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

  • Anne Hilborn
  • Nathalie Pettorelli
  • Tim Caro
  • Marcella J. Kelly
  • M. Karen Laurenson
  • Sarah M. Durant
Original Article

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.

Keywords

Predator-prey interactions Foraging behavior Behavioral flexibility Carnivore coexistence 

Notes

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.

Compliance with ethical standards

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.

Supplementary material

265_2018_2481_MOESM1_ESM.pdf (191 kb)
ESM 1 (PDF 191 kb)

References

  1. Arjo WM, Pletscher DH (1999) Behavioral responses of coyotes to wolf recolonization in northwestern Montana. Can J Zool 77:1919–1927CrossRefGoogle Scholar
  2. Balme GA, Miller JRB, Pitman RT, Hunter LTB (2017) Caching reduces kleptoparasitism in a solitary, large felid. J Anim Ecol 86:634–644CrossRefPubMedGoogle Scholar
  3. Beddington JR, Hassell MP, Lawton JH (1976) The components of arthropod predation: II. The predator rate of increase. J Anim Ecol 45:165–185CrossRefGoogle Scholar
  4. Bindoo M, Aravindan CM (1992) Influence of size and level of satiation on prey handling time in Channa striata (Bloch). J Fish Biol 40:497–502CrossRefGoogle Scholar
  5. Blumenschine RJ, Caro TM (1986) Unit flesh weights of some east African bovids. Afr J Ecol 24:273–286CrossRefGoogle Scholar
  6. Bøving PS, Post E (1997) Vigilance and foraging behaviour of female caribou in relation to predation risk. Rangifer 17:55–64CrossRefGoogle Scholar
  7. Broekhuis F, Cozzi G, Valeix M, McNutt JW, Macdonald DW (2013) Risk avoidance in sympatric large carnivores: reactive or predictive? J Anim Ecol 82:1098–1105CrossRefPubMedGoogle Scholar
  8. 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 304:65–72CrossRefGoogle Scholar
  9. Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47CrossRefGoogle Scholar
  10. 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 266:153–161CrossRefGoogle Scholar
  11. Caro TM (1987) Cheetah mothers’ vigilance: looking out for prey or for predators ? Behav Ecol Sociobiol 20:351–361CrossRefGoogle Scholar
  12. Caro TM (1994) Cheetahs of the Serengeti Plains: group living in an asocial species. University of Chicago Press, ChicagoGoogle Scholar
  13. Caro TM (1995) Short-term costs and correlates of play in cheetahs. Anim Behav 49:333–345CrossRefGoogle Scholar
  14. Cooper AB, Pettorelli N, Durant SM (2007) Large carnivore menus: factors affecting hunting decisions by cheetahs in the Serengeti. Anim Behav 73:651–659CrossRefGoogle Scholar
  15. 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 41:161–170CrossRefGoogle Scholar
  16. 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:e98846CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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 3:8–15CrossRefGoogle Scholar
  18. Durant SM (1998) Competition refuges and coexistence: an example from Serengeti carnivores. J Anim Ecol 67:370–386CrossRefGoogle Scholar
  19. Durant SM (2000a) Living with the enemy: avoidance of hyenas and lions by cheetahs in the Serengeti. Behav Ecol 11:624–632CrossRefGoogle Scholar
  20. Durant SM (2000b) Predator avoidance, breeding experience and reproductive success in endangered cheetahs, Acinonyx jubatus. Anim Behav 60:121–130CrossRefPubMedGoogle Scholar
  21. 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 26:257–268CrossRefGoogle Scholar
  22. Estes R (1991) The behavior guide to African mammals. University of California Press, BerkeleyGoogle Scholar
  23. 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 277:2089–2095CrossRefGoogle Scholar
  24. Fuller TK, Keith LB (1981) Non-overlapping ranges of coyotes and wolves in northeastern Alberta. J Mammal 62:403–405CrossRefGoogle Scholar
  25. 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 17:1771–1783CrossRefGoogle Scholar
  26. Gorman ML, Mills MG, Raath JP, Speakman JR (1998) High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature 852:1992–1994Google Scholar
  27. 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 90:1207–1216CrossRefPubMedGoogle Scholar
  28. 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 270:615–627CrossRefGoogle Scholar
  29. Hilborn A, Pettorelli N, Orme CDL, Durant SM (2012) Stalk and chase: how hunt stages affect hunting success in Serengeti cheetah. Anim Behav 84:701–706CrossRefGoogle Scholar
  30. Hunter JS, Durant SM, Caro TM (2007a) To flee or not to flee: predator avoidance by cheetahs at kills. Behav Ecol Sociobiol 61:1033–1042CrossRefGoogle Scholar
  31. Hunter JS, Durant SM, Caro TM (2007b) Patterns of scavenger arrival at cheetah kills in Serengeti National Park Tanzania. Afr J Ecol 45:275–281CrossRefGoogle Scholar
  32. Lamprecht J (1978) The relationship between food competition and foraging group size in some larger carnivores. Ethology 46:337–343Google Scholar
  33. Laurenson MK (1994) High juvenile mortality in cheetahs (Acinonyx jubatus) and its consequences for maternal care. J Zool 234:387–408CrossRefGoogle Scholar
  34. Laurenson MK (1995) Behavioral costs and constraints of lactation in free-living cheetahs. Anim Behav 50:815–826CrossRefGoogle Scholar
  35. Lima SL (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav 49:11–20CrossRefGoogle Scholar
  36. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  37. Messier F (1994) Ungulate population models with predation: a case study with the north American moose. Ecology 75:478–488CrossRefGoogle Scholar
  38. 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 292:136–141CrossRefGoogle Scholar
  39. Mukherjee S, Zelcer M, Kotler BP (2009) Patch use in time and space for a meso-predator in a risky world. Oecologia 159:661–668CrossRefPubMedGoogle Scholar
  40. Murdoch W, Briggs C, Nisbet R (2003) Consumer-resource dynamics. Princeton University Press, PrincetonGoogle Scholar
  41. Murphy KM, Felzien GS, Hornocker MG, Ruth TK (1998) Encounter competition between bears and cougars: some ecological implications. Ursus 10:55–60Google Scholar
  42. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  43. Pettorelli N, Coulson T, Durant SM, Gaillard J-M (2011) Predation, individual variability and vertebrate population dynamics. Oecologia 167:305–314CrossRefPubMedGoogle Scholar
  44. Prugh LR, Stoner CJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–791CrossRefGoogle Scholar
  45. Randall JA, Boltas King DK (2001) Assessment and defence of solitary kangaroo rats under risk of predation by snakes. Anim Behav 61:579–587CrossRefGoogle Scholar
  46. Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998CrossRefPubMedGoogle Scholar
  47. Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086CrossRefGoogle Scholar
  48. Sih A (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311CrossRefGoogle Scholar
  49. Sinclair ARE, Arcese P (1995) Serengeti II: dynamics, management, and conservation of an ecosystem, vol 2. University of Chicago Press, ChicagoGoogle Scholar
  50. 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 282:20142711CrossRefPubMedGoogle Scholar
  51. Suraci JP, Clinchy M, Dill LM, Roberts D, Zanette LY (2016) Fear of large carnivores causes a trophic cascade. Nat Commun 7:10698CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 6:8534–8545CrossRefPubMedPubMedCentralGoogle Scholar
  53. Switalski TA (2003) Coyote foraging ecology and vigilance in response to gray wolf reintroduction in Yellowstone National Park. Can J Zool 81:985–993CrossRefGoogle Scholar
  54. Toïgo C (1999) Vigilance behavior in lactating female alpine ibex. Can J Zool 77:1060–1063CrossRefGoogle Scholar
  55. 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 94:2619–2631CrossRefPubMedGoogle Scholar
  56. Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60:457–464CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Anne Hilborn
    • 1
    • 2
  • Nathalie Pettorelli
    • 2
  • Tim Caro
    • 3
  • Marcella J. Kelly
    • 1
  • M. Karen Laurenson
    • 4
  • Sarah M. Durant
    • 2
  1. 1.Department of Fish and Wildlife ConservationVirginia TechVirginiaUSA
  2. 2.Institute of ZoologyZoological Society of LondonLondonUK
  3. 3.Department of Wildlife, Fish and Conservation BiologyUniversity of CaliforniaCaliforniaUSA
  4. 4.Frankfurt Zoological SocietyMpikaZambia

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