, Volume 9, Issue 2, pp 205–216 | Cite as

The Interplay of Plant and Animal Disease in a Changing Landscape: The Role of Sudden Aspen Decline in Moderating Sin Nombre Virus Prevalence in Natural Deer Mouse Populations

  • Erin M. LehmerEmail author
  • Julie Korb
  • Sara Bombaci
  • Nellie McLean
  • Joni Ghachu
  • Lacey Hart
  • Ashley Kelly
  • Edlin Jara-Molinar
  • Colleen O’Brien
  • Kimberly Wright
Original Contribution


We examined how climate-mediated forest dieback regulates zoonotic disease prevalence using the relationship between sudden aspen decline (SAD) and Sin Nombre virus (SNV) as a model system. We compared understory plant community structure, small mammal community composition, and SNV prevalence on 12 study sites within aspen forests experiencing levels of SAD ranging from <10.0% crown fade to >95.0% crown fade. Our results show that sites with the highest levels of SAD had reduced canopy cover, stand density, and basal area, and these differences were reflected by reductions in understory vegetation cover. Conversely, sites with the highest levels of SAD had greater understory standing biomass, suggesting that vegetation on these sites was highly clustered. Changes in forest and understory vegetation structure likely resulted in shifts in small mammal community composition across the SAD gradient, as we found reduced species diversity and higher densities of deer mice, the primary host for SNV, on sites with the highest levels of SAD. Sites with the highest levels of SAD also had significantly greater SNV prevalence compared to sites with lower levels of SAD, which is likely a result of their abundance of deer mice. Collectively, results of our research provide strong evidence to show SAD has considerable impacts on vegetation community structure, small mammal density and biodiversity and the prevalence of SNV.


hantavirus Sin Nombre virus sudden aspen decline deer mice Peromyscus maniculatus forest dieback climate change 



Research support was provided by the Mountain Studies Institute, Fort Lewis College and the Fort Lewis College Foundation. We thank N. Bourjaily, D. Newbold, M. Ziemke, and numerous undergraduate research assistants for help in the field and lab. We also thank the Mancos–Dolores District of the US Forest Service, particularly Mark Krabath, District Forester, for assistance in study site selection and continued access to the sites.


  1. Adler, F.R., J.M.C. Pearce-Duvet, M.D. Dearing. 2008. How host population dynamics translate into time-lagged prevalence: an investigation of Sin Nombre Virus in deer mice. Bulletin of Math Biology. 70: 236-252.PubMedCrossRefGoogle Scholar
  2. Allen, C.D., A.K. Macalady, H. Chenchouni, D. Brachelet, N. McDowell, M. Venetier, T. Kitzberger, A. Rigling, D.D. Breashears, et al. 2010. A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management. 259: 660-684.CrossRefGoogle Scholar
  3. Botten, J.K., D. Mirowsky, M. Kusewitt, J. Bharadwaj, R.Yee, R.M. Ricci, R. Feddersen, and B. Hjelle. 2000. Experimental infection model for Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus). Proceedings of the National Academy of Sciences. 97: 10578-10583.CrossRefGoogle Scholar
  4. Botten, J., K. Mirowsky, D. Kusewitt., C.Y. Ye, K. Gottlieb, J. Prescott, and B. Hjelle. 2003. Persistent Sin Nombre virus infection in the deer mouse (Peromyscus maniculatus) model: Sites of replication and strand-specific expression. Journal of Virology. 77: 1540-1550.PubMedCrossRefGoogle Scholar
  5. Bronson, F.H. and G. Perrigo. 1987. Seasonal regulation of reproduction in Murid rodents. American Zoologist. 27: 929-940.Google Scholar
  6. Calisher, C.H., W. Sweeney, J.N. Mills, and B.J. Beaty. 1999. Natural history of Sin Nombre virus in western Colorado. Emerging Infectious Diseases. 5: 126-134.PubMedCrossRefGoogle Scholar
  7. Calisher, C.H., Root, J.J., Mills, J.N., and Beaty, B.J. 2002. Assessment of ecologic and biologic factors leading to hantavirus pulmonary syndrome, Colorado, U.S.A., Croatian Medical Journal. 43: 330-337.PubMedGoogle Scholar
  8. Calisher, C.H., K.D. Wagoner, B.R. Amman, J.J. Root, R.J. Douglass, A.J. Kuenzi, K.D. Abbott, C. Parmenter, T.L. Yates, T.G. Ksiazek, B.J. Beaty and J.N. Mills. 2007. Demographic factors associated with prevalence of antibody to Sin Nombre virus in deer mice in the western United States. Journal of Wildlife Diseases. 43:1-11.PubMedGoogle Scholar
  9. Carey, A.B. and S.M. Wilson. 2001. Induced spatial heterogeneity in forest canopies: responses of small mammals. Journal of Wildlife Management. 65: 1014-1027.CrossRefGoogle Scholar
  10. Centers for Disease Control and Prevention. 1995. Methods for trapping and sampling small mammals for virologic testing. pp. 35Google Scholar
  11. Centers for Disease Control and Prevention (2009) Case information: Hantavirus pulmonary syndrome case count and descriptive statistics. Accessed June 2010
  12. Childs, J.E., G.W. Korch, G.E. Glass, J.W. De Luc, and K.V. Shah. 1997. Epizoology of hantavirus infections in Baltimore: characteristics of infected rat populations. American Journal of Epidemiology. 126: 55-68.Google Scholar
  13. Clay, C.A., E.M. Lehmer, S. St.Jeor and M.D. Dearing. 2009a. Testing mechanisms of the dilution effect: deer mice encounter rates, Sin Nombre virus prevalence and species diversity. Ecohealth. 6: 250-259. PubMedCrossRefGoogle Scholar
  14. Clay,C.A., E. M. Lehmer, A. Prevatali, S. St. Jeor, and M. D. Dearing. 2009b. Contact heterogeneity in deer mice: implications for Sin Nombre virus transmission. Proceedings of the Royal Society of London. 276: 1305-1312.Google Scholar
  15. Collinge, S.K., W.C. Johnson, C. Ray, R. Matchett, J. Grensten, et al. 2005. Testing the generality of a trophic cascade model for plague. Ecohealth. 2: 102-112.CrossRefGoogle Scholar
  16. Converse, S.J., W.M. Block, and G.C. White. 2006. Small mammal population and habitat responses to forest thinning and prescribed fire. Forest Ecology and Management. 228: 263-273.CrossRefGoogle Scholar
  17. Cornelissen J.H.C., S. Lavorel, E. Garnier, S. Díaz, N. Buchmann, D.E., et al. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany. 51:335–380.CrossRefGoogle Scholar
  18. Dearing, M.D., Previtali, M.A., Jones, J.D., Ely, P.W., and Wood, B.A. 2009. Seasonal variation in Sin Nombre virus infections in deer mice: Preliminary results. Journal of Wildlife Diseases 45: 430-436.PubMedGoogle Scholar
  19. Dizney, L.J. and L.A. Ruedas. 2009. Increased host species diversity and decreased prevalence of Sin Nombre virus. Emerging Infectious Diseases. 15: 1012-1018.PubMedCrossRefGoogle Scholar
  20. Dobson, A.P. and P.J. Hudson. 1995. Microparasites: observed patterns in wild animal populations. Pages 52-89 in B.T. Grenfell and A.P Dobson (Eds). Ecology of Infectious Diseases in Natural Populations. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  21. Doyle, T.J., R.T. Bryan, and C.J. Peters. 1998. Viral hemorrhagic fever and hantavirus infections in the Americas. Infectious Disease Clinics of North America. 12: 95.PubMedCrossRefGoogle Scholar
  22. Fairweather ML, Geils BW, Manthei M (2008) Aspen decline on the Coconino National Forest. In: Proceedings of the 55th Western International Forest Disease Work Conference, Sedona, AZ, October 15–19, 2007, McWilliams MG (editor). Salem, OR: Oregon Department of Forestry, pp 53–62Google Scholar
  23. Feldman, H., A. Sanchez, S. Murozonov, C.F. Spiropoulou, P.E. Rollin, T.G. Ksiazek, et al. 1993. Utilzation of autopsy RNA for the synthesis of the nucleocapsid antigen of a newly recognized virus associated with hantavirus pulmonary syndrome. Virus Research. 30: 351-367.CrossRefGoogle Scholar
  24. Frey, B.R., V.J. Lieffers, E.H. Hogg, and S.M. Landhausser. 2004. Predicting landscape patterns of aspen dieback: mechanisms and knowledge gaps. Canadian Journal of Forestry Research. 34: 1379-1390.CrossRefGoogle Scholar
  25. Gashwiller, J.S. 1979. Deer mouse reproduction and its relationship to the tree seed crop. American Midland Naturalist. 102:95-104.CrossRefGoogle Scholar
  26. Getz, W.M. 2009. Disease dynamics and food webs. Plos One. 7: 1-5.Google Scholar
  27. Gilbert, K., R. Norman, K.M. Laurenson, H.W. Reid, P.J. Hudson. 2001. Disease persistence and apparent competition in a three-host community: an empirical and analytical study of large-scale, wild populations. Journal of Animal Ecology. 70: 105-1061.CrossRefGoogle Scholar
  28. Gini, C. 1912. Variabilita e mutabilita. Studi Economico-Giuridici Fac. Giurisprudenza, A. III, parte II. University of Cagliari, Cagliari, Italy, p 3-158.Google Scholar
  29. Glass, G.E., W. Livingstone, J.N. Mills, W.J. Hlady, J.B. Fine, P.E. Rolin, et al. 1998. Black Creek Canal virus infection in Sigmodon hispidus in southern Florida. American Journal of Tropical Medicine and Hygiene. 59: 699-703.PubMedGoogle Scholar
  30. Herbst M., Prescott J., Palmer A. and Schountz T. 2001. Sequence and expression analysis of deermouse interferon γ, interleukin 10, tumor necrosis factor α, and lymphotoxin α. Cytokine 17: 203-213.CrossRefGoogle Scholar
  31. Hjelle, B., S. Jenison, N. Torrez-Martines, T. Yamada, K. Nolte, R. Zumwalt, K. Macinnes, and G. Myers. 1994. A novel hantavirus associated with an outbreak of fatal respiratory disease in the southwestern United States; Evolutionary relationships to known hantaviruses. Journal of Virology. 68: 592-596.PubMedGoogle Scholar
  32. Holroyd, G.L., and K.J. Van Tighem. 1983. Ecological (biophysical) classification of Banff and Jasper National Parks. Volume III. The Wildlife Inventory. Canadian Wildlife Service for Parks Canada, Western Region, Calgary, Alberta.Google Scholar
  33. Jones, K.E., N.G. Patel, M.A. Levy, A. Storygard, D. Balk, J.L. Gittleman, and P. Daszak. 2008. Global trends in emerging infectious diseases. Nature. 452: 990-993.CrossRefGoogle Scholar
  34. Keesing, F., R.D. Holt, R.S. Ostfeld. 2001. Effects of species diversity on disease risk. Ecology Letters. 9: 485-498.CrossRefGoogle Scholar
  35. Kilpatrick, E.D. M. Terajima, F.T. Koster, M.D. Catalina, J. Cruz, and F.A. Ennis. 2004. Role of specific CD8 + T cells in the severity of a fulminant zoonotic viral hemorrhagic fever. Journal of Immunology. 172: 3297-3304.Google Scholar
  36. Kirby, R.R. and G. Beaugrand. 2009. Trophic amplification of climate warming. Proceedings of the Royal Society B. 276: 4095-4103.PubMedCrossRefGoogle Scholar
  37. Klein, S.L., Marson, A.L., Scott, A.L., Ketner, G. and Glass, G.E. 2002. Neonatal sex steroids affect responses to Seoul virus infection in male but not female Norway rats. Brain Behavior and Immunity 16: 736-746.CrossRefGoogle Scholar
  38. Klein S.L., M.C., Zink and G.E. Glass. 2004. Seoul virus increases aggressive behaviour in male Norway rats. Animal Behaviour. 67:421-429.CrossRefGoogle Scholar
  39. Lehmer, E.M., C.A. Clay, J. Boone, S. St. Jeor and M. D. Dearing. 2008. Differential Regulation of Pathogens: The Roles of Habitat Structure and Density in Predicting Prevalence of Sin Nombre Hantavirus. Oecologia. 155: 429-439.PubMedCrossRefGoogle Scholar
  40. Levin, S.A. 1976. Population dynamic models in heterogeneous environments. Annual Review of Ecology and Systematics. 7: 287-310.CrossRefGoogle Scholar
  41. Madhav, N.K, K.D. Wagoner, R.J. Douglas, J.N. Mills. 2007. Delayed density-dependent prevalence of Sin Nombre virus antibody in Montana deer mice (Peromyscus maniculatus) and implications for human disease risk. Vector-Borne Zoonotic Disease. 7: 353-364.CrossRefGoogle Scholar
  42. Michaelian, M., E.H., Hogg, R.J. Hall, E. Arsena. 2011. Massive mortality of aspen following severe drought along the southern edge of the Canadian boreal forest. Global Change Biology. 17: 2084-2094.CrossRefGoogle Scholar
  43. Miller, J.S. and L.W. Gyug. 1981. Initiation of breeding by northern Peromyscus in relation to temperature. Canadian Journal of Zoology. 59: 1094-1098.CrossRefGoogle Scholar
  44. Mills, J.N. 2006. Biodiversity loss and emerging infectious disease: An example from the rodent-borne hemorrhagic fevers. Biodiversity. 7: 9-17.CrossRefGoogle Scholar
  45. Oaten, D.K., K.W. Larsen. 2008. Stand characteristics of three forest types within the dry interior forests of British Columbia, Canada: implications for biodiversity. Forest Ecology and Management. 256: 114-120.CrossRefGoogle Scholar
  46. Ohms SR (2003) Restoration of aspen in different stages of mortality in southern Utah. M.S. Thesis. Utah State University, Logan, UTGoogle Scholar
  47. Ostfeld, R.S. 2009. Biodiversity loss and the rise of zoonotic pathogens. Clinical Microbiology and Infection. 15: 40-43.PubMedCrossRefGoogle Scholar
  48. Ostfeld, R.S. and F. Keesing. 2000a. Biodiversity loss and disease risk: the case of Lyme disease. Conservation Biology. 14: 722-728.CrossRefGoogle Scholar
  49. Ostfeld, R.S. and F. Keesing. 2000b. The function of biodiversity in the ecology of vector borne zoonotic disease. Canadian Journal of Zoology. 78: 2061-2078.CrossRefGoogle Scholar
  50. Otteson, E.W., J. Riolo, J.E. Rowe, S.T. Nichol, T.G. Ksiazek, P.E. Rollin, and S.C. St. Jeor. 1996. Occurrence of hantavirus within the rodent population of northeastern California and Nevada. American Journal of Tropical Medicine and Hygiene. 54: 127-33.PubMedGoogle Scholar
  51. Peterson EB, Peterson NM (1992) Ecology, management, and use of aspen and balsam poplar in the Prairie Provinces, Canada. Forestry Canada Northern Forest Center Species Report 1Google Scholar
  52. Stapp, P. 2007. Trophic cascades and disease ecology. EcoHealth. 4: 121-124.CrossRefGoogle Scholar
  53. Suzan, G., A. Armien, J.N. Mills, E. Marce, G. Ceballos, et al. 2008. Epidemiological considerations of rodent community composition in fragmented landscapes in Panama. Journal of Mammalogy. 89: 664-690.CrossRefGoogle Scholar
  54. Suzan, G., E. Marce, J. Tomasz Giermakowski, J.N. Mills, G. Ceballos, R.S. Ostfeld, B. Armien, J.M. Pascale, and T.L. Yates. 2009. Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. Plos One. 4:1-7.CrossRefGoogle Scholar
  55. United States Department of Agriculture (2011) Plants database. Accessed February 2011
  56. United States Forest Service (2007) Field Data Collection Procedures for Phase 2 Plots, Version 4.0. Forest Inventory and Analysis National Core Field Guide, p 224Google Scholar
  57. Van Horne, B. 1982. Density as a misleading indicator of habitat quality. Journal of Wildlife Management. 47: 893-901.CrossRefGoogle Scholar
  58. Van Mantgem, P.J., Stephenson, N.L., Byrne, J.C., Daniels, L.D., Franklin, J.F., Fule, P.Z., Harmon, M.E., Larsen, A.J., Smith, J.M., Taylor, A.H., and Veblen, T.T. 2009. Widespread increase of tree mortality rates in the western United States. Science. 23: 521-524.CrossRefGoogle Scholar
  59. Wilson, S.M. and A.B. Carey. 2000. Legacy retention versus thinning: influences on small mammals. Northwest Science. 74: 131-145.Google Scholar
  60. Worrall, J.J., L. Egeland, T. Eager, R.A. Mask, E.W. Johnson, P.A. Kemp, W.D. Shephard. 2008. Rapid mortality of Populus tremuloides in southwestern Colorado, USA. Forest Ecology and Management. 255: 686-696.CrossRefGoogle Scholar
  61. Worrall, J.J., Marchetti, S.B., Egeland, L., Mask, R.A., Eager, T., and Howell. B. 2010. Effects and etiology of sudden aspen decline in southwestern Colorado, USA. Forest Ecology and Management. 260: 638-648.CrossRefGoogle Scholar
  62. Yates, T.L., Mills, J.N., Parmenter, C.A., Ksiazek, T.G., Parmenter, R.R., Vande Castle, J.R., Cahisher, C.H., Nichol, S.T., Abbott, K.D., et al. 2002. The ecology and evolutionary history of an emergent disease: Hantavirus pulmonary syndrome. Bioscience. 52: 989-998.CrossRefGoogle Scholar

Copyright information

© International Association for Ecology and Health 2012

Authors and Affiliations

  • Erin M. Lehmer
    • 1
    Email author
  • Julie Korb
    • 1
  • Sara Bombaci
    • 1
  • Nellie McLean
    • 1
  • Joni Ghachu
    • 1
  • Lacey Hart
    • 1
  • Ashley Kelly
    • 1
  • Edlin Jara-Molinar
    • 1
  • Colleen O’Brien
    • 1
  • Kimberly Wright
    • 1
  1. 1.Department of BiologyFort Lewis CollegeDurangoUSA

Personalised recommendations