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Remarkable muscles, remarkable locomotion in desert-dwelling wildebeest

Abstract

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.

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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.

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Acknowledgements

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.

Reviewer information

Nature thanks J. E. A. Bertram, R. Hetem and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

A.M.W., N.A.C. and H.L.A.B.-B. conceived, designed and led the study; H.L.A.B.-B. and E.B. led and organized field work. A.M.W. performed veterinary procedures and biopsies. N.A.C., A.R.G.-M., M.L. and T.G.W. undertook muscle experiments and N.A.C. and A.R.G.-M. analysed and interpreted muscle data. J.C.L., A.M.W. and S.J.A. designed and built collars and weather stations. T.Y.H., A.M.W. and H.L.A.B.-B. analysed and interpreted collar data, A.M.W. made the water balance model and A.M.W. and N.A.C. wrote paper with input from all authors.

Competing interests

The authors declare no competing interests.

Correspondence to Nancy A. Curtin or Alan M. Wilson.

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).

Extended Data Fig. 2 Controlled variables for muscle length and stimulation pattern.

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. 3 Individual data points for muscle mechanical and energetic performance.

Data presented in Fig. 3, but subdivided by duty cycle. The mean is plotted, symbols and line colours are as in Fig. 3, n numbers are given in Extended Data Table 2. Source data

Extended Data Fig. 4 Efficiency versus stimulus phase for individual muscle fibre bundles from wildebeest and cows.

af, Data from wildebeest. gk, 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. gk, Data are from a different fibre bundle from a different cow. Source data

Extended Data Table 1 Subject data
Extended Data Table 2 n values
Extended Data Table 3 Minimum cost per unit impulse, values and comparison by species
Extended Data Table 4 Maximum enthalpy efficiency value for muscle fibre bundles from wildebeest and cow
Extended Data Table 5 Values of maximum enthalpy efficiency for locomotor muscles from different species
Extended Data Table 6 Calculation of cross-bridge work from enthalpy efficiency

Supplementary information

Reporting Summary

Source data

Source Data Fig. 1

Source Data Fig. 2

Source Data Fig. 3

Source Data Extended Data Fig. 2

Source Data Extended Data Fig. 3

Source Data Extended Data Fig. 4

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Further reading

Fig. 1: Locomotion of desert wildebeest.
Fig. 2: Example records.
Fig. 3: Muscle mechanical and energetic performance.
Extended Data Fig. 1: Comparison of temperature maxima and minima recorded in the collars and at weather stations.
Extended Data Fig. 2: Controlled variables for muscle length and stimulation pattern.
Extended Data Fig. 3: Individual data points for muscle mechanical and energetic performance.
Extended Data Fig. 4: Efficiency versus stimulus phase for individual muscle fibre bundles from wildebeest and cows.

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