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      Surface temperature elevated by chronic and intermittent stress

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          Abstract

          Stress in homeothermic animals is associated with raised body core temperature and altered patterns of peripheral blood flow. During acute stress, peripheral vasoconstriction causes a short-lived drop in surface temperature that can be detected non-invasively using infrared thermography (IRT). Whether and how skin temperature changes under chronic stress, and hence the potential of IRT in chronic stress detection, is unknown. We explored the impact of withdrawing environmental enrichments and intermittent routine handling on long-term skin temperature in laying hens ( Gallus gallus domesticus). Immediately following enrichment withdrawal, comb, face and eye temperature dropped, suggesting this was acutely stressful. In the 3 weeks that followed, barren-housed hens displayed behavioural markers of frustration. Whilst control birds, housed in enriched conditions, showed a decline over weeks in both comb temperature and baseline corticosterone levels, barren-housed hens had no change in comb temperature and an increase in corticosterone. By the trial end, comb temperature (but not corticosterone) was significantly higher in barren-housed hens. This change in parameters over time may reflect cumulative impacts of enrichment withdrawal in barren pens and/or, as hens were young and maturing, age-related changes in controls. Comb, face and eye temperature were also higher on days following routine handling, and comb temperature higher on other days in hens that were regularly handled for blood sampling than for a less intensive weighing protocol. Together, these data support comb, face and eye surface temperature increase as a long-term marker of stress exposure in laying hens. It is important to recognise that the strength and even direction of these effects may vary with thermoregulatory and energetic context. However, in laboratory and indoor-reared farm animals that live in carefully managed environments, IRT of the skin can potentially be used to non-invasively monitor chronic and intermittent stress exposure.

          Highlights

          • We measured surface temperature (ST) profile in hens subject to long term and intermittent stress.

          • The impact of stressors was validated using established behavioural and hormonal markers.

          • Enrichment withdrawal caused a short term drop in ST but living in a barren environment increased ST.

          • Hens also had higher ST on days following handling or when subject to more intense handling methods.

          • Thermal imaging of ST offers a non-invasive approach toward chronic stress monitoring.

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          Most cited references56

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          The neuro-symphony of stress.

          The impact of stress on brain function is increasingly recognized. Various substances are released in response to stress and can influence distinct neuronal circuits, but the functional advantages of having such a diversity of stress mediators remain unclear. Individual neurotransmitter, neuropeptide and steroid stress mediators have specific spatial and temporal niches, but these niches also overlap. In addition, the effects of individual mediators on neuronal function and plasticity are integrated, and emerging evidence suggests that there is crosstalk between them. Together, this results in the stress instruments producing an orchestrated 'symphony' that enables fine-tuned responses to diverse challenges.
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            Exposure to chronic stress downregulates corticosterone responses to acute stressors.

            We used captive European starlings (Sturnus vulgaris) to test whether corticosterone responses differed in birds held under normal laboratory conditions or conditions of chronic stress. Surprisingly, both basal corticosterone concentrations and corticosterone responses to acute stress were significantly reduced when birds were chronically stressed. To determine the mechanism underlying this reduced response, animals under both conditions were injected with lactated Ringer's solution (control), adrenocorticotropin (ACTH), arginine vasotocin (AVT), or dexamethasone (DEX). ACTH increased corticosterone concentrations above stress-induced levels in both cases, although maximum responses were lower in chronically stressed birds. AVT did not augment the corticosterone response under nonchronically stressed conditions, but it did under chronically stressed conditions. DEX reduced maximal corticosterone concentrations in both cases. Neither ovine nor rat corticotropin-releasing factor (CRF) altered normal stress responses. These data indicate that changes in responsiveness of the hypothalamic-pituitary-adrenal axis to ACTH and AVT serve to downregulate corticosterone responses during chronic stress. Furthermore, these data lead to the following hypothesis: ACTH output from the pituitary limits maximum corticosterone concentrations under normal conditions, but reduced AVT release from the hypothalamus regulates lower corticosterone concentrations under chronic stress conditions.
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              Skin temperature reveals the intensity of acute stress

              Acute stress triggers peripheral vasoconstriction, causing a rapid, short-term drop in skin temperature in homeotherms. We tested, for the first time, whether this response has the potential to quantify stress, by exhibiting proportionality with stressor intensity. We used established behavioural and hormonal markers: activity level and corticosterone level, to validate a mild and more severe form of an acute restraint stressor in hens (Gallus gallus domesticus). We then used infrared thermography (IRT) to non-invasively collect continuous temperature measurements following exposure to these two intensities of acute handling stress. In the comb and wattle, two skin regions with a known thermoregulatory role, stressor intensity predicted the extent of initial skin cooling, and also the occurrence of a more delayed skin warming, providing two opportunities to quantify stress. With the present, cost-effective availability of IRT technology, this non-invasive and continuous method of stress assessment in unrestrained animals has the potential to become common practice in pure and applied research.
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                Author and article information

                Contributors
                Journal
                Physiol Behav
                Physiol. Behav
                Physiology & Behavior
                Elsevier Science
                0031-9384
                1873-507X
                01 July 2018
                01 July 2018
                : 191
                : 47-55
                Affiliations
                [a ]Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Jarrett Building, Glasgow G61 1QH, UK
                [b ]Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Graham Kerr Building, Glasgow G12 8QQ, UK
                [c ]Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, Scottish Centre for Ecology and the Natural Environment, Rowardennan, Drymen G63 0AW, UK
                Author notes
                [* ]Corresponding author at: Centre for Behaviour & Evolution, Institute of Neuroscience, Newcastle University, Framlington Place, Newcastle Upon Tyne NE2 4HH, UK. Katherine.herborn@ 123456newcastle.ac.uk
                [1]

                Current address: Centre for Behaviour and Evolution, ION, Newcastle University, Framlington Place, Newcastle Upon Tyne NE2 4HH, United Kingdom.

                Article
                S0031-9384(18)30172-0
                10.1016/j.physbeh.2018.04.004
                5945995
                29630961
                85e606b0-7a18-4817-a6a6-b82d194e9cc3
                © 2018 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 12 January 2018
                : 3 April 2018
                : 3 April 2018
                Categories
                Article

                Anatomy & Physiology
                body temperature,chronic stress,enrichment,welfare,gallus gallus domesticus,infrared thermography

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