ABSTRACT There are complex interactions between an organism's microbiome and its response to stressors, often referred to as the ‘gut–brain axis’; however, the ecological relevance of this axis in wild animals remains poorly understood. Here, we used a chronic mild stress protocol to induce stress in wild-caught house sparrows (Passer domesticus), and compared microbial communities among stressed animals, those recovering from stress, captive controls (unstressed) and a group not brought into captivity. We assessed changes in microbial communities and abundance of shed microbes by culturing cloacal samples on multiple media to select for aerobic and anaerobic bacteria and fungi. We complemented this with cultivation-independent 16S and ITS rRNA gene amplification and sequencing, pairing these results with host physiological and immune metrics, including body mass change, relative spleen mass and plasma corticosterone concentrations. We found significant effects of stress and captivity on the house sparrow microbiomes, with stress leading to an increased relative abundance of endotoxin-producing bacteria – a possible mechanism for the hyperinflammatory response observed in captive avians. While we found evidence that the microbiome community partially recovers after stress cessation, animals may lose key taxa, and the abundance of endotoxin-producing bacteria persists. Our results suggest an overall link between chronic stress, host immune system and the microbiome, with the loss of potentially beneficial taxa (e.g. lactic acid bacteria), and an increase in endotoxin-producing bacteria due to stress and captivity. Ultimately, consideration of the host's microbiome may be useful when evaluating the impact of stressors on individual and population health.
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The effects of daily mitotane or diazepam treatment on the formation of chronic stress symptoms in newly captured wild house sparrows
Abstract Wild animals brought into captivity frequently experience chronic stress and typically need a period of time to adjust to the conditions of captivity (restraint, artificial lighting, altered diet, human presence, etc.), to which they may never fully acclimate. Changes in mass, the hypothalamic–pituitary–adrenal axis and heart rate parameters have been observed over the first week in newly captive house sparrows (Passer domesticus). In this study, we tested the effects of two drugs, diazepam and mitotane, in preventing the chronic stress symptoms caused by captivity, compared with oil-injected control animals. Diazepam is an anxiolytic that is widely prescribed in humans and other animals and has been shown in some cases to reduce physiological stress. Mitotane is an agent that causes chemical adrenalectomy, reducing the body’s capacity to produce glucocorticoid hormones. Our mitotane treatment did not cause the expected change in corticosterone concentrations. Baseline corticosterone was higher after a week in captivity regardless of the treatment group, while stress-induced corticosterone did not significantly increase above baseline after a week in captivity in any treatment group. However, mitotane treatment did have some physiological effects, as it reduced the resting heart rate and the duration of the heart rate response to a sudden noise. It also prevented the increase in nighttime activity that we observed in control animals. There was no effect of diazepam on corticosterone, resting heart rate, activity or heart rate response to a sudden noise, and no effect of either treatment on the sympathetic vs parasympathetic control of the resting heart rate. Together, these data suggest that mitotane, but not diazepam, can have a modest impact on helping house sparrows adapt to captive conditions. Easing the transition to captivity will likely make conservation efforts, such as initiating captive breeding programs, more successful.
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- NSF-PAR ID:
- 10301058
- Editor(s):
- Cooke, Steven
- Date Published:
- Journal Name:
- Conservation Physiology
- Volume:
- 8
- Issue:
- 1
- ISSN:
- 2051-1434
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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One of the biggest unanswered questions in the field of stress physiology is whether variation in chronic stress intensity will produce proportional (a gradient or graded) physiological response. We were specifically interested in the timing of the entrance into homeostatic overload, or the start of chronic stress symptoms. To attempt to fill this knowledge gap we split 40 captive house sparrows (
Passer domesticus ) into four groups (high stress, medium stress, low stress, and a captivity-only control) and subjected them to six bouts of chronic stress over a 6-month period. We varied the number of stressors/day and the length of each individual bout with the goal of producing groups that would experience different magnitudes of wear-and-tear. To evaluate the impact of chronic stress, at the start and end of each stress bout we measured body weight and three plasma metabolites (glucose, ketones, and uric acid) in both a fasted and fed state. All metrics showed significant differences across treatment groups, with the high stress group most frequently showing the greatest changes. However, the changes did not produce a consistent profile that matched the different chronic stress intensities. We also took samples after a prolonged recovery period of 6 weeks after the chronic stressors ended. The only group difference that persisted after 6 weeks was weight—all differences across groups in metabolites recovered. The results indicate that common blood metabolites are sensitive to stressors and may show signs of wear-and-tear, but are not reliable indicators of the intensity of long-term chronic stress. Furthermore, regulatory mechanisms are robust enough to recover within 6 weeks post-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. -
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.more » « less
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The acute stress response can be considered the primary evolutionary adaptation to maximise fitness in the face of unpredictable environmental challenges. However, the difficulties of assessing physiology in natural environments mean comparatively little is known about how response variation influences fitness in free-living animals. Currently, determining acute stress physiology typically involves blood sampling or cardiac monitoring. Both require trapping and handling, interrupting natural behaviour, and potentially biasing our understanding toward trappable species/individuals. Importantly, limits on repeated sampling also restrict response phenotype characterisation, vital for linking stress with fitness. Surface temperature dynamics resulting from peripheral vasomotor activity during acute stress are increasingly promoted as alternative physiological stress indicators, which can be measured non-invasively using infrared thermal imaging, overcoming many limitations of current methods. Nonetheless, which aspects of stress physiology they represent remains unclear, as the underlying mechanisms are unknown. To date, validations have primarily targeted the hypothalamic-pituitary-adrenal axis, when the sympathetic-adrenal-medullary (SAM) system is likely the primary driver of vasomotor activity during acute stress. To address this deficit, we compared eye and bill region surface temperatures – measured using thermal imaging – with SAM system activity – measured as heart-rate-variability via electrocardiogram telemetry – in wild-caught captive house sparrows (Passer domesticus), during capture and handling. We found lower body surface temperatures were associated with increased sympathetic nervous system activation. Consequently, our data confirm body surface temperatures can act as a proxy for sympathetic activation during acute stress, providing potentially transformative opportunities for linking the acute stress response with fitness in the wild.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/conphys/coaa118
