Theoretical Ecology

, Volume 5, Issue 4, pp 517–532 | Cite as

Revealing the role of predator-dependent disease transmission in the epidemiology of a wildlife infection: a model study

  • A. Yu. MorozovEmail author
Original paper


It is well known that predation/harvesting on a species subjected to an infectious disease can affect both the infection prevalence and the population dynamics. In this paper, I model predator–prey–pathogen interactions in the case where the presence of a predator indirectly affects the transmission rate of the infection in its prey. I call this phenomenon the predator-dependent disease transmission. Such a scenario can arise, for example, as a consequence of anti-predator defence behaviour, debilitating the immune system of the prey. Although being well documented, the predator-dependent disease transmission has rarely been taken into account in ecoepidemiological models. Mathematically, I consider a classical S-I-P ecoepidemiological model in which the infected and/or the healthy host can be consumed by a predator where the coefficient in the mass action transmission term is predator-dependent. Investigation of the model shows that including such a predator-dependent disease transmission can have important consequences for shaping predator–prey–pathogen interactions. In particular, this can enhance the survival of the predator, restricted in a system with a predator-independent disease transmission. I demonstrate the emergence of a disease-mediated strong Allee effect for the predator population. I also show that in the system with predator-dependent disease transmission, the predator can indirectly promote epidemics of highly virulent infectious diseases, which would die out in a predator-free system. Finally, I argue that taking into account predator-dependent disease transmission can have a destabilizing effect in a eutrophic environment, which can potentially cause the extinction of both species. I also show that including the predator-dependent disease transmission may increase the infection prevalence, and this fact will question the ‘keeping herds healthy’ hypothesis concerning the management of wildlife infections by natural predators.


Ecoepidemiology Transmission rate Predator–prey model Paradox of enrichment Anti-predator defence behaviour 



I highly appreciated Dr. Samrat Chatterjee (ICGEB, India) and Prof. S. Petrovskii (University of Leicester, UK) for a stimulating discussion on an earlier version of the manuscript.


  1. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  2. Allee WC (1938) The social life of animals. Norton, New YorkCrossRefGoogle Scholar
  3. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 34:517–547CrossRefGoogle Scholar
  4. Al-Zyoud F, Sengonca C (2004) Prey consumption preferences of Serangium parcesetosum Sicard (Col., Coccinelidae) for different prey stages, species and parasitized prey. J Pest Sci 77:197–204CrossRefGoogle Scholar
  5. Anderson RM, May RM (1979) Population biology of infectious diseases. Part I. Nature 280:361–367PubMedCrossRefGoogle Scholar
  6. Baker RL, Smith BP (1997) Conflict between antipredator and antiparasite behaviour in larval damselflies. Oecologia 109:622–628CrossRefGoogle Scholar
  7. Behringer DC, Butler MJ (2010) Disease avoidance influences shelter use and predation in Caribbean spiny lobster. Behav Ecol Sociobiol 64:747–755CrossRefGoogle Scholar
  8. Caceres C, Knight C, Hall SR (2009) Predator-spreaders: predation can enhance parasite success in a planktonic host–parasite system. Ecology 90:2850–2858PubMedCrossRefGoogle Scholar
  9. Chattopadhyay J, Bairagi N (2001) Pelicans at risk in Salton Sea—an eco-epidemiological study. Ecol Model 136:102–112CrossRefGoogle Scholar
  10. Choisy M, Rohani P (2006) Harvesting can increase severity of wildlife disease epidemics. Proc Royal Soc B 273:2025–2034CrossRefGoogle Scholar
  11. Choo K, Williams PD, Day T (2003) Predation, host mortality, and the evolution of virulence. Ecol Letters 6:310–315CrossRefGoogle Scholar
  12. Cote I, Poulin R (1995) Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology 6:159–163CrossRefGoogle Scholar
  13. Courchamp F, Clutton-Brock T, Grenfell B (1999) Inverse density dependence and the Allee effect. Trends Ecol Evol 14:405–410PubMedCrossRefGoogle Scholar
  14. Courchamp F, Berec L, Gascoigne J (2008) Allee effects in ecology and conservation. Oxford University Press, OxfordCrossRefGoogle Scholar
  15. Decaestecker E, De Meester L, Ebert D (2002) In deep trouble: habitat selection constrained by multiple enemies in zooplankton. Proc Natl Acad Sci USA 99:5481–5485PubMedCrossRefGoogle Scholar
  16. Dennis B (1989) Allee effect: population growth, critical density and the chance of extinction. Nat Res Model 3:481–538Google Scholar
  17. Diekmann O, Heesterbeek JAP, Metz JAJ (1990) On the definition and the computation of the basic reproduction ratio R 0 in models for infectious diseases in heterogeneous populations. J Math Biol 28:365–382PubMedCrossRefGoogle Scholar
  18. Duffy MA, Sivars-Becker L (2007) Rapid evolution and ecological host–parasite dynamics. Ecol Letters 10:44–53CrossRefGoogle Scholar
  19. Edgerly SJ (1994) Is group living an antipredator defense in a facultatively communal webspinner (Embiidina: Clothodidae)? J Insect Behavior 7:135–147CrossRefGoogle Scholar
  20. Freeland WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8:12–24CrossRefGoogle Scholar
  21. Friend M (2002) Avian disease at the Salton Sea. Hydrobiologia 473:293–306CrossRefGoogle Scholar
  22. Friman VP, Lindstedt C, Hiltunen T, Laakso J, Mappes J (2009) Predation on multiple trophic levels shapes the evolution of pathogen virulence. PLoS One 4(8):6761CrossRefGoogle Scholar
  23. Greenman JV, Hoyle A (2010) Pathogen exclusion from eco-epidemiological systems. Am Nat 176:149–158PubMedCrossRefGoogle Scholar
  24. Hawlena D, Abramsky Z, Bouskila A (2010) Bird predation alters infestation of desert lizards by parasitic mites. Oikos 119:730–736CrossRefGoogle Scholar
  25. Hilker FM, Schmitz K (2008) Disease-induced stabilization of predator–prey oscillations. J Theor Biol 255:299–306PubMedCrossRefGoogle Scholar
  26. Holt RD, Roy M (2007) Predation can increase the prevalence of infectious disease. Am Nat 169:690–699PubMedCrossRefGoogle Scholar
  27. Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol 61:681–692CrossRefGoogle Scholar
  28. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258PubMedCrossRefGoogle Scholar
  29. Johnson PTJ, Stanton DE, Preu ER, Forshay KJ, Carpenter SR (2006) Dining on disease: how interactions between infection and environment affect predation risk. Ecology 87:1973–1980PubMedCrossRefGoogle Scholar
  30. Johnson PTJ, Dobson A, Lafferty K, Marcogliese DJ, Memmott J, Orlofske PR, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371PubMedCrossRefGoogle Scholar
  31. Jones GA, Sieving KE, Avery ML, Meagher RL (2005) Parasitized and nonparasitized prey selectivity by an insectivorous bird. Crop Prot 24:185–189CrossRefGoogle Scholar
  32. Kabata Z (1985) Parasites and diseases of fish cultured in the tropics. Taylor & Francis, LondonGoogle Scholar
  33. Kagami M, Van Donk E, De Bruin A et al (2004) Daphnia can protect diatoms from fungal parasitism. Limnol Oceanogr 49:680–685CrossRefGoogle Scholar
  34. Kortet R, Rantala MJ, Hedrick A (2007) Boldness in anti-predator behaviour and immune defence in field crickets. Evol Ecol Res 9:185–197Google Scholar
  35. Krasnov B, Khokhlova IS, Shenbrot GI (2002) The effect of host density on ectoparasite distribution: an example of a rodent parasitized by fleas. Ecology 83:164–175CrossRefGoogle Scholar
  36. Liao CM, Yeh CH, Chen SC (2008) Predation affects the susceptibility of hard clam Meretrix lusoria to Hg-stressed birnavirus. Ecol Model 210:253–262CrossRefGoogle Scholar
  37. Malchow H, Hilker FM, Petrovskii SV, Brauer K (2004) Oscillations and waves in a virally infected plankton system. I. The lysogenic stage. Ecological Complexity 1:211–223CrossRefGoogle Scholar
  38. Matz C, Kjelleberg S (2005) Off the hook—how bacteria survive protozoan grazing. Trends Microbiol 13:302–307PubMedCrossRefGoogle Scholar
  39. McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends Ecol Evol 16(6):295–300PubMedCrossRefGoogle Scholar
  40. McCauley E, Nisbet RM, Murdoch WM, de Roos AM, Gurney WSC (1999) Large-amplitude cycles of Daphnia and its algal prey in enriched environments. Nature 402:653–656Google Scholar
  41. Morozov AY, Adamson M (2011) Evolution of virulence driven by predator–prey interaction: possible consequences for population dynamics. J Theor Biol 276:182–191CrossRefGoogle Scholar
  42. Mukherjee D (1998) Uniform persistence in a generalized prey–predator system with parasite infection. Biosystems 47:149–155PubMedCrossRefGoogle Scholar
  43. Navarro C, de Lope F, Marzal A, Møller AP (2003) Predation risk, host immune response, and parasitism. Behav Ecology 15:4Google Scholar
  44. Ostfeld RS, Holt RD (2004) Are predators good for your health? Evaluating evidence for top-down regulation of zoonotic disease reservoirs. Frontiers Ecol Environ 2:13–20CrossRefGoogle Scholar
  45. Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecol Letters 6:797–802CrossRefGoogle Scholar
  46. Parris M, Reese E, Storfer A (2006) Antipredator behavior of chytridiomycosis-infected northern leopard frog (Rana pipiens) tadpoles. Can J Zool 84:58–65CrossRefGoogle Scholar
  47. Pfennig DW (2000) Effect of predator–prey phylogenetic similarity on the fitness consequences of predation: a trade-off between nutrition and disease? Am Nat 155:335–345PubMedCrossRefGoogle Scholar
  48. Rhodes CJ, Martin AP (2010) The influence of viral infection on a plankton ecosystem undergoing nutrient enrichment. J Theor Biol 265:225–237PubMedCrossRefGoogle Scholar
  49. Rigby MC, Jokela J (2000) Predator avoidance and immune defence: costs and trade-offs in snails. Proc R Soc Lond B Biol Sci 267:171–176CrossRefGoogle Scholar
  50. Rosenzweig ML (1971) Paradox of enrichment: destabilization of exploitation ecosystems in ecological time. Science 171:385–387Google Scholar
  51. Roy S, Chattopadhyay J (2005) Disease-selective predation may lead to prey extinction. Math Methods Appl Sci 28:1257–1267CrossRefGoogle Scholar
  52. Roy M, Holt RD (2008) Effects of predation on host–pathogen dynamics in SIR models. Theor Pop Biol 73:319–331CrossRefGoogle Scholar
  53. Ryder JJ, Miller MR, White A, Knell RJ, Boots M (2007) Host–parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116:2017–2026CrossRefGoogle Scholar
  54. Sieber M, Hilker FM (2011) Prey, predators, parasites: intraguild predation or simpler community modules in disguise? J Anim Ecol 80:414–421PubMedCrossRefGoogle Scholar
  55. Siekmann I, Malchow H, Venturino E (2010) On competition of predators and prey infection. Ecological Complexity 7(44):446–457CrossRefGoogle Scholar
  56. Stiling P, Moon DC (2005) Quality or quantity: the direct and indirect effects of host plants on herbivores and their natural enemies. Oecologia 142:413–420PubMedCrossRefGoogle Scholar
  57. Thiemann GW, Wassersug RJ (2000) Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles. Biol J Linn Soc 71:513–528CrossRefGoogle Scholar
  58. Tierney JF, Huntingford FA, Crompton DW (1993) The relationship between infectivity of Schistocephalus solidus (Cestoda) and antipredator behavior of its intermediate host, the 3-spined stickleback, Gasterosteus aculeatus. Anim Behav 46:603–605CrossRefGoogle Scholar
  59. van der Veen IT (2005) Costly carotenoids: a trade-off between predation and infection risk? J Evol Biol 18:992–999CrossRefGoogle Scholar
  60. Venturino E (2010) Ecoepidemic models with disease incubation and selective hunting. J Comput Appl Math 234:2883–2901CrossRefGoogle Scholar
  61. Watve MG, Jog MM (1997) Epidemic diseases and host clustering: an optimum cluster size ensures maximum survival. J Theor Biol 184:165–169PubMedCrossRefGoogle Scholar
  62. Wilson K, Knell R, Boots M, Koch-Osborne J (2003) Group living and investment in immune defence: an interspecific analysis. J Anim Ecol 72:133–143CrossRefGoogle Scholar
  63. Yin M, Laforsch C, Lohr JN, Wolinska J (2011) Predator-induced defense makes Daphnia more vulnerable of parasites. Evolution 65:1482–1488PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of MathematicsUniversity of LeicesterLeicesterUK
  2. 2.Shirshov Institute of OceanologyMoscowRussia

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