Host-pathogen associations inferred from bloodmeal analyses of Ixodes scapularis ticks in a low biodiversity setting

Abstract

Tick-borne pathogen emergence is dependent on the abundance and distribution of competent hosts in the environment. Ixodes scapularis ticks are generalist feeders, and their pathogen infection prevalence depends on their relative feeding on local competent and non-competent hosts. The ability to determine what host a larval life stage tick fed on can help predict infection prevalence, emergence, and spread of certain tick-borne pathogens and the risks posed to public health. Here, we use a newly developed genomic target-based technique to detect the source of larval bloodmeals by sampling questing nymphs from Block Island, RI, a small island with a depauperate mammalian community. We used previously designed specific assays to target all known hosts on this island and analyzed ticks for four human pathogenic tick-borne pathogens. We determined the highest proportion of larvae fed on avian species (42.34%), white-footed mice (36.94%), and white-tailed deer (20.72%) and occasionally fed on feral cats, rats, and voles, which are in low abundance on Block Island. Additionally, larvae that had fed on white-footed mice were significantly more likely to be infected with Borrelia burgdorferi and Babesia microti, while larvae that had fed on white-footed mice or white-tailed deer were significantly more likely to be infected with, respectively, mouse- and deer-associated genotypes of Anaplasma phagocytophilum. The ability to detect a nymph's larval host allows for a better understanding of tick feeding behavior, host distribution, pathogen prevalence, and zoonotic risks to humans, which can contribute to better tick management strategies.

Importance: Tick-borne diseases, such as Lyme disease, babesiosis, and anaplasmosis, pose significant public health burdens. Tick bloodmeal analysis provides a noninvasive sampling method to evaluate tick-host associations and combined with a zoonotic pathogen assay, can generate crucial insights into the epidemiology and transmission of tick-borne diseases by identifying potential key maintenance hosts. We investigated the bloodmeals of questing Ixodes scapularis nymphs. We found that avian hosts, white-footed mice, and white-tailed deer fed the majority of larval ticks and differentially contributed to the prevalence of multiple tick-borne pathogens and pathogen genotypes in a low biodiversity island setting. Unraveling the intricate network of host-vector-pathogen interactions will contribute to improving wildlife management and conservation efforts, to developing targeted surveillance, and vector and host control efforts, ultimately reducing the incidence of tick-borne diseases and improving public health.

Keywords: Anaplasma; Babesia; Borrelia; avian; lyme disease; white-footed mouse; white-tailed deer.

Fig 1

Proportion of hosts (number of specific host types/total hosts at a specific collection site) fed on by Ixodes scapularis larvae as determined using bloodmeal analysis from questing nymphs at each of the seven collection sites. Significant differences among host types and collection sites were calculated using Fisher exact tests and then post hoc pairwise comparisons between each host type. Colored lines/brackets correspond to significant differences observed between a host type at the indicated collection site, and asterisks denote the level of significant differences (*P ≤ 0.05, **P ≤ 0.01).

Fig 2

Pathogen infection prevalence of each pathogen at each collection site from questing Ixodes scapularis nymphs from Block Island, RI. Significant differences among pathogen infection prevalence and collection sites were calculated using Fisher exact tests and then post hoc pairwise comparisons between each pathogen at each collection site. Bars indicate 95% confidence limits, and colored brackets and asterisks denote significant differences between specific pathogens at different collection sites (*P ≤ 0.05).

Fig 3

Odds ratios (Log₁₀scale) and range of the three most common inferred host species and undermined hosts (und) infected with each pathogen (excluding Borrelia miyamotoi). No bird species in this study were positive for human pathogenic Babesia microti. A Mantel-Haenszel chi-square odds ratio test was used to determine the degree of association of the most abundant pathogen types among each of the most prevalent host types. Bars signify the 95% confidence limits.

Fig 4

Anaplasma phagocytophilum human pathogenic (Ap-ha) and nonpathogenic “deer” variant 1 (Ap-V1) variant types based on host type (A) and collection site (B). Significant differences between the variant types for each host type and site were assessed using Fisher exact tests and then post hoc pairwise and row-wise comparisons (*P ≤ 0.05). Bars signify 95% confidence limits, solid black brackets denote Ap-ha comparisons, solid gray brackets denote Ap-V1 comparisons, and dashed brackets denote comparisons between Ap-ha and Ap-V1 within the same host type.