Ondi L. Crino

Effects of experimentally elevated traffic noise on nestling white-crowned sparrow stress physiology, immune function and life history

SUMMARY Roads have been associated with behavioral and physiological changes in wildlife. In birds, roads decrease reproductive success and biodiversity and increase physiological stress. Although the consequences of roads on individuals and communities have been well described, the mechanisms through which roads affect birds remain largely unexplored. Here, we examine one mechanism through which roads could affect birds: traffic noise. We exposed nestling mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) to experimentally elevated traffic noise for 5 days during the nestling period. Following exposure to traffic noise we measured nestling stress physiology, immune function, body size, condition and survival. Based on prior studies, we expected the traffic noise treatment to result in elevated stress hormones (glucocorticoids), and declines in immune function, body size, condition and survival. Surprisingly, nestlings exposed to traffic noise had lower glucocorticoid levels and improved condition relative to control nests. These results indicate that traffic noise does affect physiology and development in white-crowned sparrows, but not at all as predicted. Therefore, when evaluating the mechanisms through which roads affect avian populations, other factors (e.g. edge effects, pollution and mechanical vibration) may be more important than traffic noise in explaining elevated nestling stress responses in this species.

Proximity to a high traffic road: glucocorticoid and life history consequences for nestling white-crowned sparrows.

Roads have been associated with decreased reproductive success and biodiversity in avian communities and increased physiological stress in adult birds. Alternatively, roads may also increase food availability and reduce predator pressure. Previous studies have focused on adult birds, but nestlings may also be susceptible to the detrimental impacts of roads. We examined the effects of proximity to a road on nestling glucocorticoid activity and growth in the mountain white-crowned sparrow (Zonotrichia leucophrys oriantha). Additionally, we examined several possible indirect factors that may influence nestling corticosterone (CORT) activity secretion in relation to roads. These indirect effects include parental CORT activity, nest-site characteristics, and parental provisioning. And finally, we assessed possible fitness consequences of roads through measures of fledging success. Nestlings near roads had increased CORT activity, elevated at both baseline and stress-induced levels. Surprisingly, these nestlings were also bigger. Generally, greater corticosterone activity is associated with reduced growth. However, the hypothalamic-pituitary-adrenal axis matures through the nestling period (as nestlings get larger, HPA-activation is greater). Although much of the variance in CORT responses was explained by body size, nestling CORT responses were higher close to roads after controlling for developmental differences. Indirect effects of roads may be mediated through paternal care. Nestling CORT responses were correlated with paternal CORT responses and paternal provisioning increased near roads. Hence, nestlings near roads may be larger due to increased paternal attentiveness. And finally, nest predation was higher for nests close to the road. Roads have apparent costs for white-crowned sparrow nestlings--increased predation, and apparent benefits--increased size. The elevation in CORT activity seems to reflect both increased size (benefit) and elevation due to road proximity (cost). Whether or not roads are good or bad for nestlings remains equivocal. However, it is clear that roads affect nestlings; how or if these effects influence adult survival or reproduction remains to be elucidated.

Corticosterone exposure during development has sustained but not lifelong effects on body size and total and free corticosterone responses in the zebra finch.

Animals exposed to stress during development experience sustained morphological, physiological, neurological, and behavioral consequences. For example, elevated glucocorticoids (GCs) during development can increase GC secretion in adults. Studies have examined the sustained effects of elevated developmental GCs on total GC responses, but no study to date has examined the effect of developmental stress on corticosteroid binding globulin (CBG). CBG is a protein which binds to GCs and facilitates their transportation in blood. When bound to CBG, GCs are unavailable to interact with target tissues. Exposure to stress can decrease CBG capacity and, thus, increase free GCs (the portion of unbound GCs). We examined the long-term effects of elevated corticosterone (CORT) during development (12-28days post-hatch) on acute stress responses, negative feedback, and CBG capacity at 30, 60, and 90days post-hatch in zebra finches. Additionally, we evaluated the effect of CORT treatment on body size and condition at 28, 60, and 90days post-hatch. CORT exposed birds had higher acute stress responses at 30days post-hatch compared to control birds. However, there was no treatment effect at 60 or 90days post-hatch. CBG levels were not affected by treatment, and so free CORT estimations reflected patterns in total CORT. CORT treatment decreased growth and condition in zebra finches at 28days post-hatch, but these differences were not present at later life history stages. However, brood size had a sustained effect on body size such that birds reared in medium sized broods were larger at 28, 60, and 90days post-hatch. These results demonstrate the complexity of early environmental effects on adult phenotype and suggest that some conditions may have stronger programmatic effects than others.

Corticosterone exposure during development improves performance on a novel foraging task in zebra finches

Developmental stress affects a range of phenotypic traits in later life-history stages. These long-term effects are thought to provide information to potential mates on individual quality and the ability to cope with adversity (i.e. the developmental stress hypothesis). Developmental stress appears to affect learning broadly, but the direction of effect is not always consistent between studies. This disparity may arise from indirect effects of developmental stress on other physiological or behavioural systems, which can affect outcomes in learning paradigms. Here, we examine the effect of elevated corticosterone (the dominant avian stress hormone) during development on the ability of zebra finches, Taeniopygia guttata, to learn a novel foraging task as adults. Additionally, we evaluate treatment effects on metabolism, to determine whether changes in metabolic rate indirectly alter learning results. We found that birds exposed to elevated corticosterone during development solved a foraging task faster than control siblings. This outcome could result from differences, not in learning ability, but in motivation for reward. However, we found no difference between treatment groups in metabolic rate. Hence, our results indicate that developmental stress can increase learning ability, and suggest that the effects of stress will vary based on the type of learning studied.

Developmental stress: evidence for positive phenotypic and fitness effects in birds

The developmental environment has strong and pervasive effects on animal phenotype. Exposure to stress during development (in the form of elevated glucocorticoid hormones or food restriction) is one environmental cue that can have strong formative effects on morphology, physiology, and behavior. Although many of the effects of developmental stress appear negative, there is increasing evidence for an adaptive role of developmental stress in shaping animal phenotype. Here, we take a three-pronged approach to review studies that have uncovered positive effects of developmental stress on phenotype in birds. We focus on studies that: (1) examine phenotypic effects likely to increase fitness in offspring, (2) directly identify increased fitness in offspring, or (3) provide evidence of fitness benefits to the mother, at a cost to the offspring. Throughout, we focus on studies that evaluate the environment when assessing the ‘costs/benefits’ of phenotype alterations and examine the effects of developmental stress across life-history stages. Finally, we consider the two common methods used to simulate developmental stress: food restriction and direct hormone manipulation. Although these methods are often considered to elicit equivalent responses, there has been very little discussion of this in the literature. To this end, we review the main methods used to implement developmental stress in experimental studies and discuss how they may simulate different environmental conditions. In light of our conclusions, we propose possible avenues for future research, stressing the need for a greater focus on direct fitness metrics, longitudinal studies, and experiments in free-living animals.

Developmental stress increases reproductive success in male zebra finches

There is increasing evidence that exposure to stress during development can have sustained effects on animal phenotype and performance across life-history stages. For example, developmental stress has been shown to decrease the quality of sexually selected traits (e.g. bird song), and therefore is thought to decrease reproductive success. However, animals exposed to developmental stress may compensate for poor quality sexually selected traits by pursuing alternative reproductive tactics. Here, we examine the effects of developmental stress on adult male reproductive investment and success in the zebra finch (Taeniopygia guttata). We tested the hypothesis that males exposed to developmental stress sire fewer offspring through extra-pair copulations (EPCs), but invest more in parental care. To test this hypothesis, we fed nestlings corticosterone (CORT; the dominant avian stress hormone) during the nestling period and measured their adult reproductive success using common garden breeding experiments. We found that nestlings reared by CORT-fed fathers received more parental care compared with nestlings reared by control fathers. Consequently, males fed CORT during development reared nestlings in better condition compared with control males. Contrary to the prediction that developmental stress decreases male reproductive success, we found that CORT-fed males also sired more offspring and were less likely to rear non-genetic offspring compared with control males, and thus had greater overall reproductive success. These data are the first to demonstrate that developmental stress can have a positive effect on fitness via changes in reproductive success and provide support for an adaptive role of developmental stress in shaping animal phenotype.

Stress reactivity, condition, and foraging behavior in zebra finches: effects on boldness, exploration, and sociality.

The arid and semi-arid zones of Australia are characterized by highly variable and unpredictable environmental conditions which affect resources for flora and fauna. Environments which are highly unpredictable in terms of both resource access and distribution are likely to select for a variety of adaptive behavioral strategies, intrinsically linked to the physiological control of behavior. How unpredictable resource distribution has affected the coevolution of behavioral strategies and physiology has rarely been quantified, particularly not in Australian birds. We used a captive population of wild-derived zebra finches to test the relationships between behavioral strategies relating to food access and physiological responses to stress and body condition. We found that individuals that were in poorer body condition and had higher peak corticosterone levels entered baited feeders earlier in the trapping sequence of birds within the colony. We also found that individuals in poorer body condition fed in smaller social groups. Our data show that the foraging decisions which individuals make represent not only a trade-off between food access and risk of exposure, but their underlying physiological response to stress. Our data also suggest fundamental links between social networks and physiological parameters, which largely remain untested. These data demonstrate the fundamental importance of physiological mechanisms in controlling adaptive behavioral strategies and the dynamic interplay between physiological control of behavior and life-history evolution.

Acute Restraint Stress Alters Wheel-Running Behavior Immediately Following Stress and up to 20 Hours Later in House Mice

In vertebrates, acute stressors—although short in duration—can influence physiology and behavior over a longer time course, which might have important ramifications under natural conditions. In laboratory rats, for example, acute stress has been shown to increase anxiogenic behaviors for days after a stressor. In this study, we quantified voluntary wheel-running behavior for 22 h following a restraint stress and glucocorticoid levels 24 h postrestraint. We utilized mice from four replicate lines that have been selectively bred for high voluntary wheel-running activity (HR mice) for 60 generations and their nonselected control (C) lines to examine potential interactions between exercise propensity and sensitivity to stress. Following 6 d of wheel access on a 12L∶12D photo cycle (0700–1900 hours, as during the routine selective breeding protocol), 80 mice were physically restrained for 40 min, beginning at 1400 hours, while another 80 were left undisturbed. Relative to unrestrained mice, wheel running increased for both HR and C mice during the first hour postrestraint (P < 0.0001) but did not differ 2 or 3 h postrestraint. Wheel running was also examined at four distinct phases of the photoperiod. Running in the period of 1600–1840 hours was unaffected by restraint stress and did not differ statistically between HR and C mice. During the period of peak wheel running (1920–0140 hours), restrained mice tended to run fewer revolutions (−11%; two-tailed P = 0.0733), while HR mice ran 473% more than C (P = 0.0008), with no restraint × line type interaction. Wheel running declined for all mice in the latter part of the scotophase (0140–0600 hours), restraint had no statistical effect on wheel running, but HR again ran more than C (+467%; P = 0.0122). Finally, during the start of the photophase (0720–1200 hours), restraint increased running by an average of 53% (P = 0.0443) in both line types, but HR and C mice did not differ statistically. Mice from HR lines had statistically higher plasma corticosterone concentrations than C mice, with no statistical effect of restraint and no interaction between line type and restraint. Overall, these results indicate that acute stress can affect locomotor activity (or activity patterns) for many hours, with the most prominent effect being an increase in activity during a period of typical inactivity at the start of the photophase, 15–20 h poststressor.

Divorce in the socially monogamous zebra finch: Hormonal mechanisms and reproductive consequences.

&NA; Up to 80% of all bird species are socially monogamous. Divorce (switching partners) or pair disruption (due to the death of a partner) has been associated with decreased reproductive success, suggesting social monogamy is a strategy that may maximize fitness via coordination between partners. Previous studies have demonstrated the effects of divorce and pair disruption on immediate reproductive success. Here, we used a paired experimental design in the zebra finch (Taeniopygia guttata) to examine the hormonal mechanisms that modulate parental behavior and reproductive success in response to a partnership change (hereafter divorce). Specifically, we examined the effects of divorce on the avian stress hormone corticosterone (CORT) in both parents and nestlings, parental behaviors (incubation and nestling provisioning), prolactin (PRL), and reproductive success. We found that divorce resulted in delayed clutch initiation, reduced clutch mass, and an increase in nestling CORT response to a standardized stressor. These effects on reproductive investment and chick CORT response were not clearly determined by parental endocrine responses. Divorce had no effect on the level of parental CORT. PRL levels were highly correlated within a pair regardless of treatment, were negatively related to the investment that males made in incubation, and increased in experimental males as a result of pair disruption. This study demonstrates the fundamental impact which divorce has not only on reproduction, but also the physiological stress responses of offspring and suggests that in socially monogamous animals the maintenance of a stable partnership over time could be advantageous for long term fitness. HighlightsUp to 80% of all bird species are socially monogamous.We examined changes in corticosterone and prolactin in response to a partnership change (divorce).Divorce delayed clutch initiation and reduced clutch mass.Divorce did not affect parental corticosterone or prolactin levels.Nestlings reared by divorced parents had higher stress (corticosterone) responses.

Flight performance in the altricial zebra finch: developmental effects and reproductive consequences

Abstract The environmental conditions animals experience during development can have sustained effects on morphology, physiology, and behavior. Exposure to elevated levels of stress hormones (glucocorticoids, GCs) during development is one such condition that can have long‐term effects on animal phenotype. Many of the phenotypic effects of GC exposure during development (developmental stress) appear negative. However, there is increasing evidence that developmental stress can induce adaptive phenotypic changes. This hypothesis can be tested by examining the effect of developmental stress on fitness‐related traits. In birds, flight performance is an ideal metric to assess the fitness consequences of developmental stress. As fledglings, mastering takeoff is crucial to avoid bodily damage and escape predation. As adults, takeoff can contribute to mating and foraging success as well as escape and, thus, can affect both reproductive success and survival. We examined the effects of developmental stress on flight performance across life‐history stages in zebra finches (Taeniopygia guttata). Specifically, we examined the effects of oral administration of corticosterone (CORT, the dominant avian glucocorticoid) during development on ground‐reaction forces and velocity during takeoff. Additionally, we tested for associations between flight performance and reproductive success in adult male zebra finches. Developmental stress had no effect on flight performance at all ages. In contrast, brood size (an unmanipulated variable) had sustained, negative effects on takeoff performance across life‐history stages with birds from small broods performing better than birds from large broods. Flight performance at 100 days posthatching predicted future reproductive success in males; the best fliers had significantly higher reproductive success. Our results demonstrate that some environmental factors experienced during development (e.g. clutch size) have stronger, more sustained effects than others (e.g. GC exposure). Additionally, our data provide the first link between flight performance and a direct measure of reproductive success.