One aspect of the Reactive Scope Model is wear-and-tear, which describes a decrease in an animal’s ability to cope with a stressor, typically because of a period of chronic or repeated stressors. We investigated whether wear-and-tear due to chronic stress would accelerate a transition from phase II to phase III of fasting. We exposed house sparrows (Passer domesticus) to three weeks of daily fasts combined with daily intermittent repeated acute stressors to create chronic stress, followed by two weeks of daily fasts without stressors. We measured circulating glucose, β-hydroxybutyrate (a ketone), and uric acid in both fasted and fed states. We expected birds to be in phase II (high fat breakdown) in a fasted state, but if wear-and-tear accumulated sufficiently, we hypothesized a shift to phase III (high protein breakdown). Throughout the experiment, the birds exhibited elevated β-hydroxybutyrate when fasting but no changes in circulating uric acid, indicating that a transition to phase III did not occur. In both a fasted and fed state, the birds increased glucose mobilization throughout the experiment, suggesting wear-and-tear occurred, but was not sufficient to induce a shift to phase III. Additionally, the birds exhibited a significant decrease in weight, no change in corticosterone, and a transient decrease in neophobia with chronic stress. In conclusion, the birds appear
to have experienced wear-and-tear, but our protocol did not accelerate the transition from phase II to phase III of fasting.
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Physiological and behavioral responses of house sparrows to repeated stressors
Despite decades of research, we still lack a complete understanding of what factors influence the transition of the necessary and adaptive acute stress response to what has become known as chronic stress. This gap in knowledge has illuminated the necessity for studies that examine the thresholds between these two sides of the stress response. Here, we determine how repeated exposure to acute stressors influences physiological and behavioral responses. In this repeated measures study, house sparrows ( Passer domesticus ) were exposed to a chronic stress protocol. We took physiological and behavioral measurements before, during, and after the protocol. Blood samples were used to assess four aspects of hypothalamic-pituitary-adrenal (HPA) axis function: baseline corticosterone, stress-induced corticosterone, negative feedback, and the maximal capacity to secrete corticosterone. We also assessed bacterial killing capacity and changes in uric acid concentration. Neophobia trials were used to assess behavioral changes throughout the protocol. We found no significant changes in HPA axis regulation in any of the four aspects we tested. However, we found that uric acid concentrations and neophobia significantly decreased after only four days of the chronic stress protocol, while bacterial killing capacity did not decrease until after eight days of exposure. These results indicate that different components of the stress response can be impacted by chronic stress on different timescales. Our results further indicate the importance of assessing multiple aspects of both physiology and behavior in order to understand how exposure to chronic stress may influence ability to cope with future challenges.
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- Award ID(s):
- 1655269
- NSF-PAR ID:
- 10075208
- Date Published:
- Journal Name:
- PeerJ
- Volume:
- 6
- ISSN:
- 2167-8359
- Page Range / eLocation ID:
- e4961
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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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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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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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null (Ed.)ABSTRACT The hypothalamic–pituitary–adrenal (HPA) axis controls the release of glucocorticoids, which regulate immune and inflammatory function by modulating cytokines, white blood cells and oxidative stress via glucocorticoid receptor (GR) signaling. Although the response to HPA activation is well characterized in many species, little is known about the impacts of HPA activation during extreme physiological conditions. Hence, we challenged 18 simultaneously fasting and developing elephant seal pups with daily intramuscular injections of adrenocorticotropin (ACTH), a GR antagonist (RU486), or a combination of the two (ACTH+RU486) for 4 days. We collected blood at baseline, 2 h and 4 days after the beginning of treatment. ACTH and ACTH+RU486 elevated serum aldosterone and cortisol at 2 h, with effects diminishing at 4 days. RU486 alone induced a compensatory increase in aldosterone, but not cortisol, at 4 days. ACTH decreased neutrophils at 2 h, while decreasing lymphocytes and increasing the neutrophil:lymphocyte ratio at 4 days. These effects were abolished by RU486. Despite alterations in white blood cells, there was no effect of ACTH or RU486 on transforming growth factor-β or interleukin-6 levels; however, both cytokines decreased with the 4 day fasting progression. Similarly, ACTH did not impact protein oxidation, lipid peroxidation or antioxidant enzymes, but plasma isoprostanes and catalase activity decreased while glutathione peroxidase increased with fasting progression. These data demonstrate differential acute (2 h) and chronic (4 days) modulatory effects of HPA activation on white blood cells and that the chronic effect is mediated, at least in part, by GR. These results also underscore elephant seals' extraordinary resistance to oxidative stress derived from repeated HPA activation.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7717/peerj.4961
