoring to complement satellite observations of climate and vegetation. This approach would enable global-scale understanding of how climate change influences phenomena such as migratory timing of avian species. The enormous data sets that autonomous recorders typically generate demand automated analyses that remain largely undeveloped. We devised automated signal processing and machine learning approaches to estimate dates on which songbird communities arrived at arctic breeding grounds. Acoustically estimated dates agreed well with those determined via traditional surveys and were strongly related to the landscape's snow-free dates. We found that environmental conditions heavily influenced daily variation in songbird vocal activity, especially before egg laying. Our novel approaches demonstrate that variation in avian migratory arrival can be detected autonomously. Large-scale deployment of this innovation in wildlife monitoring would enable the coverage necessary to assess and forecast changes in bird migration in the face of climate change.

Contrasting seasonal and aseasonal environments across stages of the annual cycle in the rufous-collared sparrow, Zonotrichia capensis: Differences in endocrine function, proteome and body condition.

The timing and duration of life-history stages (LHSs) within the annual cycle can be affected by local environmental cues which are integrated through endocrine signalling mechanisms and changes in protein function. Most animals express a single LHS within a given period of the year because synchronous expression of LHSs is thought to be too costly energetically. However, in very rare and extremely stable conditions, breeding and moult have been observed to overlap extensively in rufous-collared sparrows (Zonotrichia capensis) living in valleys of the Atacama Desert-one of the most stable and aseasonal environments on Earth. To examine how LHS traits at different levels of organization are affected by environmental variability, we compared the temporal organization and duration of LHSs in populations in the Atacama Desert with those in the semiarid Fray Jorge National Park in the north of Chile-an extremely seasonal climate but with unpredictable droughts and heavy rainy seasons. We studied the effects of environmental variability on morphological variables related to body condition, endocrine traits and proteome. Birds living in the seasonal environment had a strict temporal division of LHSs, while birds living in the aseasonal environment failed to maintain a temporal division of LHSs resulting in direct overlap of breeding and moult. Further, higher circulating glucocorticoids and androgen concentrations were found in birds from seasonal compared to aseasonal populations. Despite these differences, body condition variables and protein expression were not related to the degree of seasonality but rather showed a strong relationship with hormone levels. These results suggest that animals adjust to their environment through changes in behavioural and endocrine traits and may be limited by less labile traits such as morphological variables or expression of specific proteins under certain circumstances. These data on free-living birds shed light on how different levels of life-history organization within an individual are linked to increasing environmental heterogeneity.

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.