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Researchers have long sought to understand and predict an animal’s response to stressful stimuli. Since the introduction of the concept of homeostasis, a variety of model frameworks have been proposed to describe what is necessary for an animal to remain within this stable physiological state and the ramifications of leaving it. Romero et al. (Horm Behav 55(3):375–389, 2009) introduced the reactive scope model to provide a novel conceptual framework for the stress response that assumes an animal’s ability to tolerate a stressful stimulus may degrade over time in response to the stimulus. We provide a mathematical formulation for the reactive scope model using a system of ordinary differential equations and show that this model is capable of recreating existing experimental data. We also provide an experimental method that may be used to verify the model as well as several potential additions to the model. If future experimentation provides the necessary data to estimate the model’s parameters, the model presented here may be used to make quantitative predictions about physiological mediator levels during a stress response and predict the onset of homeostatic overload.

 

When animals are sick, their physiology and behavior change in ways that can impact their offspring. Research is emerging showing that infection risk alone can also modify the physiology and behavior of healthy animals. If physiological responses to environments with high infection risk take place during reproduction, it is possible that they lead to maternal effects. Understanding whether and how high infection risk triggers maternal effects is important to elucidate how the impacts of infectious agents extend beyond infected individuals and how, in this way, they are even stronger evolutionary forces than already considered. Here, to evaluate the effects of infection risk on maternal responses, we exposed healthy female Japanese quail to either an immune-challenged (lipopolysaccharide [LPS] treated) mate or to a healthy (control) mate. We first assessed how females responded behaviorally to these treatments. Exposure to an immune-challenged or control male was immediately followed by exposure to a healthy male, to determine whether treatment affected paternity allocation. We predicted that females paired with immune-challenged males would avoid and show aggression towards those males, and that paternity would be skewed towards the healthy male. After mating, we collected eggs over a 5-day period. As an additional control, we collected eggs from immune-challenged females mated to healthy males. We tested eggs for fertilization status, embryo sex ratio, as well as albumen corticosterone, lysozyme activity, and ovotransferrin, and yolk antioxidant capacity. We predicted that immune-challenged females would show the strongest changes in the egg and embryo metrics, and that females exposed to immune-challenged males would show intermediate responses. Contrary to our predictions, we found no avoidance of immune-challenged males and no differences in terms of paternity allocation. Immune-challenged females laid fewer eggs, with an almost bimodal distribution of sex ratio for embryos. In this group, albumen ovotransferrin was the lowest, and yolk antioxidant capacity decreased over time, while it increased in the other treatments. No differences in albumen lysozyme were found. Both females that were immune-challenged and those exposed to immune-challenged males deposited progressively more corticosterone in their eggs over time, a pattern opposed to that shown by females exposed to control males. Our results suggest that egg-laying Japanese quail may be able to respond to infection risk, but that additional or prolonged sickness symptoms may be needed for more extensive maternal responses.

 

Abstract Physiological metrics are becoming popular tools for assessing individual condition and population health to inform wildlife management and conservation decisions. Corticosterone assays can provide information on how animals cope with individual and habitat-level stressors, and the recent development of feather assays is an exciting innovation that could yield important insights for conservation of wild birds. Due to the widespread enthusiasm for feather corticosterone as a potential bioindicator, studies are needed to assess the ability of this technique to detect meaningful differences in physiological stress across a variety of stressor types and intensities. We examined feather corticosterone from 144 individuals among the 13 known breeding populations of Hawaiian gallinule (Gallinula galeata sandvicensis), an endangered waterbird, on the island of O‘ahu. These ecologically independent subpopulations are known to have low genetic connectivity and movement rates and differ largely across a number of important conditions, including level of predator management, human disturbance, proximity to urban development and conspecific population density. This system is well suited for assessing the performance of feather corticosterone as a bioindicator of different known habitat-level threats common to this and many other conservation-reliant species. We found no statistically significant relationship between feather corticosterone and level of predator control, level of human disturbance, gallinule population density, percent urban cover or body condition across all sites despite the substantial difference in stressor magnitude in our dataset. We did find that gallinules in habitats with larger population densities were in worse body condition. These findings suggest that feather corticosterone is not a consistent indicator of anthropogenic impacts on populations. Furthermore, they suggest that feather corticosterone may be a poor bioindicator of known habitat-level threats for Hawaiian gallinules and that it should be used with caution in other avian taxa of conservation concern. 

Neophobia is a behavior characterized by a reluctance to approach novel objects. We measured neophobia in captive wild house sparrows (Passer domesticus) by comparing the time it took for hungry birds to approach their normal food dish compared to one that had been modified with a novel object. We tested the behavior of animals captured at different times of year to test for seasonal variation in neophobia. One group of birds tested in July approached their food dishes much more quickly than all other birds (a matter of seconds rather than minutes whether or not there was a novel object), a response that was not repeated in a subsequent July. When this possible outlier group was removed from the analysis, approach times to novel objects were not affected by season. However, animals captured and tested in October had a stronger motivation to feed (i.e., they approached unmodified food dishes faster) than birds captured at other times of the year. If we define “neophobia” as an increase in latency to approach a novel versus an unmodified food dish, then there is little evidence for underlying seasonal variation in risk assessment, although a general motivation to feed does show a seasonal pattern.

 

Although corticosterone (Cort) has been the predominant metric used to assess acute stress in birds, it does not always accurately reflect how an animal copes with a stressor. Downstream measurements may be more reliable. In the current study, we tested the hypothesis that acute increases in DNA damage could be used to assess stressor exposure. Studies have shown DNA damage increases in response to stress‐related hormones in vitro; however, this has not yet been thoroughly applied in wild animals. We exposed house sparrows (Passer domesticus) to a 30‐ or 120‐min restraint stressor and took blood samples at 0, 30, 60, and 120 min to measure Cort, DNA damage, and uric acid. Both treatments increased DNA damage and Cort, and decreased uric acid. It thus appears that DNA damage can reflect acute stressor exposure. To improve the usability of DNA damage as a metric for stress, we also tested the impacts of sample storage on DNA damage. Leaving red blood cells on ice for up to 24 hr, only slightly influenced DNA damage. Freezing blood samples for 1–4 weeks substantially increased DNA damage. These findings emphasize the importance of reducing variation between samples by assaying them together whenever possible. Overall, these results indicate that assessing DNA damage is a valid method of assessing acute stressor exposure that is suitable for both laboratory‐ and field‐based studies; however, additional research is needed on the molecular dynamics of nucleated red blood cells, including whether and how their DNA is repaired.

 

Chronic stress has been extensively studied in both laboratory and field settings; however, a conclusive and consistent phenotype has not been reached. Several studies have reported attenuation of the hypothalamic–pituitary–adrenal axis during experiments intended to cause chronic stress. We sought to determine whether this attenuation could be indicative of habituation. Importantly, we were not investigating habituation to a specific stimulus—as many stress physiology studies do—but rather we assessed how the underlying physiology and behavior changed in response to repeated stressor presentation. We exposed house sparrows (Passer domesticus) to a single stimulus twice per day at random times for 8 consecutive days. We predicted that this period of time would be long enough for the birds to determine that these acute stressors were not, in fact, dangerous and they would, therefore, acclimate. A second control group remained undisturbed for the same period of time. We measured baseline, stress‐induced, negative feedback strength, and maximum production of corticosterone as well as neophobic behavior before, during, and after this 8‐day experiment. When birds experienced a stimulus for 4 days, their negative feedback strength was significantly diminished, but recovered after the second 4 days. Additionally, perch hopping decreased and recovered in this same time frame. These data suggest that distinct physiological and behavioral responses arise when house sparrows are exposed to the same stressor for several consecutive days as opposed to many stressors layered on top of one another. Furthermore, they indicate that habituation—as with chronic stress—can appear differently depending on the metric being examined.