Association between body size and reservoir competence of mammals bearing Borrelia burgdorferi at an endemic site in the northeastern United States

Abstract

Background: The reservoirs for the Lyme disease agent, Borrelia burgdorferi, are dominated by several different small to medium sized mammals in eastern North America.

Findings: To experimentally assess the competence of different mammalian species to transmit this pathogen to ticks, we carried out quantitative species-specific PCR of individual nymphal Ixodes scapularis ticks, which had been collected as replete larvae from animals captured at a field site in eastern Connecticut and then allowed to molt in the laboratory. The mammals, in order of increasing body mass, were the white-footed mouse, pine vole, eastern chipmunk, gray squirrel, Virginia opossum, striped skunk, and common raccoon. The prevalence of infection in the nymphs and the counts of spirochetes in infected ticks allometrically scaled with body mass with exponents of -0.28 and -0.29, respectively. By species, the captured animals from the site differed significantly in the mean counts of spirochetes in the ticks recovered from them, but these associations could not be distinguished from an effect of body size per se.

Conclusions: These empirical findings as well as inferences from modeling suggest that small mammals on the basis of their sizes are more competent as reservoirs of B. burgdorferi in this environment than medium-to large-sized mammals.

Fig. 1

Box-whisker plots and regression of normalized B. burgdorferi cells per individual tick and body mass for seven Connecticut mammalian species from which larval ticks were collected after feeding and allowed to molt. Infection and bacterial counts were determined by quantitative PCR. In order of increasing size these were the white-footed mouse (n = 14), pine vole (n = 3), eastern chipmunk (n = 3), gray squirrel (n = 4), Virginia opossum (n = 4), striped skunk (n = 1), and common raccoon (n = 3). Each horizontal box indicates the first and third quartiles, and the indentation inside the box is the median. The 1.5× interquartile range is indicated by the horizontal line (whiskers) bisecting the box, and a value outside this range is indicated by an asterisk. The coefficient of determination (R ²), F statistic, and 2-tailed p value are shown

Fig. 2

Log-log regression of mean nymphal infection prevalence on body mass in nine New York mammalian species from which larval ticks and were collected after feeding and allowed to molt. The data are from Table two of reference [10]. Infection was determined by immunofluorescence assay. The species were common shrew (CS), white-footed mouse (M), short-tailed shrew (SS), eastern chipmunk (C), gray squirrel (GS), Virginia opossum (O), striped skunk (S), common raccoon (R), and white-tailed deer (D). The 95 % confidence limits for the regression, the coefficient of determination (R ²), F statistic, and 2-tailed p value are shown

Fig. 3

Discrete deterministic model of time in days to reach 10⁵ cells per gram (g) of body mass from start of infection of animals of different masses and for different in vivo growth rates (doubling time) for a bacterial pathogen that equally infectious for all tissues. See text for the description of the model. The body masses correspond to the masses of the species presented in Fig. 1