Environmental conditions for Jamestown Canyon virus correlated with population-level resource selection by white-tailed deer in a suburban landscape

Autoři: Karmen M. Hollis-Etter aff001;  Robert A. Montgomery aff002;  Dwayne R. Etter aff003;  Christopher L. Anchor aff004;  James E. Chelsvig aff004;  Richard E. Warner aff005;  Paul R. Grimstad aff006;  Diane D. Lovin aff006;  Marvin S. Godsey, Jr. aff007
Působiště autorů: Biology Department, University of Michigan-Flint, Flint, Michigan, United States of America aff001;  Department of Fisheries and Wildlife, Michigan State University, East Lansing, Michigan, United States of America aff002;  Wildlife Division Michigan Department of Natural Resources, Lansing, Michigan, United States of America aff003;  Forest Preserve District of Cook County, River Forest, Illinois, United States of America aff004;  Natural Resources and Environmental Sciences, University of Illinois Champaign-Urbana, Urbana, Illinois, United States of America aff005;  Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, United States of America aff006;  Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, Colorado, United States of America aff007
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223582


Suburban landscapes can alter spatial patterns by white-tailed deer (Odocoileus virginianus) and increase animal contact with vectors, pathogens, and humans. Close-contact relationships at a landscape level can have broad implications for disease epidemiology. From 1995–1999, we captured and radio-collared 41 deer in two suburban forest preserves in Chicago, Illinois. We collected blood to determine if animals were seronegative or seropositive for Jamestown Canyon virus and tracked deer movements within suburban habitats. We developed utilization distributions at the population-level and evaluated resource selection for seronegative and seropositive deer. We used maximum likelihood estimation for model selection via Akaike information criterion and then restricted maximum likelihood estimation to attain unbiased estimates of the parameters in the top-ranking models. The top-ranking model describing the resource selection of seronegative deer received almost the full weight of evidence (Akaike information criterion ωi = 0.93), and included the proportion of wetlands, precipitation in year t, and an interaction of the proportion of wetlands and precipitation in year t. The top-ranking model describing resource selection of seropositive deer received the full weight of evidence (Akaike information criterion ωi = 1.00). The model included distance to nearest populated place, distance to nearest river, length of road in each grid cell, precipitation in year t, and an interaction of the length of road in each grid cell and precipitation in year t. These results are valuable for mapping the spatial configuration of hotspots for Jamestown Canyon virus and could be used to educate local residents and recreationalists to reduce human exposure.

Klíčová slova:

Deer – Disease vectors – Forests – Mosquitoes – Pathogens – Surface water – Wetlands – Wildlife


1. Taylor LH, Latham SM, Woolhouse ME. Risk factors for human disease emergence. Phil Trans R Soc Lond B Bi. Sc. 2001; 356(1411):983–89.

2. Wang HH, Wang Y, Delgado MS. The transition to modern agriculture: Contract farming in developing economies. Am J Agric Econ. 2014; 96(5):1257–71.

3. Hassell JM, Begon M, Ward MJ, Fèvre EM. Urbanization and disease emergence: Dynamics at the wildlife–livestock–human interface. Trends Ecol Evol. 2017; 32(1):55–67. doi: 10.1016/j.tree.2016.09.012 28029378

4. Pecoraro HL, Day HL, Reineke R, Stevens N, Withey JC, Marzluff JM, et al. Climatic and landscape correlates for potential West Nile virus mosquito vectors in the Seattle region. J Vector Ecol. 2007; 32(1):22–28. 17633422

5. Morse SS. Emerging viruses: defining the rules for viral traffic. Perspect Biol Med. 1991; 34(3):387–409. doi: 10.1353/pbm.1991.0038 2067933

6. Morse SS. Examining the origins of emerging viruses. New York: Oxford University Press; 1993. p.10–28.

7. Junge RE, Bauman K, King M, Gompper ME. A serologic assessment of exposure to viral pathogens and Leptospira in an urban raccoon (Procyon lotor) population inhabiting a large zoological park. J Zoo Wildl Med. 2007; 38(1):18–26. doi: 10.1638/05-123.1 17469271

8. Creel S, Winnie JA Jr. Responses of elk herd size to fine-scale spatial and temporal variation in the risk of predation by wolves. Anim Behav. 2005; 69:1181–89.

9. Kjær LJ, Schauber EM, Nielsen CK. Spatial and temporal analysis of contact rates in female white-tailed deer. J Wildl Manage. 2008; 72(8):1819–25.

10. Martin J, Basille M, Van Moorter B, Kindberg J, Allainé D, Swenson JE. Coping with human disturbance: Spatial and temporal tactics of the brown bear (Ursus arctos). Can J Zool. 2010; 88(9):875–83.

11. Walter DW, Beringer J, Hansen LP, Fischer JW, Millspaugh JJ, VerCauteren KC. Factors affecting space use overlap by white-tailed deer in an urban landscape. Int J Geogr Inf Sc. 2011; 25(3):379–92.

12. Nelson R, Wilcox L, Brennan BA, Mayo D. Surveillance for arbovirus infections. Conn Epidemiol. 2002; 22:5–8.

13. Karabatsos N. International catalogue of arboviruses, including certain other viruses of vertebrates. 3rd ed. San Antonio (TX): Am Society of Trop Med Hyg for the subcommittee on Information Exchange of the American Committee on Arthropod-borne Viruses; 1985.

14. Mayo D, Karabatsos N, Scarano FJ, Brennan T, Buck D, Fiorentino T, et al. Jamestown Canyon virus: Seroprevalence in Connecticut. Emerg Infect Dis. 2001; 7(5):911–12. doi: 10.3201/eid0705.017529 11747714

15. Patriquin G, Drebot M, Cole T, Lindsay R, Schleihauf E, Johnston BL, et al. High seroprevalence of Jamestown Canyon virus among deer and humans, Nova Scotia, Canada Emerg Infect Dis. 2018; 24(1):118–21. doi: 10.3201/eid2401.170484 29260667

16. Andreadis TG, Anderson JF, Armstrong PM, Main AJ. Isolations of Jamestown Canyon virus (Bunyaviridae: Orthobunyavirus) from field-collected mosquitoes (Diptera: Culicidae) in Connecticut, USA: A ten-year analysis, 1997–2006. Vector Borne Zoonotic Dis. 2008; 8(2):175–88. doi: 10.1089/vbz.2007.0169 18386967

17. Illinois State Geological Survey [Internet]. Illinois geospatial data clearinghouse. Land cover of Illinois 1999–2000 Data. https://clearinghouse.isgs.illinois.edu/data/land-cover/land-cover-illinois-1999-2000-data.

18. Piccolo BP, Van Deelen TR, Hollis-Etter K, Etter DR, Warner RE, Anchor C. Behavior and survival of white-tailed deer neonates in two suburban forest preserves. Can J Zool. 2010; 88(5):487–495.

19. Mangudo C, Aparicio JP, Rossi GC, Gleiser RM. Tree hole mosquito species composition and relative abundances differ between urban and adjacent forest habitats in northwestern Argentina. Bull Entomol Res. 2017; 108(2):203–12. doi: 10.1017/S0007485317000700 28770688

20. Mapes DR (Illinois Agricultural Experiment Station, Urbana, IL). Soil survey of DuPage and part of Cook counties, Illinois. Report. 1979:108.

21. Ramsey CW. A drop-net deer trap. J Wildl Manage. 1968; 32(1):187–90.

22. Kilpatrick HJ, Spohr S, DeNicola AJ. Darting urban deer: Techniques and technology. Wildl Soc Bull. 1997; 25(2):542–46.

23. Kilpatrick HJ, Spohr S. Telazol®-xylazine versus ketamine-xylazine: A field evaluation for immobilizing white-tailed deer. Wildl Soc Bull. 1999; 27(3):556–70.

24. Severinghaus CA. Tooth development and wear as criteria of age in white-tailed deer. J Wildl Manage. 1949; 13(2):195–216.

25. Nixon CM, Hansen LP, Brewer PA, Chelsvig JE. Ecology of white-tailed deer in an intensively farmed region of Illinois. Wildl Monographs 1991; 118.

26. Nams VO. Locate II® user’s guide. Nova Scotia, Canada: Pacer Computer Software; 1990.

27. Etter DR, Hollis KM, Van Deelen TR, Ludwig DR, Chelsvig JE, Anchor CL, et al. Survival and movements of white-tailed deer in suburban Chicago, Illinois. J Wildl Manage. 2002; 66(2):500–10.

28. Boromisa RD, Grimstad PR. Seroconversion rates to Jamestown Canyon virus among six populations of white-tailed deer (Odocoileus virginianus) in Indiana. J Wildl Dis. 1987; 23(1):23–33. doi: 10.7589/0090-3558-23.1.23 3820426

29. Grimstad PR, Williams DG, Schmitt SM. Infection of white-tailed deer (Odocoileus virginianus) in Michigan with Jamestown Canyon virus (California serogroup) and the importance of maternal antibody viral maintenance. J Wildl Dis. 1987; 23(1):12–22. doi: 10.7589/0090-3558-23.1.12 3102763

30. Johnson DH. The comparison of usage and availability measurements for evaluating resource preference. Ecol. 1980; 61(1):65–71.

31. Ganser C, Wisely SM. Patterns of spatio-temporal distribution, abundance, and diversity in a mosquito community from the eastern Smoky Hills of Kansas. J Vector Ecol. 2013; 38(2):229–36. doi: 10.1111/j.1948-7134.2013.12035.x 24581350

32. Kernohan BJ, Gitzen RA, Millspaugh JJ. Analysis of animal space use and movements. In: Millspaugh JJ, Marzluff JM, editors. Radio tracking and animal population. San Diego (CA): Academic Press; 2001. p. 125–66.

33. Gitzen RA, Millspaugh JJ. Comparison of least-squares cross-validation bandwidth options for kernel home-range estimation. Wildl Soc Bull. 2003; 31(3):823–31.

34. Gitzen RA, Millspaugh JJ, Kernohan BJ. Bandwidth selection for fixed-kernel analysis of animal utilization distributions. J Wildl Manage. 2006; 70(5):1334–44.

35. Lele SR, Merrill EH, Keim J, Boyce MS. Selection, use, choice and occupancy: clarifying concepts in resource selection studies. J Anim Ecol. 2013; 82:1183–91. doi: 10.1111/1365-2656.12141 24499379

36. Montgomery RA, Roloff GJ, Millspaugh JJ, Nylen-Nemetchek M. Living amidst a sea of agriculture: Predicting the occurrence of Canada lynx within an ecological island. Wildlife Biol. 2014; 20:145–154.

37. Millspaugh JJ, Rota CT, Bonnot TW, Montgomery RA, Belant JL, Ayers CR, et al. Analysis of resource selection. In: Murray D, Chapron G, editors. Population ecology in practice: underused, misused, and abused methods. John Wiley and Sons; 2019.

38. Rota CT, Millspaugh JJ, Bonnot TW, Montgomery RA, Belant JL, Ayers CR, et al. Analysis of resource selection: web exercises. In: Murray D, Chapron G, editors. Population ecology in practice: underused, misused, and abused methods. John Wiley and Sons; 2019.

39. Montgomery RA, Roloff GJ. Habitat selection. In: Reference Module in Life Sciences. 2017. https://www.sciencedirect.com/science/article/pii/B9780128096338023839?via%3Dihub

40. Montgomery RA, Ver Hoef JM, Boveng PL. Spatial modeling of haul-out site use by harbor seals in Cook Inlet, Alaska. Mar Ecol Prog Ser. 2007; 341:257–264.

41. Nielson RM, Sawyer H. Estimating resource selection with count data. Ecol Evol. 2013; 3(7): 2233–2240. doi: 10.1002/ece3.617 23919165

42. Petrunenko Y, Montgomery RA, Seryodkin IV, Zaumyslova OY, Miquelle D, Macdonald DW. Spatial variation in the density and vulnerability of preferred prey in the landscape shape patterns of Amur tiger habitat use. Oikos 2016; 125:66–75.

43. Millspaugh JJ, Rittenhouse CD, Montgomery RA, Matthews WS, Slotow R. Resource selection modeling reveals potential conflicts involving reintroduced lion (Panthera leo) in Tembe Elephant Park, South Africa. J Zool. 2015; 296:124–132.

44. Illinois Department of Agriculture [Internet}. Land cover of Illinois 1991–1995. https://www2.illinois.gov/sites/agr/Resources/LandWater/Pages/Land-Cover-of-Illinois-1991-1995.aspx.

45. Illinois Natural History Survey [Internet]. Illinois GAP analysis project. https://www.inhs.illinois.edu/research/gap/landcover/.

46. Calhoun LM, Avery M, Jones L, Gunarto K, King R, Roberts J, et al. Combined sewage overflows (CSO) are major urban breeding sites for Culex quinquefasciatus in Atlanta, Georgia. Am J Trop Med Hyg. 2007; 77(3):478–84. 17827363

47. Yee DA. Tires as habitats for mosquitoes: A review of studies within the eastern United States. J Med Entomol. 2008; 45(4):581–93 18714856

48. United States Fish and Wildlife Service [Internet]. United States Department of the Interior, Fish, and Wildlife Service. National wetlands inventory; 1999. http://www.fws.gov/wetlands.

49. United States Geological Survey [Internet]. Geographic names information system (GNIS)—USGS national map downloadable data collection; 1999. https://www.sciencebase.gov/catalog/item/5825a0c2e4b01fad86db66c9.

50. Butzler SJ, Brewer CA, Stroh WJ. Establishing classification and hierarchy in populated place labeling for multiscale mapping for the National Map. Cartogr Geogr Inf Sci. 2011; 38(2):100–109.

51. Illinois State Water Survey [Internet]. Cook county precipitation network: Data collection. https://www.isws.illinois.edu/data/ccprecipnet/livedata.asp.

52. Bertram DS, McGregor IA, McFadzean JA. Mosquitoes of the colony and protectorate of the Gambia. Trans R Soc Trop Med Hyg. 1958; 52(2):135–51. doi: 10.1016/0035-9203(58)90035-x 13543903

53. Skovmand O, Ouedraogo TDA, Sanogo E, Samuelsen H, Paré Toé L, Bosselmann R, et al. Cost of integrated vector control with improved sanitation and road infrastructure coupled with the use of slow-release Bacillus sphaericus granules in a tropical urban setting. J Med Entomol. 2011; 48(4):813–21. doi: 10.1603/me10041 21845940

54. Ver Hoef JM, Cressie N, Fisher RN, Case TJ. Uncertainty and spatial linear models for ecological data. In: Humsaker CT, Goodchild MF, Friedl MA, Case TJ, editors. Spatial uncertainty in ecology: implications for remote sensing and GIS applications. New York: Springer; 2001.

55. Bonnot TW, Wildhaber ML, Millspaugh JJ, DeLonay AJ, Jacobson RB, Bryan JL. Discrete choice modeling of shovelnose sturgeon habitat selection in the Lower Missouri River. J Appl Ichthyol. 2011; 27(20):291–300.

56. Boyce MS, McDonald LL. Relating populations to habitats using resource selection functions. Trends Ecol Evol. 1999; 14(12):268–72.

57. Gustine DD, Parker KL, Lay RJ, Gillingham MP, Heard DC. Interpreting resource selection at different scales for woodland caribou in winter. J Wildl Manage. 2006; 70(6):1601–15.

58. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature. 2008; 451:990–93. doi: 10.1038/nature06536 18288193

59. Johnson BJ, Munafo K, Shappell L, Tsipoura N, Robson M, Ehrenfeld J, et al. The roles of mosquito and bird communities on the prevalence of West Nile virus in urban wetland and residential habitats. Urban Ecosyst. 2012; 15(3):513–31. doi: 10.1007/s11252-012-0248-1 25484570

60. Ozoga JJ, Verme LJ, Bienz CS. Parturition behavior and territoriality in white-tailed deer: Impact on neonatal mortality. J Wildl Manage. 1982; 46:1.

61. Nixon CM, Etter D. Maternal age and fawn rearing success for white-tailed deer in Illinois. Am Midl Nat. 1995; 133(2):290–97.

62. Issel CJ, Trainer DO, Thompson WH. Experimental studies with white-tailed deer and four California group arboviruses (LaCrosse, Trivittatus, Snowshoe Hare, and Jamestown Canyon). Am J Trop Med Hyg. 1972; 21(6):979–84. doi: 10.4269/ajtmh.1972.21.979 4635778

63. Duquette JF, Belant JL, Svoboda NJ, Beyer DE Jr, Lederle PE. Effects of maternal nutrition, resource use and multi-predator risk on neonatal white-tailed deer survival. PLoS ONE. 2014; 9(6): e100841. doi: 10.1371/journal.pone.0100841 24968318

64. Grund MD, McAninch JB, Wiggers EP. Seasonal movements and habitat use of female white-tailed deer associated with an urban park. J Wildl Manage. 2002; 66(1):123–30.

65. Carbaugh B, Vaughan JP, Bellis ED, Graves HB. Distribution and activity of white-tailed deer along an interstate highway. J Wildl Manage. 1975; 39(3):570–81.

66. Waring GH, Griffis JL, Vaugh ME. White-tailed deer roadside behavior, wildlife warning reflectors, and highway mortality. Appl Anim Behav Sc. 1991; 29:215–23.

67. Murphy RK. Serologic evidence of arboviral infections in white-tailed deer from central Wisconsin. J Wildl Dis. 1989; 25(2):300–301. doi: 10.7589/0090-3558-25.2.300 2716117

68. Neitzel DF, Grimstad PR. Serological evidence of California group and Cache Valley virus infection in Minnesota white-tailed deer. J Wildl Dis. 1991; 217(2):230–37.

69. Omeara GF, Gettman AD, Evans LF, Scheel FD. Invasion of cemeteries in Florida by Aedes albopictus. J Am Mosq Control Assoc. 1992; 8(1):1–10. 1583479

70. Trewin BJ, Kay BH, Darbro JM, Hurst TP. Increased container-breeding mosquito risk owing to drought-induced changes in water harvesting and storage in Brisbane, Australia. Int Health. 2013; (5):251–58.

71. Kilpatrick HJ, Spohr S. Spatial and temporal use of a suburban landscape by female white-tailed deer. Wildl Soc Bull. 2000; 28(4):1023–29.

72. DeNicola AJ, Weber SJ, Bridges CA, Stokes JL. Nontraditional techniques for management of overabundant deer populations. Wildl Soc Bull. 1997; 25(2):496–99.

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden