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Tick-borne disease ecology in a changing world: The influence of climate, habitat and abiotic conditions, and forest disturbance on Lyme disease ecology and risk in California

  • Author(s): MacDonald, Andrew John
  • Advisor(s): Briggs, Cheryl J
  • et al.
Abstract

Globally, the rate of emergence of infectious diseases has increased significantly over time. Vector-borne diseases in particular present one of the biggest threats to public health globally. Many of these diseases are zoonotic in nature, meaning they cycle in animal populations but can spillover to infect humans. As such, risk to humans of acquiring a zoonotic disease depends in large part on the distribution and abundance of the reservoir hosts, the species of animals that the pathogen naturally infects, as well as of the vector species. The ecology of many reservoir hosts and vectors is rapidly changing due to ongoing environmental change, which will fundamentally alter human disease risk in the future. To understand how disease risk may be forecasted to change requires an understanding of the drivers of the distribution and abundance of pathogens, disease vectors and reservoir hosts.

This research uses Lyme disease in California as a model system to understand the drivers of zoonotic disease risk on a rapidly changing planet, particularly for vector-borne diseases. Specifically, it investigates the following questions: 1) are there latitudinal differences in the seasonal activity patterns of the primary tick vector, Ixodes pacificus, in California, and might these differences be driven by climate? 2) What abiotic and environmental factors drive tick abundance and infection prevalence with the causative agent of Lyme disease, Borrelia burgdorferi sensu stricto, in southern California? 3) What are the effects of large-scale, intense ecological disturbances, namely wildfire, on the ecology of Lyme disease in the far western US?

To address these questions, I use a combination of field, laboratory and statistical methods including field collection of samples (ticks and tissue samples from host animals), DNA extraction and polymerase chain reaction (PCR) in the laboratory for analysis of infection, and statistical and GIS-based analysis of field-derived and public data sets.

I find that tick vector activity patterns in southern California are highly truncated, and tick density is significantly lower than in northern California where human Lyme disease incidence is higher. This suggests much lower tick-borne disease risk in southern California, which I broadly attribute to the hotter, drier climate in this region. This has implications for reduced tick-borne disease risk under future climate change, in contrast with the predictions made for numerous other emerging diseases (Chapter 1). Additionally, I identify dense oak woodlands as the highest risk habitats for I. pacificus tick encounter in southern California. I also find densities of small vertebrate hosts to be significant predictors of tick abundance, though found a shift in the relative importance of host availability and habitat characteristics in predicting juvenile tick abundance as California’s historic drought intensified. This finding suggests that habitat providing suitable microclimates for tick survivorship became centrally important to patterns of abundance in the face of adverse abiotic conditions. This further suggests that predicted climate change in California may act as an important limiting factor on I. pacificus populations. And, despite the low risk of human Lyme disease infection posed by I. pacificus in southern California, comparatively high rates of infection were found in other tick species, suggesting that enzootic transmission of tick-borne borreliae may be more common in southern California than previously suspected (Chapter 2).

Finally, I find that wildfire disturbance, which is projected to become more severe under climate change, initially increases tick-borne disease risk in the year following fire, with this effect reversing in subsequent years. Tick abundance was elevated in plots sampled within the perimeter of a recent wildfire in Santa Barbara County, California in the year following the fire, though declined precipitously in following years. Also notable was the finding that populations of one of the primary reservoir hosts for the Lyme bacteria, dusky-footed woodrats (Neotoma fuscipes), were eliminated within the perimeter of the fire. In contrast, populations of western fence lizards (Sceloporus occidentalis), considered to be “non-competent hosts” for the bacteria because they cleanse feeding ticks of infection and do not carry the pathogen, were unaffected by the wildfire. Taken together with significantly reduced tick populations within the fire perimeter following the fire, this evidence suggests that wildfire disturbance may ultimately reduce tick-borne disease risk for multiple years following wildfire in California (Chapter 3).

Ongoing environmental change has already led to disease emergence across the globe, with consequences for human health. Further, the way in which environmental change is expected to impact the ecology of infectious diseases is challenging to predict and poorly understood for many disease systems. My dissertation research informs some of these key gaps in our understanding of tick-borne disease in the western US under environmental change.

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