Theoretical Ecology

, 2:53 | Cite as

Invading with biological weapons: the role of shared disease in ecological invasion

  • Sally S. Bell
  • Andrew White
  • Jonathan A. Sherratt
  • Mike Boots
Original paper


Theory has been developed that examines the role of infectious disease in ecological invasions for particular natural systems. However, a general understanding of the role that shared disease may play in invasions is lacking. Here, we develop a strategic theoretical framework to determine the role of disease, in addition to competition, in ecological invasions and the expansion of species’ spatial range. We investigate the effect of different disease parameters on the replacement time of a native species by an alien invader. The outcome is critically dependent on the relative effects that the disease has on the two species and less dependent on the basic epidemiological characteristics of the interaction. This framework is also used to investigate the effect of disease on the spatial spread of the invader. Our results show an interesting phenomenon where a wave of disease spreads through the landscape ahead of the wave of replacement.


Disease models Spatial Multi-species Ecological invasions Squirrelpox Travelling waves 



We are grateful for the helpful advice of the editorial board member Mark Lewis and two anonymous referees on the manuscript. Sally S Bell is supported by an Engineering and Physical Sciences Research Council studentship award.


  1. Aliabadi BW, Juliano SA (2002) Escape from gregarine parasites affects the competitive interactions of an invasive mosquito. Biol Invasions 4:283–297CrossRefPubMedGoogle Scholar
  2. Anderson RC (1972) The ecological relationships of meningeal worm and native cervids in North America. J Wildl Dis 8:304–310PubMedGoogle Scholar
  3. Begon M, Bowers RG, Kadianakis N, Hodgkinson DE (1992) Disease and community structure: the importance of host-regulation in a host–host–pathogen model. Am Nat 139:1131–1150CrossRefGoogle Scholar
  4. Bergerud AT, Mercer WE (1989) Caribou introductions in Eastern North America. Wildl Soc Bull 17:111–120Google Scholar
  5. Boots M, Norman R (2000) Sublethal infection and the population dynamics of host–microparasite interactions. J Anim Ecol 69:517–524CrossRefGoogle Scholar
  6. Bowers RG, Turner J (1997) Community structure and the interplay between interspecific infection and competition. J Theor Biol 187:95–109PubMedCrossRefGoogle Scholar
  7. Bubb DH, Thom TJ, Lucas MC (2004) Movement and dispersal of the invasive signal crayfish Pacifastacus leniusculus in upland rivers. Freshw Biol 49:357–368CrossRefGoogle Scholar
  8. Cerenius L, Bangyeekhun E, Keyser P, Soderhall I, Soderhall K (2003) Host prophenoloxidase expression in freshwater crayfish is linked to increased resistance to the crayfish plague fungus, Aphanomyces astaci. Cell Microbiol 5:353–357PubMedCrossRefGoogle Scholar
  9. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  10. De Vries G, Hillen T, Lewis M, Muller J, Schoenfisch B (2006) A course in mathematical biology: quantitative modelling with mathematical and computational methods. Society for Industrial and Applied Mathematics, PhiladelphiaGoogle Scholar
  11. Dobson AP, Hudson PJ (1986) Parasites, disease and the structure of ecological communities. Trends Ecol Evol 1:11–15CrossRefGoogle Scholar
  12. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139PubMedCrossRefGoogle Scholar
  13. Greenman JV, Hudson PJ (1997) Infected coexistence instability with and without density dependent regulation. J Theor Biol 185:345–356CrossRefGoogle Scholar
  14. Hails RS, Crawley MJ (1991) The population dynamics of an alien insect: Andricus quercuscalicis (Hymenoptera: Cynipidae). J Anim Ecol 60:545–561CrossRefGoogle Scholar
  15. Hilker FM, Lewis MA, Seno H, Langlais M, Malchow H (2005) Pathogens can slow down or reverse invasion fronts of their hosts. Biol Invasions 7:817–832CrossRefGoogle Scholar
  16. Holdich D (2003) Ecology of the white-clawed crayfish. Conserving Nature 2000 Rivers Ecology Series No. 1. English Nature, PeterboroughGoogle Scholar
  17. Holt RD, Pickering J (1985) Infectious disease and species coexistence: a model of Lotka-Volterra form. Am Nat 126:196–211CrossRefGoogle Scholar
  18. Hoogendoorn M, Heimpel GE (2002) Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biol Control 25:224–230CrossRefGoogle Scholar
  19. Hosono Y (1998) The minimal speed of traveling fronts for a diffusive Lotka-Volterra competition model. Bull Math Biol 60:435–448CrossRefGoogle Scholar
  20. Hudson PJ, Greenman J (1998) Competition mediated by parasites: biological and theoretical progress. Trends Ecol Evol 13:387–390CrossRefGoogle Scholar
  21. Hudson PJ, Dobson AP, Newborn D (1998) Prevention of population cycles by parasite removal. Science 282:2256–2258PubMedCrossRefGoogle Scholar
  22. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204PubMedCrossRefGoogle Scholar
  23. Kot M (2001) Elements of mathematical ecology, vol. l. Cambridge University Press, CambridgeGoogle Scholar
  24. Lewis MA, Li B, Weinberger HF (2002) Spreading speed and linear determinacy for two-species competition models. J Math Biol 45:219–233PubMedCrossRefGoogle Scholar
  25. Li B, Weinberger HF, Lewis MA (2005) Spreading speeds as slowest wave speeds for cooperative systems. Math Biosci 196:82–98PubMedCrossRefGoogle Scholar
  26. Lloyd HG (1983) Past and present distribution of red and grey squirrels. Mammal Rev 13:69–80CrossRefGoogle Scholar
  27. Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137CrossRefGoogle Scholar
  28. Malchow H, Petrovskii S, Venturino E (2008) Spatiotemporal patterns in ecology and epidemiology: theory, models, simulations. Chapman & Hall/CRC Press, Boca RatonGoogle Scholar
  29. Middleton AD (1930) Ecology of the American gray squirrel in the British Isles. Proc Zoolog Soc Lond 2:809–843Google Scholar
  30. Murray JD (2002) Mathematical biology I: an introduction, 3rd edn. Springer, BerlinGoogle Scholar
  31. Oates DW, Sterner MC, Boyd E (2000) Meningeal worm in deer from western Nebraska. J Wildl Dis 36:370–373PubMedGoogle Scholar
  32. Okubo A, Maini PK, Williamson MH, Murray JD (1989) On the spatial spread of the grey squirrel in Britain. Proc R Soc Lond B Biol Sci 238:113–125PubMedCrossRefGoogle Scholar
  33. Petrovskii SV, Li B (2006) Exactly solvable models of biological invasion. Chapman & Hall/CRC, LondonGoogle Scholar
  34. Petrovskii SV, Malchow H, Hilker FM, Venturino E (2005) Patterns of patchy spread in deterministic and stochastic models of biological invasion and biological control. Biol Invasions 7:771–793CrossRefGoogle Scholar
  35. Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, Wong E, Russel L, Zern J, Aquino T, Tsomondo T (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20CrossRefGoogle Scholar
  36. Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390PubMedCrossRefGoogle Scholar
  37. Pybus MJ, Samuel WM, Welch DA, Wilke CJ (1990) Parelaphostrongylus andersoni (Nematoda: Protostrongylidae) in white-tailed deer from Michigan. J Wildl Dis 26:535–537PubMedGoogle Scholar
  38. Reynolds JC (1985) Details of the geographic replacement of the red squirrel (Sciurus vulgaris) by the grey squirrel (Sciurus carolinensis) in Eastern England. J Anim Ecol 54:149–162CrossRefGoogle Scholar
  39. Rohde K (1984) Ecology of marine parasites. Helgol Mar Res 37:5–33Google Scholar
  40. Rushton SP, Lurz PWW, Gurnell J, Fuller R (2000) Modelling the spatial dynamics of parapoxvirus disease in red and grey squirrels: a possible cause of the decline in the red squirrel in the UK? J Appl Ecol 37:997–1012CrossRefGoogle Scholar
  41. Rushton SP, Lurz PWW, Gurnell J, Nettleton P, Bruemmer C, Shirley MDF, Sainsbury AW (2006) Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain. Epidemiol Infect 134:521–533PubMedCrossRefGoogle Scholar
  42. Saenz RA, Hethcote HW (2006) Competing species models with an infectious disease. Math Biosci Eng 3:219–235Google Scholar
  43. Sala OE, Chapin FSL, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, HuberSanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge HA, Oesterheld M, LeRoy Poff N, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774PubMedCrossRefGoogle Scholar
  44. Tompkins DM, Sainsbury AW, Nettleton P, Buxton D, Gurnell J (2002) Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines. Proc R Soc Lond B Biol Sci 269:529–533CrossRefGoogle Scholar
  45. Tompkins DM, White AR, Boots M (2003) Ecological replacement of native red squirrels by invasive greys driven by disease. Ecol Lett 6:189–196CrossRefGoogle Scholar
  46. Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478Google Scholar
  47. Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16Google Scholar
  48. Weinberger HF, Lewis MA, Li B (2002) Analysis of linear determinacy for spread in cooperative models. J Math Biol 45:183–218PubMedCrossRefGoogle Scholar
  49. Weinberger HF, Lewis MA, Li B (2007) Anomalous spreading speeds of cooperative recursion systems. J Math Biol 55:207–222PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Sally S. Bell
    • 1
  • Andrew White
    • 1
  • Jonathan A. Sherratt
    • 1
  • Mike Boots
    • 2
  1. 1.Department of Mathematics and the Maxwell Institute for Mathematical SciencesHeriot-Watt UniversityEdinburghUK
  2. 2.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK

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