Skip to main content
SpringerLink
Log in

Cheetahs modify their prey handling behavior depending on risks from top predators

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

While handling large kills, mesocarnivores are particularly vulnerable to kleptoparasitism and predation from larger predators. We used 35 years of observational data on cheetah (Acinonyx jubatus) hunts in Serengeti National Park to investigate whether cheetahs’ prey handling behavior varied in response to threats from lions (Panthera leo) and spotted hyenas (Crocuta crocuta). Male cheetahs and single females, whose main threat was kleptoparasitism, minimized time on the kill by being less vigilant and eating quickly, thereby shortening their handling times. Mothers with cubs showed a different strategy that prioritized vigilance over speed of eating, which increased time spent handling prey. Vigilance allowed them to minimize the risk of their cubs being killed while giving cubs the time they need to eat at the carcass. Flexible behavioral strategies that minimize individual risk while handling prey likely allow mesocarnivores to coexist with numerous and widespread apex predators.

Significance statement

Medium-sized carnivores like cheetahs face the challenge of coexisting with larger carnivores that steal their kills and kill their cubs. We investigated how cheetahs modify their behavior on kills to minimize risks from larger predators. Using 35 years of data on 400+ cheetah hunts across 159 individuals, we found that cheetahs without cubs whose primary danger is having their kill stolen spent little time engaged in vigilance and instead ate quickly, reducing the risk of theft. Mothers with cubs, however, took a slower approach and were more vigilant while handling prey to avoid cub predation by lions and spotted hyenas. The ability of cheetahs to modify their prey handling behavior depending on the type of risk they face likely allows them to coexist with numerous larger carnivores.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arjo WM, Pletscher DH (1999) Behavioral responses of coyotes to wolf recolonization in northwestern Montana. Can J Zool 77:1919–1927

    Article  Google Scholar 

  • Balme GA, Miller JRB, Pitman RT, Hunter LTB (2017) Caching reduces kleptoparasitism in a solitary, large felid. J Anim Ecol 86:634–644

    Article  PubMed  Google Scholar 

  • Beddington JR, Hassell MP, Lawton JH (1976) The components of arthropod predation: II. The predator rate of increase. J Anim Ecol 45:165–185

    Article  Google Scholar 

  • Bindoo M, Aravindan CM (1992) Influence of size and level of satiation on prey handling time in Channa striata (Bloch). J Fish Biol 40:497–502

    Article  Google Scholar 

  • Blumenschine RJ, Caro TM (1986) Unit flesh weights of some east African bovids. Afr J Ecol 24:273–286

    Article  Google Scholar 

  • Bøving PS, Post E (1997) Vigilance and foraging behaviour of female caribou in relation to predation risk. Rangifer 17:55–64

    Article  Google Scholar 

  • Broekhuis F, Cozzi G, Valeix M, McNutt JW, Macdonald DW (2013) Risk avoidance in sympatric large carnivores: reactive or predictive? J Anim Ecol 82:1098–1105

    Article  PubMed  Google Scholar 

  • Broekhuis F, Thuo D, Hayward MW (2018) Feeding ecology of cheetahs in the Maasai Mara, Kenya and the potential for intra- and interspecific competition. J Zool 304:65–72

    Article  Google Scholar 

  • Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47

    Article  Google Scholar 

  • Carbone C, Frame L, Frame G, Malcolm J, Fanshawe J, FitzGibbon C, Schaller G, Gordon IJ, Rowcliffe JM, du Toit JT (2005) Feeding success of African wild dogs (Lycaon pictus) in the Serengeti: the effects of group size and kleptoparasitism. J Zool 266:153–161

    Article  Google Scholar 

  • Caro TM (1987) Cheetah mothers’ vigilance: looking out for prey or for predators ? Behav Ecol Sociobiol 20:351–361

    Article  Google Scholar 

  • Caro TM (1994) Cheetahs of the Serengeti Plains: group living in an asocial species. University of Chicago Press, Chicago

    Google Scholar 

  • Caro TM (1995) Short-term costs and correlates of play in cheetahs. Anim Behav 49:333–345

    Article  Google Scholar 

  • Cooper AB, Pettorelli N, Durant SM (2007) Large carnivore menus: factors affecting hunting decisions by cheetahs in the Serengeti. Anim Behav 73:651–659

    Article  Google Scholar 

  • Croy MI, Hughes RN (1991) The influence of hunger on feeding-behavior and on the acquisition of learned foraging skills by the 15-spined stickleback, Spinachia spinachia L. Anim Behav 41:161–170

    Article  Google Scholar 

  • Darnell AM, Graf JA, Somers MJ, Slotow R, Szykman Gunther M (2014) Space use of African wild dogs in relation to other large carnivores. PLoS One 9:e98846

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dunphy-Daly MM, Heithaus MR, Wirsing AJ, Mardon JSF, Burkholder DA (2010) Predation risk influences the diving behavior of a marine mesopredator. Open Ecol J 3:8–15

    Article  Google Scholar 

  • Durant SM (1998) Competition refuges and coexistence: an example from Serengeti carnivores. J Anim Ecol 67:370–386

    Article  Google Scholar 

  • Durant SM (2000a) Living with the enemy: avoidance of hyenas and lions by cheetahs in the Serengeti. Behav Ecol 11:624–632

    Article  Google Scholar 

  • Durant SM (2000b) Predator avoidance, breeding experience and reproductive success in endangered cheetahs, Acinonyx jubatus. Anim Behav 60:121–130

    Article  PubMed  CAS  Google Scholar 

  • Durant SM, Caro TM, Collins DA, Alawi RM, Fitzgibbon CD (1988) Migration patterns of Thomson’s gazelles and cheetahs on the Serengeti plains. Afr J Ecol 26:257–268

    Article  Google Scholar 

  • Estes R (1991) The behavior guide to African mammals. University of California Press, Berkeley

    Google Scholar 

  • Favreau FR, Goldizen AW, Pays O (2010) Interactions among social monitoring, anti-predator vigilance and group size in eastern grey kangaroos. Proc R Soc Lond B 277:2089–2095

    Article  Google Scholar 

  • Fuller TK, Keith LB (1981) Non-overlapping ranges of coyotes and wolves in northeastern Alberta. J Mammal 62:403–405

    Article  Google Scholar 

  • Garvey PM, Glen AS, Pech RP (2015) Foraging ermine avoid risk: behavioural responses of a mesopredator to its interspecific competitors in a mammalian guild. Biol Invasions 17:1771–1783

    Article  Google Scholar 

  • Gorman ML, Mills MG, Raath JP, Speakman JR (1998) High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 852:1992–1994

    Google Scholar 

  • Harrington LA, Harrington AL, Yamaguchi N, Thom MD, Ferreras P, Windham TR, Macdonald DW (2009) The impact of native competitors on an alien invasive : temporal niche shifts to avoid interspecific aggression. Ecology 90:1207–1216

    Article  PubMed  Google Scholar 

  • Hayward MW, Hofmeyr M, O’Brien J, Kerley GIH (2006) Prey preferences of the cheetah (Acinonyx jubatus) (Felidae: Carnivora): morphological limitations or the need to capture rapidly consumable prey before kleptoparasites arrive? J Zool 270:615–627

    Article  Google Scholar 

  • Hilborn A, Pettorelli N, Orme CDL, Durant SM (2012) Stalk and chase: how hunt stages affect hunting success in Serengeti cheetah. Anim Behav 84:701–706

    Article  Google Scholar 

  • Hunter JS, Durant SM, Caro TM (2007a) To flee or not to flee: predator avoidance by cheetahs at kills. Behav Ecol Sociobiol 61:1033–1042

    Article  Google Scholar 

  • Hunter JS, Durant SM, Caro TM (2007b) Patterns of scavenger arrival at cheetah kills in Serengeti National Park Tanzania. Afr J Ecol 45:275–281

    Article  Google Scholar 

  • Lamprecht J (1978) The relationship between food competition and foraging group size in some larger carnivores. Ethology 46:337–343

    Google Scholar 

  • Laurenson MK (1994) High juvenile mortality in cheetahs (Acinonyx jubatus) and its consequences for maternal care. J Zool 234:387–408

    Article  Google Scholar 

  • Laurenson MK (1995) Behavioral costs and constraints of lactation in free-living cheetahs. Anim Behav 50:815–826

    Article  Google Scholar 

  • Lima SL (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav 49:11–20

    Article  Google Scholar 

  • 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 

  • Messier F (1994) Ungulate population models with predation: a case study with the north American moose. Ecology 75:478–488

    Article  Google Scholar 

  • Mills MGL, Mills MEJ (2014) Cheetah cub survival revisited: a re-evaluation of the role of predation, especially by lions, and implications for conservation. J Zool 292:136–141

    Article  Google Scholar 

  • Mukherjee S, Zelcer M, Kotler BP (2009) Patch use in time and space for a meso-predator in a risky world. Oecologia 159:661–668

    Article  PubMed  Google Scholar 

  • Murdoch W, Briggs C, Nisbet R (2003) Consumer-resource dynamics. Princeton University Press, Princeton

    Google Scholar 

  • Murphy KM, Felzien GS, Hornocker MG, Ruth TK (1998) Encounter competition between bears and cougars: some ecological implications. Ursus 10:55–60

    Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Pettorelli N, Coulson T, Durant SM, Gaillard J-M (2011) Predation, individual variability and vertebrate population dynamics. Oecologia 167:305–314

    Article  PubMed  Google Scholar 

  • Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791

    Article  Google Scholar 

  • Randall JA, Boltas King DK (2001) Assessment and defence of solitary kangaroo rats under risk of predation by snakes. Anim Behav 61:579–587

    Article  Google Scholar 

  • Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998

    Article  PubMed  Google Scholar 

  • Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086

    Article  Google Scholar 

  • Sih A (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311

    Article  Google Scholar 

  • Sinclair ARE, Arcese P (1995) Serengeti II: dynamics, management, and conservation of an ecosystem, vol 2. University of Chicago Press, Chicago

    Google Scholar 

  • Smith JA, Wang Y, Wilmers CC (2015) Top carnivores increase their kill rates on prey as a response to human-induced fear. Proc R Soc B 282:20142711

    Article  PubMed  Google Scholar 

  • Suraci JP, Clinchy M, Dill LM, Roberts D, Zanette LY (2016) Fear of large carnivores causes a trophic cascade. Nat Commun 7:10698

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swanson A, Arnold T, Kosmala M, Forester J, Packer C (2016) In the absence of a “landscape of fear”: how lions, hyenas, and cheetahs coexist. Ecol Evol 6:8534–8545

    Article  PubMed  PubMed Central  Google Scholar 

  • Switalski TA (2003) Coyote foraging ecology and vigilance in response to gray wolf reintroduction in Yellowstone National Park. Can J Zool 81:985–993

    Article  Google Scholar 

  • Toïgo C (1999) Vigilance behavior in lactating female alpine ibex. Can J Zool 77:1060–1063

    Article  Google Scholar 

  • Vanak AT, Fortin D, Thaker M, Ogden M, Owen C, Greatwood L, Slotow R (2013) Moving to stay in place: behavioral mechanisms for coexistence of African large carnivores. Ecology 94:2619–2631

    Article  PubMed  Google Scholar 

  • Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Tanzania National Parks and Tanzania Wildlife Research Institute for permission to collect data. The Howard G. Buffett Foundation, Wildlife Conservation Society, Frankfurt Zoological Society (FZS), and National Geographic Society provided funds. AH’s dissertation was funded by a National Science Foundation Graduate Research Fellowship under Grant No. DGE-1048542, a National Science Foundation Doctoral Dissertation Improvement Grant Award Number 1405491, P.E.O, and Virginia Tech. We are very grateful to Dennis Minja, Helen O’Neill, Laura Simpson, Sultana Bashir, John Shemakunde, and all other research assistants on the Serengeti Cheetah Project who helped collect data. Logistical support was provided by G. and M. Russell, B. Allen, O. Newman, A. Barrett, J. Jackson, J. Dreissen, A. Geertsma, P. and L. White, C. MacConnell and the staff at Ndutu Safari Lodge, M. Borner and others at FZS, as well as T. Mariki. AH thanks Ulrike Hilborn for data entry and general support and Ray Hilborn for help with R. We also thank Dr. Matt Hayward and an anonymous reviewer for their helpful comments.

Funding

AH’s dissertation was funded by a National Science Foundation Graduate Research Fellowship under Grant No. DGE-1048542, a National Science Foundation Doctoral Dissertation Improvement Grant Award Number 1405491, P.E.O, and GTAships from Virginia Tech.

Author information

Authors and Affiliations

  1. Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, Virginia, USA

    Anne Hilborn & Marcella J. Kelly

  2. Institute of Zoology, Zoological Society of London, London, UK

    Anne Hilborn, Nathalie Pettorelli & Sarah M. Durant

  3. Department of Wildlife, Fish and Conservation Biology, University of California, Davis, California, USA

    Tim Caro

  4. Frankfurt Zoological Society, PO Box 450189, Musakanya Drive, Mpika, Zambia

    M. Karen Laurenson

Authors
  1. Anne Hilborn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nathalie Pettorelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tim Caro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcella J. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Karen Laurenson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sarah M. Durant
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne Hilborn.

Ethics declarations

Conflict of interest

The authors declare that they do not have conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by P. A. Bednekoff

Electronic supplementary material

ESM 1

(PDF 191 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hilborn, A., Pettorelli, N., Caro, T. et al. Cheetahs modify their prey handling behavior depending on risks from top predators. Behav Ecol Sociobiol 72, 74 (2018). https://doi.org/10.1007/s00265-018-2481-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-018-2481-y

Keywords

Search

Navigation