Skip to main content

Advertisement

SpringerLink
Log in

Staying safe from top predators: patterns of co-occurrence and inter-predator interactions

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

Abstract

Top predators often have cascading effects on mesopredator communities by driving behavioural changes. Using camera-trapping surveys, we explored the site-detection probability of sympatric predators and temporal overlap and examined behavioural patterns to explore hypotheses of carnivore guild interactions between and within large and small predators in the presence/absence of lion (Panthera leo) in open and closed habitat cover. We used single-season two-species occupancy models to test inter-predator interactions at 205 camera sites spread across five Protected Areas of the Maputaland Conservation Unit, South Africa. These data showed the respective associations between the presence of large carnivores and smaller carnivores. We observed that leopard (Panthera pardus) and hyena (Crocuta crocuta) tended to avoid interference encounters, as they were less likely co-detected at the same sites. There was a decrease in detection of leopard and hyena as a function of lion presence. Small predators such as the group honey badger (Mellivora capensis)-striped polecat (Ictonyx striatus) and the slender mongoose (Herpestes sanguineus) were detected less often at cameras where leopards were detected. Detection probabilities of the group badger-polecat and slender mongoose were much higher in the closed habitat than in open habitat where leopards were detected. At camera sites where hyenas were detected, badger-polecat and genet (Genetta tigrina) detection probability was much higher in the closed habitat than open habitat. Slender mongoose overlapped less temporally with large predators while others did not. Our study showed that large predator guilds can affect the probability of detecting subordinate mesopredators; therefore, reintroduction of large carnivores can have a cascading effect on subordinate carnivores, and it is necessary to consider this effect when planning recovery programmes for carnivore conservation.

Significance statement

We think this study is of importance and interest as top predators often shape mesopredator communities by inducing apparent avoidance behaviour based on associations between the presence of large carnivores and smaller carnivores. As a consequence, smaller predators use closed habitat to minimize the risk of larger predators due to intraguild interference interaction. We explored behavioural patterns of sympatric predators’ site detection probability and temporal overlap and examined hypotheses about carnivore guild interactions between leopard and spotted hyena, these two and small predators with and without lion in open and closed habitat cover. Reintroduction of one carnivore population can have cascading effects on the other, and this nature of consequences needs to be accounted when planning conservation or species recovery programmes. Therefore, we extended our study to explore these important aspects. Our study is novel as there are no studies documenting species interactions between/within large and small predators from co-occurrence patterns in South Africa.

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
Fig. 4

Similar content being viewed by others

References

  • Acebes P, Traba J, Malo JE (2012) Co-occurrence and potential for competition between wild and domestic large herbivores in a south American desert. J Arid Environ 77:39–44

    Article  Google Scholar 

  • Bailey TN (1993) The African leopard: ecology and behavior of a solitary felid. Columbia University Press, New York

    Google Scholar 

  • Berger J, Stacey PB, Bellis L, Johnson MP (2001) A mammalian predator–prey imbalance: grizzly bear and wolf extinction affect avian neotropical migrants. Ecol Appl 11:947–960

    Google Scholar 

  • Boydston EE, Kapheim KM, Van Horn RC, Smale L, Holekamp KE (2005) Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyena (Crocuta crocuta). J Zool 267:271–281

    Article  Google Scholar 

  • Brook LA, Johnson CN, Ritchie EG (2012) Effects of predator control on behaviour of an apex predator and indirect consequences for mesopredator suppression. J Appl Ecol 49:1278–1286

    Article  Google Scholar 

  • Brown JS, Laundre JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and Multimodel inference: a practice information-theoretic approach. Springer Verlag, New York

    Google Scholar 

  • Carbone C, Du Toit JT, Gordon IJ (1997) Feeding success in African wild dogs: does kleptoparasitism by spotted hyenas influence hunting group size? J Anim Ecol 66:318–326

    Article  Google Scholar 

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

    Google Scholar 

  • Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Hold RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315

    Article  Google Scholar 

  • Cozzi G, Broekhuis F, McNutt JW, Turnbull LA, Macdonald DW, Schmid B (2012) Fear of the dark or dinner by moonlight? Reduced temporal partitioning among Africa’s large carnivores. Ecology 93:2590–2599

    Article  PubMed  Google Scholar 

  • Creel S (2001) Four factors modifying the effect of competition on carnivore population dynamics illustrated by African wild dogs. Conserv Biol 15:271–274

    Article  Google Scholar 

  • Creel S, Creel NM (1996) Limitation of African wild dogs by competition with larger carnivores. Conserv Biol 10:526–538

    Article  Google Scholar 

  • Creel S, Spong G, Creel N (2001) Interspecific competition and the population biology of extinction-prone carnivores. In: Gittleman JL, Funk SM, Macdonald D, Wayne RK (eds) Carnivore conservation. Cambridge University Press, Cambridge, pp 35–60

    Google Scholar 

  • Di Bitetti MS, De Angelo CD, Di Blanco YE, Paviolo A (2010) Niche partitioning and species coexistence in a Neotropical felid assemblage. Acta Oecol 36:403–412

    Article  Google Scholar 

  • Donadio E, Buskirk SW (2006) Diet, morphology, and interspecific killing in carnivora. Am Nat 167:524–536

    Article  PubMed  Google Scholar 

  • Donovan TM, Hines J (2007) Exercises in Occupancy Modeling and Estimation, <http://www.uvm.edu/envnr/vtcfwru/spreadsheets/occupancy/occupancy.htm>

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

    Article  Google Scholar 

  • Elmhagen B, Ludwig G, Rushton SP, Helle P, Linden H (2010) Top predators, mesopredators and their prey: interference ecosystems along bioclimatic productivity gradients. J Anim Ecol 79:785–794

    CAS  PubMed  Google Scholar 

  • Finke DL, Denno RF (2006) Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades. Oecologia 149:265–275

    Article  PubMed  Google Scholar 

  • Frank DA (2008) Evidence for top predator control of a grazing ecosystem. Oikos 117:1718–1724

    Article  Google Scholar 

  • Gittleman JL (1985) Carnivore body size: ecological and taxonomic correlates. Oecologia 67:540–554

    Article  Google Scholar 

  • Hayward MW, Slotow R (2009) Temporal partitioning of activity in large African carnivores: tests of multiple hypotheses. S Afr J Wildl Res 39:109–112

    Article  Google Scholar 

  • Helldin JO, Liberg O, Glöersen G (2006) Lynx (Lynx lynx) killing red foxes (Vulpes vulpes) in boreal Sweden—frequency and population effects. J Zool 270:657–663

    Article  Google Scholar 

  • Hines JE (2006) Program PRESENCE, http://www.mbrpwrc.usgs.gov/software/doc/presence/presence.html

  • Hunter J, Caro T (2008) Interspecific competition and predation in American carnivore families. Ethol Ecol Evol 20:295–324

    Article  Google Scholar 

  • iSimangaliso Wetland Park Authority (2014) Land cover map of iSimangaliso Wetland Park. iSimangaliso Wetland Park Authority, St. Lucia Estuary, KwaZulu-Natal, 3936, South Africa

  • Kalle R, Ramesh T, Qureshi Q, Sankar K (2013) Predicting the distribution pattern of small carnivores in response to environmental factors in the western Ghats. PLoS One 8:e79295

    Article  PubMed  PubMed Central  Google Scholar 

  • Karanth KU, Sunquist ME (2000) Behavioural correlates of predation by tiger (Panthera tigris), leopard (Panthera pardus) and dhole (Cuon alpinus) in Nagarahole, India. J Zool 250:255–265

    Article  Google Scholar 

  • Kruuk H (1972) The spotted Hyaena: a study of predation and social behavior. University of Chicago Press, Chicago

    Google Scholar 

  • Lazenby BT, Dickman CR (2013) Patterns of detection and capture are associated with cohabiting predators and prey. PLoS One 8:e59846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letnic M, Koch F, Gordon C, Crowther MS, Dickman CR (2009) Keystone effects of an alien top-predator stem extinctions of native mammals. Proc R Soc Lond B 276:3249–3256

    Article  Google Scholar 

  • Lindsey PA, Romañach S, Daviesn-Mostert H (2009) The financial drivers of predator conservation on private land in South Africa. In: Hayward MW, Somers MJ (eds) The reintroduction of top-order predators. Wiley-Blackwell Publishing, Oxford, pp 321–344

    Chapter  Google Scholar 

  • Linnell JDC, Strand O (2000) Interference interactions, co-existence and conservation of mammalian carnivores. Divers Distrib 6:169–176

    Article  Google Scholar 

  • Lourenco R, Penteriani V, Rabac E (2014) Lethal interactions among vertebrate top predators: a review of concepts, assumptions and terminology. Biol Rev 89:270–283

    Article  PubMed  Google Scholar 

  • MacKenzie DI, Bailey LI, Nichols JD (2004) Investigating species co-occurrence patterns when species are detected imperfectly. J Anim Ecol 73:546–555

    Article  Google Scholar 

  • MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LI, Hines JE (2006) Occupancy estimation and modeling. Elsevier, Amsterdam

    Google Scholar 

  • Matthews WS, van Wyk AE, van Rooyen N, Botha GA (2001) Vegetation of the Tembe Elephant Park, Maputaland, South Africa. S Afr J Bot 67:573–594

    Article  Google Scholar 

  • McGee BK, Ballard WB, Nicholson KL, Cypher BL, Lemons PR, Kamler JF (2006) Effects of artificial escape dens on swift fox populations in Northwest Texas. Wildlife Soc Bull 34:821–827

    Article  Google Scholar 

  • Meredith M, Ridout M (2016) overlap: Estimates of Coefficient of Overlapping for Animal Activity Patterns. R package version 0.2.6, http://CRAN.R-project.org/package=overlap

  • Millspaugh JJ, Rittenhouse CD, Montgomery RA, Matthews WS, Slotow R (2015) Resource selection modeling reveals potential conflicts involving reintroduced lions in Tembe Elephant Park, South Africa. J Zool 296:124–132

    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 

  • Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153:492–508

    Article  Google Scholar 

  • Palomares F, Delibes M (1990) Habitat preferences of large grey mongooses Herpestes ichneumon in Spain. Acta Theriol 35:1–6

    Article  Google Scholar 

  • Palomares F, Ferreras P, Fedriani JM, Delibes M (1996) Spatial relationships between Iberian lynx and other carnivores in an area of south-western Spain. J Appl Ecol 33:5–13

    Article  Google Scholar 

  • Pasanen-Mortensen M, Pyykönen M, Elmhagen B (2013) Where lynx prevail, foxes will fail—limitation of a mesopredator in Eurasia. Glob Ecol Biogeogr 22:868–877

    Article  Google Scholar 

  • Ramesh T (2010) Prey selection and food habits of large carnivores: tiger Panthera tigris, leopard Panthera pardus and dhole Cuon alpinus in Mudumalai Tiger Reserve, Tamil Nadu. PhD thesis, Saurashtra University, Gujarat, Rajkot

  • Ramesh T, Kalle R, Sankar K, Qureshi Q (2012a) Dietary partitioning in sympatric large carnivores in a tropical forest of Western Ghats, India. Mamm Study 37:313–321

    Article  Google Scholar 

  • Ramesh T, Kalle R, Sankar K, Qureshi Q (2012b) Spatio–temporal partitioning among large carnivores in relation to major prey species in Western Ghats. J Zool 287:269–275

    Article  Google Scholar 

  • Ramesh T, Kalle R, Sankar K, Qureshi Q (2013) Dry season factors determining habitat use and distribution of mouse deer (Moschiola indica) in the Western Ghats. Eur J Wildlife Res 59:271–280

    Article  Google Scholar 

  • Ramesh T, Kalle R, Sankar K, Qureshi Q (2015) Role of body size in activity budgets of mammals in the Western Ghats of India. J Trop Ecol 31:315–323

    Article  Google Scholar 

  • Ramesh T, Kalle R, Rosenlund H, Downs CT (2016) Native habitat and protected area size matters: preserving mammalian assemblages in the Maputaland Conservation Unit of South Africa. Forest Ecol Manag 360:20–29

    Article  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. – R Foundation for Statistical Computing, Vienna, <http://www.Rproject.org/>

  • Ridout MS, Linkie M (2009) Estimating overlap of daily activity patterns from camera trap data. J Agric Biol Envir S 14:322–337

    Article  Google Scholar 

  • Ripple WJ, Beschta RL (2004) Wolves and the ecology of fear: can predation risk structure ecosystems? Bioscience 54:755–766

    Article  Google Scholar 

  • Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP (2014) Status and ecological effects of the world’s largest carnivores. Science 343:6167

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Robinson SK, Terborgh J (1995) Interspecific aggression and habitat selection by Amazonian birds. J Anim Ecol 64:1–11

    Article  Google Scholar 

  • Rosenheim JA (2004) Top predators constrain the habitat selection game played by intermediate predators and their prey. Israel J Zool 50:129–138

    Article  Google Scholar 

  • Rosenzweig ML (1966) Community structure in sympatric carnivore. J Mammal 47:602–612

    Article  Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Schaller GB (1972) The Serengeti lion: a study of predator–prey relations. University of Chicago Press, Chicago

    Google Scholar 

  • Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285

    Article  Google Scholar 

  • Seidensticker J (1976) On the ecological separation between tigers and leopards. Biotropica 8:225–234

    Article  Google Scholar 

  • Slotow R, Hunter LT (2009) Reintroduction decisions taken at the incorrect social scale devalue their conservation contribution: the African lion in South Africa. In: Hayward MW, Somers MJ (eds) The reintroduction of top-order predators. Wiley-Blackwell Publishing, Oxford, pp 43–71

    Chapter  Google Scholar 

  • Sollmann R, Furtado MM, Hofer H, Jácomo AT, Tôrres NM, Silveira L (2012) Using occupancy models to investigate space partitioning between two sympatric large predators, the jaguar and puma in Central Brazil. Mammal Biol 77:41–46

    Google Scholar 

  • Stein AB, Bourquin SL, McNutt JW (2015) Avoiding intraguild competition: leopard feeding ecology and prey caching in northern Botswana. S Afr J Wildl Res 45:247–257

    Article  Google Scholar 

  • Steinmetz R, Seuaturien N, Chutipong W (2013) Tigers, leopards, and dholes in a half-empty forest: assessing species interactions in a guild of threatened carnivores. Biol Conserv 163:68–78

    Article  Google Scholar 

  • St-Pierre C, Ouellet JP, Crete M (2006) Do competitive intraguild interactions affect space and habitat use by small carnivores in a forested landscape? Ecography 29:487–496

    Article  Google Scholar 

  • Terborgh J, Lopez L, Nunez P et al (2001) Ecological meltdown in predator-free forest fragments. Science 294:1923–1926

    Article  CAS  PubMed  Google Scholar 

  • Trinkel M, Kastberger G (2005) Competitive interactions between spotted hyenas and lions in the Etosha National Park, Namibia. Afr J Ecol 43:220–224

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Vucetich JA, Creel S (1999) Ecological interactions, social organization, and extinction risk in African wild dogs. Conserv Biol 13:1172–1182

    Article  Google Scholar 

  • Waddle JH, Dorazio RM, Walls SC, Rice KG, Beauchamp J, Schuman MJ, Mazzotti FJ (2010) A new parameterization for estimating co-occurrence of interacting species. Ecol Appl 20:1467–1475

    Article  PubMed  Google Scholar 

  • Wiens JA (1989) The ecology of bird communities. Volume 2. Processes and variations. Cambridge University Press, New York

    Book  Google Scholar 

Download references

Acknowledgments

We thank the College of Agriculture, Engineering and Science of the University of KwaZulu-Natal for the financial support of the first two authors under the Post-doctoral Research Programme. We thank iSimangaliso Wetland Park Authority and Ezemvelo KZN Wildlife for granting us permission to conduct our research activities within the protected areas. D. Rossow, N. Govender, C. Hanekom, X. Combrink and T. Bodasing are thanked for enabling data collection during field work. We thank D. Ehlers Smith for valuable editorial input in the final version. We are grateful to H. Rosenlund, B. Humphries, M. Summers, M.G. Alam, L. Thompson, M. Drabik-Hamshare and field rangers for their assistance in the field. We thank L. Grobler for the accommodation. We are grateful for the constructive comments of the reviewers.

Author information

Authors and Affiliations

  1. School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville, Pietermaritzburg, KwaZulu-Natal, 3209, South Africa

    Tharmalingam Ramesh, Riddhika Kalle & Colleen T. Downs

  2. School of Ecology and Environment Studies, Nalanda University, Rajgir, Bihar, India

    Riddhika Kalle

Authors
  1. Tharmalingam Ramesh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Riddhika Kalle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Colleen T. Downs
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Colleen T. Downs.

Ethics declarations

Funding

This study was funded by the University of KwaZulu-Natal incentive funding to CT D and postdoctoral funding to RT and RK. In addition, TR was also funded by National Research Foundation, South Africa. We are grateful to the Hans Hoheisen Trust for monies for camera traps.

Ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. As camera trapping was used, no animals were handled.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by K. E. Ruckstuhl

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramesh, T., Kalle, R. & Downs, C.T. Staying safe from top predators: patterns of co-occurrence and inter-predator interactions. Behav Ecol Sociobiol 71, 41 (2017). https://doi.org/10.1007/s00265-017-2271-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-017-2271-y

Keywords

Search

Navigation