Western gray squirrel (Rodentia: Sciuridae): A primary reservoir host of Borrelia burgdorferi in Californian oak woodlands?

Journal of Medical Entomology

Volumn 42, Issue 3, 2005, Pages 388-396

  Lane, Robert S ^a   Mun, Jeomhee ^a   Eisen, Rebecca J ^a   Eisen, Lars ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anaplasma phagocytophilum; Borrelia burgdorferi; Dermacentor occidentalis; Ixodes pacificus; Sciurus griseus

Indexed keywords

ACARI; ANAPLASMA; ANAPLASMA PHAGOCYTOPHILUM; ARTHROPODA; AVES; BORRELIA; BORRELIA BISSETTII; BORRELIA BURGDORFERI; DERMACENTOR; DERMACENTOR OCCIDENTALIS; DIPODOMYS; IXODES PACIFICUS; IXODES SCAPULARIS; MACROPUS SP.; MAMMALIA; NEOTOMA; QUERCUS; RICKETTSIA; RODENTIA; SCIURIDAE; SCIURUS CAROLINENSIS; SCIURUS GRISEUS; SPIROCHAETALES; VERTEBRATA;

EID: 19444374637     PISSN: 00222585     EISSN: None     Source Type: Journal    
DOI: 10.1093/jmedent/42.3.388     Document Type: Article

References (68)

1. Brown, R. N., and R. S. Lane. 1992. Lyme disease in California: a novel enzootic transmission cycle of Borrelia burgdorferi. Science (Wash. DC) 256: 1439-1442.
2. Brown, R. N., and R. S. Lane. 1996. Reservoir competence of four chaparral-dwelling rodents for Borrelia burgdorferi in California. Am. J. Trop. Med. Hyg. 54: 84-91.
3. Burgdorfer, W., R. S. Lane, A. G. Barbour, R. A. Gresbrink, and J. R. Anderson. 1985. The western black-legged tick, Ixodes pacificus: a vector of Borrelia burgdorferi. Am. J. Trop. Med. Hyg. 34: 925-930.
4. Carey, A. B., W. L. Krinsky, and A. J. Main. 1980. Ixodes dammini (Acari: Ixodidae) and associated ixodid ticks in south-central Connecticut, USA. J. Med. Entomol. 17: 89-99.
5. Carraway, L. N., and B. J. Verts. 1994. Sciurus griseus, pp. 1-7. In Mammalian species. No. 474. American Society of Mammalogists, Lawrence, KS.
6. Castro, M. B., W. L. Nicholson, V. L. Kramer, and J. E. Childs. 2001. Persistent infection in Neotoma fuscipes (Muridae: Sigmodontinae) with Ehrlichia phagocytophila sensu lato. Am. J. Trop. Med. Hyg. 65: 261-267.
7. Clover, J. R., and R. S. Lane. 1995. Evidence implicating nymphal Ixodes pacificus (Acari: Ixodidae) in the epidemiology of Lyme disease in California. Am. J. Trop. Med. Hyg. 53: 237-240.
8. Craine, N. G., S. E. Randolph, and P. A. Nuttall. 1995. Seasonal variation in the role of grey squirrels as hosts of Ixodes ricinus, the tick vector of the Lyme disease spirochaete, in a British woodland. Folia Parasitol. 42: 73-80.
9. Craine, N. G., P. A. Nuttall, A. C. Marriott, and S. E. Randolph. 1997. Role of grey squirrels and pheasants in the transmission of Borrelia burgdorferi sensu lato, the Lyme disease spirochaete, in the U.K. Folia Parasitol. 44: 155-160.
10. Cross, S. P. 1969. Behavioral aspects of western gray squirrel ecology. Ph.D. dissertation, University of Arizona, Tucson.
11. DeFoliart, G. R., P. R. Grimstad, and D. M. Watts. 1987. Advances in mosquito-borne arbovirus/vector research. Annu. Rev. Entomol. 32: 479-505.
12. Eisen, R. J., L. Eisen, and R. S. Lane. 2001. Prevalence and abundance of Ixodes pacificus immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occidentals) in northern California: temporal trends and environmental correlates. J. Parasitol. 87: 1301-1307.
13. Eisen, L., R. J. Eisen, and R. S. Lane. 2002. Seasonal activity patterns of Ixodes pacificus nymphs in relation to climatic conditions. Med. Vet. Entomol. 26: 235-244.
14. Eisen, L., M. C. Dolan, J. Piesman, and R. S. Lane. 2003a. Vector competence of Ixodes pacificus and I. spinipalpis (Acari: Ixodidae), and reservoir competence of the dusky-footed woodrat (Neotoma fuscipes) and the deer mouse (Peromyscus maniculatus), for Borrelia bissettii. J. Med. Entomol. 40: 311-320.
15. Eisen, R. J., L. Eisen, M. B. Castro, and R. S. Lane. 2003b. Environmentally related variability in risk of exposure to Lyme disease spirochetes in northern California: effect of climatic conditions and habitat type. Environ. Entomol. 32: 1010-1018.
16. Eisen, L., R. J. Eisen, C.-C. Chang, J. Mun, and R. S. Lane. 2004a. Acarologic risk of exposure to Borrelia burgdorferi spirochaetes: long-term evaluations in north-western California, with implications for Lyme borreliosis risk-assessment models. Med. Vet. Entomol. 18: 38-49.
17. Eisen, L., R. J. Eisen, and R. S. Lane. 2004b. The roles of birds, lizards, and rodents as hosts for the western black-legged tick, Ixodes pacificus. J. Vector Ecol. 29: 295-308.
18. Eisen, R. J., L. Eisen, and R. S. Lane. 2004c. Habitat-related variation in infestation of lizards and rodents with Ixodes ticks in dense woodlands in Mendocino County, California. Exp. Appl. Acarol. 33: 215-233.
19. Falco, R. C., D. Fish, and J. Piesman. 1996. Duration of tick bites in a Lyme disease-endemic area. Am. J. Epidemiol. 143: 187-192.
20. Fish, D., and R. C. Dowler. 1989. Host associations of ticks (Acari: Ixodidae) parasitizing medium-sized mammals in a Lyme disease endemic area of southern New York. J. Med. Entomol. 26: 200-209.
21. Foley, J. E., P. Foley, R. N. Brown, R. S. Lane, J. S. Dumler, and J. E. Madigan. 2004. Ecology of Anaplasma phagoeytophilum and Borrelia burgdorferi in the western United States. J. Vector Ecol. 29: 41-50.
22. Fritz, C. L., A. M. Kjemtrup, P. A. Conrad, G. R. Flores, G. L. Campbell, M. E. Schriefer, D. Gallo, and D. J. Vugia. 1997. Seroepidemiology of emerging tickborne infectious diseases in a northern California community. J. Infect. Dis. 175: 1432-1439.
23. Furman, D. P., and E. C. Loomis. 1984. The ticks of California (Acari: Ixodida). Bull. Calif. Insect Surv. 25: 1-239.
24. Godsey, Jr., M. S., T. E. Amundson, E. C. Burgess, W. Schell, J. P. Davis, R. Kaslow, and R. Edelman. 1987. Lyme disease ecology in Wisconsin: distribution and host preferences of Ixodes dammini, and prevalence of antibody to Borrelia burgdorferi in small mammals. Am. J. Trop. Med. Hyg. 37: 180-187.
25. Gordus, A. G., and J. H. Theis. 1993. Isolation of Borrelia burgdorferi from the blood of a bushy-tailed wood rat in California. J. Wildl. Dis. 29: 478-480.
26. Holden, K., J. T. Boothby, S. Anand, and R. F. Massung. 2003. Detection of Borrelia burgdorferi, Ehrlichia chaffeensis, and Anaplasma phagocytophilum in ticks (Acari: Ixodidae) from a coastal region of California. J. Med. Entomol. 40: 534-539.
27. Humair, P.-F., and L. Gern. 1998. Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Trop. 69: 213-227.
28. Ingles, L. G. 1947. Ecology and life history of the California gray squirrel. Calif. Fish Game 33: 139-158.
29. Jameson, E. W., Jr., and H. J. Peeters. 2004. Mammals of California. University of California Press, Berkeley, CA.
30. Kahl, O., L. Gern, L. Eisen, and R. S. Lane. 2002. Ecological research on Borrelia burgdorferi sensu lato: terminology and some methodological pitfalls, pp. 29-46. In J. S. Gray, O. Kahl, R. S. Lane, and G. Stanek [eds.], Lyme borreliosis: biology, epidemiology and control. CABI Publishing, Wallingford, United Kingdom.
31. Kohls, G. M. 1937. Hosts of the immature stages of the Pacific Coast tick Dermacentor occidentalis Neum. (Ixodidae). Public Health Rep. 52: 490-496.
32. Lane, R. S. 1990. Infection of deer mice and piñon mice (Peromyscus spp.) with spirochetes at a focus of Lyme borreliosis in northern California, U.S.A. Bull. Soc. Vector Ecol. 15: 25-32.
33. Lane, R. S. 1994. Competence of ticks as vectors of microbial agents with an emphasis on Borrelia burgdorferi, pp. 45-67. In D. E. Sonenshine and T. N. Mather [eds.], Ecological dynamics of tick-borne zoonoses. Oxford University Press, New York.
34. Lane, R. S. 1996. Risk of human exposure to vector ticks (Acari: Ixodidae) in a heavily used recreational area in northern California. Am. J. Trop. Med. Hyg. 55: 165-173.
35. Lane, R. S., and R. N. Brown. 1991. Wood rats and kangaroo rats: potential reservoirs of the Lyme disease spirochete in California. J. Med. Entomol. 28: 299-302.
36. Lane, R. S., and W. Burgdorfer. 1986. Potential role of native and exotic deer and their associated ticks (Acari: Ixodidae) in the ecology of Lyme disease in California, USA. Zentralbl. Bakteriol., Mikrobiol. Hyg. Ser. A. 263: 55-64.
37. Lane, R. S., and W. Burgdorfer. 1987. Transovarial and transstadial passage of Borrelia burgdorferi in the western black-legged tick, Ixodes pacificus (Acari: Ixodidae). Am. J. Trop. Med. Hyg. 37: 188-192.
38. Lane, R. S., and W. Burgdorfer. 1988. Spirochetes in mammals and ticks (Acari: Ixodidae) from a focus of Lyme borreliosis in California. J. Wildl. Dis. 24: 1-9.
39. Lane, R. S., and P. E. Lavoie. 1988. Lyme borreliosis in California: acarological, clinical, and epidemiological studies. Ann. N.Y. Acad. Sci. 539: 192-203.
40. Lane, R. S., and J.E. Loye. 1991. Lyme disease in California: interrelationship of ixodid ticks (Acari), rodents, and Borrelia burgdorferi. J. Med. Entomol. 28: 719-725.
41. Lane, R. S., S. A. Manweiler, H. A. Stubbs, E. T. Lennette, J. E. Madigan, and P. E. Lavoie. 1992. Risk factors for Lyme disease in a small rural community in northern California. Am. J. Epidemiol. 136: 1358-1368.
42. Lane, R. S., R. N. Brown, J. Piesman, and C. A. Peavey. 1994. Vector competence of Ixodes pacificus and Dermacentor occidentalis (Acari: Ixodidae) for various isolates of Lyme disease spirochetes. J. Med. Entomol. 31: 417-424.
43. Lane, R. S., L. E. Casher, C. A. Peavey, and J. Piesman. 1998. Modified bait tube controls disease-carrying ticks and fleas. Calif. Agric. 52(2): 43-47.
44. Lane, R. S., C. A. Peavey, K. A. Padgett, and M. Hendson. 1999. Life history of Ixodes (Ixodes) jellisoni (Acari: Ixodidae) and its vector competence for Borrelia burgdorferi sensu lato. J. Med. Entomol. 36: 329-340.
45. Lane, R. S., J. E. Foley, L. Eisen, E. T. Lennette, and M. A. Peot. 2001. Acarologic risk of exposure to emerging tick-borne bacterial pathogens in a semirural community in northern California. Vector Borne Zoonotic Dis. 1: 197-210.
46. Lane, R. S., D. B. Steinlein, and J. Mun. 2004. Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest. J. Med. Entomol. 41: 239-248.
47. Levin, M. L., W. L. Nicholson, R. F. Massung, J. W. Sumner, and D. Fish. 2002. Comparison of the reservoir competence of medium-sized mammals and Peromyscus leucopus for Anaplasma phagocytophilum in Connecticut. Vector Borne Zoonotic Dis. 2: 125-136.
48. LoGiudice, K., R. S. Ostfeld, K. A. Schmidt, and F. Keesing. 2003. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Natl. Acad. Sci. USA 100: 567-571.
49. MacLeod, J., and W. S. Gordon. 1933. Studies in tick-borne fever of sheep. I. Transmission by the tick, Ixodes ricinus, with a description of the disease produced. Parasitology 25: 273-283.
50. Magnarelli, L. A., J. F. Anderson, W. Burgdorfer, and W. A. Chappell. 1984. Parasitism by Ixodes dammini (Acari: Ixodidae) and antibodies to spirochetes in mammals at Lyme disease foci in Connecticut, USA. J. Med. Entomol. 21: 52-57.
51. Main, A. J., A. B. Carey, M. G. Carey, and R. H. Goodwin. 1982. Immature Ixodes dammini (Acari: Ixodidae) on small animals in Connecticut, USA. J. Med. Entomol. 19: 655-664.
52. Mannelli, A., U. Kitron, C. J. Jones, and T. L. Slajchert. 1993. Ixodes dammini (Acari: Ixodidae) infestation on medium-sized mammals and blue jays in northwestern Illinois. J. Med. Entomol. 30: 950-952.
53. Massung, R. F., K. Slater, J. H. Owens, W. L. Nicholson, T. N. Mather, V. B. Solberg, and J. G. Olson. 1998. Nested PCR assay for detection of granulocytic ehrlichiae. J. Clin. Microbiol. 36: 1090-1095.
54. Nicholson, W. L., S. Muir, J. W. Sumner, and J. E. Childs. 1998. Serologic evidence of infection with Ehrlichia spp. in wild rodents (Muridae: Sigmodontinae) in the United States. J. Clin. Microbiol. 36: 695-700.
55. Nicholson, W. L., M. B. Castro, V. L. Kramer, J. W. Sumner, and J. E. Childs. 1999. Dusky-footed wood rats (Neotoma fuscipes) as reservoirs of granulocytic ehrlichiae (Rickettsiales: Ehrlichieae) in northern California. J. Clin. Microbiol. 37: 3323-3327.
56. Ogden, N. H., K. Bown, B. K. Horrocks, Z. Woldehiwet, and M. Bennett. 1998. Granulocytic Ehrlichia infection in ixodid ticks and mammals in woodlands and uplands of the U.K. Med. Vet. Entomol. 12: 423-429.
57. Oteo, J. A., H. Gil, M. Barrai, A. Pérez, S. Jimenez, J. R. Blanco, V. Martinez de Artola, A. García-Pérez, and R. A. Juste. 2001. Presence of granulocytic ehrlichia in ticks and serological evidence of human infection in La Rioja, Spain. Epidemiol. Infect. 127: 353-358.
58. Peavey, C. A., and R. S. Lane. 1995. Transmission of Borrelia burgdorferi by Ixodes pacificus nymphs and reservoir competence of deer mice (Peromyscus maniculatus) infected by tick-bite. J. Parasitol. 81: 175-178.
59. Peavey, C. A., R. S. Lane, and J. E. Kleinjan. 1997. Role of small mammals in the ecology of Borrelia burgdorferi in a peri-urban park in north coastal California. Exp. Appl. Acarol. 21: 569-584.
60. Piesman, J. 1991. Experimental acquisition of the Lyme disease spirochete, Borrelia burgdorferi, by larval Ixodes dammini (Acari: Ixodidae) during partial blood meals. J. Med. Entomol. 28: 259-262.
61. Ross, R. C. 1930. California Sciuridae in captivity. J. Mammal. 11: 76-78.
62. Schoeler, G. B., and R. S. Lane. 1993. Efficiency of transovarial transmission of the Lyme disease spirochete, Borrelia burgdorferi, in the western blacklegged tick, Ixodes pacificus (Acari: Ixodidae). J. Med. Entomol. 30: 80-86.
63. Schulze, T. L., G. S. Bowen, M. F. Lakat, W. E. Parkin, and J. K. Shisler. 1986. Seasonal abundance and hosts of Ixodes dammini (Acari: Ixodidae) and other ixodid ticks from an endemic Lyme disease focus in New Jersey, USA. J. Med. Entomol. 23: 105-109.
64. Tälleklint-Eisen, L., and R. S. Lane. 1999. Variation in the density of questing Ixodes pacificus (Acari: Ixodidae) nymphs infected with Borrelia burgdorferi at different spatial scales in California. J. Parasitol. 85: 824-831.
65. Tälleklint-Eisen, L., and R. S. Lane. 2000. Spatial and temporal variation in the density of Ixodes pacificus (Acari: Ixodidae) nymphs. Environ. Entomol. 29: 272-280.
66. Vredevoe, L. K., J. R. Stevens, and B. S. Schneider. 2004. Detection and characterization of Borrelia bissettii in rodents from the central California coast. J. Med. Entomol. 41: 736-745.
67. Wright, S. A., M. A. Thompson, M. J. Miller, K. M. Knerl, S. L. Elms, J. C. Karpowicz, J. F. Young, and V. L. Kramer. 2000. Ecology of Borrelia burgdorferi in ticks (Acari: Ixodidae), rodents, and birds in the Sierra Nevada foothills, Placer County, California. J. Med. Entomol. 37: 909-918.
68. Yeh, M.-T., J. M. Bak, R. Hu, M. C. Nicholson, C. Kelly, and T. N. Mather. 1995. Determining the duration of Ixodes scapufaris (Acari: Ixodidae) attachment to tick-bite victims. J. Med. Entomol. 32: 853-858.