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  1. Abstract

    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.

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  2. Abstract

    To further elucidate the role that wear‐and‐tear plays in the transition from acute to chronic stress, we manipulated the intensity and duration of applied chronic stress to determine if behavior would respond proportionately. We brought wild house sparrows into captivity and subjected them to high‐stress, medium‐stress, low‐stress, or captivity‐only. We varied the number of stressors per day and the duration of stress periods to vary wear‐and‐tear, and thus the potential to exhibit chronic stress symptoms. The behaviors we assessed were neophobia (the fear of the new; assessed via food approach latency) and perch hopping (activity). We predicted that our birds would show proportionate decreases in neophobia and activity throughout a long‐term chronic stress paradigm. Our results indicate that neophobia is sensitive to the intensity of chronic stress, however, the birds became more neophobic, which was the opposite of what we expected. Conversely, perch hopping did not differ across treatment groups and is thus not sensitive to the intensity of chronic stress. Together, these data show that different behavioral measurements are impacted differently by chronic stress.

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  3. Abstract

    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.

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  4. Abstract

    ‘The Blob’, a mass of anomalously warm water in the Northeast Pacific Ocean peaking from 2014 to 2016, caused a decrease in primary productivity with cascading effects on the marine ecosystem. Among the more obvious manifestations of the event were seabird breeding failures and mass mortality events. Here, we used corticosterone in breast feathers (fCort), grown in the winter period during migration, as an indicator of nutritional stress to investigate the impact of the Blob on two sentinel Pacific auk species (family Alcidae). Feathers were collected from breeding females over 8 years from 2010 to 2017, encompassing the Blob period. Since Pacific auks replace body feathers at sea during the migratory period, measures of fCort provide an accumulated measure of nutritional stress or allostatic load during this time. Changes in diet were also measured using δ15N and δ13C values from feathers. Relative to years prior to the Blob, the primarily zooplanktivorous Cassin’s auklets (Ptychoramphus aleuticus) had elevated fCort in 2014–2017, which correlated with the occurrence of the Blob and a recovery period afterwards, with relatively stable feather isotope values. In contrast, generalist rhinoceros auklets (Cerorhinca monocerata) displayed stable fCort values across years and increased δ15N values during the Blob. As marine heatwaves increase in intensity and frequency due to climate change, this study provides insight into the variable response of Pacific auks to such phenomena and suggests a means for monitoring population-level responses to climatological variation.

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  5. Abstract

    Neophobia is an animal's avoidance of novelty. Animals tend to respond to novel objects by increasing their latency to approach the objects, and they eventually habituate after repeated exposure by attenuating this increased approach latency. Interestingly, the physiological stress response does not appear to have a causal link to neophobia, although acute stress can prevent animals from habituating to novel objects, possibly through a permissive effect. Chronic stress can induce an anxiety‐like state in animals, while often disrupting the ability to respond to acute stress. We thus hypothesized that chronic stress may increase neophobia and tested this by inducing chronic stress in wild‐caught European starlings (Sturnus vulgaris). Four distinct anthropogenic stressors were administered daily for 30 min each in a randomized order for 21 days. We then evaluated whether exposure to chronic stress altered the latency to approach a novel object placed on or near a food dish presented after overnight fasting. Chronically stressed birds and nonstressed controls exhibited similar initial neophobic responses to novel objects and showed similar habituation in response to repeated exposure. However, when birds were exposed to 15 min of restraint before repeated exposure to the same object, habituation was eliminated in control birds (i.e., they continued to respond with neophobia), whereas chronically stressed birds continued to show habituation as measured by attenuated approach latencies. These results demonstrate that an acute stress response (restraint) has a different impact on neophobia depending upon whether the bird is or is not concurrently exposed to chronic stress.

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  6. Abstract

    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.

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  7. Abstract

    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.

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  8. Abstract

    Animals often avoid novel objects, a behavior known as neophobia. We examined behavioral responses of captive European starlings to novel objects placed at their food dishes. Exposure occurred concurrently to food reintroduction following overnight fasting. Behavior was analyzed for 10 min via video recording. We expected an increase in avoidance behavior compared with trials in which food was reintroduced without a novel object. Seven of 10 novel objects increased latency to approach the dish. In contrast to our expectations, neither prior restraint nor exogenous corticosterone changed the neophobic response to novel objects. While exposure to a novel object increased approach latency, there was no additional effect of restraining animals in a cloth bag for 15 min before food reintroduction. Furthermore, the subcutaneous injection of corticosterone did not affect approach latency by itself, nor did it affect the response to a novel object. Finally, we expected repeated exposure to the same object to extinguishing the neophobic response, and that restraint stress would prevent habituation. Our results show that European starlings habituate rapidly to exposure to a novel object, as approach latency returned to baseline within three repeated exposures to the same object. When the repeated presentation of the object was combined with prior restraint, however, the latency to approach never returned to baseline. These results reveal that neophobia in starlings is object‐specific and that, while neither acute stress nor corticosterone directly affects the behavioral response to a novel object, acute stress appears to have a permissive effect on neophobia by inhibiting habituation.

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  9. Abstract

    Wild‐caught European starlings (Sturnus vulgaris) were exposed to a learning task to determine whether heart rate (HR) and behavior responses to the learning activated the sympathetic nervous system. Birds learned to discriminate between images of opposite convexity (concave and convex) based on shading cues in a closed economy (food only available through task completion). Once learned, the task was changed in three ways: (a) manipulating the angle and shape of the image; (b) altering the availability of the task; and (c) reversing the positive stimulus. HR, used as an index of catecholamine release, was measured during each change to determine whether having to alter previously established behaviors to learn new behaviors elicited a sympathetic response. Starlings decreased their HR during the initial discrimination training and did not alter their HR when presented with modified images or when the positive stimulus was reversed. However, HR increased when the task became unavailable and decreased upon its return, suggesting that preventing task performance was perceived as stressful. Birds also modified their behavior when tasks were changed. The number of trials per minute decreased during the reversal treatment, as did the success rate, suggesting that starlings may try to conserve energy when access to food diminishes. This is also supported by the decrease in perch hops per minute when the task was unavailable and the subsequent increase upon its return. Overall, these results suggest that learning per se does not activate the sympathetic nervous system and, therefore, is not a stressor for wild birds.

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  10. Abstract

    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.

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