The role of southern red-backed voles, Myodes gapperi, and Peromyscus mice in the enzootic maintenance of Lyme disease spirochetes in North Dakota, USA

Abstract

Lyme disease has expanded into the Great Plains of the USA. To investigate local enzootic transmission, small mammals were trapped in two forested tracts in northeastern North Dakota during 2012 and 2013. Peromyscus mice and southern red-backed voles, Myodes gapperi, comprised over 90% of all mammals captured. One site was dominated by Peromyscus (79% of 100 mammals captured). At the other site, M. gapperi (59% of 107 mammals captured) was more abundant than Peromyscus (36%). Immature stages of two tick species parasitized small mammals: Dermacentor variabilis and Ixodes scapularis. Larval I. scapularis ectoparasitism was significantly higher on Peromyscus (81% infested; 3.7 larvae per infested mouse) than M. gapperi (47% infested; 2.6 larvae per infested vole) whereas larval and nymphal D. variabilis ectoparasitism were highest on M. gapperi. Over 45% of infested rodents were concurrently infested with both tick species. Testing engorged I. scapularis larvae from Peromyscus (n = 66) and M. gapperi (n = 20) yielded xenopositivity prevalence for Borrelia burgdorferi sensu lato (s.l.) in these rodents of 6% and 5%, respectively. Progeny of field collected M. gapperi were used to determine host infectivity for a local isolate of B. burgdorferi sensu stricto (s.s.). Five M. gapperi were injected with spirochetes, infested with pathogen-free I. scapularis larvae on days 10, 20, and 40 after infection, and engorged larvae molted to nymphs. Subsamples of nymphs were tested by PCR for B. burgdorferi s. s. DNA and yielded infection rates of 56% (n = 100 nymphs tested), 75% (n = 8) and 64% (n = 31), respectively. The remaining infected nymphs were fed on BALB/c Mus musculus mice and 7 d later, mice were euthanized, and tissues were cultured for B. burgdorferi s.s. Nymphs successfully transmitted spirochetes to 13 of 18 (72%) mice that were exposed to 1-5 infected ticks. Theoretical reservoir potentials - i.e., ability to generate B. burgdorferi infected nymphs - were compared between Peromyscus and M. gapperi. At one site, Peromyscus accounted for nearly all Borrelia-infected nymphs produced (reservoir potential value of 0.935). At the other site, the reservoir potentials for Peromyscus (0.566) and M. gapperi (0.434) were comparable. The difference was attributed to differences in the relative abundance of voles versus mice between sites and the higher level of ectoparasitism by larval I. scapularis on Peromyscus versus M. gapperi at both sites. The southern red-backed vole, M. gapperi, contributes to the enzootic maintenance of Lyme disease spirochetes in North Dakota and possibly other areas where this rodent species is abundant.

Keywords: Dermacentor variabilis; Ixodes scapularis; Lyme disease; Myodes gapperi; Peromyscus; Reservoir potential.

Fig. 1.

Geographic distributions of the red backed vole, Myodes gapperi (Naughton 2012), Peromyscus leucopus, P. maniculatus (Machtinger and Williams 2020) and estimated Lyme disease prevalence in companion animals (Companion Animal Parasite Council).

Fig. 2.

Species composition of small mammals trapped at Forest River Biological Station (n = 107) and Turtle River State Park (n = 100), Grand Forks County, ND, USA, 2012 and 2013. Within each collection site, histograms having the same letter do not differ significantly from one another at the 0.05 level.

Fig. 3.

Summary of tick infestations on Peromyscus spp. and Myodes gapperi in Grand Forks County, North Dakota USA, where rodents were parasitized with either a single tick species or two tick species concurrently (=dual infestation). Pie charts show the proportion of tick life stages; where black represents larval infestations, gray represents nymphal infestations, and white represents infestations of both larvae and nymphs. The size of a pie chart is relative to the numbers of rodents collected in that category. Data are for both sites (Forest River Biological Station and Turtle River State Park) and years (2012 and 2013) combined.

Fig 4.

Phenology of larval tick ectoparasitism on Myodes gapperi and Peromyscus spp. rodents, where N = number of rodents examined. Data are for both sites and years combined, Grand Forks County, North Dakota, USA, 2012–2013.

Fig. 5.

Average number of engorged larval ticks produced per mouse following experimental co-infestation of Peromyscus leucopus mice with 20 Ixodes scapularis larvae and 20 Dermacentor variabilis larvae. Error bars signify 95% confidence limits, N=number of P. leucopus co-infested.