Revisiting Ophidiomycosis (Snake Fungal Disease) After a Decade of Targeted Research

Abstract

Emerging infectious diseases (EIDs) are typically characterized by novelty (recent detection) and by increasing incidence, distribution, and/or pathogenicity. Ophidiomycosis, also called snake fungal disease, is caused by the fungus Ophidiomyces ophidiicola (formerly "ophiodiicola"). Ophidiomycosis has been characterized as an EID and as a potential threat to populations of Nearctic snakes, sparking over a decade of targeted research. However, the severity of this threat is unclear. We reviewed the available literature to quantify incidence and effects of ophidiomycosis in Nearctic snakes, and to evaluate whether the evidence supports the ongoing characterization of ophidiomycosis as an EID. Data from Canada remain scarce, so we supplemented the literature review with surveys for O. ophidiicola in the Canadian Great Lakes region. Peer-reviewed reports of clinical signs consistent with ophidiomycosis in free-ranging, Nearctic snakes date back to at least 1998, and retrospective molecular testing of samples extend the earliest confirmed record to 1986. Diagnostic criteria varied among publications (n = 33), confounding quantitative comparisons. Ophidiomycosis was diagnosed or suspected in 36/121 captive snakes and was fatal in over half of cases (66.7%). This result may implicate captivity-related stress as a risk factor for mortality from ophidiomycosis, but could also reflect reporting bias (i.e., infections are more likely to be detected in captive snakes, and severe cases are more likely to be reported). In contrast, ophidiomycosis was diagnosed or suspected in 441/2,384 free-ranging snakes, with mortality observed in 43 (9.8 %). Ophidiomycosis was only speculatively linked to population declines, and we found no evidence that the prevalence of the pathogen or disease increased over the past decade of targeted research. Supplemental surveys and molecular (qPCR) testing in Ontario, Canada detected O. ophidiicola on 76 of 657 free-ranging snakes sampled across ~136,000 km². The pathogen was detected at most sites despite limited and haphazard sampling. No large-scale mortality was observed. Current evidence supports previous suggestions that the pathogen is a widespread, previously unrecognized endemic, rather than a novel pathogen. Ophidiomycosis may not pose an imminent threat to Nearctic snakes, but further research should investigate potential sublethal effects of ophidiomycosis such as altered reproductive success that could impact population growth, and explore whether shifting environmental conditions may alter host susceptibility.

Keywords: Ophidiomyces ophidiicola; emerging infectious disease; fungal pathogen; ophidiomycosis; qPCR; reptile; snake.

Figure 1

(A) Ophidiomycosis manifesting in gross lesions on the skin and eye of an eastern foxsnake (Pantherophis vulpinus) with a plaque of fungal hyphae growing over the eye (photo: Sheeva Nakhaie). (B) Ophidiomycosis on a queensnake (Regina septemvittata; photos: Heather Fotherby); (C,D) Gray ratsnake (Pantherophis spiloides; photos: Kenny Ruelland) from southeastern Ontario, Canada with suspect ophidiomycosis.

Figure 2

Sampling locations for snakes tested for ophidiomycosis in the Great Lakes region of Ontario, Canada, showing diagnoses based on the criteria in Table 1. Locations are shown for 542 snakes for which specific coordinates were available. A further 115 samples were tested and included in Table 2 but are not shown on the map as they were were submitted to the Canadian Wildlife Health Center without precise location data.

Figure 3

(A) The prevalence of Ophidiomyces ophidiicola (detected through PCR, qPCR, or culture) in samples collected between 2008 and 2018 and reported in the peer-reviewed literature did not increase over time. (B) The prevalence of reported observations of gross lesions suggestive of ophidiomycosis did not increase between 2007 and 2018. Data represent samples collected from 42 species (Supplementary Table 1). Size of points varies with sample size reported in each study, sample sizes for each time-point are noted the top of each panel, and the solid lines and gray-shaded areas indicate the fixed-effect model predictions and 95% confidence intervals.