Development of Snake Fungal Disease after Experimental Challenge with Ophidiomyces ophiodiicola in Cottonmouths (Agkistrodon piscivorous)

Abstract

Snake fungal disease (SFD) is a clinical syndrome associated with dermatitis, myositis, osteomyelitis, and pneumonia in several species of free-ranging snakes in the US. The causative agent has been suggested as Ophidiomyces ophiodiicola, but other agents may contribute to the syndrome and the pathogenesis is not understood. To understand the role of O. ophiodiicola in SFD, a cottonmouth snake model of SFD was designed. Five cottonmouths (Agkistrodon piscivorous) were experimentally challenged by nasolabial pit inoculation with a pure culture of O. ophiodiicola. Development of skin lesions or facial swelling at the site of inoculation was observed in all snakes. Twice weekly swabs of the inoculation site revealed variable presence of O. ophiodiicola DNA by qPCR in all five inoculated snakes for 3 to 58 days post-inoculation; nasolabial flushes were not a useful sampling method for detection. Inoculated snakes had a 40% mortality rate. All inoculated snakes had microscopic lesions unilaterally on the side of the swabbed nasolabial pit, including erosions to ulcerations and heterophilic dermatitis. All signs were consistent with SFD; however, the severity of lesions varied in individual snakes, and fungal hyphae were only observed in 3 of 5 inoculated snakes. These three snakes correlated with post-mortem tissue qPCR evidence of O. ophiodiicola. The findings of this study conclude that O. ophiodiicola inoculation in a cottonmouth snake model leads to disease similar to SFD, although lesion severity and the fungal load are quite variable within the model. Future studies may utilize this model to further understand the pathogenesis of this disease and develop management strategies that mitigate disease effects, but investigation of other models with less variability may be warranted.

Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk

“…A fungal pathogen causing growing concern is Ophidiomyces ophiodiicola , the species responsible for snake fungal disease (SFD; Lorch et al , Allender et al ). The earliest known record of SFD is from a museum specimen collected in 2000 from southern Illinois (Allender et al ).…”

“…Although numerous taxa in addition to amphibians and bats are affected by fungal pathogens, estimates of disease prevalence, pathogen prevalence on hosts, and population-level responses to these pathogens are lacking or poorly understood in many species (Fisher et al 2012, Allender et al 2016a. A fungal pathogen causing growing concern is Ophidiomyces ophiodiicola, the species responsible for snake fungal disease (SFD; Lorch et al 2015, Allender et al 2015a). The earliest known record of SFD is from a museum specimen collected in 2000 from southern Illinois (Allender et al 2016b).…”

“…Knowledge of O. ophiodiicola ecology (Allender et al 2015d, McCoy et al 2017, geographic distribution (Allender et al 2015d, Lorch et al 2016, detection (Allender et al 2016a), pathogenesis (Lorch et al 2015, Allender et al 2015a, and snake hematology (Allender et al 2015c(Allender et al , 2016b has increased over the last few years. However, unbiased estimates of O. ophiodiicola prevalence in host populations are still lacking.…”

Pharmacokinetics of nebulized and subcutaneously implanted terbinafine in cottonmouths (Agkistrodon piscivorus)

“…Ophidiomyces ophiodiicola, the causative agent of snake fungal disease (SFD), is identified as a primary pathogen in several free-ranging snake species, including pigmy rattlesnakes (Sistrurus miliarius barbouri) (Cheatwood et al, 2003), Eastern massasaugas (Sistrurus catenatus catenatus) (Allender et al, 2011(Allender et al, , 2013Robertson, Chinnadurai, Woodburn, Adkesson, & Landolfi, 2016;Tetzlaff, Allender, Ravesi, Smith, & Kingsbury, 2015), timber rattlesnakes (Crotalus horridus) (McBride et al, 2015), and several colubrids (Dolinski, Allender, Hsiao, & Maddox, 2014;Guthrie et al, 2016;Ohkura et al, 2016). Cottonmouths (Agkistrodon piscivorus) (Allender, Baker et al, 2015) and corn snakes (Pantherophis guttatus) (Lorch et al, 2015) experimentally inoculated with O. ophiodiicola were observed with clinical signs, molecular, and histopathological evidence consistent with SFD, thus determining causation. Currently, there is no reported therapy available for SFD.…”

Characterization of Metarhizium viride Mycosis in Veiled Chameleons (Chamaeleo calyptratus), Panther Chameleons (Furcifer pardalis), and Inland Bearded Dragons (Pogona vitticeps)

“…captive snakes all over the world; it is also emerging in free-ranging snake populations across the United States (1,(13)(14)(15)(16)(17)(18). Metarhizium granulomatis is a common fungal pathogen in captive veiled chameleons kept as pets as well as in zoological enclosures; it causes dermatitis and fatal granulomatous glossitis in conjunction with systemic visceral mycosis and is therefore an important differential causative pathogen for fungal dermatitis in these species (19,20).…”