Abstract

Ophidiomyces ophiodiicola (Oo) is the leading fungal pathogen of captive snakes and also causes snake fungal disease (SFD), an emerging disease of wild snakes in the United States. Necropsies on carcasses of two wild snakes collected in New Jersey in 2012, a black rat snake (Pantherophis alleghaniensis) and a Northern copperhead (Agkistrodon contortrix mokasen), showed that they died with extensive cutaneous lesions due to ophidiomycosis (SFD) and suspected ophidiomycosis, respectively (Paré, Schantz, unpublished data). This prompted a collaborative New Jersey Department of Fish and Wildlife (NJDFW) and Wildlife Conservation Society (WCS) health survey of free-ranging snakes in 2013 and 2014. The aim of the study was to determine if ophidiomycosis was present among populations of endangered timber rattlesnakes (Crotalus horridus) in the Pinelands and in the Northern Region of New Jersey and if so, to assess the impact of the disease on these populations. Known timber rattlesnake hibernacula, transient basking habitats, and gestation sites were visited from emergence in end-April/early May, and throughout the summer. Sick snakes, defined as any snake with visible skin lesions, were captured and transferred to the WCS Wildlife Health Center (WHC). Snakes were immobilized, weighed, sexed, transponded, and morphometric measurements were recorded. Whole body radiographs were obtained and blood collected. Skin lesions were described and recorded. Fecal samples, when available, were tested for parasites. Biopsies of skin lesions were collected for histopathology and fungal culture. Snakes were housed at the WHC as needed or until lesions resolved, and were then released at capture sites. Ophidiomycosis was diagnosed in snakes from the Northern Region and the Pinelands. Timber rattlesnakes were the predominantly affected species, but disease was also recorded in black rat snakes, corn snakes (Pantherophis guttatus), Northern black racers (Coluber constrictor constrictor), and Northern pine snakes (Pituophis melanoleucus melanoleucus).

Lesions in affected timber rattlesnakes were often mild, sometimes moderate, and consisted of dried crusts and focal scale necrosis, with or without subjacent tissue swelling, often over the head but also along the body. These were similar to lesions referred to over many years as “hibernation blisters” or “hibernation sores,” and traditionally dismissed by field biologists as being “normal” upon emergence from hibernacula. Hyaline, slender, parallel-walled, branching, septate hyphae were present in H&E stained tissue sections. Surface arthroconidiation, a common histologic feature of Oo skin infection, was noted in several snakes. Culture grew Oo, and identification was confirmed with molecular probes. Infection in one corn snake caused unsightly distortion of facial structures that were severe enough to warrant consideration of euthanasia, but resolved remarkably well with successive sheds. Lesions in a black rat snake were different and consisted of multiple doughy to fluctuant subcutaneous swellings scattered along the lateral and dorsal aspects of the body; these were confirmed to be Oo subcutaneous granulomas, based on histology and culture. This presentation of ophidiomycosis is atypical for SFD in wild snakes, but is not unusual in captive colubrids. Oo isolates usually fail to grow at 35°C; limited thermotolerance and increased immune efficiency may partly explain why lesions in rattlesnakes, corn snakes, and pine snakes typically resolved after successive sheds when snakes were provided with thermal support and a clean environment. Lesions in the black rat snake regressed with systemic itraconazole, but then recurred. This snake is currently on a combined itraconazole and terbinafine treatment regimen.

Results of this study indicate that Oo is present in the North Region and Pinelands ecosystems in New Jersey. Lesions identical to those labeled as hibernation sores in the past were determined to be due to Oo, suggesting the disease might have been present for over a decade in wild snakes in New Jersey. Heat and sunlight, or thermal support in captive animals, might allow for gradual spontaneous or unassisted regression of lesions with every successive shed in many, if not most, rattlesnakes.