{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T19:51:02Z","timestamp":1793476262045,"version":"4.5.0"},"reference-count":50,"publisher":"Wildlife Disease Association","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Journal of Wildlife Diseases"],"published-print":{"date-parts":[[2022,1,4]]},"abstract":"<jats:p>Ophidiomycosis, caused by the fungus Ophidiomyces ophidiicola, is an infectious disease of wild and managed snakes worldwide. Lake Erie watersnakes (LEWS; Nerodia sipedon insularum) were listed as threatened under the US Endangered Species Act from 1999 to 2011 and were first diagnosed with ophidiomycosis in 2009. Our objective was to characterize the epidemiology of ophidiomycosis in LEWS. We hypothesized that the prevalence of skin lesions, O. ophidiicola DNA, and ophidiomycosis disease categories would show spatial and temporal variation and clustering, with higher prevalence at sites with greater human disturbance and prevalence increasing over time. Snakes were captured via visual encounter surveys at five sites across four islands and visually inspected for skin lesions suggestive of ophidiomycosis; then body swabs were collected to detect O. ophidiicola DNA using quantitative PCR. Each snake was assigned an ophidiomycosis category based on the presence of skin lesions and O. ophidiicola. We evaluated 837 LEWS between 2017 and 2020 and detected ophidiomycosis at all five sites. Logistic regression analysis showed temporal and spatial variation in disease, with higher risk of apparent ophidiomycosis (lesions present and O. ophidiicola detected) at Kelleys Island State Park, compared to all other sites; in May, compared to July; and in 2019, compared to 2018. The presence of emerging herbaceous wetlands, urban land change, and certain soil types increased the odds of both lesion presence and quantitative PCR detection of O. ophidiicola. Overall, ophidiomycosis epidemiology varied among sites: the disease appeared to be endemic at most sites and emerging at one site. Ongoing efforts to monitor population health and mortality associated with disease prevalence are needed to inform mitigation aimed at reducing the impact of ophidiomycosis in LEWS.<\/jats:p>","DOI":"10.7589\/jwd-d-21-00111","type":"journal-article","created":{"date-parts":[[2022,1,4]],"date-time":"2022-01-04T06:55:50Z","timestamp":1641279350000},"page":"100-113","source":"Crossref","is-referenced-by-count":7,"title":["EPIDEMIOLOGY OF OPHIDIOMYCOSIS IN LAKE ERIE WATERSNAKES (NERODIA SIPEDON INSULARUM)"],"prefix":"10.7589","volume":"58","author":[{"given":"Ellen","family":"Haynes","sequence":"first","affiliation":[{"name":"Wildlife Epidemiology Lab, University of Illinois Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristin","family":"Stanford","sequence":"additional","affiliation":[{"name":"Franz Theodore Stone Laboratory, The Ohio State University, 878 Bayview Ave., Put-In-Bay, Ohio 43456, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Megan","family":"Gramhofer","sequence":"additional","affiliation":[{"name":"Wildlife Epidemiology Lab, University of Illinois Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn","family":"Vivirito","sequence":"additional","affiliation":[{"name":"Wildlife Epidemiology Lab, University of Illinois Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kennymac","family":"Durante","sequence":"additional","affiliation":[{"name":"Wildlife Epidemiology Lab, University of Illinois Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Allison","family":"Wright","sequence":"additional","affiliation":[{"name":"Wildlife Epidemiology Lab, University of Illinois Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Csaba","family":"Varga","sequence":"additional","affiliation":[{"name":"Department of Pathobiology, University of Illinois Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew C.","family":"Allender","sequence":"additional","affiliation":[{"name":"Wildlife Epidemiology Lab, University of Illinois Urbana-Champaign, 2001 S Lincoln Ave., Urbana, Illinois 61802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4415","reference":[{"key":"22","doi-asserted-by":"crossref","unstructured":"M. Kulldorff,  \"Commun Stat Theory Methods.\"  26, \"A spatial scan statistic.\" 1481 (1997)","DOI":"10.1080\/03610929708831995"},{"key":"21","doi-asserted-by":"crossref","unstructured":"RB King, KM Stanford, PC Jones,  \"Ecol Evol.\"  8, \"Sunning themselves in heaps, knots, and snarls: The extraordinary abundance and demography of island watersnakes.\" 7500 (2018)","DOI":"10.1002\/ece3.4191"},{"key":"2","doi-asserted-by":"crossref","unstructured":"MC Allender, D Bunick, E Dzhaman, et al.  \"J Vet Diagn Invest.\"  27, \"Development and use of a real-time polymerase chain reaction assay for the detection of Ophidiomyces ophiodiicola in snakes.\" 217 (2015b)","DOI":"10.1177\/1040638715573983"},{"key":"12","doi-asserted-by":"crossref","unstructured":"RW Clark, MN Marchand, BJ Clifford, et al.  \"Biol Conserv.\"  144, \"Decline of an isolated timber rattlesnake (Crotalus horridus) population: interactions between climate change, disease, and loss of genetic diversity.\" 886 (2011)","DOI":"10.1016\/j.biocon.2010.12.001"},{"key":"29","doi-asserted-by":"crossref","unstructured":"MP McBride, KB Wojick, TA Georoff, et al.  \"J Zoo Wildl Med.\"  46, \"Ophidiomyces ophiodiicola dermatitis in eight free-ranging timber rattlesnakes (Crotalus horridus) from Massachusetts.\" 86 (2015)","DOI":"10.1638\/2012-0248R2.1"},{"key":"40","doi-asserted-by":"crossref","unstructured":"LF Skerratt, L Berger, R Speare, et al.  \"EcoHealth.\"  4, \"Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs.\" 125 (2007)","DOI":"10.1007\/s10393-007-0093-5"},{"key":"18","doi-asserted-by":"crossref","unstructured":"ET Hileman, MC Allender, DR Bradke, et al.  \"J Wildl Manage.\"  82, \"Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk.\" 173 (2018)","DOI":"10.1002\/jwmg.21345"},{"key":"28","doi-asserted-by":"crossref","unstructured":"JM Lorch, J Lankton, K Werner, et al.  \"Mbio.\"  6, \"Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease.\" e01534 (2015)","DOI":"10.1128\/mBio.01534-15"},{"key":"44","unstructured":"SJ Tetzlaff, MJ Ravesi, MC Allender, et al.  \"Herpetol Conserv Biol.\"  12, \"Snake fungal disease affects behavior of free-ranging massasauga rattlesnakes (Sistrurus catenatus).\" 624 (2017)"},{"key":"15","doi-asserted-by":"crossref","unstructured":"MC Fisher, DA Henk, CJ Briggs, et al.  \"Nature.\"  484, \"Emerging fungal threats to animal, plant and ecosystem health.\" 186 (2012)","DOI":"10.1038\/nature10947"},{"key":"7","doi-asserted-by":"crossref","unstructured":"DS Blehert, AC Hicks, M Behr, et al.  \"Science.\"  323, \"Bat white-nose syndrome: An emerging fungal pathogen?\" 227 (2009)","DOI":"10.1126\/science.1163874"},{"key":"25","doi-asserted-by":"crossref","unstructured":"RV. Lenth,  \"J Stat Softw.\"  69, \"Least-squares means: the R package lsmeans.\" 1 (2016)","DOI":"10.18637\/jss.v069.i01"},{"key":"16","unstructured":"M Grisnik, JE Leys, D Bryan, et al.  \"Herpetol Rev.\"  49, \"Host and geographic range of snake fungal disease in Tennessee, USA.\" 682 (2018)"},{"key":"8","doi-asserted-by":"crossref","unstructured":"G Brearley, J Rhodes, A Bradley, et al.  \"Biol Rev.\"  88, \"Wildlife disease prevalence in human-modified landscapes.\" 427 (2013)","DOI":"10.1111\/brv.12009"},{"key":"4","doi-asserted-by":"crossref","unstructured":"MC Allender, DB Raudabaugh, FH Gleason, et al.  \"Fungal Ecol.\"  17, \"The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations.\" 187 (2015c)","DOI":"10.1016\/j.funeco.2015.05.003"},{"key":"5","unstructured":"SJ Baker, E Haynes, M Gramhofer, et al.  \"Herpetol Rev.\"  50, \"Case definition and diagnostic testing for snake fungal disease.\" 279 (2019)"},{"key":"9","doi-asserted-by":"crossref","unstructured":"FT Burbrink, JM Lorch, KR Lips,  \"Sci Adv.\"  3, \"Host susceptibility to snake fungal disease is highly dispersed across phylogenetic and functional trait space.\" e1701387 (2017)","DOI":"10.1126\/sciadv.1701387"},{"key":"17","doi-asserted-by":"crossref","unstructured":"E Haynes, HC Chandler, BS Stegenga, et al.  \"Sci Rep.\"  10, \"Ophidiomycosis surveillance of snakes in Georgia, USA reveals new host species and taxonomic associations with disease.\" 10870 (2020)","DOI":"10.1038\/s41598-020-67800-1"},{"key":"26","doi-asserted-by":"crossref","unstructured":"CM Lind, CM McCoy, TM Farrell,  \"J Wildl Dis.\"  54, \"Tracking outcomes of snake fungal disease in free-ranging pygmy rattlesnakes (Sistrurus miliarius).\" 352 (2018)","DOI":"10.7589\/2017-05-109"},{"key":"38","unstructured":"\"R: a Language and Environment for Statistical Computing.\"  (2018)"},{"key":"37","unstructured":"\"PRISM climate data.\"  (2020)"},{"key":"46","unstructured":"\"Web Soil Survey.\"  (2019)"},{"key":"1","doi-asserted-by":"crossref","unstructured":"MC Allender, S Baker, D Wylie, et al.  \"PLoS One.\"  10, \"Development of snake fungal disease after experimental challenge with Ophidiomyces ophiodiicola in cottonmouths (Agkistrodon piscivorous).\" e0140193 (2015a)","DOI":"10.1371\/journal.pone.0140193"},{"key":"31","doi-asserted-by":"crossref","unstructured":"CM McKenzie, PT Oesterle, B Stevens, et al.  \"Vet Pathol.\"  57, \"Ophidiomycosis in red cornsnakes (Pantherophis guttatus): Potential roles of brumation and temperature on pathogenesis and transmission.\" 825 (2020)","DOI":"10.1177\/0300985820953423"},{"key":"3","doi-asserted-by":"crossref","unstructured":"MC Allender, MJ Dreslik, SJ Wylie, et al.  \"Emerg Infect Dis.\"  17, \"Chrysosporium sp. infection in eastern massasauga rattlesnakes.\" 2383 (2011)","DOI":"10.3201\/eid1712.110240"},{"key":"6","doi-asserted-by":"crossref","unstructured":"SJ Baker, ML Niemiller, AJ Stites, et al.  \"Conserv Genet Resour.\"  12, \"Evaluation of environmental DNA to detect Sistrurus catenatus and Ophidiomyces ophiodiicola in crayfish burrows.\" 13 (2020)","DOI":"10.1007\/s12686-018-1053-9"},{"key":"10","doi-asserted-by":"crossref","unstructured":"LJ Campbell, J Burger, RT Zappalorti, et al.  \"J Fungi.\"  7, \"Soil reservoir dynamics of Ophidiomyces ophidiicola, the causative agent of snake fungal disease.\" 461 (2021)","DOI":"10.3390\/jof7060461"},{"key":"11","doi-asserted-by":"crossref","unstructured":"HC Chandler, MC Allender, BS Stegenga, et al.  \"PLoS One.\"  14, \"Ophidiomycosis prevalence in Georgia's eastern indigo snake (Drymarchon couperi) populations.\" e0218351 (2019)","DOI":"10.1371\/journal.pone.0218351"},{"key":"13","doi-asserted-by":"crossref","unstructured":"K Durante, E Haynes, K Vivirito, et al.  \"J Wildl Dis.\"  57, \"Investigating the impact of group holding on the transfer of Ophidiomyces ophidiicola DNA in free-ranging Lake Erie watersnakes (Nerodia sipedon insularum).\" 980 (2021)","DOI":"10.7589\/JWD-D-21-00010"},{"key":"14","unstructured":"\"Percent emergent herbaceous wetlands.\"  (2014)"},{"key":"19","doi-asserted-by":"crossref","unstructured":"C Homer, J Dewitz, S Jin, et al.  \"ISPRS J Photogramm Remote Sens.\"  162, \"Conterminous United States land cover change patterns 2001\u20132016 from the 2016 National Land Cover Database.\" 184 (2020)","DOI":"10.1016\/j.isprsjprs.2020.02.019"},{"key":"20","doi-asserted-by":"crossref","unstructured":"RB. King,  \"Copeia.\"  1986, \"Population ecology of the Lake Erie water snake, Nerodia sipedon insularum.\" 757 (1986)","DOI":"10.2307\/1444959"},{"key":"23","unstructured":"M. Kulldorff,  \"SaTScan\u2122 v9.6: Software for the spatial and space-time scan statistics.\"  (2018)"},{"key":"24","doi-asserted-by":"crossref","unstructured":"M Kulldorff, R Heffernan, J Hartman, et al.  \"PLoS Med.\"  2, \"A space-time permutation scan statistic for disease outbreak detection.\" e59 (2005)","DOI":"10.1371\/journal.pmed.0020059"},{"key":"27","doi-asserted-by":"crossref","unstructured":"JM Lorch, S Knowles, JS Lankton, et al.  \"Philos Trans R Soc B Biol Sci.\"  371, \"Snake fungal disease: An emerging threat to wild snakes.\" 20150457 (2016)","DOI":"10.1098\/rstb.2015.0457"},{"key":"30","doi-asserted-by":"crossref","unstructured":"CM McCoy, CM Lind, TM Farrell,  5, \"Environmental and physiological correlates of the severity of clinical signs of snake fungal disease in a population of pigmy rattlesnakes, Sistrurus miliarius. Conserv Physiol\" cow077 (2017)","DOI":"10.1093\/conphys\/cow077"},{"key":"32","unstructured":"\"Bennington series.\"  (2007)"},{"key":"33","unstructured":"\"Castalia series.\"  (2012)"},{"key":"34","unstructured":"\"National Land Cover Database 2011 legend.\"  (2011)"},{"key":"35","unstructured":"\"Multi-Resolution Land Characteristics Consortium.\"  (2016)"},{"key":"36","doi-asserted-by":"crossref","unstructured":"MD Pauza, MM Driessen, LF Skerratt,  \"Dis Aquat Organ.\"  92, \"Distribution and risk factors for spread of amphibian chytrid fungus Batrachochytrium dendrobatidis in the Tasmanian wilderness world heritage area, Australia.\" 193 (2010)","DOI":"10.3354\/dao02212"},{"key":"39","doi-asserted-by":"crossref","unstructured":"JJ Ryder, MR Miller, A White, et al.  \"Oikos.\"  116, \"Host-parasite population dynamics under combined frequency- and density-dependent transmission.\" 2017 (2007)","DOI":"10.1111\/j.2007.0030-1299.15863.x"},{"key":"41","doi-asserted-by":"crossref","unstructured":"A Spitzen-van der Sluijs, A Martel, J Asselberghs, et al.  \"Emerg Infect Dis.\"  22, \"Expanding distribution of lethal amphibian fungus Batrachochytrium salamandrivorans in Europe.\" 1286 (2016)","DOI":"10.3201\/eid2207.160109"},{"key":"42","unstructured":"\"Stata Statistical Software: Release 16.\"  (2019)"},{"key":"43","unstructured":"AG Stengle, TF Tyning, PR Sievert,  \"The biology of rattlesnakes II.\"  \"What is Normal? Observations of a possible disease process in Massachusetts timber rattlesnakes (Crotalus horridus).\" 41 (2017)"},{"key":"45","unstructured":"\"US Census.\"  (2020)"},{"key":"47","unstructured":"US Fish  and Wildlife Service  \"Fed Regist.\"  64, \"Endangered and threatened wildlife and plants; threatened status for Lake Erie Water Snakes (Nerodia sipedon insularum) on the offshore islands of western Lake Eri.\" 47126 (1999)"},{"key":"48","unstructured":"US Fish  and Wildlife Service  \"Fed Regist.\"  76, \"Endangered and threatened wildlife and plants; removal of the Lake Erie watersnake (Nerodia sipedon insularum) from the federal list of endangered and threatened wildlife.\" 50680 (2011)"},{"key":"49","doi-asserted-by":"crossref","unstructured":"WN Venables  and BD Ripley  \"Modern applied statistics with S.\"  495 (2002)","DOI":"10.1007\/978-0-387-21706-2"},{"key":"50","doi-asserted-by":"crossref","unstructured":"DM Walker, JE Leys, M Grisnik, et al.  \"ISME J.\"  13, \"Variability in snake skin microbial assemblages across spatial scales and disease states.\" 2209 (2019)","DOI":"10.1038\/s41396-019-0416-x"}],"container-title":["Journal of Wildlife Diseases"],"original-title":[],"deposited":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T07:55:58Z","timestamp":1793433358000},"score":1,"resource":{"primary":{"URL":"https:\/\/bioone.org\/journals\/journal-of-wildlife-diseases\/volume-58\/issue-1\/JWD-D-21-00111\/EPIDEMIOLOGY-OF-OPHIDIOMYCOSIS-IN-LAKE-ERIE-WATERSNAKES-NERODIA-SIPEDON-INSULARUM\/10.7589\/JWD-D-21-00111.full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,4]]},"references-count":50,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,1,1]]}},"URL":"https:\/\/doi.org\/10.7589\/jwd-d-21-00111","relation":{},"ISSN":["0090-3558","1943-3700"],"issn-type":[{"value":"0090-3558","type":"print"},{"value":"1943-3700","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,4]]}}}