Pathogen surveillance and management strategies for confiscated and free-ranging eastern box turtles (Terrapene carolina carolina)

Daleo, Maris Jean

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https://hdl.handle.net/2142/129420 Copy

Description

Title

Pathogen surveillance and management strategies for confiscated and free-ranging eastern box turtles (Terrapene carolina carolina)

Author(s)

Daleo, Maris Jean

Issue Date

2025-04-22

Director of Research (if dissertation) or Advisor (if thesis)

Allender, Matthew

Doctoral Committee Chair(s)

Allender, Matthew

Committee Member(s)

• Terio, Karen
• Whitaker, Rachel
• Adamovicz, Laura

Department of Study

School of Integrative Biology

Discipline

Ecol, Evol, Conservation Biol

Degree Granting Institution

University of Illinois Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• illegal wildlife trade
• eastern box turtle
• Terrapene carolina carolina
• pathogen surveillance
• confiscated turtle management

Abstract

The global wildlife trade, both legal and illegal, affects billions of animals annually through capture and transport, sometimes resulting in lethal outcomes. The overexploitation of chelonians is increasingly recognized as a significant driver of population declines and facilitates the spread of infectious diseases. Although there is growing global awareness of turtles as victims of the illegal wildlife trade, there is still a lack of information about how pathogen profiles can impact repatriation efforts to inform appropriate management actions when considering pathogen profiles. The complex relationships between the host, multiple pathogens, and conspecifics must be investigated to maximize conservation impact. To address deficits in knowledge of the relationship between multiple pathogens, I designed a multiplex quantitative PCR (qPCR) assay to detect four eastern box turtle (Terrapene carolina carolina) pathogens, Terrapene herpesvirus 1 (TerHV1), Terrapene adenovirus (TerAdv), box turtle Mycoplasmopsis sp. (BTMyco), and frog virus 3 (FV3) within a single DNA sample. I could, then, apply the information gained from co-detections to efficiently investigate the complex pathogen profile of two groups of confiscated eastern box turtles. Managing live animals confiscated from the illegal wildlife trade can be critical for conservation, and best practices are needed to determine how to appropriately manage confiscated turtles. In the first management example, 56 turtles, from a group of 96 confiscated turtles, were housed outdoors in six different tubs and allowed to brumate over winter. This led to 100% mortality, likely due to FV3 infection and widespread co-detections of multiple pathogens. In a second group of confiscated turtles that were intercepted the following year, I received 17 eastern box turtles that I sampled for 13 months to investigate longitudinal pathogen shedding patterns of FV3, TerHV1, TerAdv, and BTMyco. Observed pathogen prevalence values varied by month, and the probability of detecting pathogens in an infected turtle during a given month was generally low (TerHV1 = 32.7%, TerAdv = 21.2%, and BTMyco = 49.9%). After two deaths, the remaining 15 confiscated eastern box turtles were sampled for these four pathogens during 8-week trials with different housing groups and environmental temperatures within a temperature-controlled chamber: 1) individually housed at two temperatures, 2) group housed at cold temperatures, 3) group housed within a temperature gradient, 4) group housed at warm temperatures, and 5) individually housed at warm temperatures. Pathogen prevalence varied weekly but was highest when housed together at a temperature gradient (BTMyco = 100%, TerAdv = 100%, TerHV1 = 46%). More co-detections and deaths (n = 2) occurred when the environmental temperature was warm, and weekly pathogen shedding was lowest when the turtles were individually housed. Using a sensitivity analysis, I was able to determine the diagnostic sensitivities for different testing frequencies for BTMyco, TerHV1, and TerAdv within different housing conditions. With information about these pathogens in confiscated turtles, I utilized ecological modeling methods to determine detection probabilities and unbiased prevalence estimates in free-ranging turtles. I used a dynamic occupancy model and a Cormack-Jolly-Seber model to determine the unbiased prevalence of BTMyco, TerAdv, and TerHV1 in free-ranging turtles, as well as the impact of those pathogens on turtle survival. I used data previously detected over seven years (2016 – 2022) from five populations (N= 778 turtles). Annual survival ranged from 71.2%-88.1% across all five populations, and I failed to find evidence that any of these three pathogens influenced survival; however, the unbiased prevalence of these pathogens was much higher than raw prevalence values, indicating these pathogens may be common in free-ranging populations. To determine how the pathogen profile of confiscated turtles would impact a recipient free-ranging population, I simulated a value that represents the pathogen impact of a free-ranging box turtle population if repatriation efforts of a confiscated turtle population were to occur. This simulation incorporated random binomial distributions of pathogen status within RStudio into an online, user-friendly application through Shiny. Each pathogen was then weighed based on its impact on survival, in which pathogens that have greater influence on survival (like FV3) are given a higher weight. When simulating scores of the free-ranging (N = 778) and confiscated box (N = 17) turtle population populations, the pathogen impact score of the free-ranging population was 0.204, and the health score of the confiscated population was 0.423. The overlap between the populations’ pathogen impact scores was 50.3%, so if this confiscated population were released, the free-ranging health score would increase to 0.31. The application is user-friendly and allows users to change their pathogen prevalence values, the impact of the pathogen prevalence, population size, and simulation year. This approach provides a simplified yet reproducible framework for making informed decisions about releasing confiscated turtles based on their pathogen status and external signs of illness. Further investigation of chelonian pathogens and their impact on health should continue to ensure the safety of confiscated and free-ranging turtles.

Graduation Semester

2025-05

Type of Resource

Thesis

Handle URL

https://hdl.handle.net/2142/129420

Copyright and License Information

Copyright 2025 Maris Daleo

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