Wildlife reservoirs and sentinels for vector-borne zoonoses in northern Canada
Warming temperatures continue to impact arthropod diversity, density, and distribution in the Canadian Arctic. Consequently, arboviruses and other pathogens that rely on vector transmission have become a growing wildlife and public health concern. As the western Arctic is the most rapidly warming region of Canada and indeed the globe (along with Antarctica), it is imperative to obtain baselines and detect changes in the distribution of vector-borne pathogens, potential reservoirs, and pathogenesis in wildlife hosts. In this thesis, we characterize the prevalence of three groups of vector-borne pathogens in northern Canadian wildlife (California serogroup viruses (CSV), Bartonella spp. and Francisella tularensis bacteria). We also reveal aspects of the disease ecology for these viruses and bacteria, including potential reservoirs and transmission mechanisms. First, we completed a large-scale survey of wildlife in northern Canada for exposure to CSV. Antibodies were detected in all large mammals, including caribou (63%), arctic fox (4%), red fox (12%), and polar bear (28%), and associations with climate and biological factors were identified for polar bears. Both summer air temperatures and sex were significantly correlated with CSV exposure, indicating that climate warming and movement from sea ice onto land increased exposure to CSV in polar bears. Seroprevalence identified in caribou herds from Nunavut (80%) and Northwest Territories (83%) raised questions about their role as a potential reservoir species for Jamestown Canyon virus (JCV), the CSV that is established in cervids in temperate regions of North America. This led to work with captive reindeer (Rangifer tarandus) at the University of Alaska Fairbanks. We determined that reindeer in this herd (housed outdoors) are exposed to CSV under natural conditions, with almost all animals naturally exposed after 2 summers of life. Experimental exposure of naïve and low titre reindeer to JCV demonstrated that they become viremic for up to five days with no observable symptoms, thus serving as reservoirs for JCV and potentially suitable amplifying hosts for mosquitoes. Second, we characterized the diversity of Bartonella communities in rodent reservoirs and revealed a complex web of Bartonella transmission between arctic foxes and their prey species, including rodents and migratory Ross’s and lesser snow geese in the central Canadian Arctic. Most importantly, we found that Bartonella transmission to foxes may occur via nest fleas during nest predation, emphasizing the role of migratory birds as transporters of invertebrate vectors and their pathogens. During this project, we also observed, for the first time, abnormal fur loss on arctic foxes in this population and identified a novel cryptic species of lice that carry an uncharacterized species of Baronella. Finally, we determined exposure of resident arctic foxes at Karrak Lake, Nunavut over the past decade to Francisella tularensis. Antibodies to F. tularensis were correlated with rodent abundance and climate factors associated with rodent survival (spring temperatures, spring snow cover and average summer precipitation), indicating that rodents play an important role in transmission in northern Canada and that young foxes are ideal sentinels for annual transmission risk due to their role as scavengers and predators. The Arctic is not generally considered a hotbed of vector-borne disease, and our work on CSV demonstrates that this is a naïve assumption, with caribou serving as a heavily exposed and potentially asymptomatic reservoir, and that exposure of polar bears may be increasing as they spend more time on land. Our work on Bartonella demonstrates the importance of massive seasonal migrations of birds in introducing temperate species of these intracellular bacteria into transmission of endemic species between rodents (their normal reservoirs) and arctic fox. Our reporting that a newly documented species of fox lice (not a recent introduction of dog lice) is causing fur loss and pelt damage to arctic fox has significance for management and for better understanding the phylogenetic relationships of these highly host specific ectoparasites. And finally, our work on tularemia demonstrates the utility of long-term wildlife health monitoring to better understand the role of native Arctic species in the transmission dynamics of these zoonotic pathogens above the tree line. Together, this thesis reveals a narrative of disease ecology current with climatic changes in one of the most dynamic and remote regions on Earth, where close relationships with wildlife and the land are ecologically and culturally significant.
Wildlife, Vector-borne disease, Bartonella, California serogroup viruses, Francisella tularensis, tularemia, arboviruses, climate change, Arctic, zoonoses
Doctor of Philosophy (Ph.D.)