Graham D. Fairhurst

Experimental relationships between levels of corticosterone in plasma and feathers in a free-living bird

SUMMARY Integrated measures of corticosterone (CORT), such as from feathers (CORTf), have intuitive appeal because they incorporate both the duration and amplitude of glucocorticoid secretion. An association between CORTf and plasma CORT has never been shown in wild birds, and it is unclear as to when and whether these measures should be correlated, given that they are fundamentally different yet related measures of physiology. We hypothesized that CORTf should correlate with instantaneous measurements of plasma CORT when the latter reflect sustained changes in the activity of the hypothalamic–pituitary–adrenal (HPA) axis. To test this, we experimentally manipulated levels of plasma CORT in wild nestling tree swallows (Tachycineta bicolor) using 5 day time-release CORT pellets, and measured plasma CORT and growth parameters before, during and at the end of hormone manipulation (days 7, 9 and 11 post-hatch, respectively). CORTf and plasma CORT were significantly positively related only when the latter was at its highest and most variable among individuals (day 9). A similar relationship was expected at day 11, but plasma CORT had returned to near-original levels. Nestlings with higher CORTf were smaller, lighter and less likely to fledge, but we did not detect seasonal effects on CORTf. Our results clearly demonstrate that CORTf from free-living birds can reflect plasma CORT, but correlations may not always be expected, especially if elevations in plasma CORT are relatively modest and of short duration. Our work suggests that CORTf is best used to study the activity of the HPA axis over relatively long time frames and can be used effectively to advance avian ecology.

Variation in immune function, body condition, and feather corticosterone in nestling Tree Swallows (Tachycineta bicolor) on reclaimed wetlands in the Athabasca oil sands, Alberta, Canada.

In the Athabasca oil sands region of northern Alberta, mining companies are evaluating reclamation using constructed wetlands for integration of tailings. From May to July 2008, reproductive performance of 40 breeding pairs of tree swallows (Tachycineta bicolor), plus growth and survival of nestlings, was measured on three reclaimed wetlands on two oil sands leases. A subset of nestlings was examined for i) feather corticosterone levels, ii) delayed-type hypersensitivity response, and iii) innate immune function. Nestlings on one of two wetlands created with oil sands process affected material (OSPM) were heavier and had greater wing-lengths, and mounted a stronger delayed-type hypersensitivity response compared those on the reference wetland. Corticosterone was significantly higher in male nestlings on one of two OSPM-containing wetland compared to the reference wetland. Body condition of 12-day-old female nestlings was inversely related to feather corticosterone. Under ideal weather conditions, reclaimed wetlands can support healthy populations of aerially-insectivorous birds.

Does Environmental Enrichment Reduce Stress? An Integrated Measure of Corticosterone from Feathers Provides a Novel Perspective

Enrichment is widely used as tool for managing fearfulness, undesirable behaviors, and stress in captive animals, and for studying exploration and personality. Inconsistencies in previous studies of physiological and behavioral responses to enrichment led us to hypothesize that enrichment and its removal are stressful environmental changes to which the hormone corticosterone and fearfulness, activity, and exploration behaviors ought to be sensitive. We conducted two experiments with a captive population of wild-caught Clarks nutcrackers (Nucifraga columbiana) to assess responses to short- (10-d) and long-term (3-mo) enrichment, their removal, and the influence of novelty, within the same animal. Variation in an integrated measure of corticosterone from feathers, combined with video recordings of behaviors, suggests that how individuals perceive enrichment and its removal depends on the duration of exposure. Short- and long-term enrichment elicited different physiological responses, with the former acting as a stressor and birds exhibiting acclimation to the latter. Non-novel enrichment evoked the strongest corticosterone responses of all the treatments, suggesting that the second exposure to the same objects acted as a physiological cue, and that acclimation was overridden by negative past experience. Birds showed weak behavioral responses that were not related to corticosterone. By demonstrating that an integrated measure of glucocorticoid physiology varies significantly with changes to enrichment in the absence of agonistic interactions, our study sheds light on potential mechanisms driving physiological and behavioral responses to environmental change.

Feather corticosterone of a nestling seabird reveals consequences of sex-specific parental investment

Offspring of long-lived species should face costs of parental trade-offs that vary with overall energetic demands encountered by parents during breeding. If sex differences exist in how parents make the trade-off, sex-specific differences may exist in the contribution of each parent to those costs. Adaptations of offspring facing such costs are not well understood, but the hormone corticosterone probably plays a role. We manipulated breeding effort in Corys shearwaters (Calonectris diomedea) to increase costs to offspring and used an integrated measure of corticosterone from chick feathers to investigate how experimental variation in parental investment influences offspring physiology. Average foraging trip duration and foraging efficiency (FE) of breeding pairs were not related to chick corticosterone, but sex biases in FE were. Adult male investment was more strongly related to chick corticosterone than was female investment. Importantly, we show for the first time suppression of adrenocortical activity in nestling Procellariiform seabirds, and explain how our results indicate an adaptive mechanism invoked by chicks facing increased costs of parental trade-offs.

Measuring corticosterone in feathers: Strengths, limitations, and suggestions for the future.

The recently introduced technique of measuring corticosterone in feathers currently provides the longest-term measure of corticosterone in birds. This review examines the strengths, weaknesses, and unresolved technical issues of the feather corticosterone technique. Feather corticosterones major strengths are that it provides: a retrospective assessment of corticosterone physiology, including information from absent (unseen) or dead (e.g. museum specimens) individuals; a long-term measure of corticosterone exposure over the period of feather growth (days-weeks), integrating both baseline and responses to stressors; and flexible, minimally-invasive, sampling. However, researchers considering this technique should be aware of its limitations. Feather corticosterone only reflects hormone exposure during feather growth and, when sampling during molt, corticosterone titers and ecological conditions may not be representative of the majority of the annual cycle. Synchronization of molt is often unknown for a population, requiring assumptions when making inter-individual comparisons. Additionally, unresolved technical issues include: assessing whether corticosterone is the only hormone measured by assays; determining deposition dynamics to fully understand connections between feather and plasma corticosterone titers; studying the longevity and stability of corticosterone in the feather; establishing the impact of feather size and color on corticosterone deposition; and understanding the causes and implications of corticosterone variation along the length of the feather. Notwithstanding the above limitations and technical challenges, determining corticosterone titers in feathers is proving to be a useful technique for exploring some ecological and physiological correlates in individual birds. Given the unique perspective that feather corticosterone offers, we suggest that this measure complement, not replace, plasma measurements.

Can synchronizing feather-based measures of corticosterone and stable isotopes help us better understand habitat–physiology relationships?

Physiological mechanisms link the environment with population dynamics, and glucocorticoid hormones are of particular interest because they respond adaptively to environmental change and can influence vertebrate reproduction and fitness. We tested a novel approach of synchronizing feather-based measures of corticosterone (the primary avian glucocorticoid; CORTf) and ratios of stable isotopes (SIs) of C (δ13C) and N (δ15N) to provide information about environmental conditions and an integrated physiological response to those conditions over the same period of feather synthesis. Using a fragmented metapopulation of Dupont’s larks Chersophilus duponti, an endangered steppe songbird, we analyzed interrelationships among CORTf, δ13C, δ15N, and the physical environment, including measures of habitat loss and fragmentation. CORTf was not related to any habitat variable measured directly. However, we detected a significant spatial structure to CORTf values and food availability, with greater similarity in both at smaller spatial scales. Using SIs as proxies for the local environment, we found CORTf was negatively related to δ13C. Values of CORTf, δ13C, and the relationship between the two were likely driven by variation in agricultural land use surrounding lark habitat patches. Our feather-based approach revealed that individual physiology was sensitive to environmental conditions (e.g., an interaction of food availability and variation in habitat) at a local scale, but not patch or landscape scales. Combining CORTf and SIs may be a promising tool because it can provide individual-based information about habitat, physiology, and their relationship during the same time period.

Synchronizing feather-based measures of corticosterone and carotenoid-dependent signals: what relationships do we expect?

Carotenoids produce many of the red, orange and yellow signal traits of birds, and individuals must trade off utilizing carotenoids for physiological processes versus ornamentation. Proximate mechanisms regulating this trade-off are poorly understood, despite their importance for expression of color signals. Corticosterone (CORT) may play a significant mechanistic role in signal expression because it mobilizes energy substrates and influences foraging behavior. We used a unique feather-based approach to test whether CORT mediates expression of carotenoid-based coloration. First, we investigated relationships between levels of CORT from feathers (CORTf) and carotenoid-based plumage signals in common redpolls (Acanthis flammea). Then, we determined how the width of growth bars and probability of having fault bars on feathers varied with CORTf, specifically whether these metrics reflected developmental costs of elevated CORT (“stress” hypothesis) or represented an individual’s quality (“quality” hypothesis). CORTf correlated positively with the strength of carotenoid signals, but only in adult males. However, also in adult males, CORTf was positively related to width of feather growth bars and negatively with probability of having fault bars, providing support for the quality hypothesis. Overall, CORTf was lower in adult males than in females or young males, possibly due to dominance patterns. Our results indicate that CORT may indirectly benefit feather quality, potentially by mediating the expression of carotenoid signals. We place our sex-specific findings into a novel framework that proposes that the influences of CORT in mediating carotenoid-based plumage traits will depend on the extent to which carotenoids are traded off between competing functions.

Assessing costs of carrying geolocators using feather corticosterone in two species of aerial insectivore

Despite benefits of using light-sensitive geolocators to track animal movements and describe patterns of migratory connectivity, concerns have been raised about negative effects of these devices, particularly in small species of aerial insectivore. Geolocators may act as handicaps that increase energetic expenditure, which could explain reported effects of geolocators on survival. We tested this ‘Energetic Expenditure Hypothesis’ in 12 populations of tree swallows (Tachycineta bicolor) and barn swallows (Hirundo rustica) from North America and Europe, using measurements of corticosterone from feathers (CORTf) grown after deployment of geolocators as a measure of physiology relevant to energetics. Contrary to predictions, neither among- (both species) nor within-individual (tree swallows only) levels of CORTf differed with respect to instrumentation. Thus, to the extent that CORTf reflects energetic expenditure, geolocators apparently were not a strong handicap for birds that returned post-deployment. While this physiological evidence suggests that information about migration obtained from returning geolocator-equipped swallows is unbiased with regard to levels of stress, we cannot discount the possibility that corticosterone played a role in reported effects of geolocators on survival in birds, and suggest that future studies relate corticosterone to antecedent factors, such as reproductive history, and to downstream fitness costs.

Habitat quality affects early physiology and subsequent neuromotor development of juvenile black-capped chickadees.

In songbirds, the ability to learn and render the species-specific song is influenced by the development of both the song nuclei in the brain and the syrinx (birds vocal apparatus) early in the birds life. In black-capped chickadees (Poecille atricapillus), habitat quality is known to affect song structure, with birds in high-quality habitat (mature forest) having a higher song consistency than birds in low-quality habitat (young forest). Although this difference is suspected to stem from differences in development, the developmental status of juvenile birds in either habitat remains unexplored. In this study, we used ptilochronology and feather corticosterone to compare the conditional state of juvenile chickadees in young and mature forest during two distinct periods of song learning - the sensory phase, which occurs prior to settlement, and the sensorimotor phase, which occurs post-settlement. A sample of juvenile males was captured and euthanized several weeks prior to their first breeding season to compare the development of song center nuclei and syrinx in both habitats. The corticosterone levels of natally-grown feathers were greater among birds that settled in mature than young forests - as these feathers were grown pre-settlement, they reflect differences in physiology during the sensory phase. This difference in conditional state is reflected by differences in syrinx and song center nuclei development later during the sensorimotor phase - birds in young forest have smaller syrinx, and moderately-larger RA, than birds in mature forest. Those differences could be responsible for the difference in consistency in song structure observed across habitats. The difference in physiological state across habitats, combined with potential compounding effect of differences in winter resources between habitats, could influence the difference in syrinx and neural development seen in juvenile males during the early spring, and influence the males ability to learn and render their species-specific song.

Light-level geolocators reveal covariation between winter plumage molt and phenology in a trans-Saharan migratory bird

Contingent individual performance can depend on the environment experienced at previous life-stages. Migratory birds are especially susceptible to such carry-over effects as they periodically travel between breeding ranges and ‘wintering’ areas where they may experience broadly different ecological conditions. However, the study of carry-over effects is hampered by the difficulty of tracking vagile organisms throughout their annual life-cycle. Using information from light-level geolocators on the barn swallow (Hirundo rustica), we tested if feather growth bar width (GBW), a proxy of feather growth rate which depends on individual condition, and wing isometric size and shape predict the phenology of subsequent migration. GBW did not predict duration of wintering but negatively predicted the duration of spring migration and arrival date to the breeding sites, suggesting that migration phenology is not constrained by molt, and individuals in prime condition achieve both faster molt and earlier arrival. Wing morphology did not predict migration duration, as expected if wing shape were optimized for foraging, rather than migration performance, in this aerially foraging, insectivorous bird. Thus, we showed for the first time that migration phenology in a long-distance migratory bird covaries with body condition during wintering, as reflected by the growth rate of feathers.