Geography, deer, and host biodiversity shape the pattern of lyme disease emergence in the thousand islands archipelago of Ontario, Canada

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Werden, Lisa ^a,b   Barker, Ian K ^a,c   Bowman, Jeff ^d   Gonzales, Emily K ^e   Leighton, Patrick A ^f   Lindsay, L Robbin ^g   Jardine, Claire M ^a,c  

^a UNIVERSITY OF GUELPH   (Canada)

^b PARKS CANADA   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d ONTARIO MINISTRY OF NATURAL RESOURCES   (Canada)

^e UNIVERSITY OF VICTORIA   (Canada)

^f UNIVERSITÉ DE MONTRÉAL   (Canada)

^g PUBLIC HEALTH AGENCY OF CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AIR TEMPERATURE; ARTICLE; BIODIVERSITY; BORRELIA BURGDORFERI; CANADA; CONTROLLED STUDY; DEER; DISEASE CARRIER; GEOGRAPHICAL VARIATION (SPECIES); HOST PATHOGEN INTERACTION; INFECTION RISK; IXODES SCAPULARIS; LYME DISEASE; MAMMAL; MOUSE; NONHUMAN; NYMPH; PEROMYSCUS; PEROMYSCUS LEUCOPUS; POPULATION ABUNDANCE; SPECIES RICHNESS; TRANSPORT HOST; UNITED STATES; VEGETATION DYNAMICS;

ANIMALS; BIODIVERSITY; BORRELIA BURGDORFERI; CONFIDENCE INTERVALS; DEER; GEOGRAPHY; HOST-PARASITE INTERACTIONS; ISLANDS; IXODES; LINEAR MODELS; LYME DISEASE; NYMPH; ONTARIO; SEASONS; SPECIES SPECIFICITY;

EID: 84897441572     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085640     Document Type: Article

References (80)

1. Ogden NH, Lindsay LR, Hanincová K, Barker IK, Bigras-Poulin M, et al. (2008) Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada now and with climate change. Int J Health Geogr 7: 24.
2. Ostfeld RS, Keesing F, Schauber EM, Schmidt KA (2002) Ecological context of Lyme disease: Biodiversity, habitat fragmentation, and risk of infection. In: Aguirre AA, Ostfeld RS, Tabor GM, House C, Pearl MC, editors. Conservation Medicine: Ecological Health in Practice. New York: Oxford University Press. pp. 207-291.
3. Diuk-Wasser MA, Gatewood AG, Cortinas MR, Yaremych-Hamer S, Tsao J, et al. (2006) Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. J Med Entomol 43: 166-176. (Pubitemid 44743521)
4. Eisen L, Lane RS (2002) Vectors of Borrelia burgdorferi sensu lato. In: Gray JS, Kahl O, Lane RS, Stanek G, editors. Lyme Borreliosis: Biology, Epidemiology and Control. New York: CABI Publishing. pp. 91-115.
5. Telford S, Mather T, Moore S, Wilson M, Spielman A (1988) Incompetence of deer as reservoirs of the Lyme disease spirochete. Am J Trop Med Hyg 39: 105-109.
6. Rand PW, Lubelczyk C, Lavigne GR, Elias S, Holman MS, et al. (2003) Deer density and the abundance of Ixodes scapularis (Acari: Ixodidae). J Med Entomol 40: 179-184. (Pubitemid 37399442)
7. Piesman J (2002) Ecology of Borrelia burgdorferi sensu lato in North America. In: Gray JS, Kahl O, Lane RS, Stanek G, editors. Lyme Borreliosis: Biology, Epidemiology and Control. New York: CABI Publishing. pp. 223-249.
8. Kurtenbach K, Sewell H, Ogden NH, Randolph SE, Nuttal PA (1998) Serum complement sensitivity as a key factor in Lyme disease ecology. Infect Immun 66: 1248-1251. (Pubitemid 28101172)
9. Jordan RA, Schulze TL, Jahn MB (2007) Effects of reduced deer density on the abundance of Ixodes scapularis (Acari: Ixodidae) and Lyme disease incidence in a northern New Jersey endemic area. J Med Entomol 44: 752-757. (Pubitemid 47442054)
10. Stafford III KC (1993) Reduced abundance of Ixodes scapularis (Acari: Ixodidae) with exclusion of deer by electric fencing. J Med Entomol 30: 986-996.
11. Daniels TJ, Fish D (1995) Effect of deer exclusion on the abundance of immature Ixodes scapularis (Acari: Ixodidae) parasitizing small and medium-sized mammals. J Med Entomol 32: 5-11.
12. Rand PW, Lubelczyk C, Holman MS, Lacombe EH, Smith RP (2004) Abundance of Ixodes scapularis (Acari: Ixodidae) after complete removal of deer from an isolated offshore island, endemic for Lyme disease. J Med Entomol 41: 779-784. (Pubitemid 38991518)
13. Jordan RA, Schulze TL (2005) Deer browsing and the distribution of Ixodes scapularis (Acari: Ixodidae) in Central New Jersey forests. Environ Entomol 34: 801-806. (Pubitemid 41113263)
14. Ostfeld RS, Canham CD, Oggenfuss K, Winchcombe RJ, Keesing F (2006) Climate, deer, rodents, and acorns as determinants of variation in Lyme disease risk. PLoS Biol DOI: 10.1371/journal.pbio.0040145.
15. Giardina AR, Schmidt KA, Schauber EM, Ostfeld RS (2000) Modeling the role of songbirds and rodents in the ecology of Lyme disease. Can J Zool 78: 2184-2197. (Pubitemid 32145112)
16. LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F (2003) The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci U S A 100: 567-571. (Pubitemid 36126092)
17. Brisson D, Dykhuizen DE, Ostfeld RS (2008) Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proc Biol Sci 275: 227-235. (Pubitemid 350174590)
18. Spielman A, Levine JF, Wilson ML (1984) Vectorial capacity of North American Ixodes ticks. Yale J Biol Med 57: 507-513. (Pubitemid 15151037)
19. Mather TN, Wilson ML, Moore SI, Ribeiro JMC, Spielman A (1989) Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete (Borrelia burgdorferi). Am J Epidemiol 130: 143-150. (Pubitemid 19179393)
20. Anderson JM, Norris DE (2006) Genetic diversity of Borrelia burgdorferi sensu stricto in Peromyscus leucopus, the primary reservoir of Lyme disease in a region of endemicity in southern Maryland. Appl Environ Microbiol 72: 5331-5341.
21. Brunner JL, LoGiudice K, Ostfeld RS (2008) Estimating reservoir competence of Borrelia burgdorferi hosts: Prevalence and infectivity, sensitivity, and specificity. J Med Entomol 45: 139-147. (Pubitemid 351219225)
22. Ostfeld RS, Keesing F (2000) Biodiversity and disease risk: The case of Lyme disease. Conserv Biol 14: 722-728. (Pubitemid 30390728)
23. Ginsberg HS, Buckley PA, Balmforth MG, Zhioua E, Mitra S, et al. (2005) Reservoir competence of native North American birds for the Lyme disease spirochete, Borrelia burgdorferi. J Med Entomol 42: 445-449. (Pubitemid 40722135)
24. Hanincová K, Kurtenbach K, Diuk-Wasser M, Brei B, Fish D (2006) Epidemic spread of Lyme borreliosis, northeastern United States. Emerg Infect Dis 12: 604-611.
25. Keesing F, Brunner J, Duerr S, Killilea M, LoGiudice K, et al. (2009) Hosts as ecological traps for the vector of Lyme disease. Proc Biol Sci 276: 3911-3919.
26. Ostfeld RS (2011) Lyme disease: the ecology of a complex system. New York: Oxford University Press. 216 p.
27. Van Buskirk J, Ostfeld RS (1995) Controlling Lyme disease by modifying the density and species composition of tick hosts. Ecol Appl 5: 1133-1140. (Pubitemid 3004275)
28. Schmidt KA, Ostfeld RS (2001) Biodiversity and the dilution effect in disease ecology. Ecology 82: 609-619. (Pubitemid 32175310)
29. LoGiudice K, Duerr STK, Newhouse MJ, Schmidt KA, Killilea ME, et al. (2008) Impact of host community composition on Lyme disease risk. Ecology 89: 2841-2849.
30. Bouchard C, Beauchamp G, Nguon S, Trudel L, Milord F, et al. (2011) Associations between Ixodes scapularis ticks and small mammal hosts in a newly endemic zone in southeastern Canada: implications for Borrelia burgdorferi transmission. Ticks Tick Borne Dis DOI: 10.1016/j.ttbdis.2011.03.005.
31. Ogden NH, Tsao JI (2009) Biodiversity and Lyme disease: Dilution or amplification? Epidemics 1: 196-206.
32. Schulze TL, Jordan RA, Hung RW (1995) Suppression of subadult Ixodes scapularis (Acari: Ixodidae) following removal of leaf litter. J Med Entomol 32: 730-733.
33. Bertrand MR, Wilson ML (1996) Microclimate-dependent survival of unfed adult Ixodes scapularis (Acari: Ixodidae) in nature: life cycle and study design implications. J Med Entomol 33: 619-627. (Pubitemid 126429425)
34. Ogden NH, Lindsay LR, Beauchamp G, Charron D, Maarouf A, et al. (2004) Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. J Med Entomol 41: 622-633. (Pubitemid 38991497)
35. Lindsay LR, Barker IK, Surgeoner GA, McEwan SA, Gillespie TJ, et al. (1995) Survival and development of Ixodes scapularis (Acari: Ixodidae) under various climatic conditions in Ontario, Canada. J Med Entomol 32: 143-152.
36. Vail SG, Smith G (2002) Vertical movement and posture of blacklegged tick (Acari: Ixodidae) nymphs as a function of temperature and relative humidity in laboratory experiments. J Med Entomol 39: 842-846. (Pubitemid 135693339)
37. Ogden NH, Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, et al. (2006) Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Parasitol 36: 63-70. (Pubitemid 43049698)
38. Ogden NH, Lindsay LR, Leighton PA (2013) Predicting the rate of invasion of the agent of Lyme disease Borrelia burgdorferi. J Appl Ecol DOI: 10.1111/1365-2664.12050.
39. Ogden NH, Trudel L, Artsob H, Barker IK, Beauchamp G, et al. (2006) Ixodes scapularis ticks collected by passive surveillance in Canada: Analysis of geographic distribution and infection with Lyme borreliosis agent Borrelia burgdorferi. J Med Entomol 43: 600-609. (Pubitemid 44734956)
40. Ogden NH, Lindsay LR, Morshed M, Sockett PN, Artsob H (2008) The rising challenge of Lyme borreliosis in Canada. Canada Communicable Disease Report 34(1): 1-19.
41. White DJ, Chang H, Benach JL, Bosler EM, Meldrum SC, et al. (1991) The geographic spread and temporal increase of the Lyme disease epidemic. JAMA 266: 1230-1236.
42. Glavanakov S, White DJ, Caraco T, Lapenis A, Robinson GR, et al. (2001) Lyme disease in New York State: Spatial pattern at a regional scale. Am J Trop Med Hyg 65: 538-545. (Pubitemid 33134589)
43. Jackson CA, Lovrich SD, Agger WA, Callister SM (2002) Reassessment of a Midwestern Lyme disease focus for Borrelia burgdorferi and the human granulocytic ehrlichiosis agent. J Clin Microbiol 40: 2070-2073. (Pubitemid 34596386)
44. Hoen AG, Margos G, Bent SJ, Diuk-Wasser MA, Barbour A, et al. (2009) Phylogeography of Borrelia burgdorferi in the eastern United States reflects multiple independent Lyme disease emergence events. Proc Natl Acad Sci U S A 106: 15013-15018.
45. Ogden NH, Lindsay LR, Morshed M, Sockett PN, Artsob H (2009) The emergence of Lyme disease in Canada. CMAJ 180: 1221-1222.
46. Ogden NH, Bouchard C, Kurtenbach K, Margos G, Lindsay LR, et al. (2010) Active and passive surveillance and phylogenetic analysis of Borrelia burgdorferi elucidate the process of Lyme disease risk emergence in Canada. Environ Health Perspect 118: 909-914.
47. Hamer SA, Tsao JI, Walker ED, Hickling GJ (2010) Invasion of the Lyme disease vector Ixodes scapularis: Implications for Borrelia burgdorferi endemicity. EcoHealth 7: 47-63.
48. Leighton PA, Koffi JK, Pelcat Y, Lindsay LR, Ogden NH (2012) Predicting the speed of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J Appl Ecol DOI: 10.1111/j.1365-2664.2012.02112.x.
49. Hall-Baker PA, Nieves E Jr, Jajosky RA, Adams DA, Sharp P, et al. (2010) Summary of notifiable diseases - United States, 2008. Morbidity and Mortality Weekly Reports 57: 1-94.
50. Werden L (2012) Factors Affecting the Abundance of Blacklegged Ticks (Ixodes scapularis) and the Prevalence of Borrelia burgdorferi in Ticks and Small Mammals in the Thousand Islands Region. M.Sc. thesis. Guelph: University of Guelph.
51. Lindsay LR, Barker IK, Surgeoner GA, McEwan SA, Gillespie TJ, et al. (1998) Survival and development of the different life stages of Ixodes scapularis (Acari: Ixodidae) held within four habitats on Long Point, Ontario, Canada. J Med Entomol 35: 189-199. (Pubitemid 128462271)
52. Yuval B, Spielman A (1990) Duration and regulation of the developmental cycle of Ixodes dammini (Acari: Ixodidae). J Med Entomol 27: 196-201.
53. Durden LA, Keirans JE (1996) Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: Taxonomy, identification key, distribution, hosts and medical/veterinary importance. Maryland: Thomas Say Publications in Entomology: Entomological Society of America. 95 p.
54. Bouchard C, Leighton P, Nguon S, Trudel L, Milord F, et al. (2013) Harvested white-tailed deer as sentinel hosts for early establishing Ixodes scapularis populations and risk from vector-borne zoonoses in southeastern Canada. J Med Entomol 50: 384-393.
55. Eder T (2002) Mammals of Ontario. Edmonton: Lone Pine Publishing. 215 p.
56. Thompson L (2010) A pathway analysis candidate gene approach to seasonal reproductive timing in mammals with a focus on period and casein kinase 1 in Peromyscus. M.Sc. thesis. Peterborough: Trent University.
57. Ostfeld RS, Schauber EM, Canham CD, Keesing F, Jones CG, et al. (2001) Effects of acorn production and mouse abundance on abundance and Borrelia burgdorferi infection prevalence of nymphal Ixodes scapularis ticks. Vector Borne Zoonotic Dis 1: 55-63.
58. Schulze TL, Jordan RA, Schulze CJ, Hung RW (2009) Precipitation and temperature as predictors of the local abundance of Ixodes scapularis (Acari: Ixodidae) nymphs. J Med Entomol 46: 1025-1029.
59. Neff DJ (1968) The pellet-group count technique for big game trend, census, and distribution: A review. J Wildl Manage 32: 597-614.
60. Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Modell 135: 147-186. (Pubitemid 32102782)
61. Diuk-Wasser MA, Vourc'h G, Cislo P, Hoen AG, Melton F, et al. (2010) Field and climate-based model for predicting the density of host-seeking nymphal Ixodes scapularis, an important vector of tick-borne disease agents in the eastern United States. Glob Ecol Biogeogr 19: 504-514.
62. Dormann CF, McPherson JM, Araújo MB, Bivand R, Bolliger J, et al. (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30: 609-628. (Pubitemid 350060576)
63. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach, Second edition. New York: Springer. 488 p.
64. Zuur A, Leno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. New York: Springer Science+ Business Media LLC. 574 p.
65. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge: Cambridge University Press. 556 p.
66. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Available: http://www.R-project.org/. Accessed 1 December 2011.
67. Madhav NK, Brownstein JS, Tsao JI, Fish D (2004) A dispersal model for the range expansion of blacklegged tick (Acari: Ixodidae). J Med Entomol 41: 842-852. (Pubitemid 39403927)
68. Ogden NH, Lindsay LR, Hanincová K, Barker IK, Bigras-Poulin M, et al. (2008) Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol 74: 1780-1790. (Pubitemid 351400132)
69. Christopherson RW, Byrne ML (2009) Geosystems: an introduction to physical geography, Second Canadian edition. Toronto: Pearson Education Canada. 736 p.
70. Allan BF, Keesing F, Ostfeld RS (2003) Effect of forest fragmentation on Lyme disease risk. Conserv Biol 17: 267-272. (Pubitemid 36234419)
71. Nupp TE, Swihart RK (1998) Effects of forest fragmentation on population attributes of white-footed mice and eastern chipmunks. J Mammal 79: 1234-1243. (Pubitemid 128485078)
72. Krohne DT, Hoch GA (1999) Demography of Peromyscus leucopus populations on habitat patches: The role of dispersal. Can J Zool 77: 1247-1253. (Pubitemid 129528576)
73. Bowman J, Cappuccino N, Fahrig L (2002) Patch size and population density: the effect of immigration behavior. Conservation Ecology 6(1): 9. Available: http://www.consecol.org/vol6/iss1/art9. Accessed 28 February 2013.
74. Van Wieren J, Broadfoot J, Gonzales E (2008) St. Lawrence Islands National Park hyperabundant deer management plan. Mallorytown: Parks Canada. 25 p.
75. Ginsberg HS, Zhioua E (1996) Nymphal survival and habitat distribution of Ixodes scapularis and Amblyomma americanum ticks (Acari: Ixodidae) on Fire Island, New York, USA. Exp Appl Acarol 20: 533-544.
76. Guerra M, Walker E, Jones C, Paskewitz S, Cortinas MR, et al. (2002) Predicting the risk of Lyme disease: Habitat suitability for Ixodes scapularis in the north central United States. Emerg Infect Dis 8: 289-297. (Pubitemid 34266267)
77. Tälleklint L, Jaenson TGT (1996) Relationship between Ixodes ricinus density and prevalence of infection with Borrelia-like spirochetes and density of infected ticks. J Med Entomol 33: 805-811. (Pubitemid 126429452)
78. Gray JS, Kahl O, Robertson JN, Daniel M, Estrada-Peña A, et al. (1998) Lyme borreliosis habitat assessment. Zentralbl Bakteriol 287: 211-228. (Pubitemid 28202521)
79. Randolph SE, Dobson AD (2012) Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology 139: 847-63.
80. Swei A, Ostfeld RS, Lane RS, Briggs CJ (2011) Impact of the experimental removal of lizards on Lyme disease risk. Proc Biol Sci 278: 2960-2978.