Skip to main content
SpringerLink
Log in

Landscape structure influences continental distribution of hantavirus in deer mice

  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

We hypothesized that landscape structure affects movement of individuals through the landscape, which affects the rate and pattern of disease transmission. Based on this hypothesis, we predicted a relationship between landscape structure and disease incidence in spatially structured populations. We tested this prediction for hantavirus incidence in deer mice (Penomysens moniculatus), using a novel index of habitat fragmentation for transect data. A series of four stepwise logistic regression analyses were conducted on serological and ecological data from 2837 mice from 101 sites across Canada. The significant variables, ranked in decreasing order of size of their effect on virus incidence were: human buildings, landscape composition (amount of deer mouse habitat in the 1-km radius landscape surrounding each site), landscape configuration (fragmentation of deer mouse habitat in the 1-km radius landscape surrounding each site), mean annual temperature, and seasonal variation. Our results suggest that epidemiological models should consider not only the demographic structure of the host population, but its spatial structure as well, as inferred from landscape structure. Landscape structure can have a greater effect on the pattern of distribution of a virus in its host population than other ecological variables such as climate and seasonal change. The usefulness of landscape data in epidemiological models depends on the use of the appropriate spatial scale, which can be determined empirically. Epidemiological models with a spatially structured host population can benefit from the explicit consideration of landscape structure.

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

Similar content being viewed by others

References

  • Andreassen, H.P., Ims, R.A. and Stenseth, N.D. 1996. Discontinuous habitat corridors: Effects on male root vole movements. J. Appl. Ecol. 33: 555–560.

    Google Scholar 

  • Ashton, W.D. 1972. The logit transformation, with special reference to its uses in bioassay. Griffin's statistical monographs & courses, no. 32. Charles Griffin and Company, London, UK.

    Google Scholar 

  • Baars, M.A. 1979. Patterns of movement of radioactive carabid beetles. Oecologia 44: 125–140.

    Google Scholar 

  • Baker, R.H. 1968. Habitats and distribution. In Biology of Peromyscus (RODENTIA). Edited by J.A. King Special publication no. 2. 593 p. The American Society of Mammalogists.

  • Barry, R.E., Botje, M.A. and Grantham, L.B. 1984. Vertical stratification of Peromyscus leucopus and P. maniculatus in southwestern Virginia. J. Mammal. 65: 145–148.

    Google Scholar 

  • Blair, W.F. 1950. Ecological factors in speciation of Peromyscus. Evolution 4: 253–275.

    Google Scholar 

  • Bowers, M.A. and Dooley, J.L. 1999. A controlled, hierarchical study of habitat fragmentation responses at the individual, patch, and landscape scale. Landscape Ecol. 14: 381–389.

    Google Scholar 

  • Bowers, M.A., Gregario, K., Brame, C.J., Matter, S.F. and Dooley, J.L. 1996. Use of space and habitats by meadow voles at the home-range, patch and landscape scales. Oecologia 105: 107–115.

    Google Scholar 

  • Buckner, C.A. and Shure, D.J. 1985. The response of Peromyscus to forest opening size in the southern Appalachian Mountains. J. Mammal. 66: 299–307.

    Google Scholar 

  • Carleton, M.D. 1989. Systematics and evolution. In Advances in the study of Peromyscus (RODENTIA). Edited by G.L. Kirkland and J.N. Layne. 366 p. Texas Tech University Press. Lubbock, TX, USA.

    Google Scholar 

  • Centres for Disease Control. 1994. Enzyme immunoassay for detection of IgG antibody to Hantavirus in rodents.

  • Charrier, S., Petit, S. and Burel, F. 1997. Movements of Abax parallelepipedus (Coleoptera, Carabidae) in woody habitats of a hedgerow network landscape: a radio-tracing study. Agriculture, Ecosystems and Environment 61: 133–144.

    Google Scholar 

  • Childs, J.E., Ksiazek, T.G., Spiropoulou, C.F., Krebs, J.W., Morzunov, S., Maupin, G.O., Gage, K.L., Rollin, P.E., Sarisky, J., Enscore, R.E., Frey, J.K., Peters, C.J. and Nichol, S.T. 1994. Serologic and Genetic Identification of Peromyscus maniculatus as the Primary Rodent Reservoir for a New Hantavirus in the Southwestern United States. J. Infec. Diseas. 169: 1271–1280.

    Google Scholar 

  • Chizhikov V.E., Hörling, J., Lundkvist, Å, Jonsson, M., Ivanov, L.I., Niklasson, B., Tkachenko, E.A., Peters, C.J. and Nichol, S.T. 1996. Genetic and serologic analysis of hantaviruses isolated from Microtus fortis trapped in far eastern Russia. American Society for Virology 15th annual meeting, July 13–17, 1996, London, Ontario, Canada.

  • Collins, R.J. and Barrett, G.W. 1997. Effects of habitat fragmentation on meadow vole (Microtus pennsylvanicus) population dynamics in experiment landscape patches. Landscape Ecol. 12: 63–76.

    Google Scholar 

  • Diaz, M, T. Santos and Telleria, J.L. 1999. Effects of forest fragmentation on the winter body condition and population parameters of a habitat generalist, the wood mouse Apodemus sylvaticus: a test of hypotheses. Acta Oecologica 20: 39–49.

    Google Scholar 

  • Diffendorfer J.E., Gaines, M.S. and Holt, R.D. 1995. Habitat fragmentation and movements of three small mammals (Sigmodon, Microtus, and Peromyscus). Ecology 76: 827–839.

    Google Scholar 

  • Dooley, J.L. and Bowers, MA 1998. Demographic responses to habitat fragmentation – experimental tests at the landscape and patch scale. Ecology 79: 969–980.

    Google Scholar 

  • Dunning, J.B., Danielson, J.B. and Pulliam, H.R. 1992. Ecological processes that affect populations in complex landscapes. Oikos 65: 169–175.

    Google Scholar 

  • Ecoregions Working Group. 1989. Ecoclimatic regions of Canada, first approximation. Ecological Land Classification Series No.23. Environment Canada.

  • Fahrig, L. 1997. Relative effects of habitat loss and fragmentation on species extinction. J. Wildl. Manage. 61: 603–610.

    Google Scholar 

  • Fahrig, L. and Merriam, G. 1994. Conservation of fragmented populations. Cons. Biol. 8: 50–59.

    Google Scholar 

  • Godfryd, A. and Hansell, R.I.C. 1986. Prediction of birdcommunity metrics in urban woodlots. In Wildlife 2000: modelling habitat relationships of terrestrial vertebrates. Edited by J. Verner, M.L. Morrison and C.J. Ralph. pp 321–326. University of Wisconsin Press, Madison, WI, USA.

    Google Scholar 

  • Gustafson, E.J. and Parker, G.R. 1994. Using an index of habitat patch proximity for landscape design. Landscape and Urban Planning 29: 117–130.

    Google Scholar 

  • Hansson, L. 1991. Dispersal and connectivity in metapopulations. Biol. J. Linnean Soc. 42: 89–103.

    Google Scholar 

  • Henein, K. and Merriam, G. 1990. The elements of connectivity where corridor quality is variable. Landscape Ecol. 4: 157–170.

    Google Scholar 

  • Hooper, E.T. 1968. Classification. In Biology of Peromyscus (RODENTIA). Special publication no. 2. 593 p. Edited by J.A. King. The American Society of Mammalogists.

  • Kaufman D.W. and Kaufman, G.A. 1989. Population biology. In Advances in the study of Peromyscus (RODENTIA). 366 p. Edited by G.L. Kirkland and J.N. Layne. Texas Tech University Press. Lubbock, TX, USA.

    Google Scholar 

  • Kitron, U. 1998. Landscape ecology and epidemiology of vectorborne diseases – tools for spatial-analysis. J. Med. Entomol. 35: 435–445.

    Google Scholar 

  • Kremsater, L. and Bunnell, F.L. 1999. Edge effects: theory, evidence and implications to management of western North American forests. In Forest fragmentation: wildlife and management implications pp. 117–153. Edited by J.A. Rochelle, L.A. Lehmann and J. Wisniewski. Brill, Boston, MA, USA.

    Google Scholar 

  • Lawton, J.H., Nee, S., Letcher, A.J. and Harvey, P.H. 1994. Animal distributions: patterns and processes. In Large-scale ecology and conservation biology pp. 41–59. Edited by P.J. Edwards, R.M. May and N.R. Webb. Oxford Scientific, London, UK.

    Google Scholar 

  • LeDuc, J. 1987. Epidemiology of hantaan and related viruses. Laboratory Animal Science 37: 413–418.

    Google Scholar 

  • Lee H.W. and van der Groen, G. 1989. Hemorrhagic fever with renal syndrome. Progr. Med. Virol. 36: 62–102.

    Google Scholar 

  • Manson, R.H., Ostfeld, R.S. and Canham, C.D. 1999. Responses of a small mammal community to heterogeneity along forest-old-field edges. Landscape Ecol. 14: 355–367.

    Google Scholar 

  • Matter, S.F. 1996. Interpatch movement of the red milkweed beetle, Tetraopes tetraophthalmus: Individual responses to patch size and isolation. Oecologia 105: 447–453.

    Google Scholar 

  • Morris, D.W. 1992. Scales and costs of habitat selection in heterogeneous landscapes. Evol. Ecol. 6: 412–432.

    Google Scholar 

  • Morzunov, S.P., St Jeor, S.C., Rowe, J., Artsob, H., Ksiazek, T.G., Peters, C.J. and Nichol, S.T. 1996. North American Peromyscus-borne hantaviruses: co-evolution with specific rodent hosts and geographic domination. American Society for Virology 15th annual meeting, July 13–17, 1996, London, Ontario, Canada.

  • Nee, S. 1994. How populations persist. Nature 367: 123–124.

    Google Scholar 

  • Nichol, S.T., Spiropoulou, C.F., Morzunov, S., Rollin, P.W., Ksiazek, T.G., Feldmann, H., Sanchez, A., Childs, J., Zaki, S. and Peters, C.J. 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262: 914–917.

    Google Scholar 

  • O'Neill R.V., Krummel, J.R., Gardner, R.H., Sugihara, G., Jackson, B., DeAngelis, D.L., Milne, B.T., Turner, M.G., Zygmunt, B., Christensen, S.W., Dale, V.H. and Graham, R.L. 1988. Indices of landscape pattern. Landscape Ecol. 1: 153–162.

    Google Scholar 

  • Ostfeld, R.S., Cepeda, O.M., Hazler, K.R. and Miller, M.D. 1995. Ecology of lyme-disease – habitat associations of ticks (Ixodes scapularis) in a rural landscape. Ecol. Appl. 5: 353–361.

    Google Scholar 

  • Parren S.G. and Capen, D.R. 1985. Local distribution and coexistence of two species of Peromyscus in Vermont. J. Mammal. 66: 36–44.

    Google Scholar 

  • Pielou E.C. 1977. Mathematical ecology. 385 p. Wiley-Interscience Publications, New York, NY, USA.

    Google Scholar 

  • Pither, J. and Taylor, P.D. 1998. An experimental assessment of landscape connectivity. Oikos 83: 166–174.

    Google Scholar 

  • Rijnsdorp, A.D. 1980. Pattern of movement in and dispersal from a Dutch forest of Carabus problematicus Hbst. (Coleoptera, Carabidae). Oecologia 45: 274–281.

    Google Scholar 

  • Rosenberg, K.V. and Raphael, M.G. 1986. Effects of forest fragmentation on vertebrates in Douglas-fir forests. In Wildlife 2000: modelling habitat relationships of terrestrial vertebrates. pp. 263–272. Edited by J. Verner, M.L. Morrison and C.J. Ralph. University of Wisconsin Press, Madison, WI, USA.

    Google Scholar 

  • Rowe, J.E., St Jeor, S.C., Riolo, J., Otteson, E.W., Monroe, M.C., Henderson, W.W., Ksiazek, T.G., Rollin, P.E. and Nichol, S.T. 1995. Coexistence of several novel Hantaviruses in rodents indigenous to North America. Virology 213: 122–130.

    Google Scholar 

  • SAS Institute. 1996. SAS user's guide: statistics, Version 6.12. SAS institute Inc., Cary, NC, USA.

    Google Scholar 

  • Sekgororoane, G.B. 1995. Relative abundance, richness, and diversity of small mammals at induced forest edges. Can. J. Zool. 73: 1432–1437.

    Google Scholar 

  • Stah, C.D. 1980. Vertical nesting distribution of two species of Peromyscus under experimental conditions. J. Mammal. 61: 141–143.

    Google Scholar 

  • Stickel, L.F. 1968. Home range and travels. In Biology of Peromyscus (RODENTIA). Edited by J.A. King. Special publication no. 2. 593 p. The American Society of Mammalogists.

  • Taylor. P.D., Fahrig, L., Henein, K. and Merriam, G. 1993. Connectivity is a vital element of landscape structure. Oikos 68: 571–573.

    Google Scholar 

  • Taylor, P.D. and Merriam, G. 1996. Habitat fragmentation and parasitism of a forest damselfly. Landscape Ecol. 11: 181–189.

    Google Scholar 

  • Teferi, T. and Millar, J.S. 1993. Long distance homing by the deer mouse, Peromyscus maniculatus. Can. Field Nat. 107: 109–111.

    Google Scholar 

  • Terman, C.R. 1968. Population dynamics. In Biology of Peromyscus (RODENTIA). Edited by J.A. King. Special publication no. 2. 593 p. The American Society of Mammalogists.

  • Tischendorf, L. and Fahrig, L. 2000a. On the usage and measurement of landscape connectivity. Oikos 90: 7–19

    Google Scholar 

  • Tischendorf, L. and Fahrig, L. 2000b. How should we measure landscape connectivity? Landsc Ecol 15: 633–641.

    Google Scholar 

  • Wallin, H. and Ekbom, B.D. 1988. Movements of carabid beetles (Coleoptera Carabidae) inhabiting cereal fields: A field tracing study. Oecologia 77: 39–43.

    Google Scholar 

  • Wecker, S.C. 1963. The role of early experience in habitat selection by the prairie deer mouse, Peromyscus maniculatus bairdi. Ecol. Monographs 33: 307–325.

    Google Scholar 

  • Wolff, J.O. 1989. Social Behaviour. In Advances in the study of Peromyscus (RODENTIA). Edited by Kirkland G.L. Jr. and J.N. Layne. Texas Tech University Press. Lubbock, TX, USA.

    Google Scholar 

  • Wolff, J.O. and Hurlbutt, B. 1982. Day refuges of Peromyscus leucopus and Peromyscus maniculatus. J. Mammal. 63: 666–668.

    Google Scholar 

  • Wolff, J.O., Schauber, E.M. and Edge, W.D. 1997. Effects of habitat loss and fragmentation on the behaviour and demography of gray-tailed voles. Cons. Biol. 11: 945–956.

    Google Scholar 

  • Yahner, R.H. 1992. Dynamics of a small mammal community in a fragmented forest. Am. Midl. Nat. 127: 381–391.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Landscape Ecology Laboratory, Ottawa-Carleton Institute of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario, Canada, K1S 5B6

    Jean P. Langlois, Lenore Fahrig & Gray Merriam

  2. Canadian Science Centre for Human and Animal Health, 1015 Arlington Street, Winnipeg, Manitoba, R3E 3R2, Canada

    Harvey Artsob

Authors
  1. Jean P. Langlois
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lenore Fahrig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gray Merriam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harvey Artsob
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Langlois, J.P., Fahrig, L., Merriam, G. et al. Landscape structure influences continental distribution of hantavirus in deer mice. Landscape Ecology 16, 255–266 (2001). https://doi.org/10.1023/A:1011148316537

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011148316537

Search

Navigation