Urban Tick Ecology in Oklahoma City
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URBAN TICK ECOLOGY IN OKLAHOMA CITY: TICK DISTRIBUTION, PATHOGEN PREVALENCE AND AVIAN INFESTATION ACROSS AN URBANIZATION GRADIENT By MEGAN A ROSELLI Bachelor of Science in Biology Wilkes University Wilkes-Barre, Pennsylvania 2015 Submitted to the Faculty of the Graduate College of the Oklahoma State University in partial fulfillment of the requirements for the Degree of MASTER OF SCIENCE May, 2019 URBAN TICK ECOLOGY IN OKLAHOMA CITY: TICK DISTRIBUTION, PATHOGEN PREVALENCE AND AVIAN INFESTATION ACROSS AN URBANIZATION GRADIENT Thesis Approved: Scott R. Loss Thesis Co-Adviser Bruce H. Noden Thesis Co-Adviser W. Sue Fairbanks ii ACKNOWLEDGEMENTS A thesis takes a village, and there are so many people and organizations that made my thesis possible. Funding for my thesis was provided by the Oklahoma Center for the Advancement of Science and Technology (OCAST) and USDA/NIFA hatch grants. Additional funding for my degree program was provided by an Oklahoma State University Graduate Fellowship and a scholarship endowed by Robert L. Lochmiller II. First and foremost, I thank my advisors Drs. Scott Loss and Bruce Noden whose ideas, guidance, edits, and support significantly improved my thesis and entire graduate school experience. I also thank my committee member, Dr. Sue Fairbanks, who provided invaluable help with methodology and provided fresh new perspectives on my results. My project would not have been possible without numerous people who assisted with fieldwork: Dawn Brown, Caitlin Laughlin, Caleb McKinney, and Liam Whiteman. Urban fieldwork is difficult and unique, and I was lucky to have the help of a hard- working, adaptable group of people. I also thank those who volunteered their time to assist with field work, including Jared Elmore, Kelsey Elmore, Sirena Lao, Matthew Fullerton, Alexis Cole, and my advisors. I sincerely thank the numerous undergraduates who assisted with lab work: Alexis Cole, Melissa Crouch, Cari Lewis, Victoria Pickens, and Aliyah Starnes. I always say “we do all our own stunts” in regards to lab work, and I couldn’t have done it without such dedicated group (including my advisor Dr. Bruce Noden). Thank you to all my previous mentors for showing me a career in science is iii Acknowledgements reflect the views of the author and are not endorsed by committee members or Oklahoma State University. possible, Drs. Jeffery Stratford, Michael Steele, Ned Fetcher, Desiree Narango and Richard Feldman, and Hannah Webber and Seth Benz. I thank the staff, faculty, and graduate students from the Entomology Plant Pathology and Natural Resource Ecology and Management departments at Oklahoma State University. I was lucky to have the support and guidance of two departments during my thesis. I especially thank my lab mates: Jared Elmore, Matthew Fullerton, Paulina Harron, Sirena Lao, Shishir Paudel and Corey Riding. Additional thanks to Samantha Cady, Jonathan and Samantha Harris, Ashley and Malcom Knoch, Angela Riley, and Dr. Timothy O’Connell. Finally, I thank my family and friends (who I consider my family at this point) for supporting me even when I plan on doing something a little unbelievable, like move to Oklahoma to study ticks and birds. Thank you to my parents, Kevin Roselli, Melissa Kresge, my second set of parents, Bobbi Bond, and Michael Schmoyer, my sister, Abigail Roselli, my honorary brother Chase Rios, my friends Ally Hothouse, Leo Macaluso, and Sarah Szwydko, my grandparents David and Judith Kresge and Lynda Roselli, and my companion, Apollo. I dedicate this thesis to my late grandfather and number one fan, Frank Roselli. iv Acknowledgements reflect the views of the author and are not endorsed by committee members or Oklahoma State University. Name: MEGAN ROSELLI Date of Degree: MAY, 2019 Title of Study: URBAN ECOLOGY OF TICKS IN OKLAHOMA CITY: TICK DISTRIBUTION, PATHOGEN PREVALENCE, AND AVIAN INFESTATION ACROSS AN URBANIZATION GRADIENT Major Field: NATURAL RESOURCE ECOLOGY AND MANAGEMENT Abstract: Urbanization has been linked to the emergence and increased prevalence of many vector-borne diseases, including tick-borne diseases. Despite the growing public health importance of tick-borne diseases, little is known about how they are influenced by urbanization in North America, especially in the central U.S. where several pathogens occur at or near their highest levels of incidence nationally. To understand how urbanization effects tick-borne disease, we investigated tick distribution, tick-bone pathogen prevalence, and tick-host interactions across a gradient of urbanization in Oklahoma City, Oklahoma, USA. At 16 parks and greenspaces we collected ticks using CO2 traps and flagging, measured temperature and humidity during tick sampling, conducted vegetation surveys, and used trail cameras to estimate an index of deer abundance. Adult ticks were tested for Rickettsia sp., Ehrlichia sp., Anaplasma sp., Borrelia sp., and Francisella tularensis. Additionally, we mist-netted birds during the breeding season, sampled them for ticks. Our results indicate there is a risk of encountering ticks and pathogens across the entire urbanization gradient from exurban areas to the urban core, although some tick species and pathogens (Dermacentor variabilis and Ehrlichia ewingii) may be less common in intensely urbanized areas. We also found that vegetation, temperature, and moisture variables predict tick abundance and that these correlates vary among species. The index of deer abundance was positively correlated with A. maculatum and D. variabilis abundance but unrelated to A. americanum abundance, but urbanization intensity did not influence either the proportion of birds with ticks or the tick load of infested birds. Our results suggest that urban residents are at risk for encountering a tick-borne disease, and it’s unlikely that deer by themselves are driving tick abundance in Oklahoma City since such a large proportion of birds were infested with ticks. Public health officials and land managers can use such information about parks and their surroundings to focus public education and land management efforts designed to reduce tick-borne disease prevalence. v TABLE OF CONTENTS Chapter Page I. MULTI SCALE DRIVERS OF TICK DISTRIBUTION AND TICK-BORNE PATHOGEN PREVALENCE ACROSS AN URBANIZATION GRADIENT IN A MAJOR METROPOLITAN AREA IN THE U.S. GREAT PLAINS .....................1 Abstract ....................................................................................................................1 Introduction ..............................................................................................................2 Methods....................................................................................................................5 Study design and site selection ..........................................................................5 Tick collection ...................................................................................................7 Vegetation sampling ..........................................................................................8 Deer camera trapping .........................................................................................9 Molecular testing .............................................................................................10 Statistical analysis ............................................................................................12 Results ....................................................................................................................16 Factors influencing tick abundance .................................................................16 Association between deer abundance and tick abundance ..............................18 Factors influencing pathogen prevalence .........................................................19 Discussion ..............................................................................................................21 Factors influencing tick abundance .................................................................22 Association between deer abundance and tick abundance ..............................24 Factors influencing pathogen prevalence .........................................................25 Conclusions ............................................................................................................28 Acknowledgments..................................................................................................30 References ..............................................................................................................29 Tables and Figures .................................................................................................41 Appendix ................................................................................................................49 II. VARIATION IN TICK INFESTATION OF BIRDS ACROSS A GRADIENT OF URBANIZATION INTENSITY IN A MAJOR METROPOLITAN AREA IN THE U.S. GREAT PLAINS ...........................................................................................64 Abstract ..................................................................................................................64 Introduction ............................................................................................................65 Methods..................................................................................................................68 Results ....................................................................................................................73