High burdens of Ixodes scapularis larval ticks on white-tailed deer may limit Lyme disease risk in a low biodiversity setting

Abstract

An inverse relationship between biodiversity and human health has been termed the ‘dilution effect’ paradigm. In the case of tick-borne infections such as Lyme disease, the key assumption is that Borrelia burgdorferi sensu lato abundance is increased by the loss of less competent (dilution) hosts as biodiversity declines. White-tailed deer play a dual role in the pathogen cycle, as key reproductive hosts for adult ticks and incompetent hosts for the pathogen. While the role of deer as hosts of adult ticks is well established, the extent to which deer also feed immature ticks and reduce the proportion infected is unknown because of logistic constraints in measuring this empirically. We estimated the proportion of larvae that fed on deer in an extremely species-poor community on Block Island, RI, where tick nymphal infection prevalence was found to be lower than expected. In 2014, we measured the density, larval tick burdens, and realized reservoir competence of small mammal and bird hosts on Block Island, RI. In 2015, we measured the infection prevalence of host-seeking Ixodes scapularis nymphs resulting from larvae fed on available hosts in 2014. We back-estimated the proportion of larvae expected to have fed on deer in 2014 (the only unknown parameter) to result in the nymphal infection prevalence observed in 2015. Back-estimation predicted that 29% of larval ticks must have fed on deer to yield the observed 30% nymphal infection prevalence. In comparison, the proportion of larvae feeding on mice was 44% and 27% on birds. Our study identified an influential role of deer in reducing nymphal tick infection prevalence and a potential role as dilution hosts if the reduction in nymphal infection prevalence outweighs the role of deer as tick population amplifiers. Because both deer and competent hosts may increase in anthropogenic, fragmented habitats, the links between fragmentation, biodiversity, and Lyme disease risk may be complex and difficult to predict. Furthermore, a nonlinear relationship between deer abundance and Lyme disease risk would reduce the efficacy of deer population reduction efforts to control Lyme disease.