Large mammals that live in arid and/or desert environments can cope with seasonal and local variations in rainfall, food and climate1 by moving long distances, often without reliable water or food en route. The capacity of an animal for this long-distance travel is substantially dependent on the rate of energy utilization and thus heat production during locomotion—the cost of transport2,3,4. The terrestrial cost of transport is much higher than for flying (7.5 times) and swimming (20 times)4. Terrestrial migrants are usually large1,2,3 with anatomical specializations for economical locomotion5,6,7,8,9, because the cost of transport reduces with increasing size and limb length5,6,7. Here we used GPS-tracking collars10 with movement and environmental sensors to show that blue wildebeest (Connochaetes taurinus, 220 kg) that live in a hot arid environment in Northern Botswana walked up to 80 km over five days without drinking. They predominantly travelled during the day and locomotion appeared to be unaffected by temperature and humidity, although some behavioural thermoregulation was apparent. We measured power and efficiency of work production (mechanical work and heat production) during cyclic contractions of intact muscle biopsies from the forelimb flexor carpi ulnaris of wildebeest and domestic cows (Bos taurus, 760 kg), a comparable but relatively sedentary ruminant. The energetic costs of isometric contraction (activation and force generation) in wildebeest and cows were similar to published values for smaller mammals. Wildebeest muscle was substantially more efficient (62.6%) than the same muscle from much larger cows (41.8%) and comparable measurements that were obtained from smaller mammals (mouse (34%)11 and rabbit (27%)). We used the direct energetic measurements on intact muscle fibres to model the contribution of high working efficiency of wildebeest muscle to minimizing thermoregulatory challenges during their long migrations under hot arid conditions.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
The authors declare that all relevant processed data supporting the findings of this study are available as Source Data. Further data are available from the corresponding authors upon reasonable request.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Schmidt-Nielsen, K. Desert Animals: Physiological Problems of Heat and Water (Clarendon, Oxford, 1965).
Hedenström, A. Optimal migration strategies in animals that run: a range equation and its consequences. Anim. Behav. 66, 631–636 (2003).
Hein, A. M., Hou, C. & Gillooly, J. F. Energetic and biomechanical constraints on animal migration distance. Ecol. Lett. 15, 104–110 (2012).
Tucker, V. A. The energetic cost of moving about: walking and running are extremely inefficient forms of locomotion. Much greater efficiency is achieved by birds, fish—and bicyclists. Am. Sci. 63, 413–419 (1975).
Taylor, C. R., Heglund, N. C. & Maloiy, G. M. O. Energetics and mechanics of terrestrial locomotion. I. Metabolic energy consumption as a function of speed and body size in birds and mammals. J. Exp. Biol. 97, 1–21 (1982).
Kram, R. & Taylor, C. R. Energetics of running: a new perspective. Nature 346, 265–267 (1990).
Wilson, A. M., Watson, J. C. & Lichtwark, G. A. Biomechanics: a catapult action for rapid limb protraction. Nature 421, 35–36 (2003).
Alexander, R., Maloiy, G. M. O., Njau, R. & Jayes, A. Mechanics of running of the ostrich (Struthio camelus). J. Zool. 187, 169–178 (1979).
Alexander, R., Maloiy, G. M. O., Ker, R., Jayes, A. & Warui, C. The role of tendon elasticity in the locomotion of the camel (Camelus dromedarius). J. Zool. 198, 293–313 (1982).
Wilson, A. M. et al. Locomotion dynamics of hunting in wild cheetahs. Nature 498, 185–189 (2013).
Barclay, C. J. Efficiency of fast- and slow-twitch muscles of the mouse performing cyclic contractions. J. Exp. Biol. 193, 65–78 (1994).
Hetem, R. S., Maloney, S. K., Fuller, A., Meyer, L.C. & Mitchell, D. Validation of a biotelemetric technique, using ambulatory miniature black globe thermometers, to quantify thermoregulatory behaviour in ungulates. J. Exp. Zool. 307A, 342–356 (2007).
Estes, R. The Behavior Guide to African Mammals Vol. 64 (Univ. California Press, Berkeley, 1991).
Kuo, A. D. A simple model of bipedal walking predicts the preferred speed-step length relationship. J. Biomech. Eng. 123, 264–269 (2001).
Bertram, J. E. Constrained optimization in human walking: cost minimization and gait plasticity. J. Exp. Biol. 208, 979–991 (2005).
Kohn, T. A., Curry, J. W. & Noakes, T. D. Black wildebeest skeletal muscle exhibits high oxidative capacity and a high proportion of type IIx fibres. J. Exp. Biol. 214, 4041–4047 (2011).
Woledge, R. C. The energetics of tortoise muscle. J. Physiol. 197, 685–707 (1968).
Williams, T. L. Experimental analysis of the gait and frequency of locomotion in the tortoise, with a simple mathematical description. J. Physiol. 310, 307–320 (1981).
Barclay, C. J. Energetics of contraction. Compr. Physiol. 5, 961–995 (2015).
Butler, P. J. et al. Respiratory and cardiovascular adjustments during exercise of increasing intensity and during recovery in thoroughbred racehorses. J. Exp. Biol. 179, 159–180 (1993).
Hetem, R. S., Maloney, S. K., Fuller, A. & Mitchell, D. Heterothermy in large mammals: inevitable or implemented? Biol. Rev. Camb. Philos. Soc. 91, 187–205 (2016).
Valeix, M. et al. Behavioral adjustments of African herbivores to predation risk by lions: spatiotemporal variations influence habitat use. Ecology 90, 23–30 (2009).
MacFarlane, W. V., Howard, B., Haines, H., Kennedy, P. & Sharpe, C. M. Hierarchy of water and energy turnover of desert mammals. Nature 234, 483–484 (1971).
Maloiy, G. M. O. Water economy of the Somali donkey. Am. J. Physiol. 219, 1522–1527 (1970).
Wilson, A. M. et al. Biomechanics of predator–prey arms race in lion, zebra, cheetah and impala. Nature 554, 183–188 (2018).
Dewhirst, O. P. et al. Improving the accuracy of estimates of animal path and travel distance using GPS drift-corrected dead reckoning. Ecol. Evol. 6, 6210–6222 (2016).
Hubel, T. Y. et al. Energy cost and return for hunting in African wild dogs and cheetahs. Nat. Commun. 7, 11034 (2016).
Hubel, T. Y. et al. Additive opportunistic capture explains group hunting benefits in African wild dogs. Nat. Commun. 7, 11033 (2016).
West, T. G. et al. Power output of skinned skeletal muscle fibres from the cheetah (Acinonyx jubatus). J. Exp. Biol. 216, 2974–2982 (2013).
Barclay, C. J., Woledge, R. C. & Curtin, N. A. Is the efficiency of mammalian (mouse) skeletal muscle temperature dependent? J. Physiol. 588, 3819–3831 (2010).
Kretzschmar, K. M. & Wilkie, D. R. The use of the Peltier effect for simple and accurate calibration of thermoelectric devices. Proc. R. Soc. Lond. B 190, 315–321 (1975).
Woledge, R. C., Curtin, N. A. & Homsher, E. Energetic aspects of muscle contraction. Monogr. Physiol. Soc. 41, 1–357 (1985).
Hill, A. Trails and Trials in Physiology (E. Arnold, London, 1965).
Phillips, S. K., Takei, M. & Yamada, K. The time course of phosphate metabolites and intracellular pH using 31P NMR compared to recovery heat in rat soleus muscle. J. Physiol. 460, 693–704 (1993).
Curtin, N. A. & Woledge, R. C. Efficiency of energy conversion during sinusoidal movement of white muscle fibres from the dogfish, Scyliorhinus canicula. J. Exp. Biol. 183, 137–147 (1993).
Barclay, C. J. Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J. Physiol. 497, 781–794 (1996).
Curtin, N. A. & Woledge, R. C. Efficiency of energy conversion during shortening of muscle fibres from the dogfish Scyliorhinus canicula. J. Exp. Biol. 158, 343–353 (1991).
Rumble, J. R. (ed.) CRC Handbook of Chemistry and Physics 99th edn (CRC, Boca Raton, 2018).
Hetem, R. S. et al. 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, 1111–1119 (2010).
Maloiy, G. M. O. Water metabolism of East African ruminants in arid and semi-arid regions. Z. Tierzuecht. Zuechtungsbiol. 90, 219–228 (1973).
We thank R. Woledge for contributing to early design of experiments; C. Barclay for helping us to fabricate the thermocouple elements; our field assistants, N. Terry and M. Claase; A. R. Wilson for logistical support and editorial contributions; M. Flyman (Department of Wildlife and National Parks) for his support and enthusiasm and J. O’Connor and P. O’Riordan (Dawn Meats, Bedford) for enabling cow muscle collection. Funding was provided by the EPSRC (EP/H013016/1), BBSRC (BB/J018007/1) and ERC (323041). A Botswana Research Permit EWT 8/36/4 was held by A.M.W. and A.M.W. was a registered Botswana veterinarian.
Nature thanks J. E. A. Bertram, R. Hetem and the other anonymous reviewer(s) for their contribution to the peer review of this work.
Extended data figures and tables
Extended Data Fig. 1 Comparison of temperature maxima and minima recorded in the collars and at weather stations.
The number of working collar sensors varied; therefore, a median was taken from all available data on each day and the maximum and minimum value for each day, which was then averaged over each month. The monthly maximum temperature (mean ± s.d.) was 5.6 ± 0.6 °C higher at the weather stations than the collars and the monthly minimum temperature was, on average, 3.6 ± 1.1 °C lower at the weather stations than the collars. n = 12. Ambient temperature exceeded body temperature of 38 °C (horizontal dashed line) during nine months of the year. Note weather stations were 10 km away from the river in the dry season range, while animals were in the wet season range to the east from November to April approximately. (Fig. 1b, c).
a, Pattern of lever movement. Frequency of 0.5 Hz and peak-to-peak amplitude 18% Lo (10% Lo). Lo is the fibre bundle length at which isometric force was greatest. Values for cow experiments are in parentheses, where they are different than those for wildebeest. b, Stimulus duty cycles used in the experiments. Top to bottom, duty cycle of 0.1, 0.2, 0.3 and 0.4 (0.2 and 0.3). c, Stimulus phases used in the experiments. Top to bottom: phase −0.2, −0.1, 0, 0.1, 0.2 and 0.3. (−0.2 to 0.1). Phase = 0.0 corresponds to the stimulus starting when shortening starts. In this example, DC = 0.4. Source data
Extended Data Fig. 4 Efficiency versus stimulus phase for individual muscle fibre bundles from wildebeest and cows.
a–f, Data from wildebeest. g–k, Data from cows. Relationship between stimulus phase and efficiency during three cycles of movement at 0.5 Hz for stimulus duty cycles (DC). Circle, DC = 0.4; square, DC = 0.3; triangle, DC = 0.2; diamond, DC = 0.1. Efficiency = power per rate of heat + work output. a, b, d, Data are from a different muscle fibre bundle each from a different wildebeest. c, Data are the average of the values shown in e and f, which are results for two fibre bundles from the same wildebeest. g–k, Data are from a different fibre bundle from a different cow. Source data