Skip to main content

Advertisement

SpringerLink
Log in

Horizontal disease transmission in lions from behavioural interfaces via social network analysis

  • Original Paper
  • Published:
Mammal Research Aims and scope Submit manuscript

Abstract

The degree of relatedness and an interacting unifying central member can exacerbate disease transmission within a social group. The severity of the disease depends on the route, dose and frequency of infection. Group-living social mammals thus have the ability to exacerbate the spread of the disease. Lions Panthera leo are social carnivores with individuals interacting on a regular basis. We used observations of lion behaviours to define potential transmission routes between individuals and the likely spread of diseases in the lion population of the Kruger National Park. This allowed description of the epidemiology of bovine tuberculosis to mimic and predict the potential rate of horizontal disease transmission within lion prides. Social network analysis allowed us to identify the most important pride members and the implications of interactions with these members for spreading disease in prides. Three prides in the southern region of the Kruger National Park comprised degrees of relatedness within prides that predict variable links between pride members. The interactive behaviour of young lions with each other, a key element of learning in social mammals, play a key role in dictating contact rates that enhance disease transmission. Even so, within prides, R0 < 1 predicts that bovine tuberculosis should disappear from a pride. Persistence of the disease as noted for lions in Kruger can only realize through unlikely transmissions or through feeding on infected prey. Our results support lions as a spill-over host.

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
Fig. 5

Similar content being viewed by others

References

  • Arsenault R, Owen-Smith N (2002) Facilitation versus competition in grazing herbivore assemblages. Oikos. 97:313–318

    Article  Google Scholar 

  • Ayele WY, Neill SD, Zinstag J, Weiss MG, Pavlik I (2004) Bovine tuberculosis: an old disease but a new threat to Africa. Int J Tuberculosis Lung Disease. 8(8):924–937

    CAS  Google Scholar 

  • Bertram BBR (1975) The social system of lions. Sci Am 232:54–65

    Article  Google Scholar 

  • Caraco T, Wolf LL (1975) Ecological determinants of group sizes of foraging lions. Am Nat 109(967):343–352

    Article  Google Scholar 

  • Craft ME, Hawthorne P, Packer C, Dobson AP (2008) Dynamics of a multihost pathogen in a carnivore community. J Anim Ecol 77:1257–1264

    Article  CAS  Google Scholar 

  • Craft, M.E., Volz, E., Packer, C. & Meyers, L.A. 2010. Disease transmission in territorial populations: the small-world network of Serengeti lions. J R Soc.

  • Creel S, Creel NM (2002) The African wild dog: behaviour, ecology and conservation. Princeton University Press, Princeton

    Book  Google Scholar 

  • Cross PC, Heisey DM, Bowers JA, Hay CT, Wolhuter J, Buss P, Hofmeyr M, Michel AL, Bengis RG, Bird TLF, Du Toit JT, Getz WM (2009) Disease, predation and demography: assessing the impacts of bovine tuberculosis on African buffalo by monitoring at individual and population levels. J Appl Ecol 46:467–475

    Article  Google Scholar 

  • Csardi G. & Nepuszi T (2006). The igraph software package for complex network research. Int J Complex Syst 1695. http://igraph.org. Accessed 26/04/2019

  • Davidson Z, Valeix M, Van Lestren F, Loveridge AJ, Hunt JJ, Murindagomo F, Macdonald DW (2013) Seasoanl diet and prey reference of the African lion in a waterhole-driven semi-arid savanna. PLoS One. 8(2):e55182

    Article  CAS  Google Scholar 

  • De Lisle GW, Bengis RG, Schmitt SM, O’brien DJ (2002) Tuberculosis in free-ranging wildlife: Detection, diagnosis and management. Rev Sci Tech: International Office of Epizootics 21(2):317–334

    Article  Google Scholar 

  • du Bothma JP (2006) Game Ranch Management, 4th edn. Van Schaik Publishers, Paarl

    Google Scholar 

  • Estrada E (2012) The structure of complex networks: theory and applications. OUP Oxford, Oxford

    Google Scholar 

  • Ferreira SM, Funston PJ (2010) Estimating lion population variables: prey and disease effects in Kruger National Park, South Africa. Wildlife Research, 37, 194–206

  • Ferreira SM, Maruping NT, Schoultz D Smit, TR (2013) Effects of the number of people on efficient capture and sample collection: A lion case study. Journal of the South African Veterinary Association. https://doi.org/10.4102/jsava.v84i1.131

  • Fox J (2005) The R Commander: A Basic Statistics Graphical User Interface to R. Journal of Statistical Software 14(9):1–42

  • Fulford GR, and Roberts MG (2002) The metapopulation dynamics of an infectious disease: tuberculosis in possums. Theor Popul Biol 61:15–29

  • Funston PJ, Mills MGL, Richardson PRK, Van Jaarsveld AS (2003) Reduceddispersal and opportunistic territory acquisition inmale lions (Panthera leo).J. Zool. 259(2): 131–142

  • Gertenbach WPD (1983) Landscape of the Kruger National Park. Koedoe. 26:9–121

    Article  Google Scholar 

  • Hagberg AA, Schult DA & Swart PJ 2008. Exploring network structure, dynamics and function using NetworkX. Proceedings of the 7th Python in Science Conference. Varoquaux, G, Vaught T & Millman J (Eds), Pasadena, California. 11– 15.

  • Hess G (1996) Disease in metapopulation models: Implications for conservation. Ecology. 77(5):1617–1632

    Article  Google Scholar 

  • Holekamp KE, Sakai ST, Lundrigan BL (2007) Social intelligence in the spotted hyena (Crocuta crocuta). Philos Trans R Soc London B: Biological Sciences. 362(1480):523–538

    Article  Google Scholar 

  • Keet DF, Friek NP, Penrith ML, Michel A, Huchzermeyer H (1996) Tuberculosis in buffaloes (Syncerus caffer) iin the Kruger National Park: spread of the disease to other species. Onderstepoort J Vet Res 63:239–244

    PubMed  CAS  Google Scholar 

  • Keet DF, Kriek NPJ, Bengis RG, Michel AL (2001) Tuberculosis in kudus (Tragelaphus strepsiceros) in the Kruger National Park. Onderstepoort J Vet Res 68:225–230

    PubMed  CAS  Google Scholar 

  • Keet DF, Michel AL, Bengis RG, Becker P, Van Dyk DS, Van Vuuren M, Rutten VPMG, Penzhorn BL (2010) Intradermal tuberculin testing of wild African lions (Panthera leo) naturally exposed to infection with Mycobacterium bovis. Vet Microbiol 144:384–391

    Article  CAS  Google Scholar 

  • Kosmala M, Miller P, Ferreira S, Funston P, Keet D, Packer C (2016) Estimating wildlife disease dynamics in a complex system using an approximate Bayesian computation framework. Ecol Appl. 26(1):295–308

    Article  Google Scholar 

  • Maas M, Keet DF, Rutten VPMG, Heesterbeek JAP, & Nielen M 2012. Assessing the impacts of feline immunodeficiency virus and bovine tuberculosis co-infection in African lions. Proc R Soc B. (www.rspb.royalsocietypublishing.org). Accessed October 2013.

  • Mccomb K, Moss C, Durant SM, Baker L, Sayialel S (2001) Matriarchs as repositories of social knowledge in African elephants. Science. 292(5516):491–494

    Article  CAS  Google Scholar 

  • Michel AL, Bengis RG, Keet DF, Hofmeyr M, De Klerk LM, Cross PC, Jolles AE, Cooper D, Whyte IJ, Buss P, Godfroid J (2006) Wildlife tuberculosis in South African conservation areas: implications and challenges. Vet Mircobiology 112:91–100

    CAS  Google Scholar 

  • Morris RS, Pfeiffer DU, Jackson R (1994) The epidemiology of Mycobacterium bovis infections. Vet Microbiol 40:153–177

    Article  CAS  Google Scholar 

  • Newman MEJ (2004) Analysis of weighted networks. Physics Review E 70(5):056131

    Article  CAS  Google Scholar 

  • Newman MEJ, Leicht E.A (2007) Mixture models and exploratory analysis in networks. 104 (23) 9564–9569. https://doi.org/10.1073/pnas.0610537104

  • Packer C & Pusey AE 1997. Divided we fall: cooportaion among lions. Sci Am 32–39.

  • Packer C, Altizer S, Appel M, Brown E, Martenson J, O’Brien SJ, Roelke-Parker M, Hofmann-Lehmann R, Lutz H (1999) Viruses of the Serengeti: patterns of infection and mortality in African lions. J Anim Ecol. 68:1161–1178

    Article  Google Scholar 

  • Packer C, Hilbron R, Mosser A, Kissui B, Borner M, Hopcroft G, Wilmshhurst J, Mduma S, Sinclair ARE (2005) Ecological change, group territoriality and population dynamics in Serengeti lions. Science. 307:390–393

    Article  CAS  Google Scholar 

  • Pusey AE, Packer C (1994) Non-offspring nursing in social carnivores: minimizing the costs. Behav Ecol 5(4):362–375

    Article  Google Scholar 

  • R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Renwick AR, White PCL, Bengis RG (2007) Bovine tuberculosis in southern African wildlife: a multi-species host-pathogen system. Epidemol Infect 135:529–540

    Article  CAS  Google Scholar 

  • Rodwell TC, Friek NP, Bengis RG, Whyte IJ, Viljoen PC, De Vos V, Boyce W (2001a) Prevalence of Bovine tuberculosis in African buffalo at Kruger National Park. J Wildl Dis 37(2):258–264

    Article  CAS  Google Scholar 

  • Smuts GL, Whyte IJ, Dearlove TW (1977) A mass capture technique for lions. E Afr Wildl J 15:81–87

    Article  Google Scholar 

  • Valeix M, Loveridge AJ, Chamaille-Jammes S, Davidson Z, Murindagomo F, Fritz H, Macdonald DW (2009) Behavioural adjustments of African herbivores to predation risk by lions: Spatiotemporal variations influence habitat use. Ecology. 90(1):23–30

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The opportunity to conduct this research in the Kruger National Park was only possible thanks to South African National Parks, particularly S. F., Tshwane University of Technology and guidance from P.J. F. The Scientific Services staff, Veterinary Wildlife Services and the Office of the State Veterinarians in the Kruger National Park are acknowledged for their help in coordinating and executing the study. For their support and time, the staff at Jock Safari Lodge, the chopper pilots of Airwing and the camp managers, field and section rangers of the Kruger National Park are thanked. Special thanks go to the game guards who regularly walked into certain danger and adventure. The Ajubatus Foundation and the Tshwane University of Technology, particularly the Department of Nature Conservation, are deeply thanked for their logistical support. Special thank you to M. Hofmeyr, P. Buss, T. Smit, D. Scholtz, K. Makutulela N. Maputla, K. Young and S. Midzi.

Author information

Author notes

  1. N. T. Maruping-Mzileni, S. M. Ferreira, P. J. Funston, F. Kalala Mutombo and V. Goodall contributed equally to this work.

Authors and Affiliations

  1. Scientific Services, South African National Parks, Kimberley, Northern Cape, 8031, South Africa

    N. T. Maruping-Mzileni

  2. Scientific Services, South African National Parks, Skukuza, Mpumalanga, 1350, South Africa

    S. M. Ferreira

  3. Panthera, New York, NY, 10018, USA

    P. J. Funston

  4. Department of Mathematics, University of Lubumbashi, Lubumbashi, DRC, 1825, South Africa

    F. Kalala Mutombo

  5. Department of Statistics, Nelson Mandela University, Port Elizabeth, 6031, South Africa

    V. Goodall

Authors
  1. N. T. Maruping-Mzileni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. M. Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. J. Funston
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Kalala Mutombo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. Goodall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. T. Maruping-Mzileni.

Additional information

Communicated by: Thales Renato Ochotorena de Freitas

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maruping-Mzileni, N.T., Ferreira, S.M., Funston, P.J. et al. Horizontal disease transmission in lions from behavioural interfaces via social network analysis. Mamm Res 65, 709–718 (2020). https://doi.org/10.1007/s13364-020-00526-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13364-020-00526-7

Keywords

Search

Navigation