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01 Snake Fungal Disease

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Known Species Affected:
Acrochordus sp.
Chilabothrus inornatus
Corallus hortulana
Eunectes Murinus
Eunectes notaeus
Boiga irregularis
Cemophora coccinea
Coluber constrictor
Drymarchon couperi
Lampropeltis californiae
Lampropeltis elapsoides
Lampropeltis getula
Lampropeltis nigra
Lampropeltis triangulum
Dinodon rufozonatum
Masticophis flagellum
Opheodrys aestivus
Pantherophis alleghaniensis
Pantherophis emoryi
Pantherophis guttatus
Pantherophis obsoletus
Pantherophis ramspottii
Pantherophis spiloides
Pantherophis vulpinus
Pituophis ruthveni
Pituophis catenifer
Storeria dekayi
Storeria occipitomaculata
Carphophis amoenus
Diadophis punctatus
Farancia abacura
Farancia erytrogramma
Heterodon platirhinos
Hydrodynastes gigas
Hoplocephalus bungaroides
Naja atra
Subsessor bocourti
Natrix helvetica
Natrix tessellata
Nerodia clarkii
Nerodia erythrogaster
Nerodia fasciata
Neropdia rhombifer
Nerodia sipedon
Nerodia taxispilota
Regina septevittata
Thamnophis proximus
Thamnophis radix
Thamnophis saurita
Thamnophis sirtalis
Virginia valeriae
Phyton bivittatus
Pythin regius
Python sebae
Agkistrodon contortrix
Agkistrodon piscivorus
Crotalus adamanteus
Crotalus horridus
Sistrrus catenatus
Sistrurus miliarius
Vipera berus
(Allender et al., 2020; Nicola et al., 2022)
Cause of the Disease

The fungus Ophidiomyces ophiodiicola, characterized as a saprobic organism, causes snake fungal disease in multiple snake species [9]. A saprobic organism can break down and feed on dead and decaying organic matter. O. ophiodiicola has demonstrated this ability through its tolerance to a wide range of environmental conditions, including dry conditions, pH levels ranging from 5 to 11, temperature levels ranging from 7 to 35 degrees Celsius, and its utilization of complex carbon, nitrogen, and natural sulfur compounds. Additionally, the fungus can grow on certain dead organisms and tissues; this collectively suggests that O. ophiodiicola functions as an opportunistic pathogen when infecting snakes [3,9]. This means that that the fungus can infect snakes that are already stressed or injured, but it can also act as a primary pathogen that is capable of causing disease in healthy individuals [2]. This makes the disease especially difficult to manage and prevent. Another study by Campbell et al. (2021) demonstrated that O. ophiodiicola could grow in soil lacking a native microbial community, likely due to limited resources and the production of metabolites that inhibited the fungal pathogen's development. Overall, O. ophiodiicola's ability to remain in the environment is a concern for exposure and reinfection of wild snakes.  

Factors that contribute to O. ophiodiicola's ability to cause disease include the production of enzymes that break down skin and tissue, such as keratinase, lipase, and gelatinase [13]. Keratinase enables the fungus to break down keratin, a major component of snakeskin and scales, thereby allowing it to penetrate the outermost layer of the skin. Lipase is the enzyme responsible for the breakdown of lipids with gelatinase activity, could lead to a weakened skin protective barrier. Although breaks in the skin, such as cuts, abrasions, or ulcers, are not needed to initiate O. ophiodiicola infection, they could increase the likelihood of disease and the development of visible lesions [17]. This ability to infect intact skin highlights the level of threat snake fungal disease can pose to wild snake populations.

History

The fungal pathogen causing snake fungal disease was initially grouped as a member of the Chrysosporium anamorph of Nannizziopsis vriesii (CANV) complex and later named as Chrysosporium ophiodiicola, before being reclassified as Ophidiomyces ophiodiicola [13]. Due to advances in molecular diagnostics, it was revealed that CANV included multiple distinct pathogens, including Nannizziopsis spp., and Paranannizziopsis spp. [5]. This improved understanding allowed scientists to track and manage the diseases.

Unusual skin lesions have been reported in wild snakes for years, with the earliest confirmed detection of O. ophiodiicola at the University of Wisconsin Zoological Museum being from a specimen collected in Florida in 1945. The other confirmed cases from this museum included specimens in Wisconsin in 1953 and Tennessee in 1973 [15]. In 2006, a rapid decline in timber rattlesnakes (Crotalus horridus) in New Hampshire illustrated how disease can interact with intense climate changes, inbreeding, and habitat fragmentation to drive a population to potential extinction. Although researchers did not identify the pathogen causing the skin and mouth infections in those timber rattlesnakes, fungal infection was suspected [8]. The origin of O. ophiodiicola is still unknown [9].

Additionally, two particular cases were crucial for understanding snake fungal disease and its threat to snake populations: a captive rat snake (Elaphe obsoleta) and, in 2008, a wild eastern massasauga rattlesnake (Sistrurus catenatus) [2,18]. The captive rat snake in Georgia, often featured in educational programs, presented with masses in its right lower jaw and right eye. This disease-causing agent was not identified due to a lack of matches with known fungi, which led to the new species Chrysosporium ophiodiicola [18]. Sometime later, the same fungus was identified in Illinois in wild eastern massasauga rattlesnakes. As this snake population was an endangered species and the disease had never been seen before, the level of concern was high. Allender and his colleagues (2011) reported no cases of clinical signs associated with Chrysosporium ophiodiicola among these eastern massasauga rattlesnakes from 2000 to 2007. These findings established snake fungal disease as an emerging conservation problem.

Clinical Signs and Progression

Skin lesions are the most common symptom of snake fungal disease, though the infection could spread to deeper tissues and systems. While some snakes may have visible symptoms, others can be asymptomatic, meaning they show no noticeable signs [5]. These lesions can worsen over time with swelling, fluid buildup, blisters, discoloration, nodules, and crusts that eventually separate to form ulcers. Further severity of the infectious disease may include progression into internal organs (e.g., kidneys, muscles, lungs, eyes, or reproductive organs), abnormal shedding, lethargy, loss of appetite, or necrosis of cutaneous or subcutaneous layers [17,19]. Additional areas impacted include behavioral changes (i.e., early surfacing from hibernacula), thermoregulation, higher stress levels, and lower fat reserves [9]. Although snake fungal disease is often presented as a skin disease, complications can make it life-threatening [14].

Transmission and Epidemiology

Snake fungal disease has affected a wide range of snake species across North America. At least 52 snake species are known to be susceptible to snake fungal disease in North America [19]. Overall, O. ophiodiicola has been reported in 31 states in the United States, primarily in the eastern and southern regions (Figure 1) [7]. Although it is not as well-documented or monitored, other regions of the world have also been affected [12].

Research has suggested that the transmission of snake fungal disease is influenced by environmental reservoirs, direct contact between snakes, and seasonal conditions. Direct contact with an infected snake is most likely to occur during brumation (i.e., the reptilian equivalent of mammalian hibernation) when snakes share a burrow [16]. A study conducted by Campbell and his colleagues (2021) demonstrated that O. ophiodiicola was highly detected in soil from hibernacula (i.e., sheltered sites where snakes remain over winter and remain inactive). Snakes can also spread infection through their skin shedding, as fungal hyphae and conidia could still be present [14].

Additionally, a study by Friedman and colleagues (2024) reported positive results for O. ophiodiicola in topsoil, suggesting that although this has not been thoroughly studied, soil could serve as an environmental reservoir for O. ophiodiicola. Lastly, lower temperatures, especially during brumation, are associated with increased fungal infections because the immune system's ability to fight infections is reduced during these times [11]. Snakes may bask to raise their body temperature, thereby decreasing fungal growth [14].

Diagnosis

Snake fungal disease diagnosis commonly involves laboratory testing and physical examination to identify the pathogen involved and evidence of fungal infection in deeper tissue. The diagnostic process starts with observations of skin abnormalities in snakes that could indicate fungal infection [7]. However, the most reliable way to confirm the presence of O. ophiodiicola is through polymerase chain reaction (PCR) testing on visible skin lesions or tissue biopsies, including scale clippings or shed skin. PCR testing amplifies and detects specific DNA sequences associated with the fungal pathogen [5]. Additionally, histopathological testing can identify fungal invasion by examining tissue under the microscope for fungal structures. These include hyphae, thread-like strands, and arthroconidia, spores produced by the fungus (Figure 2) [1].  

Treatment and Prevention

Laboratory testing has shown that O. ophiodiicola is sensitive to antifungal medications such as terbinafine, itraconazole, and voriconazole [19]. However, treatment plans for snake fungal disease remain a challenge, as shown by Allender and colleagues (2015), who reported that antifungal medication was ineffective on an eastern massasauga snake. In captive settings, habitat management includes disinfecting enclosures and equipment to limit the environmental persistence of the fungus; this can be done with 3-10% bleach or 70% ethanol [19]. Because the fungus can survive in soil, it is essential to clean footwear after walking in a snake habitat. Members of the public should also avoid moving snakes between sites. Public surveillance and reporting can help monitor snake fungal disease [13]. As treating wild populations could be impossible, these are the best options to keep the spread under control.

Further Research

Despite increasing concern about snake fungal disease, significant knowledge gaps remain, and further research is needed. Researchers are still investigating the role of environmental reservoirs in the transmission of O. ophiodiicola and its distribution in understudied regions, including parts of the Global South [9]. Additionally, scientists still do not fully understand how snake fungal disease can lead to death in wild snakes, but it is likely due to a combination of factors rather than a single cause [17]. The importance of continued research and long-term monitoring is crucial for understanding the impact and management of this emerging disease.  

References

1. Allain, S. J. R., Leech, D. I., Hopkins, K., Seilern-Moy, K., Fernandez, J. R. R., Griffiths, R. A. & Lawson, B. (2024). Characterisation, prevalence and severity of skin lesions caused by ophidiomycosis in a population of wild snakes. Scientific Reports, 14(5162). https://doi.org/10.1038/s41598-024-55354-5

2. Allender, M. C., Dreslik, M., Wylie, S., Phillips, C., Wylie, D. B., Maddox, C., Delaney, M. A. & Kinsel, M. J. (2011). Chrysosporium sp. Infection in eastern massasauga rattlesnakes. Emerging Infectious Disease, 17(12), 2383-2384. https://doi.org/10.3201/eid1712.110240

3. Allender, M. C., Raudabaugh, D. B., Gleason, F. H. & Miller, A. N. (2015). The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations. Fungal Ecology, 17, 187-196. https://doi.org/10.1016/j.funeco.2015.05.003

4. Allender, M. C., Ravesi, M. J., Haynes, E., Ospina, E., Petersen, C., Phillips, C. A. & Lovich, R. (2020). Ophidiomycosis, an emerging fungal disease of snakes: Targeted surveillance on military lands and detection in the western US and Puerto Rico. PLoS ONE, 15(1). https://doi.org/10.1371/journal.pone.02404

5. Bohuski, E., Lorch, J. M., Griffin, K. M. & Blehert, D. S. (2015). TaqMan real-time polymerase chain reaction for detection of Ophidiomyces ophiodiicola, the fungus associated with snake fungal disease. BMC Veterinary Research, 11(95). https://doi.org/10.1186/s12917-015-0407-8

6. Campbell, L. J., Burger, J., Zappalorti, R. T., Bunnell, J. F., Winzeler, M. E., Taylor, D. R. & Lorch, J. M. (2021). Soil reservoir dynamics of Ophidiomyces ophidiicola, the causative agent of snake fungal disease. Journal of Fungi, 7(6). https://doi.org/10.3390/jof7060461

7. Chandler, H. C., Allender, M. C., Stegenga, B. S., Haynes, E., Ospina, E. & Stevenson, D. J. (2019) Ophidiomycosis prevalence in Georgia's Eastern Indigo Snake (Drymarchon couperi) populations. PLoS ONE 14(6). https://doi.org/10.1371/journal.pone.0218351

8. Clark, R. W., Marchand, M. N., Clifford, B. J., Stechert, R. & Stephens, S. (2011). Decline of an isolated timber rattlesnake (Crotalus horridus) population: Interactions between climate change, disease, and loss of genetic diversity. Biological Conservation, 144(2), 886-891. https://doi.org/10.1016/j.biocon.2010.12.001

9. Dallas, J. W., Ghotbi, M., Rurik, A. J., King, T., Rubin, R. T., Cummins, C., Alexander, N. R., Martinez, T. A., Wilson, I. B., Foster, E., Madera, M. A., Crick, J. E. & Walker, D. M. (2026). Oo-No: Ophidiomyces ophidiicola-bacterial interactions and the role of skin lipids in development of ophidiomycosis. PLoS Pathogens, 22(1). https://doi.org/10.1371/journal.ppat.1013875

10. Davy, C. M., Shirose, L., Campbell, D., Dillon, R., McKenzie, C., Nemeth, N., Braithwaite, T., Cai, H., Degazio, T., Dobbie, T., Egan, S., Fotherby, H., Litzgus, J. D., Manorome, P., Marks, S., Paterson, J. E., Sigler, L., Slavic, D., Slavik, E., Urquhart, J. & Jardine, C. (2021) Revisiting ophidiomycosis (snake fungal disease) after a decade of targeted research. Frontiers Veterinary Science, 8: 665805. https://doi.org/10.3389/fvets.2021.665805

11. Dillon, R. M., Paterson, J. E., Manorome, P., Ritchie, K., Shirose, L., Slavik, E. & Davy, C. M. (2022).  Seasonal and interspecific variation in the prevalence of Ophidiomyces ophidiicola and Ophidiomycosis in a community of free-ranging snakes. Journal of Wildlife Disease, 58(4), 791-802. https://doi.org/10.7589/JWD-D-21-00134

12. Friedeman, N., Carter, E., Kingsbury, B. A., Ravesi, M. J., Josimovich, J. M., Matthews, M. & Jordan, M. A. (2024) Environmental associations of Ophidiomyces ophidiicola, the causative agent of ophidiomycosis in snakes. PLoS ONE, 19(10). https://doi.org/10.1371/journal.pone.0310954

13. Lorch, J. M., Knowles, S., Lankton, J. S., Michell, K., Edwards, J. L., Kapfer, J. M., Staffen, R. A., Wild, E. R., Schmidt, K. Z., Ballmann, A. E., Blodgett, D., Farrell, T. M., Glorioso, B. M., Last, L. A., Price, S. J., Schuler, K. L., Smith, C. E., Wellehan, J. F. X. & Blehert, D. S. (2016). Snake fungal disease: an emerging threat to wild snakes. Philosophical Transactions B, 371(1709). https://doi.org/10.1098/rstb.2015.0457

14. Lorch, J. M., Lankton, J., Werner, K., Falendysz, E. A., McCurley, K. & Blehert, D. S. (2015). Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. mBio, 6(6). https://doi.org/10.1128/mBio.01534-15

15. Lorch, J. M., Price, S. J., Lankton, J. S. & Drayer, A. N. (2021). Confirmed cases of ophidiomycosis in museum specimens from as early as 1945, United States. Emerging Infectious Diseases, 27 (7), 1986-1989. https://doi.org/10.3201/eid2707.204864

16. McKenzie, C. M., Oesterle, P. T., Stevens, B., Shirose, L., Mastromonaco, G. F., Lillie, B. N., Davy, C. M., Jardine, C. M. & Nemeth, N. M. (2020). Ophidiomycosis in red cornsnakes (Pantherophis guttatus): Potential roles of brumation and temperature on pathogenesis and transmission. Veterinary Pathology, 57(6), 825-837. https://doi.org/10.1177/0300985820953423

17. Nicola, M. R. D., Coppari, L., Notomista, T. & Marini, D. (2022). Ophidiomyces ophidiicola detection and infection: a global review on a potential threat to the world's snake populations. European Journal of Wildlife Research, 68(64). https://doi.org/10.1007/s10344-022-01612-8

18. Rajeev, S., Sutton, D. A., Wickes, B. L., Miller, D. L., Giri, D., Van Meter M., Thompson, E. H., Rinaldi, M. G., Romanelli, A. M., Cano, J. F. & Guarro, J. (2008). Isolation and characterization of a new fungal species, Chrysosporium ophiodiicola, from a mycotic granuloma of a black rat snake (Elaphe obsoleta obsoleta). Journal of Clinical Microbiology, 47(4), 1264-1268. https://doi.org/10.1128/JCM.01751-08

19. Schilliger, L., Paillusseau, C., François, C. & Bonwitt, J. (2023). Major emerging fungal diseases of reptiles and amphibians. Pathogens, 12 (429). https://doi.org/10.3390/pathogens12030429