Behavioral Ecology and Sociobiology

, Volume 69, Issue 7, pp 1153–1161

Temporal shifts in activity of prey following large predator reintroductions

  • Craig J. Tambling
  • Liaan Minnie
  • Jordana Meyer
  • Elizabeth W. Freeman
  • Rachel M. Santymire
  • John Adendorff
  • Graham I. H. Kerley
Original Paper

Abstract

The response of prey to predation risk varies through time and space. These responses relate to trade-offs between foraging and predator avoidance. Following the extirpation of predators from many landscapes, the responses related to predator avoidance may have been lost or diluted. Investigating the activity pattern of prey species on comparable landscapes with and without large predators provides an opportunity to understand how predators may shape prey activity and behaviour. Using camera trap data from neighbouring fenced sections of the Addo Elephant National Park (Eastern Cape, South Africa), we investigated the activity patterns of species exposed to large predators, where the predators were only present in one of the sections. Our results suggest that prey species at risk of predation (e.g., buffalo, kudu and warthog) are more likely to be active diurnally when co-existing with nocturnally active predators, thereby reducing the activity overlap with these predators. In the absence of predators, kudu and buffalo were more active at night resulting in a low overlap in activity between sections. Warthog activity was predominantly diurnal in both sections, resulting in a high overlap in activity between sections. The presence of predators reduced the nocturnal activity of warthogs from 6 to 0.6 % of all warthog captures in each section. Elephants, which are above the preferred prey weight range of the predators and therefore have a low risk of predation, showed higher overlap in activity periodicity between predator-present and predator-absent areas. Our findings suggest that maintaining prey with their predators has the added benefit of conserving the full spectrum of prey adaptive behaviours.

Keywords

African buffalo Diel pattern Kudu Lion Predator–prey interaction Spotted hyaena 

Supplementary material

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ESM 1(DOCX 1594 kb)

References

  1. Akbaba B, Ayaş Z (2012) Camera trap study on inventory and daily activity patterns of large mammals in a mixed forest in north-western Turkey. Mammalia 76:43–48CrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B, Walker S (2013) Lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-5 edn, http://CRAN.R-project.org/package=lme4
  3. Beest FM, Vander Wal E, Stronen AV, Paquet PC, Brook RK (2013) Temporal variation in site fidelity: scale-dependent effects of forage abundance and predation risk in a non-migratory large herbivore. Oecologia 173:409–420PubMedCrossRefGoogle Scholar
  4. Berger J, Swenson JE, Persson I-L (2001) Recolonizing carnivores and naïve prey: conservation lessons from Pleistocene extinctions. Science 291:1036–1039PubMedCrossRefGoogle Scholar
  5. Boshoff AF, Landman M, Kerley GIH, Bradfield M (2007) Profiles, views and observations of visitors to the Addo Elephant National Park, Eastern Cape, South Africa. S Afr J Wildl Res 37:189–196CrossRefGoogle Scholar
  6. Caro TM (2005) Antipredator defenses in birds and mammals. University of Chicago Press, ChicagoGoogle Scholar
  7. Clements HS, Tambling CJ, Hayward MW, Kerley GIH (2014) An objective approach to determining the weight ranges of prey preferred by and accessible to the five large African carnivores. PLoS ONE 9:e101054PubMedCentralPubMedCrossRefGoogle Scholar
  8. Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201PubMedCrossRefGoogle Scholar
  9. Creel S, Winnie JA Jr (2005) Responses of elk herd size to fine-scale spatial and temporal variation in the risk of predation by wolves. Anim Behav 69:1181–1189CrossRefGoogle Scholar
  10. Cresswell W, Lind J, Quinn JL (2010) Predator-hunting success and prey vulnerability: quantifying the spatial scale over which lethal and non-lethal effects of predation occur. J Anim Ecol 79:556–562PubMedCrossRefGoogle Scholar
  11. Davidson Z, Valeix M, Van Kesteren F, Loveridge AJ, Hunt JE, Murindagomo F, Macdonald DW (2013) Seasonal diet and prey preference of the African lion in a waterhole-driven semi-arid savanna. PLoS ONE 8:e55182PubMedCentralPubMedCrossRefGoogle Scholar
  12. du Toit JT, Yetman CA (2005) Effects of body size on the diurnal activity budgets of African browsing ruminants. Oecologia 143:317–325PubMedCrossRefGoogle Scholar
  13. Eriksen A, Wabakken P, Zimmermann B et al (2011) Activity patterns of predator and prey: a simultaneous study of GPS-collared wolves and moose. Anim Behav 81:423–431CrossRefGoogle Scholar
  14. Fenn MGP, Macdonald DW (1995) Use of middens by red foxes: risk reverses rhythms of rats. J Mammal 76:130–136CrossRefGoogle Scholar
  15. Foggo A, Attrill MJ, Frost MT, Rowden AA (2003) Estimating marine species richness: an evaluation of six extrapolative techniques. Mar Ecol Prog Ser 248:15–26CrossRefGoogle Scholar
  16. Griffin PC, Griffin SC, Waroquiers C, Mills LS (2005) Mortality by moonlight: predation risk and the snowshoe hare. Behav Ecol 16:938–944CrossRefGoogle Scholar
  17. Hayward MW (2006) Prey preferences of the spotted hyaena (Crocuta crocuta) and degree of dietary overlap with the lion (Panthera leo). J Zool 270:606–614CrossRefGoogle Scholar
  18. Hayward MW, Hayward GJ (2006) Activity patterns of reintroduced lion Panthera leo and spotted hyaena Crocuta crocuta in the Addo Elephant National Park, South Africa. Afr J Ecol 45:135–141CrossRefGoogle Scholar
  19. Hayward MW, Hayward MD (2012) Waterhole use by African fauna. S Afr J Wildl Res 42:117–127CrossRefGoogle Scholar
  20. Hayward MW, Hofmeyr M, O'Brien J, Kerley GIH (2007) Testing predictions of the prey of the lion (Panthera leo) derived from modelled prey preferences. J Wildl Manag 71:1567–1575CrossRefGoogle Scholar
  21. Hayward MW, Kerley GIH (2005) Prey preferences of the lion (Panthera leo). J Zool 267:309–322CrossRefGoogle Scholar
  22. Hayward MW, Slotow R (2009) Temporal partitioning of activity in large African carnivores: tests of multiple hypotheses. S Afr J Wildl Res 39:109–125CrossRefGoogle Scholar
  23. Hayward MW, Somers MJ (2009) Reintroduction of top-order predators: using science to restore one of the drivers of biodiversity. In: Hayward MW, Somers MJ (eds) Reintroduction of top-order predators. Conservation science and practice, No 5 edn. Wiley-Blackwell, Oxford, pp 1–9CrossRefGoogle Scholar
  24. Hopcraft JGC, Olff H, Sinclair ARE (2010) Herbivores, resources and risks: alternating regulation along primary environmental gradients in savannas. Trends Ecol Evol 25:119–128PubMedCrossRefGoogle Scholar
  25. Kronfeld-Schor N, Dayan T, Elvert R, Haim A, Zisapel N, Heldmaier G (2001) On the use of the time axis for ecological separation: diel rhythms as an evolutionary constraint. Am Nat 158:451–457PubMedCrossRefGoogle Scholar
  26. Lima SL (2002) Putting predators back into behavioral predator–prey interactions. Trends Ecol Evol 17:70–75CrossRefGoogle Scholar
  27. Linkie M, Rideout MS (2011) Assessing tiger–prey interactions in Sumatran rainforests. J Zool 284:224–229CrossRefGoogle Scholar
  28. Loveridge AJ, Hunt JE, Murindagomo F, Macdonald DW (2006) Influence of drought on predation of elephant (Loxodonta africana) calves by lions (Panthera leo) in an African wooded savannah. J Zool 270:523–530CrossRefGoogle Scholar
  29. Maloney SK, Moss G, Cartmell T, Mitchell D (2005) Alteration in diel activity patterns as a thermoregulatory strategy in black wildebeest (Connochaetes gnou). J Comp Physiol A 191:1055–1064CrossRefGoogle Scholar
  30. Meredith M, Rideout M (2014) Overlap: estimates of coefficient of overlapping for animal activity patterns. 0.2.2 edn, http://CRAN.R-project.org/package=overlap
  31. Mills MGL, Biggs HC, Whyte IJ (1995) The relationship between rainfall, lion predation and population trends in African herbivores. Wildl Res 22:75–88CrossRefGoogle Scholar
  32. Monterroso P, Alves PC, Ferreras P (2013) Catch me if you can: diel activity patterns of mammalian prey and predators. Ethology 119:1044–1056CrossRefGoogle Scholar
  33. Mucina L, Rutherford MC (2006) The vegetation of South Africa, Lesotho and Swaziland. South African National Biodiversity Institute, PretoriaGoogle Scholar
  34. Muggeo VMR (2008) Segmented: an R package to fit regression models with broken-line relationships. R News 8:20–25Google Scholar
  35. Nouvellet P, Rasmussen GSA, Macdonald DW, Courchamp F (2012) Noisy clocks and silent sunrises: measurement methods of daily activity pattern. J Zool 286:179–184CrossRefGoogle Scholar
  36. Nyafu K (2009) Warthog as an introduced species in the Eastern Cape. MSc, Nelson Mandela Metropolitan University, Port ElizabethGoogle Scholar
  37. Ohashi H, Saito M, Horie R et al (2013) Differences in the activity pattern of the wild boar Sus scrofa related to human disturbance. Eur J Wildl Res 59:167–177CrossRefGoogle Scholar
  38. Oksanen J, Blanchet FG, Kindt R et al. (2012) Vegan: community ecology package. R package version 2.0-5 edn, http://CRAN.R-project.org/package=vegan
  39. Owen-Smith N (2014) Spatial ecology of large herbivore populations. Ecography 37:416–430Google Scholar
  40. Owen-Smith N, Goodall V (2014) Coping with savanna seasonality: comparative daily activity patterns of African ungulates as revealed by GPS telemetry. J Zool 293:181–191CrossRefGoogle Scholar
  41. Owen-Smith N, Mills MGL (2008a) Predator–prey size relationships in an African large-mammal food web. J Anim Ecol 77:173–183PubMedCrossRefGoogle Scholar
  42. Owen-Smith N, Mills MGL (2008b) Shifting prey selection generates contrasting herbivore dynamics within a large-mammmal predator–prey web. Ecology 89:1120–1133PubMedCrossRefGoogle Scholar
  43. Polansky L, Wittemyer G, Cross PC, Tambling CJ, Getz WM (2010) From moonlight to movement and synchronized randomness: Fourier and wavelet analyses of animal location time series data. Ecology 91:1506–1518PubMedCentralPubMedCrossRefGoogle Scholar
  44. Power RJ, Compion RXS (2009) Lion predation on elephants in the Savuti, Chobe National Park, Botswana. Afr Zool 44:36–44CrossRefGoogle Scholar
  45. Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509CrossRefGoogle Scholar
  46. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  47. R Development Core Team (2011) R: a language and environment for statistical computing. 2.12.0 edn. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
  48. Rideout MS, Linkie M (2009) Estimating overlap of daily activity patterns from camera trap data. J Agric Biol Environ Stat 14:322–337CrossRefGoogle Scholar
  49. Ripple WJ, Estes JA, Beschta RL et al. (2014) Status and ecological effects of the world’s largest carnivores. Science 343Google Scholar
  50. Roth T, Lima S (2007) The predatory behavior of wintering Accipiter hawks: temporal patterns in activity of predators and prey. Oecologia 152:169–178PubMedCrossRefGoogle Scholar
  51. Rovero F, Jones T, Sanderon J (2005) Notes on Abbott’s duiker (Cephalophus spadix True 1890) and other forest antelopes of Mwanihana Forest, Udzungwa Mountains, Tanzania, as revealed by camera-trapping and direct observations. Trop Zool 18:13–23CrossRefGoogle Scholar
  52. Schaller GB (1972) The Serengeti lion: a study of predator–prey relations. Wildlife behavior and ecology series. The University of Chicago Press, Chicago, Illinois, USAGoogle Scholar
  53. Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621CrossRefGoogle Scholar
  54. Sinclair ARE, Mduma S, Brashares JS (2003) Patterns of predation in a diverse predator–prey system. Nature 425:288–290PubMedCrossRefGoogle Scholar
  55. Skead CJ (2007) Historical incidence of the larger land mammals in the broader Eastern Cape, 2nd edn. Centre for African Conservation Ecology, Port ElizabethGoogle Scholar
  56. Skinner JD, Chimimba CT (2005) The mammals of the southern African subregion. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  57. Tambling CJ, Druce D, Hayward M, Castley JG, Adendorf J, Kerley GIH (2012) Spatial and temporal changes in group dynamics and range use enable anti-predator responses in African buffalo. Ecology 93:1297–1304PubMedCrossRefGoogle Scholar
  58. Tambling CJ, du Toit JT (2005) Modelling wildebeest population dynamics: implications of predation and harvesting in a closed system. J Appl Ecol 42:431–441CrossRefGoogle Scholar
  59. Tambling CJ, Minnie L, Adendorff J, Kerley GIH (2013) Elephants facilitate impact of large predators on small ungulate prey species. Basic Appl Ecol 14:694–701CrossRefGoogle Scholar
  60. Valeix M, Fritz H, Loveridge AJ, Davidson Z, Hunt JE, Murindagomo F, Macdonald DW (2009) Does the risk of encountering lions influence African herbivore behaviour at waterholes? Behav Ecol Sociobiol 63:1483–1494CrossRefGoogle Scholar
  61. Wentworth J, Tambling C, Kerley G (2011) Evidence for prey selection by spotted hyaena in the Eastern Cape, South Africa. Acta Theriol 56:389–392CrossRefGoogle Scholar
  62. Winterbach HEK, Bothma JP (1998) Activity patterns of the Cape buffalo Syncerus caffer caffer in the Willem Pretorious Game Reserve, Free State. S Afr J Wildl Res 28:73–81Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Craig J. Tambling
    • 1
  • Liaan Minnie
    • 1
  • Jordana Meyer
    • 2
    • 3
  • Elizabeth W. Freeman
    • 2
  • Rachel M. Santymire
    • 3
  • John Adendorff
    • 4
  • Graham I. H. Kerley
    • 1
  1. 1.Centre for African Conservation Ecology, Department of ZoologyNelson Mandela Metropolitan UniversityPort ElizabethSouth Africa
  2. 2.New Century CollegeGeorge Mason UniversityFairfaxUSA
  3. 3.Davee Center for Epidemiology and EndocrinologyLincoln Park ZooChicagoUSA
  4. 4.Addo Elephant National ParkSouth African National ParksAddoSouth Africa

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