Climate change is altering the physiology and phenology of an arctic hibernator.

Climate warming is rapid in the Arctic, yet impacts to biological systems are unclear because few long-term studies linking biophysiological processes with environmental conditions exist for this data-poor region. In our study spanning 25 years in the Alaskan Arctic, we demonstrate that climate change is affecting the timing of freeze-thaw cycles in the active layer of permafrost soils and altering the physiology of arctic ground squirrels (Urocitellus parryii). Soil freeze has been delayed and, in response, arctic ground squirrels have delayed when they up-regulate heat production during torpor to prevent freezing. Further, the termination of hibernation in spring has advanced 4 days per decade in females but not males. Continued warming and phenological shifts will alter hibernation energetics, change the seasonal availability of this important prey species, and potentially disrupt intraspecific interactions.

Songbirds initiate migratory flights synchronously relative to civil dusk.

BACKGROUND: Each spring and fall billions of songbirds depart on nocturnal migrations across the globe. Theory suggests that songbirds should depart on migration shortly after sunset to maximize their potential for nightly flight duration or to time departure with the emergence of celestial cues needed for orientation and navigation. Although captive studies have found that songbirds depart during a narrow window of time after sunset, observational studies have found that wild birds depart later and more asynchronously relative to sunset than predicted. METHODS: We used coded radio tags and automated radio-telemetry to estimate the time that nearly 400 individuals from nine songbird species departed their breeding or wintering grounds across North America. We also assessed whether each species was most likely beginning long-distance migratory flights at departure or instead first making non-migratory regional flights. We then explored variation in nocturnal departure time by post-departure movement type, species, age, sex, and season. RESULTS: We found that 90% of individuals from species that were likely initiating long-distance migratory flights departed within 69 min of civil dusk, regardless of species, season, age, or sex. By contrast, species that likely first made non-migratory regional movements away from the migratory destination departed later and more asynchronously throughout the night. Regardless of post-departure movement type, 98% of individuals departed after civil dusk but otherwise showed no preference in relation to twilight phase. CONCLUSIONS: Although the presence of celestial orientation cues at civil dusk may set a starting point for departure each night, the fact that species likely beginning long-distance migration departed earlier and more synchronously relative to civil dusk than those first making non-migratory regional movements is consistent with the hypothesis that departing promptly after civil dusk functions to maximize the potential for nightly flight duration and distance. By studying the onset of migration, our study provides baseline information about departure decisions that may enhance our understanding of departure timing throughout migration.

Effects of Spring Warming on Seasonal Neuroendocrinology and Activation of the Reproductive Axis in Hibernating Arctic Ground Squirrels.

Many animals adjust the timing of seasonal events, such as reproduction, molt, migration, and hibernation, in response to interannual variation and directional climate-driven changes in temperature. However, the mechanisms by which temperature influences seasonal timing are relatively under-explored. Seasonal timing involves retrograde signaling in which thyrotropin (TSH) in the pars tuberalis (PT) alters expression of thyroid hormone (TH) deiodinases (Dio2/Dio3) in tanycyte cells lining the third ventricle of the hypothalamus. This, in turn, affects the availability of triiodothyronine (T3) within the mediobasal hypothalamus-increased hypothalamic T3 restores a summer phenotype and activates the reproductive axis in long-day breeders. Recently, we showed that retrograde TH signaling is activated during late hibernation in arctic ground squirrels (Urocitellus parryii) held in constant darkness and constant ambient temperature. Sensitivity of seasonal pathways to nonphotic cues, such as temperature, is likely particularly important to hibernating species that are sequestered in hibernacula during spring. To address this issue, we exposed captive arctic ground squirrels of both sexes to an ecologically relevant increase in ambient temperature (from -6 to -1°C) late in hibernation and examined the effects of warming on the seasonal retrograde TSH/Dio/T3 signaling pathway, as well as downstream elements of the reproductive axis. We found that warmed males tended to have higher PT TSHß expression and significantly heavier testis mass whereas the TSH/Dio/T3 signaling pathway was unaffected by warming in females, although warmed females exhibited a slight decrease in ovarian mass. Our findings suggest that temperature could have different effects on gonadal growth in male and female arctic ground squirrels, which could lead to mismatched timing in response to rapid climate change.

A cross-taxonomic perspective on the integration of temperature cues in vertebrate seasonal neuroendocrine pathways.

The regulation of seasonality has been an area of interest for decades, yet global climate change has created extra urgency in the quest to understand how sensory circuits and neuroendocrine control systems interact to generate flexibility in biological timekeeping. The capacity of temperature to alter endogenous or photoperiod-regulated neuroendocrine mechanisms driving seasonality, either as a direct cue or through temperature-dependent effects on energy and metabolism, is at the heart of this phenological flexibility. However, until relatively recently, little research had been done on the integration of temperature information in canonical seasonal neuroendocrine pathways, particularly in vertebrates. We review recent advances from research in vertebrates that deepens our understanding of how temperature cues are perceived and integrated into seasonal hypothalamic thyroid hormone (TH) signaling, which is a critical regulator of downstream seasonal phenotypic changes such as those regulated by the BPG (brain-pituitary-gonadal) axis. Temperature perception occurs through cutaneous transient receptor potential (TRP) neurons, though sensitivity of these neurons varies markedly across taxa. Although photoperiod is the dominant cue used to trigger seasonal physiology or entrain circannual clocks, across birds, mammals, fish, reptiles and amphibians, seasonality appears to be temperature sensitive and in at least some cases this appears to be related to phylogenetically conserved TH signaling in the hypothalamus. Nevertheless, the exact mechanisms through which temperature modulates seasonal neuroendocrine pathways remains poorly understood.

Hypothalamic remodeling of thyroid hormone signaling during hibernation in the arctic ground squirrel.

Hibernation involves prolonged intervals of profound metabolic suppression periodically interrupted by brief arousals to euthermy, the function of which is unknown. Annual cycles in mammals are timed by a photoperiodically-regulated thyroid-hormone-dependent mechanism in hypothalamic tanycytes, driven by thyrotropin (TSH) in the pars tuberalis (PT), which regulates local TH-converting deiodinases and triggers remodeling of neuroendocrine pathways. We demonstrate that over the course of hibernation in continuous darkness, arctic ground squirrels (Urocitellus parryii) up-regulate the retrograde TSH/Deiodinase/TH pathway, remodel hypothalamic tanycytes, and activate the reproductive axis. Forcing the premature termination of hibernation by warming animals induced hypothalamic deiodinase expression and the accumulation of secretory granules in PT thyrotrophs and pituitary gonadotrophs, but did not further activate the reproductive axis. We suggest that periodic arousals may allow for the transient activation of hypothalamic thyroid hormone signaling, cellular remodeling, and re-programming of brain circuits in preparation for the short Arctic summer.

Sex-Differences in Phenology: A Tinbergian Perspective.

Shifts in the timing of cyclic seasonal life-history events are among the most commonly reported responses to climate change, with differences in response rates among interacting species leading to phenological mismatches. Within a species, however, males and females can also exhibit differential sensitivity to environmental cues and may, therefore, differ in their responsiveness to climate change, potentially leading to phenological mismatches between the sexes. This occurs because males differ from females in when and how energy is allocated to reproduction, resulting in marked sex-differences in life-history timing across the annual cycle. In this review, we take a Tinbergian perspective and examine sex-differences in timing of vertebrates from adaptive, ontogenetic, mechanistic, and phylogenetic viewpoints with the goal of informing and motivating more integrative research on sexually dimorphic phenologies. We argue that sexual and natural selection lead to sex-differences in life-history timing and that understanding the ecological and evolutionary drivers of these differences is critical for connecting climate-driven phenological shifts to population resilience. Ontogeny may influence how and when sex-differences in life-history timing arise because the early-life environment can profoundly affect developmental trajectory, rates of reproductive maturation, and seasonal timing. The molecular mechanisms underlying these organismal traits are relevant to identifying the diversity and genetic basis of population- and species-level responses to climate change, and promisingly, the molecular basis of phenology is becoming increasingly well-understood. However, because most studies focus on a single sex, the causes of sex-differences in phenology critical to population resilience often remain unclear. New sequencing tools and analyses informed by phylogeny may help generate hypotheses about mechanism as well as insight into the general "evolvability" of sex-differences across phylogenetic scales, especially as trait and genome resources grow. We recommend that greater attention be placed on determining sex-differences in timing mechanisms and monitoring climate change responses in both sexes, and we discuss how new tools may provide key insights into sex-differences in phenology from all four Tinbergian domains.

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.

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.

Extreme spring conditions in the Arctic delay spring phenology of long-distance migratory songbirds.

Arctic regions are warming rapidly, with extreme weather events increasing in frequency, duration, and intensity just as in other regions. Many studies have focused on how shifting seasonality in environmental conditions affects vegetation phenology, while far fewer have examined how the breeding phenology of arctic fauna responds. We studied two species of long-distance migratory songbirds, Lapland longspurs, Calcarius lapponicus, and white-crowned sparrows, Zonotrichia leucophrys gambelii, across five consecutive breeding seasons in northern Alaskan tundra. We aimed to understand how spring environmental conditions affected breeding cycle phenology, including the timing of arrival on breeding grounds, territory establishment, and clutch initiation. Spring temperatures, precipitation, and snow-free dates differed significantly among years, with 2013 characterized by unusually late snow cover. In response, we found a significant delay in breeding-cycle phenology for both study species in 2013 relative to other study years: the first bird observed was delayed by 6-10 days, with mean arrival by 3-6 days, territory establishment by 6-13 days, and clutch initiation by 4-10 days. Further, snow cover, temperature, and precipitation during the territory establishment period were important predictors of clutch initiation dates for both species. These findings suggest that Arctic-breeding passerine communities may have the flexibility required to adjust breeding phenology in response to the increasingly extreme and unpredictable environmental conditions-although future generations may encounter conditions that exceed their current range of phenological flexibility.

Effects of a social cue on reproductive development and pre-alternate molt in seasonally breeding migrant and resident female songbirds (Zonotrichia leucophrys).

To time reproduction optimally, birds have evolved diverse mechanisms by which they respond to environmental changes that help them anticipate and prepare for the breeding season. While residents initiate reproductive preparation and breed in the same geographic location, migrant birds simultaneously prepare for breeding and migration far from their breeding grounds. As a result, it is hypothesized that migrant and resident birds use environmental cues differently to prepare to breed and that there is adaptive specialization in mechanisms regulating reproductive preparation. Specifically, residents are expected to rely more on non-photic cues (e.g. food, temperature, social cues) than migrants. We tested this general prediction using a social cue manipulation. First, we compared the effects of subspecies-appropriate recorded male song on reproductive development in migrants and residents on a naturally increasing photoperiod. Second, we tested the sensitivity of migrant-specific life history events (fattening and pre-alternate molt) to song treatment. After 82 days, residents had higher luteinizing hormone and greater ovarian development than migrants, but song treatment had no effect on these metrics in either subspecies. Song advanced pre-alternate molt but had no effect on fattening in migrants. While our study does not support specialization in social cue use in migrants and residents, it is consistent with findings in the literature of specialization in photoperiodic response. It also demonstrates for the first time that social cues can influence molt in a migrant species. Additional findings from a pilot study looking at responses to a live male suggest it is important to test other kinds of social cues.

How birds cope physiologically and behaviourally with extreme climatic events.

As global climate change progresses, the occurrence of potentially disruptive climatic events such as storms are increasing in frequency, duration and intensity resulting in higher mortality and reduced reproductive success. What constitutes an extreme climatic event? First we point out that extreme climatic events in biological contexts can occur in any environment. Focusing on field and laboratory data on wild birds we propose a mechanistic approach to defining and investigating what extreme climatic events are and how animals cope with them at physiological and behavioural levels. The life cycle of birds is made up of life-history stages such as migration, breeding and moult that evolved to match a range of environmental conditions an individual might expect during the year. When environmental conditions deteriorate and deviate from the expected range then the individual must trigger coping mechanisms (emergency life-history stage) that will disrupt the temporal progression of life-history stages, but enhance survival. Using the framework of allostasis, we argue that an extreme climatic event in biological contexts can be defined as when the cumulative resources available to an individual are exceeded by the sum of its energetic costs-a state called allostatic overload. This allostatic overload triggers the emergency life-history stage that temporarily allows the individual to cease regular activities in an attempt to survive extreme conditions. We propose that glucocorticoid hormones play a major role in orchestrating coping mechanisms and are critical for enduring extreme climatic events.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'.

The effect of extreme spring weather on body condition and stress physiology in Lapland longspurs and white-crowned sparrows breeding in the Arctic.

Climate change is causing rapid shifts in temperature while also increasing the frequency, duration, and intensity of extreme weather. In the northern hemisphere, the spring of 2013 was characterized as extreme due to record high snow cover and low temperatures. Studies that describe the effects of extreme weather on phenology across taxa are limited while morphological and physiological responses remain poorly understood. Stress physiology, as measured through baseline and stress-induced concentrations of cortisol or corticosterone, has often been studied to understand how organisms respond to environmental stressors. We compared body condition and stress physiology of two long-distance migrants breeding in low arctic Alaska - the white-crowned sparrow (Zonotrichia leucophrys) and Lapland longspur (Calcarius lapponicus) - in 2013, an extreme weather year, with three more typical years (2011, 2012, and 2014). The extended snow cover in spring 2013 caused measureable changes in phenology, body condition and physiology. Arrival timing for both species was delayed 4-5days compared to the other three years. Lapland longspurs had reduced fat stores, pectoralis muscle profiles, body mass, and hematocrit levels, while stress-induced concentrations of corticosterone were increased. Similarly, white-crowned sparrows had reduced pectoralis muscle profiles and hematocrit levels, but in contrast to Lapland longspurs, had elevated fat stores and no difference in mass or stress physiology relative to other study years. An understanding of physiological mechanisms that regulate coping strategies is of critical importance for predicting how species will respond to the occurrence of extreme events in the future due to global climate change.

The stress response is attenuated during inclement weather in parental, but not in pre-parental, Lapland longspurs (Calcarius lapponicus) breeding in the Low Arctic.

Birds breeding at high latitudes can be faced with extreme weather events throughout the breeding season. In response to environmental perturbations, vertebrates activate the hypothalamic-pituitary-adrenal (HPA) axis and synthesize corticosterone, which promotes changes in behavior and physiology to help the animal survive. The parental care hypothesis suggests that the HPA axis activity should be downregulated during the parental stage of breeding to prevent nest abandonment. However, it is unknown what happens to HPA axis activity in response to severe weather at the transition from the pre-parental to parental stages of breeding. We sampled baseline corticosterone levels and the time course of corticosterone elevation over 60min of restraint stress and assessed body condition and fat stores in Lapland longspurs (Calcarius lapponicus) breeding in the Low Arctic in the presence and absence of snowstorms. The results showed that during the pre-parental stage, HPA axis activity was up-regulated in response to snowstorms, with corticosterone levels continuing to increase through 60min of restraint. However, once birds were parental, HPA axis activity was unaffected by snowstorms and levels peaked at 10min. Fat levels and body condition did not change in response to snowstorms but fat levels declined in males during the pre-parental stage. These data suggest that the parental care hypothesis can be applied to severe storm events; parental birds restrained the activity of the HPA axis, likely to focus on the reproductive effort that is already underway, while pre-parental birds greatly upregulated HPA axis activity in response to snowstorms to maximize self-preservation.

Annual Hematocrit Profiles in Two Subspecies of White-Crowned Sparrow: A Migrant and a Resident Comparison.

Hematocrit is an easily measured parameter that can be used to assess changes in oxygen carrying capacity necessitated by fluctuations in metabolic demands. Most hematocrit studies draw conclusions from changes in hematocrit that occur over a small sampling interval without an understanding of the variation that exists across the annual cycle. White-crowned sparrows provide an excellent model system due to the existence of a resident subspecies (Zonotrichia leucophrys nuttalli) that serves as a natural control for a migrant subspecies (Zonotrichia leucophrys gambelii). Comparing these two subspecies allows for the investigation of adaptive physiological changes at each life-history stage (i.e., migration, breeding, molt, etc.) in response to changing metabolic demands. Of particular interest, this subspecies comparison, by both calendar month and life-history stage, allows for the separation of adaptive increases in hematocrit due to migration from the natural seasonal variation in hematocrit. Hematocrit levels for males and females ranged throughout the year between 42%-47% and 40%-47% in the resident and between 45%-58% and 45%-56% in the migrant. In both subspecies, hematocrit levels were elevated during the breeding season compared to the nonbreeding season, and levels were reduced in females during egg laying. When grouped by life-history stage, hematocrit levels were always higher in the migrant compared to the resident. During the months in which migration occurred, hematocrit levels were 10%-12% higher in the migrant compared to the resident subspecies. These data suggest differential regulation of hematocrit between the two subspecies that may be attributed to phenotypic plasticity or genetic differences.

Breeding on the leading edge of a northward range expansion: differences in morphology and the stress response in the arctic Gambel's white-crowned sparrow.

Individuals at the forefront of a range shift are likely to exhibit phenotypic traits that distinguish them from the population breeding within the historic range. Recent studies have examined morphological, physiological and behavioral phenotypes of individuals at the edge of their range. Several studies have found differences in the hypothalamic-pituitary-adrenal (HPA) axis activity in response to acute restraint stress in individuals at the range limits. HPA axis activation leads to elevations in glucocorticoids that regulate physiology and behavior. Here we compare the hormonal profiles and morphometrics from Gambel's white-crowned sparrows (Zonotrichia leucophrys gambelii) breeding at the northern limit of the population's range to those birds breeding within the historic population range. Birds breeding at the northern limit experienced a harsher environment with colder temperatures; however, we found no differences in arthropod prey biomass between the northern limit and more southern (historic) sites. Males at the northern limit had higher body condition scores (mass corrected for body size) compared to individuals within the historic range, but no differences were found in beak and tarsus lengths, wing chord, muscle profile or fat stores. In males during the pre-parental stage, before breeding commenced, HPA axis activity was elevated in birds at the northern limit of the range, but no differences were found during the parental or molt stages. Females showed no differences in HPA axis activity during the parental stage. This study suggests that "pioneering" individuals at the limits of their breeding range exhibit physiology and morphology that are distinct from individuals within the historic range.

Greater shrub dominance alters breeding habitat and food resources for migratory songbirds in Alaskan arctic tundra.

Climate warming is affecting the Arctic in multiple ways, including via increased dominance of deciduous shrubs. Although many studies have focused on how this vegetation shift is altering nutrient cycling and energy balance, few have explicitly considered effects on tundra fauna, such as the millions of migratory songbirds that breed in northern regions every year. To understand how increasing deciduous shrub dominance may alter breeding songbird habitat, we quantified vegetation and arthropod community characteristics in both graminoid and shrub dominated tundra. We combined measurements of preferred nest site characteristics for Lapland longspurs (Calcarius lapponicus) and Gambel's White-crowned sparrows (Zonotrichia leucophrys gambelii) with modeled predictions for the distribution of plant community types in the Alaskan arctic foothills region for the year 2050. Lapland longspur nests were found in sedge-dominated tussock tundra where shrub height does not exceed 20 cm, whereas White-crowned sparrows nested only under shrubs between 20 cm and 1 m in height, with no preference for shrub species. Shrub canopies had higher canopy-dwelling arthropod availability (i.e. small flies and spiders) but lower ground-dwelling arthropod availability (i.e. large spiders and beetles). Since flies are the birds' preferred prey, increasing shrubs may result in a net enhancement in preferred prey availability. Acknowledging the coarse resolution of existing tundra vegetation models, we predict that by 2050 there will be a northward shift in current White-crowned sparrow habitat range and a 20-60% increase in their preferred habitat extent, while Lapland longspur habitat extent will be equivalently reduced. Our findings can be used to make first approximations of future habitat change for species with similar nesting requirements. However, we contend that as exemplified by this study's findings, existing tundra modeling tools cannot yet simulate the fine-scale habitat characteristics that are critical to accurately predicting future habitat extent for many wildlife species.