Disease effects on reproduction can cause population cycles in seasonal environments

Journal of Animal Ecology

Volumn 77, Issue 2, 2008, Pages 378-389

  Smith, Matthew J ^a,c   White, Andrew ^a   Sherratt, Jonathan A ^a   Telfer, Sandra ^b   Begon, Michael ^b   Lambin, Xavier ^c  

^a HERIOT WATT UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Cowpox virus; Density dependence; Disease model; Population dynamics; Seasonal forcing

Indexed keywords

DENSITY DEPENDENCE; DISEASE; FECUNDITY; HOST-PARASITE INTERACTION; PARASITE; POPULATION CYCLE; POPULATION DYNAMICS; REPRODUCTION; VIRUS;

ANIMAL; ARTICLE; ARVICOLINAE; BIOLOGICAL MODEL; ENVIRONMENT; FEMALE; HOST PARASITE INTERACTION; MALE; PARASITOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; POPULATION DENSITY; POPULATION DYNAMICS; POPULATION GROWTH; REPRODUCTION; RODENT; RODENT DISEASE; SEASON;

ANIMALS; ARVICOLINAE; ENVIRONMENT; FEMALE; HOST-PARASITE INTERACTIONS; MALE; MODELS, BIOLOGICAL; POPULATION DENSITY; POPULATION DYNAMICS; POPULATION GROWTH; REPRODUCTION; RODENT DISEASES; RODENTIA; SEASONS;

ENGLAND; EURASIA; EUROPE; KIELDER FOREST; NORTHUMBERLAND; UNITED KINGDOM; WESTERN EUROPE;

COWPOX VIRUS; MICROTUS AGRESTIS; MURIDAE; RODENTIA;

EID: 38849133690     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2007.01328.x     Document Type: Article

References (68)

1. Adams, V.J., Markus, M.B., Kwitshana, Z.L., Dhansay, M.A., van der Merwe, L., Walzl, G. Fincham, J.E. (2006) Recall of intestinal helminthiasis by HIV-infected South Africans and avoidance of possible misinterpretation of egg excretion in worm/HIV co-infection analyses. BMC Infectious Diseases, 6, 88.
2. Albon, S.D., Stien, A., Irvine, R.J., Langvatn, R., Ropstad, E. Halvorsen, O. (2002) The role of parasites in the dynamics of a reindeer population. Proceedings of the Royal Society of London, Series B, Biological Sciences, 269, 1625 1632.
3. Alonso, D., McKane, A.J. Pascual, M. (2007) Stochastic amplification in epidemics. Journal of the Royal Society Interface, 4, 575 582.
4. Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M. Rohani, P. (2006) Seasonality and the dynamics of infectious diseases. Ecology Letters, 9, 467 484.
5. Anderson, R.M. May, R.M. (1981) The population-dynamics of micro-parasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences, 291, 451 524.
6. Barlow, N.D. Kean, J.M. (1998) Simple models for the impact of rabbit calicivirus disease (RCD) on Australasian rabbits. Ecological Modelling, 109, 225 241.
7. Bierman, S.M., Fairbairn, J.P., Petty, S.J., Elston, D.A., Tidhar, D. Lambin, X. (2006) Changes over time in the spatiotemporal dynamics of cyclic populations of field voles (Microtus agrestis L.). American Naturalist, 167, 583 590.
8. Birtles, R.J., Hazel, S.M., Bennett, M., Bown, K., Raoult, D. Begon, M. (2001) Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiology and Infection, 126, 323 329.
9. Boots, M. Norman, R. (2000) Sublethal infection and the population dynamics of host-microparasite interactions. Journal of Animal Ecology, 69, 517 524.
10. Bown, K.J., Begon, M., Bennett, M., Birtles, R.J., Burthe, S., Lambin, X., Telfer, S., Woldehiwet, Z. Ogden, N.H. (2006) Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? Vector-Borne and Zoonotic Diseases, 6, 404 410.
11. Bown, K.J., Begon, M., Bennett, M., Woldehiwet, Z. Ogden, N.H. (2003) Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases, 9, 63 70.
12. Bown, K.J., Bennett, M. Begon, M. (2004) Flea-borne Bartonelia grahamii and Bartonelia taylorii in bank voles. Emerging Infectious Diseases, 10, 684 687.
13. Bradley, J.E. Jackson, J.A. (2004) Immunity, immunoregulation and the ecology of trichuriasis and ascariasis. Parasite Immunology, 26, 429 441.
14. Burthe, S., Telfer, S., Begon, M., Bennett, M., Smith, A. Lambin, X. (in press) Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival. Journal of Animal Ecology, in press.
15. Burthe, S., Telfer, S., Lambin, X., Bennett, M., Carslake, D., Smith, A. Begon, M. (2006) Cowpox virus infection in natural field vole Microtus agrestis populations: delayed density dependence and individual risk. Journal of Animal Ecology, 75, 1416 1425.
16. Cavanagh, R.D., Lambin, X., Ergon, T., Bennett, M., Graham, I.M., van Soolingen, D. Begon, M. (2004) Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti). Proceedings of the Royal Society of London, Series B, Biological Sciences, 271, 859 867.
17. Chitty, D. (1954) Tuberculosis among wild voles: with a discussion of other pathological conditions among certain mammals and birds. Ecology, 35, 227 237.
18. Cox, F.E.G. (2001) Concomitant infections, parasites and immune responses. Parasitology, 122, S23 S38.
19. Daszak, P., Cunningham, A.A. Hyatt, A.D. (2000) Wildlife ecology - emerging infectious diseases of wildlife - threats to biodiversity and human health. Science, 287, 443 449.
20. Dobson, A.P. Hudson, P.J. (1992) Regulation and stability of a free-living host-parasite system - Trichostrongylus tenuis in red grouse. 2. Population models. Journal of Animal Ecology, 61, 487 498.
21. Druilhe, P., Tall, A. Sokhna, C. (2005) Worms can worsen malaria: towards a new means to roll back malaria? Trends in Parasitology, 21, 359 362.
22. Dushoff, J., Plotkin, J.B., Levin, S.A. Earn, D.J.D. (2004) Dynamical resonance can account for seasonality of influenza epidemics. Proceedings of the National Academy of Sciences USA, 101, 16915 16916.
23. Elton, C., Davis, D.H.S. Findlay, G.M. (1935) An epidemic among voles (Microtus agrestis) on the Scottish border in the spring of 1934. Journal of Animal Ecology, 4, 277 288.
24. Ergon, T. (2003) Fluctuating Life-History Traits in Overwintering Field Voles (Microtus agrestis). University of Oslo, Oslo.
25. Ergon, T., MacKinnon, J.L., Stenseth, N.C., Boonstra, R. Lambin, X. (2001) Mechanisms for delayed density-dependent reproductive traits in field voles, Microtus agrestis: the importance of inherited environmental effects. Oikos, 95, 185 197.
26. Fichet-Calvet, E., Giraudoux, P., Quere, J.P., Ashford, R.W. Delattre, P. (2003) Is the prevalence of Taenia taeniaeformis in Microtus arvalis dependent on population density? Journal of Parasitology, 89, 1147 1152.
27. Fichet-Calvet, E., Kia, E.B., Giraudoux, P., Quere, J.P., Delattre, P. Ashford, R.W. (2004) Frenkelia parasites in a small mammal community. Dynamics of infection and effect on the host parasite. Journal de la Societe Francaise de Parasitologie, 11, 301 310.
28. Findlay, G.M. Middleton, A.D. (1934) Epidemic disease among voles (Microtus) with special reference to Toxoplasma. Journal of Animal Ecology, 3, 150 160.
29. Greenman, J.V. Benton, T.G. (2003) The amplification of environmental noise in population models: causes and consequences. American Naturalist, 161, 225 239.
30. Greenman, J.V. Benton, T.G. (2005) The frequency spectrum of structured discrete time population models: its properties and their ecological implications. Oikos, 110, 369 389.
31. Greenman, J., Kamo, M. Boots, M. (2004) External forcing of ecological and epidemiological systems: a resonance approach. Physica D - Nonlinear Phenomena, 190, 136 151.
32. Hansen, T.F., Stenseth, N.C. Henttonen, H. (1999) Multiannual vole cycles and population regulation during long winters: an analysis of seasonal density dependence. American Naturalist, 154, 129 139.
33. Harvell, C.D., Mitchell, C.E., Ward, J.R., Altizer, S., Dobson, A.P., Ostfeld, R.S. Samuel, M.D. (2002) Ecology - climate warming and disease risks for terrestrial and marine biota. Science, 296, 2158 2162.
34. He, D. Earn, D.J.D. (2007) Epidemiological effects of seasonal oscillations in birth rates. Theoretical Population Biology, 72, 274 291.
35. Hornfeldt, B. (2004) Long-term decline in numbers of cyclic voles in boreal Sweden: analysis and presentation of hypotheses. Oikos, 107, 376 392.
36. Hosseini, P.R., Dhondt, A.A. Dobson, A. (2004) Seasonality and wildlife disease: how seasonal birth, aggregation and variation in immunity affect the dynamics of Mycoplasma gallisepticum in house finches. Proceedings of the Royal Society of London, Series B, Biological Sciences, 271, 2569 2577.
37. Hudson, P.J., Dobson, A.P. Newborn, D. (1998) Prevention of population cycles by parasite removal. Science, 282, 2256 2258.
38. Ireland, J.M., Mestel, B.D. Norman, R.A. (2007) The effect of seasonal host birth rates on disease persistence. Mathematical Biosciences, 206, 31 45.
39. Ireland, J.M., Norman, R.A. Greenman, J.V. (2004) The effect of seasonal host birth rates on population dynamics: the importance of resonance. Journal of Theoretical Biology, 231, 229 238.
40. Jolles, A.E., Etienne, R.S. Olff, H. (2006) Independent and competing disease risks: implications for host populations in variable environments. American Naturalist, 167, 745 757.
41. Keeling, M.J. Grenfell, B.T. (2002) Understanding the persistence of measles: reconciling theory, simulation and observation. Proceedings of the Royal Society of London, Series B, Biological Sciences, 269, 335 343.
42. Keeling, M.J., Rohani, P. Grenfell, B.T. (2001) Seasonally forced disease dynamics explored as switching between attractors. Physica D - Nonlinear Phenomena, 148, 317 335.
43. Koelle, K., Pascual, M. Yunus, M. (2005) Pathogen adaptation to seasonal forcing and climate change. Proceedings of the Royal Society, Series B, Biological Sciences, 272, 971 977.
44. Lambin, X., Krebs, C.J., Moss, R., Stenseth, N.C. Yoccoz, N.G. (1999) Population cycles and parasitism. Science, 286, 2425a.
45. Lambin, X. Yoccoz, N.G. (2001) Adaptive precocial reproduction in voles: reproductive costs and multivoltine life-history strategies in seasonal environments. Journal of Animal Ecology, 70, 191 200.
46. McKane, A.J. Newman, T.J. (2004) Stochastic models in population biology and their deterministic analogs. Physical Review E, 70, 1 19.
47. Niklasson, B., Nyholm, E., Feinstein, R.E., Samsioe, A. Hornfeldt, B. (2006) Diabetes and myocarditis in voles and lemmings at cyclic peak densities - induced by Ljungan virus? Oecologia, 150, 1 7.
48. Noyes, H.A., Ambrose, P., Barker, F., Begon, M., Bennet, M., Bown, K.J. Kemp, S.J. (2002) Host specificity of Trypanosoma (Herpetosoma) species: evidence that bank voles (Clethrionomys glareolus) carry only one T. (H.) evotomys 18S rRNA genotype but wood mice (Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology, 124, 185 190.
49. Olsson, G.E., White, N., Ahlm, C., Elgh, F., Verlemyr, A.C., Juto, P. Palo, R.T. (2002) Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerging Infectious Diseases, 8, 924 929.
50. Pedersen, A.B. Fenton, A. (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution, 22, 133 139.
51. Redpath, S.M., Mougeot, F., Leckie, F.M., Elston, D.A. Hudson, P.J. (2006) Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecology Letters, 9, 410 418.
52. Roberts, M.G., Dobson, A.P., Arneberg, P., de Leo, G.A., Kerecek, R.C., Manfredi, M.T., Lanfranchi, P. Zaffaroni, E. (2002) Parasite community ecology and biodiversity. The Ecology of Wildlife Diseases (eds P.J. Hudson, A.P. Rizzoli, B.T. Grenfell, H. Heesterbeek A.P. Dobson pp. 63 82. Oxford University Press, Oxford.
53. Sachs, J.D. Hotez, P.J. (2006) Fighting tropical diseases. Science, 311, 1521 1521.
54. Singleton, G.R., Brown, P.R., Pech, R.P., Jacob, J., Mutze, G.J. Krebs, C.J. (2005) One hundred years of eruptions of house mice in Australia - a natural biological curio. Biological Journal of the Linnean Society, 84, 617 627.
55. Smith, A., Telfer, S., Burthe, S., Bennett, M. Begon, M. (2006a) A role for vector-independent transmission in rodent trypanosome infection? International Journal for Parasitology, 36, 1359 1366.
56. Smith, M.J., White, A., Lambin, X., Sherratt, J.A. Begon, M. (2006b) Delayed density-dependent season length alone can lead to rodent population cycles. American Naturalist, 167, 695 704.
57. Soveri, T., Henttonen, H., Rudback, E., Schildt, R., Tanskanen, R., Husu-Kallio, J., Haukisalmi, V., Sukura, A. Laakkonen, J. (2000) Disease patterns in field and bank vole populations during a cyclic decline in central Finland. Comparative Immunology, Microbiology and Infectious Diseases, 23, 73 89.
58. Stenseth, N.C. (1999) Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos, 87, 427 461.
59. Stenseth, N.C., Samia, N.I., Viljugrein, H., Kausrud, K.L., Begon, M., Davis, S., Leirs, H., Dubyanskiy, V.M., Esper, J., Ageyev, V.S., Klassovskiy, N.L., Pole, S.B. Chan, K.S. (2006) Plague dynamics are driven by climate variation. Proceedings of the National Academy of Sciences USA, 103, 13110 13115.
60. Stenseth, N.C., Viljugrein, H., Saitoh, T., Hansen, T.F., Kittilsen, M.O., Bolviken, E. Glockner, F. (2003) Seasonality, density dependence, and population cycles in Hokkaido voles. Proceedings of the National Academy of Sciences USA, 100, 11478 11483.
61. Stone, L., Olinky, R. Huppert, A. (2007) Seasonal dynamics of recurrent epidemics. Nature, 446, 533 536.
62. Telfer, S., Begon, M., Bennett, M., Bown, K.J., Burthe, S., Lambin, X., Telford, G. Birtles, R. (2007) Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics. Parasitology, 134, 413 425.
63. Telfer, S., Bennett, M., Bown, K., Carslake, D., Cavanagh, R., Hazel, S., Jones, T. Begon, M. (2005) Infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents. Oikos, 109, 317 322.
64. Telfer, S., Bennett, M., Bown, K., Cavanagh, R., Crespin, L., Hazel, S., Jones, T. Begon, M. (2002) The effects of cowpox virus on survival in natural rodent populations: increases and decreases. Journal of Animal Ecology, 71, 558 568.
65. Tompkins, D.M. Begon, M. (1999) Parasites can regulate wildlife populations. Parasitology Today, 15, 311 313.
66. Tompkins, D.M., Dobson, A.P., Arneberg, P., Begon, M.E., Cattadori, I.M., Greenman, J.V., Heesterbeek, J.A.P., Hudson, P.J., Newborn, D., Pugliese, A., Rizzoli, A.P., Rosa, R., Rosso, F. Wilson, K. (2002) Parasites and host population dynamics. The Ecology of Wildlife Diseases (eds P. J. Hudson, A.P. Rizzoli, B.T. Grenfell, H. Heesterbeek A.P. Dobson), pp. 45 62. Oxford University Press, Oxford.
67. Turchin, P. (2003) Complex Population Dynamics: a Theoretical/Empirical Synthesis, 1st edn. Princeton University Press, Princeton and Oxford.
68. White, A., Bowers, R.G. Begon, M. (1996) Host-pathogen cycles in self-regulated forest insect systems: resolving conflicting predictions. American Naturalist, 148, 220 225.