Ectoparasite Ecology and Disease Exposure in Black-Footed Ferrets (Mustela nigripes) and Associated Mammals in Conata Basin/Badlands National Park, South Dakota

Abstract

The black-footed ferret (Mustela nigripes; ferret), one of North America’s most endangered mammals, persists within prairie dog (Cynomys spp.) burrow systems where disease remains a major obstacle to their recovery. While plague (Yersinia pestis) is well recognized as a primary threat, tularemia, a bacterial disease caused by Francisella tularensis and vectored by ticks and other ectoparasites, also occurs in grassland ecosystems. However, ferrets appear capable of surviving tularemia infection, although the ecological drivers, biological impact, and vector pathways involved in exposure remain unknown. Our objective was to determine variables that explain ferret exposure to tularemia over time, evaluate ectoparasites found on ferrets and their prey, and determine the role of ectoparasites in pathogen transmission to ferrets. We found two mite species on black-footed ferrets that are not parasitic or of pathogenic concern. Serological analyses indicated that 6.3% of ferret serum samples (81/1277) were seropositive for tularemia between 2002-2024. Ferrets recaptured within 5-12 months showed changes in serostatus, indicating that antibodies do not persist long-term. We identified Ixodes sculptus and Ixodes kingi on ferrets as well as on grasshopper mice (Onychomys leucogaster), Peromyscus spp., and several other small mammals. A total of 304 (91.4%) ferrets and 173 (27%) small mammals carried at least one tick, and grasshopper mice were more often parasitized (54%) than other small mammal species. Adult I. sculptus and I. kingi are common on ferrets, whereas small mammals primarily carried larval and nymphal life stages. Unlike many Ixodes spp. that quest above ground on vegetation, these ticks appear to be nidicolous, remaining within burrow systems, where ferrets and their prey interact, for one or more of their life stages,. Standard surface-based sampling techniques for ticks were ineffective for detecting Ixodes spp. in prairie dog colonies. Additionally, no ticks or fleas collected from seropositive ferrets were positive for F. tularensis DNA via PCR analysis. Tularemia periodically emerges and re-emerges in grassland ecosystems, and black-footed ferrets can seroconvert and survive infection. Their antibody responses appear to be short-lived despite repeated exposure and the relationship between these antibodies and pathogen memory remains unknown. Although ticks, mites, and fleas are common on ferrets, none of the ticks collected from seropositive individuals tested PCR-positive for Francisella tularensis, suggesting that the specific ticks sampled are unlikely vectors, though transmission could have occurred from ticks that detached prior to surveillance. As a result, experimental vector-competency testing for Ixodes kingi and I. sculptus remains warranted. These Ixodes species occur primarily within prairie dog burrows and on vertebrate hosts rather than on the prairie surface, indicating that effective surveillance should prioritize belowground sampling and host-based collections instead of conventional surface methods. Overall, tularemia is likely not a significant conservation concern for black-footed ferret populations, but continued research into tularemia ecology and vector dynamics is needed.