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Modeling the Health of Free-Living Illinois Herptiles: an Integrated Approach Incorporating Environmental, Physiologic, Spatiotemporal, and Pathogen Factors

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Modeling the Health of Free-Living Illinois Herptiles: an Integrated Approach Incorporating Environmental, Physiologic, Spatiotemporal, and Pathogen Factors MODELING THE HEALTH OF FREE-LIVING ILLINOIS HERPTILES: AN INTEGRATED APPROACH INCORPORATING ENVIRONMENTAL, PHYSIOLOGIC, SPATIOTEMPORAL, AND PATHOGEN FACTORS BY LAURA ADAMOVICZ DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in VMS-Comparative Biosciences in the Graduate College of the University of Illinois at Urbana-Champaign, 2019 Urbana, Illinois Doctoral Committee: Assistant Professor Matthew Allender, Chair and Research Director Professor CheMyong Jay Ko Associate Professor Megan Mahoney Assistant Professor Rebecca Smith Professor Mark Mitchell, Louisiana State University Sharon Deem, Saint Louis Zoo Institute for Conservation Medicine ABSTRACT Human expansion has contributed to an unprecedented global environmental crisis and significantly impacted the stability of many wildlife populations. The health of wildlife populations influences their ability to recover from a complex array of anthropogenic and natural stressors. Promotion of positive health status may improve conservation outcomes in wild animals. However, wildlife health status is dynamic and determined by a variety of factors. Studying such a complex system requires a comprehensive approach with careful consideration of multiple determinants simultaneously. The purpose of this dissertation is to holistically characterize health in three herptile species of conservation concern in Illinois by combining traditional veterinary health assessments with environmental and spatio-temporal data within a modeling framework. The main objective is to identify the best means of assessing wellness in wild herptiles to inform management strategies which support robust population health. Health was investigated in three species of conservation concern in Illinois: the eastern box turtle (Terrapene carolina carolina), the ornate box turtle (Terrapene ornata ornata), and the silvery salamander (Ambystoma platineum) over the course of three years using a combination of physical examination, qPCR pathogen screening, and clinical pathology (box turtles). Mortality events were characterized as they occurred and spatiotemporal data were used to screen for locations and times associated with pathogen presence or poor health outcomes. Diagnostic tests including hematology, plasma biochemistry, protein electrophoresis, venous blood gas, hemoglobin-binding protein, and erythrocyte sedimentation rate were investigated for clinical utility in box turtles, and a novel qPCR assay for detection of Mycoplasma sp. in box turtles was developed and validated. Health models were generated for each study species and used to identify drivers of poor health, determine the most clinically useful diagnostic tests for ii each species, and generate management recommendations supporting good individual and population health. Health assessment in silvery salamanders (N = 770) identified a parasite (Amphibiocystidium sp.) that has never been previously detected in the Midwest and characterized significant larval mortality due to ranavirus (FV3). Poor health was best predicted by the additive effects of year, location, FV3 detection, and the presence of fresh traumatic injuries. FV3 is considered to represent a threat to silvery salamanders in Illinois, and recommendations for future research include characterization of silvery salamander biology and ecology, continued health monitoring to identify emerging threats, and focused study on ranavirus to identify potential management interventions. Ornate box turtle (N = 168) health assessment revealed a high prevalence of shell lesions associated with predator trauma (51-59% annually). There was no association between pathogen detection (Terrapene herpesvirus 1, Terrapene adenovirus), clinical signs of illness, and clinical pathology alterations. Poor health was best predicted by the presence of active or inactive shell lesions and deviations from population median values for total leukocyte count, eosinophils, basophils, and heterophil:lymphocyte (H:L) ratios. Population viability analysis revealed that annual removal of two adult female turtles above background mortality rates dramatically increased the probability of population extinction within the next century (54-97%). Continued health assessment (including hematology), mesopredator control, and disease screening of newly introduced turtles to prevent novel pathogen ingress was recommended to support individual and population wellness for ornate box turtles. Eastern box turtle (N = 507) health assessment uncovered mortality events due to FV3 and a suspected necrotizing soft tissue infection. Detection of other pathogens (Terrapene adenovirus, Terrapene herpesvirus 1, Mycoplasma sp., Salmonella iii typhimurium) was not related to health status. Poor health was best predicted by the presence of active shell lesions, clinical signs of upper respiratory disease (URD), and deviations from population median values for total leukocyte count and H:L. PVA revealed that annual removal of 1 - 5 adult female turtles above background mortality rates dramatically increased the probability of population extinction within the next century for all populations, but the effects were especially pronounced in small populations from fragmented and degraded habitats. FV3 is considered a conservation threat for eastern box turtles, especially in smaller populations like the one at Kickapoo State Park which experience recurrent ranavirus outbreaks in both amphibians and turtles. Forest management to promote habitat quality, consideration of box turtle activity patterns when planning burn schedules, road signage to decrease vehicular strikes, additional research into ranavirus dynamics in natural systems, and continued health assessment to monitor trends and identify new threats were recommended to support individual and population wellness. This dissertation demonstrates the feasibility of modeling health in wildlife and illustrates its use for determining drivers of poor health, identifying clinically useful diagnostic tests, and generating management recommendations which support overall individual and population wellness, improve conservation outcomes, and promote herptile and ecosystem health. iv ACKNOWLEDGEMENTS This dissertation has been made possible by many people, and I feel that I should start at the beginning in acknowledging them. First, I would like to thank my parents for encouraging my love of animals – especially creepy-crawly insects, reptiles, and amphibians, which are not the typical favorite taxa of young girls. I also thank Maryanne and Richard Hahn for taking me under their wing as a teenager at the Catoctin Zoo and instilling my passion for conservation, especially of herptile species. I would also not be here today without some excellent veterinary mentors that have helped shape my professional trajectory, including (in no particular order) Sharon Deem, Greg Lewbart, Ellen Bronson, Vanessa Grunkemeyer, and many others. The adage “it takes a village” doesn’t even come close to covering the number of people it took to make this dissertation happen. I am incredibly grateful to John Rucker and the turtle dogs, all the student members of the Turtle Team that helped collect my data, and especially to the student leaders of this project including Kayla Boers, Megan Britton, Marta Kelly, Samantha Johnson, and John Winter. The passion and dedication of this group is inspiring, and their good attitudes are infectious. My population-level data would also be woefully incomplete without the contributions of several ecologists, post-docs, and grad students affiliated with the Illinois Natural History Survey including Chris Phillips, Michael Dreslik, Sarah Baker, Ethan Kessler, and Kelsey Low. The hard work, knowledge, and good humor of this group made all the long, hot (and cold!) fieldwork days much more enjoyable. I have also received a huge amount of help from my lab mates Jeremy Rayl and Ellen Haynes and our laboratory technician Emilie Ospina. Thanks for being a sounding board for ideas and sharing food, laughs, and caffeine these last few years! v I thank my committee members, Sharon Deem, Mark Mitchell, Rebecca Smith, Megan Mahoney, and Jay Ko for their advice and guidance during this project. I also thank my major advisor, Matt Allender, for his continual support throughout this process, and the Comparative Biosciences Department for their generous scholarship funding. Additional funding for this project was provided by the Friends of Nachusa and a State Wildlife Grant (T-104-R-1). Last, but not least, I thank my husband Nick for his help, flexibility, and love through all the moving and stress of vet school, internships, and grad school. This has been an amazing learning experience, and I am proud to present my dissertation and contribute to existing scientific knowledge about health and disease in free-living herptiles. vi TABLE OF CONTENTS CHAPTER 1: INTRODUCTION ........................................................................................1 CHAPTER 2: LITERATURE REVIEW .............................................................................6 PART I: DIAGNOSTIC TECHNIQUES ..........................................................................41 CHAPTER 3: TISSUE ENZYME ACTIVITIES IN FREE-LIVING EASTERN BOX TURTLES (TERRAPENE CAROLINA CAROLINA) ....................................42 CHAPTER 4: VENOUS BLOOD GAS IN FREE-LIVING EASTERN BOX TURTLES (TERRAPENE CAROLINA CAROLINA) AND EFFECTS OF PHYSIOLOGIC, DEMOGRAPHIC, AND ENVIRONMENTAL
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