Larger antelopes are sensitive to heat stress throughout all seasons but smaller antelopes only during summer in an African semi-arid environment

Abstract

Heat stress can limit the activity time budget of ungulates due to hyperthermia, which is relevant for African antelopes in ecosystems where temperature routinely increases above 40 °C. Body size influences this thermal sensitivity as large bodied ungulates have a lower surface area to volume ratio than smaller ungulates, and therefore a reduced heat dissipation capacity. We tested whether the activity pattern during the day of three antelope species of different body size—eland, blue wildebeest and impala—is negatively correlated with the pattern of black globe temperature (BGT) during the day of the ten hottest days and each season in a South African semi-arid ecosystem. Furthermore, we tested whether the larger bodied eland and wildebeest are less active than the smaller impala during the hottest days and seasons. Our results show that indeed BGT was negatively correlated with the diurnal activity of eland, wildebeest and impala, particularly during summer. During spring, only the activity of the larger bodied eland and wildebeest was negatively influenced by BGT, but not for the smallest of the three species, the impala. We argue that spring, with its high heat stress, coupled with poor forage and water availability, could be critical for survival of these large African antelopes. Our study contributes to understanding how endothermic animals can cope with extreme climatic conditions, which are expected to occur more frequently due to climate change.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Acocks J (1988) Memoirs of the botanical survey South Africa. Botanical Research Institute, Pretoria

    Google Scholar 

  2. Ahrestani FS, Van Langevelde F, Heitkönig IMA, Prins HHT (2012) Contrasting timing of parturition of Chital Axis axis and gaur Bos gaurus in tropical South India—the role of bodymass and seasonal forage quality. Oikos 121:1300–1310

    Article  Google Scholar 

  3. Bartholomew GA (1964) The roles of physiology and behaviour in the maintenance of homeostasis in the desert environment. In: Hughes GM, editor. Homeostatis and feedback mechanisms. Symposia of the society for experimental biology. Cambridge University Press, London, pp 7–29

  4. Beekman JH, Prins HHT (1989) Feeding strategies of sedentary large herbivores in East Africa, with emphasis on the African buffalo, Syncerus caffer. Afr J Ecol 27:129–147

    Article  Google Scholar 

  5. Bell R (1971) A grazing ecosystem in the Serengeti. Sci Am 225:86–93

    Article  Google Scholar 

  6. Bradley SR, Deavers DR (1980) A re-examination of the relationship between thermal conductance and body weight in mammals. Comp Biochem Physiol A Physiol 65:465–476

    Article  Google Scholar 

  7. Brown JS (1999) Vigilance, patch use and habitat selection: foraging under predation risk. Evol Ecol Res 1:49–71

    Google Scholar 

  8. Bunnell FL, Gillingham MP (1985) Foraging behaviour: Dynamics of dinning out. In: Hudson RJ, White RG (eds) Bioenergetics of wild herbivores. CRC, Boca Raton, pp 53–99

    Google Scholar 

  9. Cabanac M (1996) The place of behaviour in physiology. In: Fregly MJ, Blatteis CM (eds) Hand book of physiology. American Physiological Society and Oxford University Press, Oxford, pp 1523–1536

    Google Scholar 

  10. Calder WA (1984) Size, function and life history. Harvard University Press, Cambridge

    Google Scholar 

  11. Choshniak I, Ben-Kohav N, Taylor C, Robertshaw D, Barnes R, Dobson A, Belkin V, Shkolnik A (1995) Metabolic adaptations for desert survival in the Bedouin goat. Am J Physiol Regul Integr Comp Physiol 268:1101

    Google Scholar 

  12. Demment M, Van Soest P (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat 125:641–672

    Article  Google Scholar 

  13. du Toit JT, Yetman CA (2005) Effects of body size on the diurnal activity budgets of African browsing ruminants. Oecologia 143:317–325

    Article  Google Scholar 

  14. Dunbar RIM, Korstjens AH, Lehmann J (2009) Time as an ecological constraint. Biol Rev 84:413–429

    CAS  Article  Google Scholar 

  15. Fuller A, Moss DG, Skinner JD, Jessen PT, Mitchell G, Mitchell D (1999) Brain, abdominal and arterial blood temperatures of free-ranging eland in their natural habitat. Pflügers Arch 438:671–680

    CAS  Article  Google Scholar 

  16. Haim A, Skinner JD (1991) A comparative study of metabolic rates and thermoregulation of two African antelopes, the steenbok Raphicerus campestris and the blue duiker Cephalophus monticola. J Therm Biol 16:145–148

    Article  Google Scholar 

  17. Hetem RS, Maloney SK, Fuller A, Meyer LC, Mitchell D (2007) Validation of a biotelemetric technique, using ambulatory miniature black globe thermometers, to quantify thermoregulatory behaviour in ungulates. J Exp Zool A Ecol Genet Physiol 307:342–356

    Article  Google Scholar 

  18. Hetem RS, Mitchell D, Maloney SK, Meyer LCR, Fick LG, Kerley GIH, Fuller A (2008) Fever and sickness behavior during an opportunistic infection in a free-living antelope, the greater kudu Tragelaphus strepsiceros. Am J Physiol Regul Integr Comp Physiol 294:246–254

    Article  Google Scholar 

  19. Hetem RS, de Witt BA, Fick LG, Fuller A, Kerley GIH, Meyer LCR, Mitchell D, Maloney SK (2009) Body temperature, thermoregulatory behaviour and pelt characteristics of three colour morphs of springbok Antidorcas marsupialis. Comp Biochem Physiol A Mol Integr Physiol 152:379–388

    Article  Google Scholar 

  20. Hetem R, Strauss W, Fick L, Maloney S, Meyer L, 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 Biochem Syst Environ Physiol 180:1111–1119

    Article  Google Scholar 

  21. Hofmeyr MD (1981) Thermal physiology of selected African ungulates with emphasis on the physical properties of the pelage [PhD thesis]. University of Cape Town, Cape Town, South Africa

  22. Huey R (1991) Physiological consequences of habitat selection. Am Nat 137:91–115

    Article  Google Scholar 

  23. Hut RA, Kronfeld-Schor N, Van der Vinne V, De la Iglisia H (2012) In search of temporal niche: environmental factors. Progr in Brain Res 199:281

    Article  Google Scholar 

  24. Illius A, Gordon I (1987) The allometry of food intake in grazing ruminants. J Anim Ecol 56:989–999

    Article  Google Scholar 

  25. IPCC et al (2007) Climate change 2007: The physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. IPCC, Cambridge

    Google Scholar 

  26. Jarman P (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–267

    Article  Google Scholar 

  27. Kinahan AA, Pimm SL, van Aarde RJ (2007) Ambient temperature as a determinant of landscape use in the savanna elephant, Loxodonta africana. J Therm Biol 32:47–58

    Article  Google Scholar 

  28. Klein DR, Fairall N (1986) Comparative foraging behaviour and associated energetics of Impala and Blesbok. J Appl Ecol 23:489–502

    Article  Google Scholar 

  29. Leuthold BM, Leuthold W (1978) Daytime activity patterns of gerenuk and giraffe in Tsavo National Park, Kenya. Afr J Ecol 16:231–243

    Article  Google Scholar 

  30. Lewis JG (1977) Game domestication for animal production in Kenya: activity patterns of eland, oryx, buffalo and zebu cattle. J Agric Sci 89:551–563

    Article  Google Scholar 

  31. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  32. Lima SL, Zollner PA (1996) Towards a behavioral ecology of ecological landscapes. Trends Ecol Evol 11:131–135

    CAS  Article  Google Scholar 

  33. Lyon B (2009) Southern Africa summer drought and heat waves: observations and coupled model behavior. J Clim 22:6033–6046

    Article  Google Scholar 

  34. Malechek JC, Benton MS (1976) Behavior of range cows in response to winter weather. J Range Manage 29:9–12

    Article  Google Scholar 

  35. Maloiy GMO, Hopcraft D (1971) Thermoregulation and water relations of two east African antelopes: the hartebeest and impala. Comp Biochem Physiol A Physiol 38:525–534

    CAS  Article  Google Scholar 

  36. Maloiy G, Kanui T, Towett P, Wambugu S, Miaron J, Wanyoike M (2008) Effects of dehydration and heat stress on food intake and dry matter digestibility in East African ruminants. Comp Biochem Physiol A Mol Integr Physiol 151:185–190

    CAS  Article  Google Scholar 

  37. Maloney S, Moss G, Cartmell T, Mitchell D (2005) Alteration in diel activity patterns as a thermoregulatory strategy in black wildebeest Connochaetes gnou. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:1055–1064

    Article  Google Scholar 

  38. Maloney S, Fuller A, Mitchell D (2009) Climate change: is the dark Soay sheep endangered? Biol Lett 5:826

    Article  Google Scholar 

  39. McNab BK (2002) Short-term energy conservation in endotherms in relation to body mass, habits, and environment. J Therm Biol 27:459–466

    Article  Google Scholar 

  40. Mduma SAR, Sinclair ARE, Hilborn R (1999) Food regulates the Serengeti wildebeest: a 40-year record. J Anim Ecol 68:1101–1122

    Article  Google Scholar 

  41. Midgley DC, Pitman WV, Middleton BJ (1994) Surface water resources of South Africa 1990. Water Research Commission, Pretoria, South Africa

    Google Scholar 

  42. Natori Y, Porter WP (2007) Model of Japanese serow Capricornis crispus energetics predicts distribution on Honshu, Japan. Ecol Appl 17:1441–1459

    Article  Google Scholar 

  43. O’Connor TG, Kiker GA (2004) Collapse of the Mapungubwe society: vulnerability of pastoralism to increasing aridity. Clim Change 66:49–66

    Article  Google Scholar 

  44. Ogutu JO, Piepho HP, Dublin HT, Bhola N, Reid RS (2008) Rainfall influences on ungulate population abundance in the Mara-Serengeti ecosystem. J Anim Ecol 77:814–829

    CAS  Article  Google Scholar 

  45. Owen-Smith N (1988) Megaherbivores: The influence of very large size in ecology. Cambridge University Press, Cambridge

    Google Scholar 

  46. Owen-Smith N (1994) Foraging responses of Kudus to seasonal changes in food resources: elasticity in constraints. Ecology 75:1050–1062

    Article  Google Scholar 

  47. Owen-Smith N (1998) How high ambient temperature affects the daily activity and foraging time of a subtropical ungulate, the greater kudu Tragelaphus strepsiceros. J Zool 246:183–192

    Article  Google Scholar 

  48. Peter RH (1986) The ecological implications of body size. Cambridge University Press, New York

    Google Scholar 

  49. Phillips PK, Heath JE (1995) Dependency of surface temperature regulation on body size in terrestrial mammals. J Therm Biol 20:281–289

    Article  Google Scholar 

  50. Porter WB, Gates DM (1969) Thermodynamic equilibria of animals with environment. Ecol Monogr 39:227–244

    Article  Google Scholar 

  51. Porter WP, Kearney M (2009) Size, shape, and the thermal niche of endotherms. Proc Natl Acad Sci USA 106:19666–19672

    CAS  Article  Google Scholar 

  52. Porter WP, Budaraju S, Stewart WE, Ramankutty N (2000) Calculating climate effects on birds and mammals: Impacts ob biodiversity, conservation, population parameters and global community structure. Amer Zool 40:597–630

    Article  Google Scholar 

  53. Prins HHT, Van Langevelde F (2008) Assembling a diet from different places. In: Prins HHT, Van Langevelde F (eds) Resource ecology. Spatial and temporal dynamics of foraging. Springer, Dordrecht, The Netherlands, pp 129–155

    Google Scholar 

  54. Schmidt-Nielsen K (1975) Scaling in biology: the consequences of size. J Exp Zool 194:297–307

    Google Scholar 

  55. Schmidt-Nielsen K (1984) Why is animal size so important? Cambridge University Press, New York

    Google Scholar 

  56. Shrestha AK, Van Wieren SE, Van Langevelde F, Fuller A, Hetem RS, Meyer LCR, De Bie S, Prins HHT (2012) Body temperature variation of South African antelopes in two climatically contrasting environments. J Therm Biol 37:171–178

    Article  Google Scholar 

  57. Sih A, Stamps J, Yang LH, McElreath R, Ramenofsky M (2010) Behavior as a key component of integrative biology in a human-altered world. Integr Comp Biol 50:934–944

    Article  Google Scholar 

  58. Speakman JR, Król EC (2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79:726–746

    Google Scholar 

  59. Taylor CR (1974) Low metabolism of Zebu cattle during droughts: A domestic animal strategy for survival in hot desert. Proceeding of international congress in physiological science. Jerusalem satellite symposium, p 1

  60. Vernon HM (1932) The measurement of radiant heat in relation to human comfort. J Ind Hyg Toxicol 14:95–111

    Google Scholar 

  61. Wang T, Hung C, Randall D (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68:223–251

    Article  Google Scholar 

  62. Warburton M, Schulze R, Maharaj M (2005) Is South Africa’s temperature changing? An analysis of trends from daily records, 1950–2000. Climate change and water resources in Southern Africa: studies on scenarios, impacts, vulnerabilities and adaptation. WRC report 1430/1/05. Water Research Commission, Pretoria, South Africa

  63. Willmer P, Stone G, Johnston I (2005) Environmental physiology of animals. Blackwell Publishing, Oxford

    Google Scholar 

  64. Zar J (2009) Biostatistical analysis. Prentice-Hall Englewood Cliffs, New Jersey

    Google Scholar 

Download references

Acknowledgments

We thank South African National Park, in particular Dr. Rina Grant and Dr. Stefanie Freitag (scientific services), Dr. Peter Buss, Grant Knight, Dr. Danny Govender, Nmo Khosi and Dr. Jenny Joubert (veterinary wildlife services), Stefan Stellier and rangers (Mapungubwe National Park). Finally, we would like to thank the Brain Function Research Group and Central Animal Services, University of Witwatersrand, South Africa for hosting Anil Shrestha and providing research equipment. This research was funded by Shell Research Foundation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to A. K. Shrestha.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Shrestha, A.K., van Wieren, S.E., van Langevelde, F. et al. Larger antelopes are sensitive to heat stress throughout all seasons but smaller antelopes only during summer in an African semi-arid environment. Int J Biometeorol 58, 41–49 (2014). https://doi.org/10.1007/s00484-012-0622-y

Download citation

Keywords

  • Activity pattern
  • Body size
  • Heat stress
  • Diurnal
  • Nocturnal
  • Thermoregulation