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      Body Temperature during Hibernation Is Highly Correlated with a Decrease in Circulating Innate Immune Cells in the Brown Bear ( Ursus arctos): A Common Feature among Hibernators?

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          Abstract

          Background: Hibernation involves periods of severely depressed metabolism (torpor) and decreases in body temperature (Tb). Small arctic mammals (<5kg), in which Tb generally drop drastically, display leukopenia during hibernation. This raised the question of whether the decreased leukocyte counts in mammalian hibernators is due to torpor per se or is secondary to low Tb. The present study examined immune cell counts in brown bears ( Ursus arctos), where torpor is only associated with shallow decreases in Tb. The results were compared across hibernator species for which immune and Tb data were available.

          Methods and Results: The white blood cell counts were determined by flow cytometry in 13 bears captured in the field both during summer and winter over 2 years time. Tb dropped from 39.6±0.8 to 33.5±1.1°C during hibernation. Blood neutrophils and monocytes were lower during hibernation than during the active period (47%, p= 0.001; 43%, p=0.039, respectively), whereas no change in lymphocyte counts was detected (p=0.599). Further, combining our data and those from 10 studies on 9 hibernating species suggested that the decline in Tb explained the decrease in innate immune cells (R 2=0.83, p<0.0001).

          Conclusions: Bears have fewer innate immune cells in circulation during hibernation, which may represent a suppressed innate immune system. Across species comparison suggests that, both in small and large hibernators, Tb is the main driver of immune function regulation during winter dormancy. The lack of a difference in lymphocyte counts in this context requires further investigations.

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          Most cited references39

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          Hibernation in black bears: independence of metabolic suppression from body temperature.

          Black bears hibernate for 5 to 7 months a year and, during this time, do not eat, drink, urinate, or defecate. We measured metabolic rate and body temperature in hibernating black bears and found that they suppress metabolism to 25% of basal rates while regulating body temperature from 30° to 36°C, in multiday cycles. Heart rates were reduced from 55 to as few as 9 beats per minute, with profound sinus arrhythmia. After returning to normal body temperature and emerging from dens, bears maintained a reduced metabolic rate for up to 3 weeks. The pronounced reduction and delayed recovery of metabolic rate in hibernating bears suggest that the majority of metabolic suppression during hibernation is independent of lowered body temperature.
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            Temperature-Dependent Growth of Geomyces destructans, the Fungus That Causes Bat White-Nose Syndrome

            White-nose syndrome (WNS) is an emergent disease estimated to have killed over five million North American bats. Caused by the psychrophilic fungus Geomyces destructans, WNS specifically affects bats during hibernation. We describe temperature-dependent growth performance and morphology for six independent isolates of G. destructans from North America and Europe. Thermal performance curves for all isolates displayed an intermediate peak with rapid decline in performance above the peak. Optimal temperatures for growth were between 12.5 and 15.8°C, and the upper critical temperature for growth was between 19.0 and 19.8°C. Growth rates varied across isolates, irrespective of geographic origin, and above 12°C all isolates displayed atypical morphology that may have implications for proliferation of the fungus. This study demonstrates that small variations in temperature, consistent with those inherent of bat hibernacula, affect growth performance and physiology of G. destructans, which may influence temperature-dependent progression and severity of WNS in wild bats.
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              Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology

              White-nose syndrome (WNS) is causing unprecedented declines in several species of North American bats. The characteristic lesions of WNS are caused by the fungus Geomyces destructans, which erodes and replaces the living skin of bats while they hibernate. It is unknown how this infection kills the bats. We review here the unique physiological importance of wings to hibernating bats in relation to the damage caused by G. destructans and propose that mortality is caused by catastrophic disruption of wing-dependent physiological functions. Mechanisms of disease associated with G. destructans seem specific to hibernating bats and are most analogous to disease caused by chytrid fungus in amphibians.
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                Author and article information

                Journal
                Int J Med Sci
                Int J Med Sci
                ijms
                International Journal of Medical Sciences
                Ivyspring International Publisher (Sydney )
                1449-1907
                2013
                11 March 2013
                : 10
                : 5
                : 508-514
                Affiliations
                1. Department of Clinical Medicine, School of Health and Medical Sciences, Örebro University, SE-701 82 Örebro, Sweden.
                2. Department of Forestry and Wildlife Management, Hedmark University College, Campus Evenstad NO-2418 Elverum, Norway.
                3. Section of Arctic Veterinary Medicine, Norwegian School of Veterinary Science, NO-9292 Tromsø, Norway.
                4. Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden.
                5. Department of Cardiology, Örebro University Hospital, SE-701 85 Örebro, Sweden.
                6. Université de Strasbourg, IPHC, 23 rue Becquerel 67087 Strasbourg, France, CNRS, UMR7178, 67037 Strasbourg, France.
                Author notes
                ✉ Corresponding author: Eva Särndahl, School of Health and Medical Sciences/KFC, Örebro University Hospital, SE-701 85 Örebro, Sweden. Phone: +46 19 602 6653 (+46 707 43 0897 cell) Fax: +46 19 602 6650 e-mail: eva.sarndahl@ 123456oru.se .

                Competing Interests: The authors have declared that no competing interest exists.

                Article
                ijmsv10p0508
                10.7150/ijms.4476
                3607235
                23532623
                27da98e7-f2c8-4bdb-be0c-a9b4a53386f8
                © Ivyspring International Publisher. This is an open-access article distributed under the terms of the Creative Commons License (http://creativecommons.org/licenses/by-nc-nd/3.0/). Reproduction is permitted for personal, noncommercial use, provided that the article is in whole, unmodified, and properly cited.
                History
                : 16 April 2012
                : 10 February 2013
                Categories
                Research Paper

                Medicine
                brown bear,hibernation,innate immunity,leukocytes,torpor.,ursus arctos
                Medicine
                brown bear, hibernation, innate immunity, leukocytes, torpor., ursus arctos

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