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Three African antelope species with varying water dependencies exhibit similar selective brain cooling

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Abstract

The use of selective brain cooling, where warm arterial blood destined for the brain is cooled in the carotid rete via counter-current heat exchange when in close proximity to cooler venous blood, contributes to the conservation of body water. We simultaneously measured carotid blood and hypothalamic temperature in four gemsbok, five red hartebeest and six blue wildebeest to assess the extent to which these free-living animals, with varying water dependency, routinely rely on selective brain cooling. We investigated the hypothesis that innate differences in selective brain cooling exist in large, sympatric artiodactyls with varying water dependency. All three species used selective brain cooling, without any discernible differences in three selective brain cooling indices. GLMMs revealed no species differences in the threshold temperature for selective brain cooling (z = 0.79, P = 0.43), the magnitude (z = −0.51, P = 0.61), or the frequency of selective brain cooling use (z = −0.47, P = 0.64), after controlling for carotid blood temperature and black globe temperature. Comparison of anatomical attributes of the carotid retes of the three species revealed that the volume (F 2,9 = 5.54, P = 0.03) and height (F 2,9 = 5.43, P = 0.03) of the carotid rete, per kilogram body mass, were greater in the red hartebeest than in the blue wildebeest. Nevertheless, intraspecific variability in the magnitude, the frequency of use, and the threshold temperature for selective brain cooling exceeded any interspecific variability in the three indices of selective brain cooling. We conclude that the three species have similar underlying ability to make use of selective brain cooling in an environment with freely available water. It remains to be seen to what extent these three species would rely on selective brain cooling, as a water conservation mechanism, when challenged by aridity, a condition likely to become prevalent throughout much of southern Africa under future climate change scenarios.

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Acknowledgments

This study was funded through a National Research Foundation (NRF) Thuthuka grant (Grant Code: 76248), the University of the Witwatersrand Medical Faculty Research Endowment Fund, the University of South Africa’s MDSP Plus programme, and the British Ecological Society’s Overseas Bursary and Fellowship Scheme (Grant Code: 3201/3973), all awarded to WMS, and the Harry Oppenheimer Fellowship awarded to DM. This publication was also made possible (in part) by a grant from the Carnegie Corporation of New York and a Faculty of Health Sciences Research Committee minor capex grant awarded to RSH. The statements made and views expressed are, however, solely the responsibility of the authors. We thank Rooipoort Nature Reserve for access to their facilities and De Beers Consolidated for permission to carry out the research on their property. We also thank Emma Rambert for veterinary support and animal capture, Mary-Ann Costello, Benjamin Rey, Zipho Zwane and Linda Fick for assistance during gruelling field surgery, Gregg Gibbs and Herb Friedl for animal recovery, and Duncan MacFadyen (E. Oppenheimer and Son) and Andrew Stainthorpe (Manager: Rooipoort Nature Reserve) for enthusiastic support. Theunis Broekman assisted with silicone cast preparations, Bridget Mitchell and Joy Atalan assisted with cast preparation and John Maina advised on measurement options. Richard McFarland provided valuable insights into the use of GLMMs.

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Correspondence to W. Maartin Strauss.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. The Animal Ethics Screening Committee of the University of the Witwatersrand approved the procedures (clearance 2011/36/05). Permits to conduct the research were provided by the Department of Environment and Nature Conservation, Northern Cape Province, South Africa (permits Fauna 846/2011 and 848/2011).

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Communicated by G. Heldmaier.

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Strauss, W.M., Hetem, R.S., Mitchell, D. et al. Three African antelope species with varying water dependencies exhibit similar selective brain cooling. J Comp Physiol B 186, 527–540 (2016). https://doi.org/10.1007/s00360-016-0968-2

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