Heather E. Watts

Synopsis: Glucocorticoids facilitate the integration of environmental information and coordination of organismal responses to perturbations. Circulating glucocorticoids are hypothesized to depend on an individual’s environment and condition (i.e., state) to facilitate surviving challenges while minimizing fitness costs. Studies specifically focused on sources of individual variation in circulating glucocorticoids are critical to understanding state-dependent modulation of glucocorticoids and integrated phenotypes more broadly. Such studies can also provide insight into the evolution and adaptive significance of circulating glucocorticoids. Here, we repeatedly sample individuals before and during food restriction to identify how and when food availability and intrinsic differences (i.e., body condition and telomere length), including those of social partners, covary with glucocorticoids in captive Red Crossbills (Loxia curvirostra), a nomadic songbird that specializes on foraging for conifer seeds. Conifer seeds are ephemeral resources produced during unpredictable, but locally synchronous, masting events. Fluctuating food availability and social cues, change the behavior and glucocorticoid physiology of Red Crossbills. Pairs consisting of an adult and juvenile were food restricted using an environmental manipulation known to induce socially mediated changes in glucocorticoid signaling. Baseline and stress-induced glucocorticoids were measured before and during food restriction. Amongst adults, stress-induced glucocorticoids declined following food restriction and positively covaried with telomere length, independent of food availability. These results support the hypothesis that the acute glucocorticoid response is adaptively modulated based on environmental conditions and individual differences in state as measured by telomere length. Under food restriction, juvenile baseline glucocorticoids negatively covaried with body condition and the telomere lengths of adult social partners. The covariation between adult telomere lengths and juvenile baseline glucocorticoids suggests that telomere lengths of adults may relate to adult phenotypes, a hypothesis supported by the covariation between adult telomeres and stress-induced glucocorticoids. Further, as patterns were absent before food restriction, our results demonstrate how environmental challenges can reveal the importance of intrinsic differences to organismal responses and social cues. This study leverages a non-model organism experiencing an ecologically relevant environmental challenge to exemplify how intrinsic differences, including those of social partners, can modulate an endocrine mediator of organismal responses to environmental perturbations.

Social information (ie gathered from other individuals) can be an important information source for animal decision-making related to foraging and movement. For instance, social information in the form of acoustic cues can be used to locate food sources. The ability to accurately assess declines in food availability or quality in order to make movement decisions can also impact fitness. However, little is known about whether the acoustic cues produced by animals differ when food is in decline and could therefore be used as a source of information in this context. To test this hypothesis, we conducted a study on the effect of food availability on the vocal behavior of pine siskin (Spinus pinus). Pine siskins are gregarious, nomadic finches that feed on seeds that fluctuate irregularly and dramatically in abundance. We recorded and characterized the vocalizations of wild-caught birds in captivity under two experimental conditions: unlimited food and a 20% reduction in food availability. Birds called more frequently when food restricted and increased the production of two specific types of calls (Types B and C). For both of these call types, the minimum frequency was higher when birds were food restricted, and for C calls the median, peak dominant, and peak fundamental frequencies were also higher. We further tested whether changes in acoustic frequency were associated with circulating corticosterone levels, as is predicted by the hypothesis that circulating glucocorticoid levels mediate changes in acoustic frequency in response to food restriction, and found only limited evidence to support the hypothesis.

Urbanization reflects a major form of environmental change impacting wild birds globally. Whereas urban habitats may provide increased availability of water, some food items, and reduced predation levels compared to rural, they can also present novel stressors including increased light at night, ambient noise, and reduced nutrient availability. Urbanization can also alter levels of brood parasitism, with some host species experiencing elevated levels of brood parasitism in urban areas compared to rural areas. Though the demographic and behavioral consequences of urbanization and brood parasitism have received considerable attention, their consequences for cellular‐level processes are less understood. Telomeres provide an opportunity to understand the cellular consequences of different environments as they are a well‐established metric of biological state that can be associated with residual lifespan, disease risk, and behavior, and are known to be sensitive to environmental conditions. Here we examine the relationships between urbanization, brood parasitism, and blood telomere lengths in adult and nestling song sparrows Melospiza melodia . Song sparrows are a North American songbird found in both urban and rural habitats that experience high rates of brood parasitism by brown‐headed cowbirds Molothrus ater in the urban, but not the rural, sites in our study system. Among adults and nestlings from non‐parasitized nests, we found no differences in relative telomere lengths between urban and rural habitats. However, among urban nestlings, the presence of a brood parasite in the nest was associated with significantly shorter relative telomere lengths compared to when a brood parasite was absent. Our results suggest a novel, indirect, impact of urbanization on nestling songbirds through the physiological impacts of brood parasitism.

Temperate winters can impose severe conditions on songbirds that threaten survival, including shorter days and often lower temperatures and food availability. One well-studied mechanism by which songbirds cope with such conditions is seasonal acclimatization of thermal metabolic traits, with strong evidence for both preparative and responsive changes in thermogenic capacity (i.e., the ability to generate heat) to low winter temperatures. However, a bird’s ability to cope with seasonal extremes or unpredictable events is likely dependent on a combination of behavioral and physiological traits that function to maintain allostatic balance. The ability to cope with reduced food availability may be an important component of organismal response to temperate winters in songbirds. Here, we compare responses to experimentally reduced food availability at different times of year in captive red crossbills (Loxia curvirostra) and pine siskins (Spinus pinus)—two species that cope with variable food resources and live in cold places—to investigate seasonal changes in the organismal response to food availability. Further, red crossbills are known to use social information to improve responses to reduced food availability, so we also examine whether the use of social information in this context varies seasonally in this species. We find that pine siskins and red crossbills lose less body mass during time-restricted feedings in late winter compared to summer, and that red crossbills further benefit from social information gathered from observing other food-restricted red crossbills in both seasons. Observed changes in body mass were only partially explained by seasonal differences in food intake. Our results demonstrate seasonal acclimation to food stress and social information use across seasons in a controlled captive environment and highlight the importance of considering diverse physiological systems (e.g., thermogenic, metabolic, digestive, etc.) to understand organismal responses to environmental challenges.

Many animals rely on photoperiodic and non-photoperiodic environmental cues to gather information and appropriately time life-history stages across the annual cycle, such as reproduction, molt, and migration. Here, we experimentally demonstrate that the reproductive physiology, but not migratory behavior, of captive Pine Siskins (Spinus pinus) responds to both food and social cues during the spring migratory-breeding period. Pine Siskins are a nomadic finch with a highly flexible breeding schedule and, in the spring, free-living Pine Siskins can wander large geographic areas and opportunistically breed. To understand the importance of non-photoperiodic cues to the migratory-breeding transition, we maintained individually housed birds on either a standard or enriched diet in the presence of group-housed heterospecifics or conspecifics experiencing either the standard or enriched diet type. We measured body condition and reproductive development of all Pine Siskins and, among individually housed Pine Siskins, quantified nocturnal migratory restlessness. In group-housed birds, the enriched diet caused increases in body condition and, among females, promoted reproductive development. Among individually housed birds, female reproductive development differed between treatment groups whereas male reproductive development did not. Specifically, individually housed females showed greater reproductive development when presented with conspecifics compared to heterospecifics. The highest rate of female reproductive development, however, was observed among individually housed females provided the enriched diet and maintained with group-housed conspecifics on an enriched diet. Changes in nocturnal migratory restlessness did not vary by treatment group or sex. By manipulating both the physical and social environment, this study demonstrates how multiple environmental cues can affect the timing of transitions between life-history stages with differential responses between sexes and between migratory and reproductive systems.

Our understanding of state-dependent behaviour is reliant on identifying physiological indicators of condition. Telomeres are of growing interest for understanding behaviour as they capture differences in biological state and residual lifespan. To understand the significance of variable telomere lengths for behaviour and test two hypotheses describing the relationship between telomeres and behaviour (i.e. the causation and the selective adoption hypotheses), we assessed if telomere lengths are longitudinally repeatable traits related to spring migratory behaviour in captive pine siskins ( Spinus pinus ). Pine siskins are nomadic songbirds that exhibit highly flexible, facultative migrations, including a period of spring nomadism. Captive individuals exhibit extensive variation in spring migratory restlessness and are an excellent system for mechanistic studies of migratory behaviour. Telomere lengths were found to be significantly repeatable ( R = 0.51) over four months, and shorter pre-migratory telomeres were associated with earlier and more intense expression of spring nocturnal migratory restlessness. Telomere dynamics did not vary with migratory behaviour. Our results describe the relationship between telomere length and migratory behaviour and provide support for the selective adoption hypothesis. More broadly, we provide a novel perspective on the significance of variable telomere lengths for animal behaviour and the timing of annual cycle events.