Date of Award

Spring 5-11-2019

Level of Access Assigned by Author

Open-Access Thesis

Degree Name

Doctor of Philosophy (PhD)

Department

Earth Sciences

Advisor

Kirk A. Maasch

Second Committee Member

Allison M. Gardner

Third Committee Member

Kate Beard-Tisdale

Additional Committee Members

Laura N. Rickard

Norman T. Anderson

Abstract

Lyme disease is caused by the bacterial spirochete Borrelia burgdorferi, which is transmitted through the bite of an infected blacklegged (deer) tick (Ixodes scapularis). Geographic invasion of I. scapularis in North America has been attributed to causes including 20th century reforestation and suburbanization, burgeoning populations of the white-tailed deer (Odocoileus virginianus) which is the primary reproductive host of I. scapularis, tick-associated non-native plant invasions, and climate change. Maine, USA, is a high Lyme disease incidence state, with a history of increasing I. scapularis abundance and northward range expansion. This thesis addresses the question: “To what extent has the range expansion of blacklegged ticks in Maine been associated with climate change, deer, and other factors?” using a long-term, passive surveillance dataset (1990-2013) of I. scapularis in Maine.

Chapter 1 characterized temporal trends in I. scapularis submissions rate (an index of abundance) and phenology, in Maine’s northern (7 counties) versus southern (9 counties) tier. In the northern tier the I. scapularis submission rate and season duration increased throughout the duration of the time series, indicating I. scapularis was emergent but not established. By contrast, in the southern tier, submissions rate and season duration increased initially but after about 13 years leveled off, indicating I. scapularis was established by the mid-2000s. Winter and fall average minimum temperatures increased in the northern tier and summer relative humidity in both tiers increased. I. scapularis submission rates and phenological changes were correlated with relative humidity statewide. Generally, I. scapularis submission rates and phenological changes were correlated with winter warming, but predominantly in the northern tier and only the early half of the time series for the southern tier. Though northern tier climate appears to have become more permissive over time, current ecological suitability for I. scapularis in the northern tier may be limited due to low deer densities, which averaged ~5/mi2. In the southern tier, deer densities were higher and correlated with I. scapularis submissions rate. However, a number of other, unknown population-limiting mechanisms could have been operating to keep I. scapularis in the southern tier at a dynamic equilibrium since the mid-2000s. Also observed was a correlation between Lyme incidence and I. scapularis in the northern but not southern tier. This may represent decoupling of reported disease incidence and entomological risk as measured simply by tick abundance and Borrelial infection prevalence. This discrepancy suggested that disease discovery had increased through greater clinician and patient awareness and testing effort, and/or that acarological risk may be a more nuanced function of diverse, variously virulent strain types in multiple pathogens borne by I. scapularis.

Chapter 2 used a generalized additive mixed model (GAMM) to model linear and nonlinear relationships between nymphal I. scapularis abundance and predictors, while allowing for spatiotemporal dependencies within and among wildlife management districts. I. scapularis nymphs increased with increasing deer densities up to ~13 deer/mi2, but beyond this threshold tick abundance did not vary with deer density. This result corroborated the idea of a saturating relationship between I. scapularis and deer density. It was also consistent with empirical studies suggesting deer density must be lowered below ~8-13/mi2 to lower I. scapularis abundance enough to lower Lyme disease. The model also indicated that more ticks were associated with higher relative humidity, warmer minimum winter temperatures and more degree-day accumulation, and that without deer >4/mi2 warmer winters would not increase nymphal abundance. The Maine Department of Inland Fisheries and Wildlife northern tier goals range from 10-15/mi2 and southern tier goals from 15-20/mi2 for 2030 (MEIFW 2017). We recommended deer densities be kept to ≤10/mi2 in all of Maine’s northern tier to mitigate likely increases in ticks due to future warming. Suburbanization and presence of tick-associated non-native plants did not enter the model because they co-occurred with deer.

Chapter 3 ascertained that Lyme incidences on the off-shore, unbridged islands of Maine have been above the statewide average and at least on par with those seen on other offshore islands in Massachusetts and Rhode Island. Increasing I. scapularis abundance and Lyme incidence have been attributed to high deer densities by some residents of these island communities. Burgeoning deer densities on some of these islands have led to various deer management histories along with a good deal of conflict on how to manage deer populations. We summarized the burden of Lyme disease, entomological risk, and deer management histories on these islands. We also polled island residents in 2016 to quantify the level of concern about the Lyme disease problem and assess the level of support for deer herd reduction on their islands. A 2016 survey of island residents indicated that other deer-related problems, namely vehicle collisions and garden and forest damage, motivated support for deer reduction as much as Lyme disease. We recommended efforts to keep deer density ≤15/mi2 and to remove invasive plant species--particular Japanese barberry—from the landscape. The benefits of these measures will extend beyond vector tick control to improved deer and forest health.

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