Multiple causes of variable tick burdens on small-mammal hosts

Blood meals by blacklegged ticks (Ixodes scapularis) on vertebrate hosts serve to transmit the agents of several zoonotic diseases, including Lyme disease, human babesiosis, and human granulocytic anaplasmosis, between host and tick. If ticks are aggregated on hosts, a small proportion of hosts may be responsible for most transmission events. Therefore, a key element in understanding and controlling the transmission of these pathogens is identifying the group(s) or individuals feeding a disproportionate number of ticks. Previous studies of tick burdens, however, have focused on differences in mean annual burdens between one or a few groups of hosts, ignoring both the strong seasonal dynamics of I. scapularis and their aggregation on hosts. We present a statistical modeling framework that predicts burdens on individual hosts throughout the year as a function of temporal-, site-, and individual-specific attributes, as well as the degree of aggregation in a negative binomial distribution. We then fit alternate versions of this model to an 11-year data set of I. scapularis burdens on white-footed mice (Peromyscus leucopus) and eastern chipmunks (Tamias striatus) to explore which factors are important to predicting tick burdens. We found that tick burdens are a complex function of many extrinsic and intrinsic factors, including seasonality. Specifically: (1) burdens on mice and chipmunks increased with densities of host-seeking ticks in a manner that suggests hosts become saturated. (2) Chipmunks draw larval ticks away from mice, which are efficient reservoirs of the Lyme disease bacterium, and mice draw nymphs away from chipmunks, which are key nymphal hosts. (3) While individual correlates were statistically important, the relationships were complex, and no group or correlate (sex, age, mass) could explain which hosts fed a disproportionate number of ticks. (4) Ticks were strongly aggregated on hosts within and across groups suggesting that some undiscovered quality of individual hosts was responsible for the aggregation. (5) Those individuals that fed more nymphs than expected, and are thus more likely to be infected with the Lyme disease agent, also tend to feed and infect more larvae than expected. Predicting which individuals those are is not yet possible.