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.

Genetic mechanisms and biological processes underlying host response to ophidiomycosis (Snake Fungal Disease) inferred from tissue-specific transcriptome analyses

“…Finally, SFD is difficult to diagnose in the wild (42) and our results suggest that possibly like as is the case of white nose syndrome, physiological impacts of SFD may start to cause deterioration of internal organs before clinical signs are manifested on the skin (77). A potential avenue for future research would be to study gene expression through time during early or late stages of O. ophidiicola infection to document changes before and after the onset of clinical signs.…”

“…Finally, SFD is difficult to diagnose in the wild (42) and our results suggest that possibly like as is the case of white nose syndrome, physiological impacts of SFD may start to cause deterioration of internal organs before clinical signs are manifested on the skin (77).…”

“…Clinical signs of ophidiomycosis vary among individuals, from general signs such as lethargy, skin lesions, excessive shedding, to crusts, granulomas, corneal opacity, and ulcers on the head and body in more severe cases (29). Ophidiomycosis has the potential to cause widespread morbidity and mortality in snakes (31,32,35,40,41) but the mode of infection, specific mechanisms of pathology, and physiological responses by infected individuals are unclear despite the value of this information for understanding and mitigating the impact of this disease (29,42). Specifically, the two key elements of SFD pathology that are still unknown are (a) Is the snake host response is localized to the skin, as in the case of Bd infections in amphibians, or whether SFD is more systemic disease, like the white nose syndrome in bats?…”

Population genetic analysis of Ophidiomyces ophidiicola, the causative agent of snake fungal disease, indicates recent introductions to the USA

“…Hybridization between lineages is also expected to occur more frequently in regions with high Oo prevalence (i.e., more opportunities for co-infections). Thus far, in-depth studies of Oo prevalence in snake communities have been very limited in their geographic scope (e.g., [20,38,39]). Future work would be beneficial to understand the relationship between prevalence and the abundance of hybrid strains.…”

“…Snake fungal disease (SFD or ophidiomycosis) is often cited as a fungal EID afflicting wildlife [17, 18], although the extent to which SFD is actively emerging is difficult to quantitatively assess [19, 20]. The disease first gained attention in 2008 when severe fungal infections manifested in a well-studied population of eastern massasauga rattlesnakes ( Sistrurus catenatus ) in Illinois, USA [21].…”