Abstract
To conserve body water, mammals may reduce evaporative water loss by storing heat, allowing core body temperature to rise more than usual during the day, and to fall more than usual during the cooler night, so demonstrating heterothermy. It has been proposed that elephants are heterothermic, but body temperature never has been measured in elephants over 24 h at environmental temperatures higher than body temperature, where elephants would have to rely on evaporative cooling to maintain homeothermy. We used ingested temperature data loggers to record core temperature of four partly free-ranging savanna elephants exposed to high solar radiation and environmental temperatures that exceeded core temperature (> 36 °C) in their natural habitat. The elephants maintained core temperature at an average 36.6 °C within narrow daily limits of about 1.3 °C. While mean 24-h core temperature increased with maximum air temperature, it did not increase with mean air temperature. Maximum and minimum daily core temperatures also did not change with maximum air temperatures. As a result, core temperature range remained constant despite large variations in daily air temperatures. Contrary to the view that elephants exhibit heterothermy to cope with heat, savanna elephants in their natural habitat with access to adequate resources of food and water, and able to use thermoregulatory behaviour, maintained homeothermy.



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References
Alamer M (2006) Physiological responses of Saudi Arabia indigenous goats to water deprivation. Small Ruminant Res 63:100–109
Aschoff J (1982) The circadian rhythm of body temperature as a function of body size. In: Taylor C, Johansen K, Bolis L (eds) A comparison of animal physiology. Cambridge University Press, Cambridge, pp 173–187
Bouâouda H, Achâaban MR, Ouassat M, Oukassou M, Piro M, Challet E, El Allali K, Pévet P (2014) Daily regulation of body temperature rhythm in the camel (Camelus dromedarius) exposed to experimental desert conditions. Physiol Rep 2(9):.e12151
Boyles JG, Smit B, McKechnie AE (2011) A new comparative metric for estimating heterothermy in endotherms. Physiol Biochem Zool 84:115–123
Brown-Brand T, Yanagi T, Xin H, Gates R, Bucklin R, Ross G (2003) A new telemetry system for measuring core body temperature in livestock and poultry. Appl Eng Agric 19:583–589
Dunkin RC, Wilson D, Way N, Johnson K, Williams TM (2013) Climate influences thermal balance and water use in African and Asian elephants: physiology can predict drivers of elephant distribution. J Exp Biol 216:2939–2952
Elder WH, Rodgers DH (1975) Body temperature in the African elephant as related to ambient temperature. Mammalia 39:395–400
Finch VA, Robertshaw D (1979) Effect of dehydration on thermoregulation in eland and hartebeest. Am J Physiol Regul Integr Comp Physiol 237:192–196
Fuller A, Moss D, Skinner J, Jessen P, Mitchell G, Mitchell D (1999) Brain, abdominal and arterial blood temperatures of free-ranging eland in their natural habitat. Pflügers Arch Eur J Appl Physiol 438:671–680
Fuller A, Mitchell D, Maloney SK, Hetem RS (2016) Towards a mechanistic understanding of the responses of large terrestrial mammals to heat and aridity associated with climate change. Clim Change Responses 3(1):10. https://doi.org/10.1186/s40665-016-0024-1
Green A, Gates R, Lawrence L (2005) Measurement of horse core body temperature. J Therm Biol 30:370–377
Hetem RS, Malony SK, Fuller A, Meyer LCR, Mitchell D (2007) Validation of a biotelemetric technique, using ambulatory miniature black globe thermometers, to quantify thermoregulatory behaviour in ungulates. J Exp Zool 307:342–356
Hetem RS, Strauss WM, Fick LG, Maloney SK, Meyer LCR, Shobrak M, Fuller A, Mitchell D (2010) Variation in the daily rhythm of body temperature of free-living Arabian oryx (Oryx leucoryx): does water limitation drive heterothermy? J Comp Physiol B 180(70):1111–1119
Hetem RS, Strauss WM, Fick LG, Maloney SK, Meyer LCR, Shobrak M, Fuller A, Mitchell D (2011) Does size matter? Comparison of body temperature and activity of free-living Arabian oryx (Oryx leucoryx) and the smaller Arabian sand gazelle (Gazella subgutturosa marica) in the Saudi desert. J Comp Physiol B 182:437–449
Hetem RS, Maloney SK, Fuller A, Mitchell D (2016) Heterothermy in large mammals: inevitable or implemented? Biol Rev 91:187–205
Hidden PA (2009) Thermoregulation in African elephants (Loxodonta africana). MSc thesis, University of Witwatersrand, Johannesburg
Hiley P (1975) How the elephant keeps its cool. Natural History 84:34–40
Kinahan AA, Inge-Moller R, Bateman PW, Kotze A, Scantlebury M (2007) Body temperature daily rhythm adaptations in African savanna elephants (Loxodonta africana). Physiol Behav 92:560–565
Kusuda S, Wakimoto T, Nishimura K, Kawakami S, Okuda K, Saito E, Shimada T, Sakamoto H, Yanagimoto H, Seitaro WADA, Nishio K (2007) Relationship between body temperature and ovarian cycle in Asian and African elephants. J Reprod Dev 53(5):1099–1105
Leggett K (2008) Diurnal activities of the desert-dwelling elephants in northwestern Namibia. Pachyderm 45:20–33
Maloney SK, Marsh MK, McLeod SR, Fuller A (2017) Heterothermy is associated with reduced fitness in wild rabbits. Biology letters 13(12):20170521
McKechnie AE, Mzilikazi N (2011) Heterothermy in afrotropical mammals and birds: a review. Integr Comp Biol 51:349–363
McKenzie JE, Osgood DW (2004) Validation of a new telemetric core temperature monitor. J Therm Biol 29(7):605–611
Mitchell D, Maloney S, Jessen C, Laburn H, Kamerman P, Mitchell G, Fuller A (2002) Adaptive heterothermy and selective brain cooling in arid-zone mammals. Comp Biochem Physiol B 131:571–585
Mitchell D, Snelling EP, Hetem RS, Maloney SK, Strauss WM, Fuller A (2018) Revisiting concepts of thermal physiology: predicting responses of mammals to climate change. J Anim Ecol. https://doi.org/10.1111/1365-2656.12818
Mole MA, D’Araujo SR, van Aarde RJ, Mitchell D, Fuller A (2016) Coping with heat: behavioural and physiological responses of savanna elephants in their natural habitat. Conserv Physiol 4(1):cow044. https://doi.org/10.1093/conphys/cow044
Ostrowski S, Williams JB, Ismael K (2003) Heterothermy and the water economy of free-living Arabian oryx (Oryx leucoryx). J Exp Biol 206:1471–1478
Pinheiro J, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1–113
R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-90051-07-0,URL http://www.R-project.org/
Ramey EM, Ramey RR, Brown LM, Kelley ST (2013) Desert-dwelling African elephants (Loxodonta africana) in Namibia dig wells to purify drinking water. Pachyderm 53(66):.e72
Rowe MF, Bakken GS, Ratliff JJ, Langman VA (2013) Heat storage in Asian elephants during submaximal exercise: behavioural regulation of thermoregulatory constraints on activity in endothermic gigantotherms. J Exp Biol 216:1774–1785
Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90(3):891–926. https://doi.org/10.1111/brv.12137
Schmidt-Nielsen K, Schmidt-Nielsen B, Jarnum SA, Houpt TR (1957) Body temperature of the camel and its relation to water economy. Am J Physiol 188:103–112
Viljoen PJ (1989) Spatial distribution and movements of elephants (Loxodonta africana) in the northern Namib Desert region of the Kaokoveld, South West Africa/Namibia. J Zool 219(1):1–19
Weissenböck NM, Schober F, Fluch G, Weiss C, Paumann T, Schwarz C, Arnold W (2010) Reusable biotelemetric capsules: a convenient and reliable method for measuring core body temperature in large mammals during gut passage. J Therm Biol 35(3):147–153
Weissenböck NM, Arnold W, Ruf T (2012) Taking the heat: thermoregulation in Asian elephants under different climatic conditions. J Comp Physiol B 182:311–319
Acknowledgements
Logistical support was provided by Elephants Without Borders and the University of Witwatersrand’s Brain Function Research Group. The staff of Abu Camp provided field assistance and logistical support. The research was sanctioned by the Botswana Department of Wildlife and National Parks. Financial support for this study was provided by the Paul G. Allen Family Foundation via Elephants Without Borders, the International Fund for Animal Welfare and the University of Pretoria.
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The datasets generated during the current study are available from the corresponding author on reasonable request.
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All procedures were approved by the Animal Use and Care Committee at the University of Pretoria (Ref: EC073-12).
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Communicated by I.D. Hume.
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Mole, M.A., Rodrigues DÁraujo, S., van Aarde, R.J. et al. Savanna elephants maintain homeothermy under African heat. J Comp Physiol B 188, 889–897 (2018). https://doi.org/10.1007/s00360-018-1170-5
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DOI: https://doi.org/10.1007/s00360-018-1170-5