Descriptive Epidemiology for Turtles Admitted to the North Carolina State University College of Veterinary Medicine Turtle Rescue Team

Wildlife health provides insight into ecosystem health and the impact of human activities on the environment (Welsh and Ollivier 1998; Hilti and Merenlender 2000). Wild amphibian populations are considered especially vulnerable to alterations in the environment and have become a major focus for environmental health studies (Welsh and Ollivier 1998; Alford and Richards 1999; Caro and O'Doherty 1999; Hilti and Merenlender 2000). Wild reptiles, especially chelonians, demonstrate the effects of human population expansion and environmental modification in their mortality and morbidity patterns, with worldwide population declines often attributed to human activity (Hartup 1996; Caro and O'Doherty 1999; Brown and Sleeman 2002; Aguirre and Lutz 2004; Rivas et al. 2014). Most of the epidemiological data available have been derived from wildlife-hospital and primary-care-facility medical records. Turtles comprise a significant portion of wildlife cases admitted to care facilities, and several studies have been performed to investigate causes of morbidity and mortality in wild turtles (Hartup 1996; Brown and Sleeman 2002; Rivas et al. 2014; Schenk and Souza 2014). One organization dedicated to wild reptile care is the North Carolina State University College of Veterinary Medicine Turtle Rescue Team (TRT), which generates medical records from which epidemiological data can be extracted (Lewbart et al. 2005).

The TRT is a veterinary-student–run organization that admits and treats sick and injured wild turtles. Veterinary students in their first 3 y of the Doctor of Veterinary Medicine program, with guidance from a faculty mentor and technician, are responsible for all aspects of patient care, including case management, diagnostic testing, and coordination with local wildlife rehabilitators for recovery and release. In operation since 1996, the TRT has treated almost 4,000 turtles, and this large volume of cases has provided students with an excellent introduction to wildlife rehabilitation and medicine and has resulted in several clinical research publications as well as case series (e.g., Willer et al. 2003; Case et al. 2005; Saelinger et al. 2006; Minter et al. 2010; Royal et al. 2012). The goals of the TRT are to provide veterinary students with an opportunity to manage clinical wildlife cases, provide optimal medical care to native sick and injured wild turtles, and to provide clinical case records as a platform for dissemination of information concerning native chelonian species. The objective of this retrospective review is to describe and summarize the basic information available on TRT turtle cases from 1996 to 2012 in archival records held by the North Carolina State University Libraries Special Collections Research Center with the goal of encouraging further research into morbidity and mortality of wild turtles through these records and the additional years of records now available.

We manually compiled and reviewed original paper medical records from 2,666 cases comprising 2,613 turtles and 53 other animals admitted to the TRT between 1996 and 2012. Records for seven turtles that could not be released and were adopted between 2008 and 2012 are considered active medical records and we did not include them in this data set. Each medical record contains a patient admissions form filled out by the rescuer, a physical examination recording sheet, and a day-by-day description of treatment and husbandry performed for each turtle. Data extracted by a single case reviewer (L. Stranahan) and organized into a computerized database (Microsoft Excel 2010) included patient identification number and name, admission date, last entry date, species, sex and reproductive status, location where found, clinical diagnosis, and final disposition; missing data were noted. An additional “Miscellaneous File Contents” section lists any additional information included in each record, including blood work, culture, biopsy, or cytology results, radiographs, drug labels, and anesthesia and surgery records. We calculated length of stay from the admission and last entry dates. We assigned county classification based on the location provided by the rescuer. We redacted house numbers from private home locations for privacy reasons.

We separated diagnoses into categories including vehicular trauma (hit by car), animal attack, garden-equipment–related trauma (hit by lawnmower), fishing-equipment trauma, other human-induced injury, pet surrender, aural abscessation, nutritional disorders, infection, organ prolapse, buoyancy disorder, neurologic disorder, unknown trauma (subdivided into injury to carapace, plastron, limbs, or head), and unknown. TRT veterinary students with approval by attending clinicians determined clinical diagnoses based on case history, physical examination, and ancillary diagnostic testing. TRT made all diagnoses of trauma based on case history provided by the rescuer as well as physical examination findings consistent with trauma. We defined animal attack as trauma caused by wild and domestic animals, including dogs and cats. Garden-equipment–related trauma included injuries due to lawnmowers, weed whackers, and manual tools, including shovels and plows. Fishing-equipment trauma was related to injury via fishing hooks, fishing line, and netting. The category of other human-induced injury included turtles that were either accidentally or intentionally harmed by humans outside of the previously specified trauma categories. We defined pet surrender as animals that had been removed from the wild and kept as pets before being surrendered to the TRT.

TRT diagnosed aural abscessation based largely on physical presentation (swelling medial to the tympanum) and occasionally by surgical examination of the middle ear. A diagnosis of nutritional disorder, largely consisting of hypovitaminosis A and dehydration, relied on physical examination findings such as emaciation, swelling of the orbit, etc., and occasionally via blood chemistry profiles. A diagnosis of infection included upper respiratory infection, ocular infection, and soft tissue infection including abscessation on the skin and plastron. Organ prolapse refers to prolapse of the reproductive or gastrointestinal tract. Buoyancy disorder related to turtles that had difficulty staying afloat or were unable to maintain a normal position in water. Turtles classified into the category of neurologic disorder displayed abnormal mentation or behavior, such as swimming in circles, without gross evidence of trauma. Finally, we placed animals for which there was no recorded diagnosis into the category of unknown. We performed all statistical analyses using Microsoft Excel 2010.

Between 1996 and 2012, TRT documented 2,613 turtle cases (Table S1, Supplemental Material). Additionally, 53 cases representing other reptilian and amphibian species, including frogs, toads, snakes, and lizards (Table A1, Archived Material), are included in the records but we excluded them from further analysis. The number of turtle cases followed a significant increasing trend during these years (r = 0.72; P = 0.001247). Twelve native species of turtle were represented (see Table 1), the most predominant being the eastern box turtle Terrapene carolina (n = 1,378). Species was undetermined for 84 turtles. Nonnative species from the wild included 26 red-eared sliders Trachemys scripta elegans, and 1 gopher tortoise Gopherus polyphemus. The TRT also examined eight nonnative turtles used in research studies or as part of a museum collection. The sex distribution of 511 turtles was unspecified but those of known sex were evenly distributed, with a sex ratio of approximately 1:1. Two hundred and two of the 1,058 females admitted were gravid. The majority of these arrived in May and June.

Two thousand and thirty-nine turtles came from 63 North Carolina counties, 17 turtles arrived from other states, and for 557 cases state of origin was not listed. Absolute numbers of turtles from 1996 to 2012 from each county are shown on the map of North Carolina (Figure 1). The majority of turtles were brought from the three counties closest to the North Carolina State University College of Veterinary Medicine: Wake County (n = 1,137), Durham County (n = 199), and Orange County (n = 99). Of the 2,318 turtles whose ultimate disposition was recorded (Table 2), just over half were released to the wild. Records for the remaining 295 turtles were unclear regarding the status of the turtles. Length of stay under TRT care either in the hospital or with rehabilitators ranged from 1 to 640 d with a median of 20 d.

The most common of the clinical problems was vehicular trauma (n = 1,577; Table 3). Other human-related interactions such as garden equipment and fish-equipment–related trauma, other human-induced injury, and pet surrender represented an additional 153 clinical problems, leaving turtle presentation reportedly associated with human contact at 1,730 cases. Animal attacks comprised 152 diagnoses, with 137 reported as domestic canine encounters. Trauma due to unknown causes represented 222 cases. Other disorders such as infection, aural abscessation, nutritional disorder, neurologic disorder, buoyancy disorder, or prolapse comprised 372 cases. An additional 101 turtles were healthy.

The epidemiological data presented here are similar to information collected in other states. Trauma, most frequently following human encounters, is the most common diagnosis in wild turtle populations at a level of 48% (Hartup 1996) to 74% of total cases (Brown and Sleeman 2002). Previous studies have similarly found vehicular trauma to be the most common subcategory of trauma (Hartup 1996; Brown and Sleeman 2002; Rivas et al. 2014; Schenk and Souza 2014). Paralleling other population studies (Illinois, Tennessee, and Virginia), most garden-equipment–related trauma involved lawnmowers, most animal attacks were due to domestic canines, and fishing-equipment–related injuries were most often due to swallowing or implantation of a fishing hook (Hartup 1996; Brown and Sleeman 2002). In terms of medical diagnoses, aural abscessation was present only in eastern box turtles and was not observed in any other species, a detail consistent with other studies (Brown and Sleeman 2002). A concern of previous studies was the potential bias toward human-related causes of injury and mortality in wild turtle populations treated at wildlife hospitals, especially in densely populated urban and suburban communities (Brown and Sleeman 2002). Our data are likely similarly biased because of the manner in which turtles are brought to the TRT by humans who discover the injured turtles. We did not analyze and compare causes of morbidity and mortality in wild turtles from rural or less populated areas with causes in turtles from urban areas.

The decision to make the medical records publicly available through the North Carolina State University Libraries within 2 y of case admission complements efforts to promote an understanding of morbidity and mortality causes and rates in local turtle populations, and to provide descriptive epidemiological data concerning turtles brought to the TRT. Quality and depth of TRT record-keeping has improved from 1996 to 2012, with changes and expansions in the data collection forms over the time of the archive and greater attention to recording the final disposition of cases. There are a large number of unknowns in the records for data of wildlife management interest, such as county or location where the turtle was originally encountered, as well as smaller numbers of unknowns for species identification and gravidity. This could reflect the often hurried nature of the data collection encounter between veterinary student and the rescuer, the strong emphasis on clinical care response within the intake environment, and the limited investigation of those characteristics in turtles that were euthanized on arrival. For example, reviewers asked about the presence of other variables in the data set such as age, shell measurements, and weights. Approximate age or juvenile status are not consistently noted in the records; and, it is not clear whether turtles whose sex was not reported were juveniles or were adults that simply were not sexed, because many severely injured turtles were euthanized at or shortly upon arrival and thus had limited evaluation. Shell measurements were also not taken generally, but could be useful as an indicator of juvenile status or general health and may be included as part of the initial physical examination for turtles in the future. Weights were recorded fairly consistently for all cases and are available in the individual records, but were not part of this basic descriptive-statistics summarization. To increase the utility of TRT medical records for epidemiological and wildlife management research, more attention may need to be paid to the nonclinical components of the record-keeping.

The data provided in records of turtles presented to the TRT from numerous counties across North Carolina, including rural, suburban, and urban environments, serve as a rare resource for documenting, exploring, and comparing the causes of morbidity and mortality in wild turtle populations and their relationship with human activity and habitat encroachment. Although the thousands of medical records relate to native North Carolina turtles, many of the presenting problems, management techniques, and case resolutions apply to turtles in other parts of the country and internationally. This searchable case listing will give clinicians and researchers a means of saving time in locating relevant cases, improving animal welfare, and increasing our knowledge of wildlife medicine and rehabilitation. The TRT case records exclusive of the current year and immediate past year may be consulted onsite by researchers at the North Carolina State University Libraries Special Collections Research Center, which collects primary source material in strategic efforts to support teaching, learning, and research. Within these collections are the University Archives, which collect, preserve, and make accessible primary resource materials that document the history and development of the university and its continued service to the people of North Carolina. Beyond collecting the institutional records of North Carolina State, the University Archives also collect material from hundreds of student organizations, including the TRT. In addition to the TRT records, the State University Libraries Special Collections Research Center actively builds and makes accessible rare and unique materials in strategic collecting areas that include Veterinary Medicine, Zoological Health, and Animal Rights and Welfare, among others. These include the medical records and intake logs from 2003 to 2009 for the Piedmont Wildlife Center (http://www.lib.ncsu.edu/findingaids/mc00457/). Information within these collections provide ample opportunity for learning more about morbidity and mortality patterns in wildlife in association with human populations.

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any supplemental material. Queries should be directed to the corresponding author for the article.

The paper records of the Turtle Rescue Team described in this article are available in the North Carolina State University Libraries Special Collections Research Center in the collection entitled, North Carolina State University, Student and Other Organizations, Turtle Rescue Team Records 1996–2014. The collection guide, which provides detailed information about the records, is available online at http://www.lib.ncsu.edu/findingaids/ua021_517/. North Carolina State University Libraries Special Collections Research Center contact information is also available online at http://www.lib.ncsu.edu/scrc/request. The spreadsheet of extracted case data used to inform this report is included as Supplemental Material.

Table S1. Turtle case records from the North Carolina State University Turtle Rescue Team; 1996–2012 (trtrecords1996.2012dryadsubmission.xls). Description and summary of basic information available on Turtle Rescue Team turtle cases from 1996 to 2012 in archival records held by the North Carolina State University Libraries Special Collections Research Center for research into morbidity and mortality of wild turtles.

Variables are case number, name of animal as assigned by TRT, beginning date of chart, ending date of chart, days observed, species, sex, gravidity, location, county, presenting problem, problem description, outcome, other file contents present (Misc File Contents), and staff notes.

Found at DOI: http://dx.doi.org/10.3996/072015-JFWM-056.S1 (870 KB XLS).

Please note: The Journal of Fish and Wildlife Management is not responsible for the content or functionality of any archived material. Queries should be directed to the corresponding author for the article.

To cite this archived material, please cite both the journal article (formatting found in the Abstract section of this article) and the following recommended format for the archived material.

Table A1. Nonturtle case records from 1996 to 2012.

Description and summary of basic information available on TRT nonturtle cases from 1996 to 2012 in archival records held by the North Carolina State University Libraries Special Collections Research Center for research into morbidity and mortality of wild reptiles and amphibians.

Variables are case number, name of animal as assigned by TRT, beginning date of chart, ending date of chart, days observed, species, sex, gravidity, location, county, presenting problem, problem description, outcome, other file contents present (Misc File Contents), and staff notes.

Recommended format for the archived material.

Stranahan L, Alpi KM, Passingham RK, Kosmerick TJ, Lewbart GA,. 2016. Data from: descriptive epidemiology for turtles admitted to the North Carolina State University College of Veterinary Medicine Turtle Rescue Team. Journal of Fish and Wildlife Management online in advance of print. http://dx.doi.org/10.3996/072015-JFWM-056. Also available at Dryad Digital Repository. http://dx.doi.org/10.5061/dryad.2b89t (16 KB XLSX).

The authors gratefully acknowledge the careful work of the hundreds of TRT students who entered data into the medical records. We were guided by previous analyses of selected cases: Dr Cheryl Hoggard (North Carolina State University College of Veterinary Medicine [CVM] Class of 1998) analyzed data prior to 2000; and Dr Arit Friedenthal (North Carolina State University CVM Class of 2009) provided her analysis of cases from 2003 to 2007, assisted by Dr Peter Cowen. Carly Dohse (North Carolina State University CVM Class of 2017) participated in some of the initial case-data extraction. Jeff Essic (Data Services Librarian, North Carolina State University Libraries) created the map presenting the distribution of turtle cases. Finally, we are grateful to the anonymous reviewers and the Associate Editor for improving the quality and clarity of this work.

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