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Predation risk constrains herbivores’ adaptive capacity to warming

Nature Ecology & Evolution volume 4, pages 1069–1074 (2020)Cite this article

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Abstract

Global warming compels larger endothermic animals to adapt either physiologically or behaviourally to avoid thermal stress, especially in tropical ecosystems. Their adaptive responses may however be compromised by other constraints, such as predation risk or starvation. Using an exceptional camera-trap dataset spanning 32 protected areas across southern Africa, we find that intermediate-sized herbivores (100–550 kg) switch activity to hotter times of the day when exposed to predation by lions. These herbivores face a tight window for foraging activity being exposed to nocturnal predation and to heat during the day, suggesting a trade-off between predation risk and thermoregulation mediated by body size. These findings stress the importance of incorporating trophic interactions into climate change predictions.

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Fig. 1: Herbivore constraints in African savannas.
Fig. 2: Lion presence changes herbivore activity patterns.
Fig. 3: Diel activity patterns in absence (blue) or presence (red) of lion (Panthera leo).

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Data availability

The data are located on the Dryad Digital Repository: https://doi.org/10.5061/dryad.6m905qfvx.

Code availability

R code of all analyses is available via the Dryad Digital Repository: https://doi.org/10.5061/dryad.6m905qfvx.

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Acknowledgements

We thank the Ezemvelo KZN Wildlife management and research staff for their help and logistical support while undertaking this study. The camera-trap surveys were funded by Panthera (with support from Peace Parks Foundation and Cartier) and run with the help of staff and volunteers from Wildlife ACT and Siyafunda Conservation. Furthermore, M.P.V. has been financially supported by the AfricanBioServices project which received funding from the European Union’s Horizon 2020 research and innovation programme under grant no. 641918. We thank J. L. Atkins, R. S. Hetem, H. Olff, N. Owen-Smith and R. M. Pringle for their comments on earlier versions of the manuscript.

Author information

Authors and Affiliations

  1. Institute of Environmental Sciences, Leiden University, Leiden, the Netherlands

    Michiel P. Veldhuis

  2. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

    Michiel P. Veldhuis

  3. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, the Netherlands

    Michiel P. Veldhuis

  4. Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, Sweden

    Tim R. Hofmeester & Joris P.G.M. Cromsigt

  5. Panthera, New York, NY, USA

    Guy Balme & Ross T. Pitman

  6. Institute for Communities and Wildlife in Africa, Department of Biological Sciences, University of Cape Town, Rondebosch, South Africa

    Guy Balme & Ross T. Pitman

  7. Ezemvelo KZN Wildlife, Cascades, South Africa

    Dave J. Druce

  8. School of Life Sciences, University of KwaZulu-Natal, Scottsville, South Africa

    Dave J. Druce

  9. Department of Zoology, Nelson Mandela Metropolitan University, Port Elizabeth, South Africa

    Joris P.G.M. Cromsigt

  10. Environmental Sciences Group, Copernicus Institute of Sustainable Development, Utrecht University, Utrecht, the Netherlands

    Joris P.G.M. Cromsigt

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Contributions

M.P.V. and J.P.M.G.C. conceived the study and developed the concept. G.B., R.T.P. and D.J.D. contributed data. T.R.H. and M.P.V. analysed the data. M.P.V. and J.P.M.G.C. wrote the first draft of the manuscript and all authors contributed revisions.

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Correspondence to Michiel P. Veldhuis.

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Extended data

Extended Data Fig. 1 Overview of 32 protected areas in South Africa with camera-trap surveys and 17 South African Weather Service stations.

Background colour represent mean annual temperature (WorldClim.org). Lions were either present (circles) or absent (triangle).

Extended Data Fig. 2 Daily temperature distributions during the 73 camera-trap surveys in 32 protected areas in South Africa.

A, hourly temperature records for an example survey (Zingela 2017). Line represents the hourly mean, dots are individual observations. B, temperature averaged by hour for the 73 surveys and C, relative temperature for each survey (standardized between 0 and 1).

Extended Data Fig. 3 Diel activity patterns of larger carnivores.

Wild dog (A; n = 751 detections), leopard (n = 6,833 detections), cheetah (n = 487 detections), spotted hyena (n = 5,331 detections), lion (n = 2,657 detections) and all carnivores combined (F; n = 16,059 detections). Species are ordered by increasing body mass, which is presented in kilograms below the scientific name. Dark grey represents 95% confidence interval around the estimated activity pattern, grey background represents period of high carnivore activity.

Extended Data Fig. 4 Diel activity patterns of the 29 herbivores in protected areas with lions (red) or without lions (blue).

Species are ordered by increasing body mass, which is presented in kilograms below the scientific name. Grey background represents period of high carnivore activity (Extended Data Fig. 3). Coloured area around the estimates represents the 95% confidence interval.

Extended Data Fig. 5 Lion (Panthera leo) dietary preferences based on Jacobs’ index (mean±SE) of 48 lion populations across Africa at differing prey densities.

Data from ref. 30. Only species recorded in lion diet more than once were included in the dataset. Vertical lines represent the preferred prey range used in this study (100-550kg).

Extended Data Fig. 6 Herbivore detections at each camera-trap location are not related to the number of lion detections.

(Linear Mixed Model: F1,22.4=0.09, P=0.77, n=39 surveys). Only herbivore species in the preferred prey range of lion (100-550kg) were included in this analysis.

Extended Data Fig. 7 Camera-trap locations for Hluhluwe-iMfolozi Park.

An example of how cameras were distributed across protected areas. The most Southern part of the area is managed as a wilderness area where tourist and research access is limited and was thus excluded in this study.

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Veldhuis, M.P., Hofmeester, T.R., Balme, G. et al. Predation risk constrains herbivores’ adaptive capacity to warming. Nat Ecol Evol 4, 1069–1074 (2020). https://doi.org/10.1038/s41559-020-1218-2

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