{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T21:55:32Z","timestamp":1791237332121,"version":"4.1.0"},"reference-count":52,"publisher":"American Association of Zoo Veterinarians","issue":"2","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Journal of Zoo and Wildlife Medicine"],"published-print":{"date-parts":[[2026,3,25]]},"abstract":"<jats:p>Eastern box turtles (Terrapene carolina carolina) are declining range-wide due to anthropogenic factors, including the illegal wildlife trade. Infectious diseases that cause high morbidity and mortality, such as frog virus 3 (family Iridoviridae, genus Ranavirus, species Rana1), may also threaten this species in managed-care and free-ranging settings. High rates of infectious disease transmission are documented within the illegal wildlife trade; however, the impact of diseases on health, survival, and ultimate disposition of confiscated turtles is not thoroughly described. In July 2021, 96 eastern box turtles were seized by the US Fish and Wildlife Service while illegally en route to Asia and were relocated to three zoos via the Association of Zoos and Aquariums' Saving Animals from Extinction American Turtles program. From July\u2013August, 35 individuals were selected for pathogen surveillance, of which (94%) were qPCR positive for frog virus 3 (FV3; recently renamed Ranavirus rana1), 100% were positive for Mycoplasmopsis sp. (BTMyco), 80% were positive for Terrapene herpesvirus 1 (TerHV1), and 60% were positive for Terrapene adenovirus (TerAdv). At least two pathogens were co-detected in each turtle. Forty of the original 96 turtles died (31 of the 35 tested turtles), and in September 2021, the surviving 56 (4 from the subset of 35) turtles were transferred to the University of Illinois. These remaining turtles tested qPCR positive for FV3 (32%), BTMyco (64%), TerAdv (64%), TerHV1 (66%), Terrapene herpesvirus 2 (18%), and human-pathogenic Leptospira spp. (2%). Multiple pathogens were co-detected in 41 turtles (73%). All 56 turtles brumated over winter in 2021 and were found dead in May 2022, with autolysis limiting diagnostic necropsy. The complete mortality of 96 confiscated eastern box turtles demonstrates that poor health and disease transmission negatively impact the welfare and survival of illegally traded animals.<\/jats:p>","DOI":"10.1638\/2025-0081","type":"journal-article","created":{"date-parts":[[2026,3,25]],"date-time":"2026-03-25T05:54:47Z","timestamp":1774418087000},"page":"228-237","source":"Crossref","is-referenced-by-count":0,"title":["LARGE-SCALE DISEASE-ASSOCIATED MORTALITY EVENT OF EASTERN BOX TURTLES (TERRAPENE CAROLINA CAROLINA) CONFISCATED DUE TO THE ILLEGAL WILDLIFE TRADE"],"prefix":"10.1638","volume":"57","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9228-9213","authenticated-orcid":false,"given":"Maris J.","family":"Daleo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles J.","family":"Innis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura A.","family":"Adamovicz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher J.","family":"Bonar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dave","family":"Collins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carly R.","family":"Harkey","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melissa","family":"Joblon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Kennedy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica N.","family":"Lovstad","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brianne E.","family":"Phillips","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karen A.","family":"Terio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julie","family":"Thompson-Slacum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn A.","family":"Tuxbury","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kimberlee B.","family":"Wojick","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew C.","family":"Allender","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1213","reference":[{"key":"35","doi-asserted-by":"publisher","unstructured":"RJ Ossiboff, BL Raphael, AD Ammazzalorso, et al.  \"J Wildl Dis.\"  51, \"A Mycoplasma species of Emydidae turtles in the Northeastern USA.\" 466 (2015)","DOI":"10.7589\/2014-04-086"},{"key":"2","doi-asserted-by":"publisher","unstructured":"MC Allender, D Bunick, MA. Mitchell,  \"J Virol Methods.\"  188, \"Development and validation of TaqMan quantitative PCR for detection of frog virus 3-like virus in eastern box turtles (Terrapene carolina carolina).\" 121 (2013)","DOI":"10.1016\/j.jviromet.2012.12.012"},{"key":"4","doi-asserted-by":"publisher","unstructured":"WA Alvarez, PM Gibbons, S Rivera, et al.  \"Vet Parasitol.\"  193-, \"Development of a quantitative PCR for rapid and sensitive diagnosis of an intranuclear coccidian parasite in Testudines (TINC), and detection in the critically endangered Arakan forest turtle (Heosemys depressa).\" 66 (2013)","DOI":"10.1016\/j.vetpar.2012.11.029"},{"key":"5","doi-asserted-by":"publisher","unstructured":"K Apakupakul, M Duncan, K Subramaniam, et al.  \"J Wildl Dis.\"  60, \"Ranavirus (frog virus 3) infection in free-living three-toed box turtles (Terrapene mexicana triunguis) in Missouri, USA.\" 151 (2024)","DOI":"10.7589\/jwd-d-23-00057"},{"key":"9","doi-asserted-by":"publisher","unstructured":"DR Brown, BC Crenshaw, GS McLaughlin, et al.  \"Int J Syst Evol Microbiol.\"  45, \"Taxonomic analysis of the tortoise Mycoplasmas Mycoplasma agassizii and Mycoplasma testudinis by 16S rRNA gene sequence comparison.\" 348 (1995)","DOI":"10.1099\/00207713-45-2-348"},{"key":"12","unstructured":"CK. Dodd,  \"USGS [Internet].\"  \"North American box turtles (Terrapene) listed under CITES Appendix II.\" (1995)"},{"key":"15","doi-asserted-by":"publisher","unstructured":"AI Engel, L Adamovicz, JFX Wellehan, et al.  \"J Virol Methods.\"  2020, \"Development and validation of a quantitative PCR assay for detection of Terrapene herpesvirus 2 in eastern box turtles (Terrapene carolina carolina).\" 113968","DOI":"10.1016\/j.jviromet.2020.113968"},{"key":"16","doi-asserted-by":"publisher","unstructured":"SL Farkas  and J. G\u00e1l  \"Vet Microbiol.\"  138, \"Adenovirus and mycoplasma infection in an ornate box turtle (Terrapene ornata ornata) in Hungary.\" 169 (2009)","DOI":"10.1016\/j.vetmic.2009.03.016"},{"key":"19","doi-asserted-by":"publisher","unstructured":"D Franzen-Klein, L Adamovicz, D McRuer, et al.  \"J Zoo Wildl Med.\"  50, \"Prevalence of box turtle adenovrius in eastern box turtles (Terrapene carolina carolina) presented to a wildlife rehabilitation center in Virginia, USA.\" 769 (2020)","DOI":"10.1638\/2018-0238"},{"key":"20","doi-asserted-by":"publisher","unstructured":"SA Grant, J-F Bienentreu, ST Vila\u00e7a, et al.  \"Dis Aquat Organ.\"  134, \"Low intraspecific variation of Frog virus 3 with evidence for novel FV3-like isolates in central and northwestern Canada.\" 1 (2019)","DOI":"10.3354\/dao03354"},{"key":"21","doi-asserted-by":"publisher","unstructured":"MJ Gray  and VG. Chinchar  \"Ranaviruses.\"  (2015)","DOI":"10.1007\/978-3-319-13755-1"},{"key":"22","doi-asserted-by":"publisher","unstructured":"JC Hausmann, AN Wack, MC Allender, et al.  \"J Zoo Wildl Med.\"  46, \"Experimental challenges study of FV3-like ranavirus infection in previously FV3-like ranavirus infected eastern box turtles (Terrapene carolina carolina) to assess infection and survival.\" 732 (2015)","DOI":"10.1638\/2015-0022.1"},{"key":"23","unstructured":"\"ICTV Report.\"  \"Iridoviridae: Ranavirus.\" (2025)"},{"key":"29","doi-asserted-by":"publisher","unstructured":"R. E. Levin,  \"Food Biotech.\"  23, \"The use of molecular methods for detecting and discriminating Salmonella associated with foods\u2014a review.\" 313 (2009)","DOI":"10.1080\/08905430903320982"},{"key":"30","doi-asserted-by":"publisher","unstructured":"B Malorny, C Bunge, R. Helmuth,  \"J Microbiol Methods.\"  70, \"A real-time PCR for the detection of Salmonella Enteritidis in poultry meat and consumption eggs.\" 245 (2007)","DOI":"10.1016\/j.mimet.2007.04.013"},{"key":"31","doi-asserted-by":"publisher","unstructured":"J Mao, RP Hedrick, VG. Chinchar,  \"Virol.\"  229, \"Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses.\" 212 (1997)","DOI":"10.1006\/viro.1996.8435"},{"key":"32","doi-asserted-by":"publisher","unstructured":"DL Miller, AP Pessier, P Hick, et al.  \"Ranaviruses: Lethal pathogens of ectothermic vertebrates.\"  \"Comparative pathology of ranaviruses and diagnostic techniques.\" 171 (2015)","DOI":"10.1007\/978-3-319-13755-1_7"},{"key":"33","doi-asserted-by":"publisher","unstructured":"KA Moorhead, LA Adamovicz, MC. Allender,  \"J Virol Methods.\"  327, \"Development and analytical validation of a novel quantitative PCR assay for the detection of Trachemys herpesvirus 1.\" 114941 (2024)","DOI":"10.1016\/j.jviromet.2024.114941"},{"key":"34","doi-asserted-by":"publisher","unstructured":"A Mozer  and S. Prost  \"Forensic Sci Int: Animals Environ.\"  3, \"An introduction to illegal wildlife trade and its effects on biodiversity and society.\" 100064 (2023)","DOI":"10.1016\/j.fsiae.2023.100064"},{"key":"36","doi-asserted-by":"publisher","unstructured":"J Pallister, S Goldie, B Coupar, et al.  \"J Virol Methods.\"  146, \"Bohle iridovirus as a vector for heterologous gene expression.\" 419 (2007)","DOI":"10.1016\/j.jviromet.2007.08.016"},{"key":"37","doi-asserted-by":"publisher","unstructured":"AM Picco, JL Brunner, JP. Collins,  \"J Wildl Dis.\"  43, \"Susceptibility of the endangered California tiger salamander, Ambystoma californiense, to ranavirus infection.\" 286 (2007)","DOI":"10.7589\/0090-3558-43.2.286"},{"key":"38","doi-asserted-by":"publisher","unstructured":"MG Ruder, AB Allison, DL Miller, et al.  \"J Am Vet Med Assoc.\"  237, \"Pathology in practice.\" 783 (2010)","DOI":"10.2460\/javma.237.7.783"},{"key":"39","doi-asserted-by":"publisher","unstructured":"E Salzmann, E M\u00fcller, RE. Marschang,  \"J Zoo Wildl Med.\"  52, \"Detection of testadenoviruses and atadenoviruses in tortoises and turtles in Europe.\" 223 (2021)","DOI":"10.1638\/2020-0078"},{"key":"40","doi-asserted-by":"publisher","unstructured":"K Sch\u00f6nb\u00e4chler, H Segner, B Amphimaque, et al.  \"J Zoo Wildl Med.\"  53, \"Health assessment of captive and free-ranging European pond turtles (Emys orbicularis) in Switzerland.\" 159 (2022)","DOI":"10.1638\/2020-0117"},{"key":"41","doi-asserted-by":"publisher","unstructured":"A Sigouin, M Pinedo-Vasquez, R Nasi, et al.  \"J Appl Ecol.\"  54, \"Priorities for the trade of less charismatic freshwater turtle and tortoise species.\" 345 (2017)","DOI":"10.1111\/1365-2664.12797"},{"key":"45","doi-asserted-by":"publisher","unstructured":"CB Stanford, JB Iverson, AGJ Rhodin, et al.  \"Cur Biol.\"  30, \"Turtles and tortoises are in trouble.\" R721 (2020)","DOI":"10.1016\/j.cub.2020.04.088"},{"key":"48","doi-asserted-by":"publisher","unstructured":"P.P. van Dijk,  \"The IUCN Red List of Threatened Species.\"  \"Terrapene carolina.\" e.T21641A97428179 (2011)","DOI":"10.2305\/IUCN.UK.2011-1.RLTS.T21641A9303747.en"},{"key":"49","doi-asserted-by":"publisher","unstructured":"ST Vila\u00e7a, J-F Bienentreu, CR Brunetti, et al.  \"J Virol.\"  93-, \"Frog virus 3 genomes reveal prevalent recombination between ranavirus lineages and their origins in Canada.\" (2019)","DOI":"10.1128\/jvi.00765-19"},{"key":"50","doi-asserted-by":"publisher","unstructured":"JM Winter, L Mumm, LA Adamovicz, et al.  \"J Zoo Wildl Med.\"  51, \"Characterizing the epidemiology of historic and novel pathogens in Blanding's turtles (Emydoidea blandgii).\" 606 (2020)","DOI":"10.1638\/2019-0154"},{"key":"46","doi-asserted-by":"publisher","unstructured":"NK Stilwell, RJ Whittington, PM Hick, et al.  \"Dis Aquat Organ.\"  128, \"Partial validation of a TaqMan real-time quantitative PCR for the detection of ranaviruses.\" 105 (2018)","DOI":"10.3354\/dao03214"},{"key":"14","doi-asserted-by":"publisher","unstructured":"T Easter, J Trautmann, M Gore, et al.  \"People Nat.\"  5, \"Media portrayal of the illegal trade in wildlife: The case of turtles in the US and implications for conservation.\" 758 (2023)","DOI":"10.1002\/pan3.10448"},{"key":"3","doi-asserted-by":"publisher","unstructured":"MC Allender, MA Mitchell, T Torres, et al.  \"J Comp Pathol.\"  149, \"Pathogenicity of frog virus 3-like virus in red-eared slider turtles (Trachemys scripta elegans) at two environmental temperatures.\" 356 (2013)","DOI":"10.1016\/j.jcpa.2013.01.007"},{"key":"47","doi-asserted-by":"publisher","unstructured":"DR VanDevanter, P Warrener, L Bennett, et al.  \"J Clin Microbiol.\"  34, \"Detection and analysis of diverse herpesviral species by consensus primer PCR.\" 1666 (1996)","DOI":"10.1128\/jcm.34.7.1666-1671.1996"},{"key":"1","doi-asserted-by":"publisher","unstructured":"L Adamovicz, MC Allender, G Archer, et al.  \"PLoS One.\"  13, \"Investigation of multiple mortality events in eastern box turtles (Terrapene carolina carolina).\" e0195617 (2018)","DOI":"10.1371\/journal.pone.0195617"},{"key":"10","doi-asserted-by":"publisher","unstructured":"CE Butkus, MC Allender, CA Phillips, et al.  \"J Zoo Wildl Med.\"  48, \"Detection of ranavirus using bone marrow harvested from mortality events in eastern box turtles (Terrapene carolina carolina).\" 1210 (2017)","DOI":"10.1638\/2017-0098.1"},{"key":"44","doi-asserted-by":"publisher","unstructured":"LD Smythe, IL Smith, GA Smith, et al.  \"BMC Infect Dis.\"  2, \"A quantitative PCR (TaqMan) assay for pathogenic Leptospira spp.\" 13 (2002)","DOI":"10.1186\/1471-2334-2-13"},{"key":"11","doi-asserted-by":"publisher","unstructured":"R De Voe, K Geissler, S Elmore, et al.  \"J Zoo Wildl Med.\"  35, \"Ranavirus-associated morbidity and mortality in a group of captive eastern box turtles (Terrapene carolina carolina).\" 534 (2004)","DOI":"10.1638\/03-037"},{"key":"17","doi-asserted-by":"publisher","unstructured":"SD Farnsworth  and RA. Seigel  \"Transp Res Rec.\"  2362, \"Responses, movements, and survival of relocated box turtles during construction of the intercounty connector highway in Maryland.\" 1 (2013)","DOI":"10.3141\/2362-01"},{"key":"25","doi-asserted-by":"publisher","unstructured":"LP Kane, MC Allender, G Archer, et al.  \"J Wildl Dis.\"  53, \"Prevalence of Terrapene herpesvirus 1 in free-ranging eastern box turtles (Terrapene carolina carolina) in Tennessee and Illinois, USA.\" 285 (2017)","DOI":"10.7589\/2016-06-138"},{"key":"27","doi-asserted-by":"publisher","unstructured":"SJA Kimble, AJ Johnson, RN Williams, et al.  \"Ecohealth.\"  14, \"A severe ranavirus outbreak in captive, wild-caught box turtles.\" 810 (2017)","DOI":"10.1007\/s10393-017-1263-8"},{"key":"42","doi-asserted-by":"publisher","unstructured":"RR Sim, MC Allender, LK Crawford, et al.  \"J Zoo Wildl Med.\"  47, \"Ranavirus epizootic in captive eastern box turtles (Terrapene carolina carolina) with concurrent herpesvirus and mycoplasma infection: management and monitoring.\" 256 (2016)","DOI":"10.1638\/2015-0048.1"},{"key":"18","doi-asserted-by":"publisher","unstructured":"SH Feldman, J Wimsatt, RE Marchang, et al.  \"J Wildl Dis.\"  42, \"A novel mycoplasma detected in association with upper respiratory disease syndrome in free-ranging eastern box turtles (Terrapene carolina carolina) in Virginia.\" 279 (2006)","DOI":"10.7589\/0090-3558-42.2.279"},{"key":"26","doi-asserted-by":"publisher","unstructured":"LP Kane, D Bunick, M Abd-Eldaim, et al.  \"J Virol Methods.\"  232, \"Development and validation of quantitative PCR for detection of Terrapene herpesvirus 1 utilizing free-ranging eastern box turtles (Terrapene carolina carolina).\" 57 (2016)","DOI":"10.1016\/j.jviromet.2016.02.002"},{"key":"43","doi-asserted-by":"publisher","unstructured":"RR Sim, TM Norton, E Bronson, et al.  \"Vet Microbiol.\"  175, \"Identification of a novel herpesvirus in captive Eastern box turtles (Terrapene carolina carolina).\" 218 (2015)","DOI":"10.1016\/j.vetmic.2014.11.029"},{"key":"7","doi-asserted-by":"publisher","unstructured":"GA Archer, CA Phillips, L Adamovicz, et al.  \"J Zoo Wildl Med.\"  48, \"Detection of copathogens in free-ranging eastern box turtles (Terrapene carolina carolina) in Illinois and Tennessee.\" 1127 (2017)","DOI":"10.1638\/2017-0148R.1"},{"key":"8","doi-asserted-by":"publisher","unstructured":"J Braun, M Schrenzel, C Witte, et al.  \"J Wildl Dis.\"  50, \"Molecular methods to detect Mycoplasma spp. and testudinid herpesvirus 2 in desert tortoises (Gopherus agassizii) and implications for disease management.\" 757 (2014)","DOI":"10.7589\/2013-09-231"},{"key":"52","doi-asserted-by":"publisher","unstructured":"SB Yonkers, R Schneider, DR Reavill, et al.  \"J Vet Diagn Invest.\"  27, \"Coinfection with a novel fibropapilloma-associated herpesvirus and a novel Spirorchis sp. in an Eastern box turtle (Terrapene carolina) in Florida.\" 408 (2015)","DOI":"10.1177\/1040638715589612"},{"key":"13","doi-asserted-by":"publisher","unstructured":"A Doszpoly, JFX Wellehan, AL Childress, et al.  \"Infect Genet Evol.\"  17, \"Partial characterization of a new adenovirus lineage discovered in testudinoid turtles.\" 106 (2013)","DOI":"10.1016\/j.meegid.2013.03.049"},{"key":"6","doi-asserted-by":"publisher","unstructured":"AC Aplasca, V Titus, RJ Ossiboff, et al.  \"J Wildl Dis.\"  55, \"Health assessment of free-ranging chelonians in an urban section of the Bronx river, New York, USA.\" 352 (2019)","DOI":"10.7589\/2017-12-304"},{"key":"24","doi-asserted-by":"publisher","unstructured":"AJ Johnson, AP Pessier, JFX Wellehan, et al.  \"J Wildl Dis.\"  44, \"Ranavirus infection of free-ranging and captive box turtles and tortoises in the United States.\" 851 (2008)","DOI":"10.7589\/0090-3558-44.4.851"},{"key":"51","doi-asserted-by":"publisher","unstructured":"DB Woodburn, MJ Kinsel, CP Poll, et al.  \"Vet Pathol.\"  58, \"Shell lesions associated with Emydomyces testavorans infection in freshwater aquatic turtles.\" 578 (2021)","DOI":"10.1177\/0300985820985217"},{"key":"28","doi-asserted-by":"publisher","unstructured":"SR Klee, J Tyczka, H Ellerbrok, et al.  \"BMC Microbiol.\"  6, \"Highly sensitive real-time PCR for specific detection and quantification of Coxiella burnetii.\" 2 (2006)","DOI":"10.1186\/1471-2180-6-2"}],"container-title":["Journal of Zoo and Wildlife Medicine"],"original-title":[],"deposited":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T21:08:07Z","timestamp":1791234487000},"score":1,"resource":{"primary":{"URL":"https:\/\/bioone.org\/journals\/journal-of-zoo-and-wildlife-medicine\/volume-57\/issue-2\/2025-0081\/LARGE-SCALE-DISEASE-ASSOCIATED-MORTALITY-EVENT-OF-EASTERN-BOX-TURTLES\/10.1638\/2025-0081.full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,3,25]]},"references-count":52,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2026,6,1]]}},"URL":"https:\/\/doi.org\/10.1638\/2025-0081","relation":{},"ISSN":["1042-7260","1937-2825"],"issn-type":[{"value":"1042-7260","type":"print"},{"value":"1937-2825","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,3,25]]}}}