fungal ecology 17 (2015) 187e196 available at www.sciencedirect.com ScienceDirect journal homepage: www.elsevier.com/locate/funeco The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations Matthew C. ALLENDERa,1, Daniel B. RAUDABAUGHb,d,1, Frank H. GLEASONc,*, Andrew N. MILLERd aDepartment of Comparative Biosciences, University of Illinois, Urbana, IL, USA bDepartment of Plant Biology, University of Illinois, Urbana, IL, USA cSchool of Biological Sciences, A12, University of Sydney, NSW 2006, Australia dIllinois Natural History Survey, University of Illinois, Champaign, IL, USA article info abstract Article history: Ophidiomyces ophiodiicola, the causative agent of snake fungal disease, is a serious emerging Received 17 December 2014 fungal pathogen of North American-endemic and captive snakes. We provide a detailed Revision received 4 April 2015 literature review, introduce new ecological and biological information and consider aspects Accepted 7 May 2015 of O. ophiodiicola that need further investigation. The current biological evidence suggests Available online 18 June 2015 that this fungus can persist as an environmental saprobe in soil, as well as colonizing living Corresponding editor: hosts. Not unlike other emerging fungal pathogens, many fundamental questions such as Matt Fisher the origin of O. ophiodiicola, mode of transmission, environmental influences, and effective treatment options still need to be investigated. Keywords: ª 2015 Elsevier Ltd and The British Mycological Society. All rights reserved. Emerging fungal pathogen Herpetology Massasaugas Pitvipers Snake fungal disease Wildlife diseases Introduction Pseudogymnoascus destructans, causing white-nose syndrome in North American bat populations (Blehert et al., 2009). One of True fungal pathogens have been increasingly associated with the latest emerging fungal pathogens of vertebrate animal free-ranging wildlife epidemics. Two recently studied exam- populations, Ophidiomyces ophiodiicola, was first observed in ples include the effects of chytridriomycosis, caused by 2006 affecting populations of pitvipers in the eastern United Batrachochytrium dendrobatidis, on global frog populations States (Clark et al., 2011), and later confirmed in Eastern (Skerratt et al., 2007) and the asexual ascomycete, Massasaugas (Sistrurus catenatus) from Illinois in 2008 * Corresponding author. Tel.: þ61 2 9971 2071. E-mail address: [email protected] (F.H. Gleason). 1 This text was written initially by Matthew C. Allender and Daniel B. Raudabaugh with equal participation and subsequently edited by Frank H. Gleason and Andrew N. Miller. http://dx.doi.org/10.1016/j.funeco.2015.05.003 1754-5048/ª 2015 Elsevier Ltd and The British Mycological Society. All rights reserved. 188 M.C. Allender et al. (Allender et al., 2011). With the current rate of decline in global biodiversity, it is apparent that wildlife diseases similar to those described above are serving as threats to population declines potentially resulting in species extinctions. Fisher et al. (2012) described a model or concept for anal- ysis of emerging infectious fungal diseases in animal and plant populations and ecosystem health in general. This model is useful for the study of newly emerging highly viru- lent agents of disease such as the snake fungal pathogen, O. ophiodiicola (see Table 1). Ophidiomyces ophiodiicola (formerly Chrysosporium ophiodii- cola) is currently placed in the order Onygenales (Ascomycota) within the family Onygenaceae(Sigler et al., 2013). This fungus is closely related to other species of Onygenaceae within the Fig 1 e Current known US distribution of O. ophiodiicola. Chrysosporium anamorph Nannizziopsis vriesii (CANV) complex States where O. ophiodiicola is known to occur are grey, that causes dermal lesions in reptiles (Sigler et al., 2013). The based on previous reports (Allender et al., 2011; Sleeman genus Ophidiomyces currently contains only one species, O. et al., 2014) and unpublished data (MCA). ophiodiicola, and it is known to infect only snakes leading to the syndrome Snake Fungal Disease (SFD) which causes wide- spread morbidity and mortality across the eastern United Since 2008, Eastern Massasaugas from the Carlyle Lake States (Fig 1)(Allender et al., 2013; Sigler et al., 2013; Sleeman, population in Illinois have been diagnosed with SFD 2013). (Fig 5AeD) (Allender et al., 2011, 2015). Free-range infected Historically, several case reports of skin disease in snakes massasaugas display skin lesions, which vary from pustules were confirmed (Pare and Jacobson, 2007) or suspected to be or nodules to severe swelling of the skin (Allender et al., 2011). CANV or CANV-like. However, since publication of the Infections in this species have been known to invade deep description of the genus Ophidiomyces in 2013 and with the use muscle tissue and infect muscle and bone (Allender et al., of advanced molecular techniques, it is now thought that 2011). Prior to 2014, lesions were thought to only affect the many of these infections may have been caused by O. ophio- head and neck of snakes, but lesions have now been observed diicola. An outbreak of fungal mycosis with clinical signs in the skin of the entire body in massasaugas in Michigan consistent with SFD was seen in pigmy rattlesnakes (S. mil- (Tetzlaff et al., 2015). In 2006, a population of timber rattle- iarius) in Florida in the early 2000’s, but neither Ophidiomyces snakes (Crotalus horridus) in New Hampshire was observed nor CANV were identified in that case (Cheatwood et al., 2003). with lesions on the head, neck, and body consistent with SFD This outbreak included 42 pigmy rattlesnakes, one garter (Clark et al., 2011). The authors hypothesized that environ- snake (Thamnophis sp.), and a ribbon snake (Thamnophis sau- mental conditions (increased rainfall) were likely the explan- ritus) within a 2 yr period, and retrospectively the authors ation for the increased prevalence and/or severity as no other identified an additional 59 pigmy rattlesnakes with signs lesions were noted in their follow-up study in 2009 (Clark consistent with mycotic disease (Cheatwood et al., 2003). et al., 2011). To date, all reports related to pitvipers have While these were not confirmed to be SFD at that time, it been consistently associated with dermatitis. highlights the need to utilize advanced molecular techniques While infections have been observed with great frequency for accurate identification of the etiological agent during in pitvipers (Cheatwood et al., 2003; Allender et al., 2011; Clark mycotic outbreaks. et al., 2011; Smith et al., 2013; Tetzlaff et al., 2015), there are numerous reports of CANV or SFD in nonvenomous colubrid snakes (Jacobson, 1980; Vissiennon et al., 1999; Nichols et al., 1999; Bertelsen et al., 2005; Rajeev et al., 2009; Dolinski et al., 2014). The manifestation of SFD in North American colubrids Table 1 e Properties of emerging infectious diseases of Ophidiomyces which fit the Fisher model snakes is variable and has included pneumonia, ocular infections, and subcutaneous nodules (Rajeev et al., 2009; Properties of emerging Ophidiomyces ophiodiicola infectious diseases Sleeman, 2013; Dolinski et al., 2014). A case of O. ophiodiicola was observed in a captive black rat snake (Elaphe obsoleta Propagules for rapid transmission Conidia obsoleta) with a subcutaneous nodule (Rajeev et al., 2009). In Threshold host population size Unknown addition, mycosis was observed in the skin as well as a more for disease persistence Host species resistant to disease Some host species systemic invasion involving the lungs and eye (one case) and Ecotypes with high virulence Yes lungs and liver (one case) of garter snakes (Vissiennon et al., Long-lived environmental stages Conidia and hyphae 1999; Dolinski et al., 2014). growing on detritus While the presence of the fungus causing infections in Generalist and opportunist Yes individuals is concerning, the role that it might play in pop- pathogens ulation declines is more alarming. A timber rattlesnake pop- Alternative hosts Yes ulation in New Hampshire consisted of 40 individuals pre- Sexual life cycle Not known in this species Transport of infected species International Animal Trade SFD; however, by the conclusion of that particular study, the entire population was reduced to 19 individuals (Clark et al., History, ecology, and epidemiology of O. ophiodiicola 189 Fig 2 e Morphology and carbon utilization of O. ophiodiicola. (A) Ophidiomyces ophiodiicola isolate on PDA at 25 d; left is the upper surface of the colony, right is the bottom of the plate. (B) Ophidiomyces ophiodiicola asexual reproduction via arthroconidia demonstrating schizolytic dehiscence and (C) stalked aleurioconidia. Ophidiomyces ophiodiicola growth at after 25 d on (D) autoclaved Carassius sp., (E) autoclaved Locusta migratoria and (F) autoclaved Lentinula edodes Growth of O. ophiodiicola after 20 d (G) demineralized Pleoticus muelleri exoskeletons and (H) demineralized and deproteinated exoskeletons. All size bars [ 5 mm. 2011). While many factors are affecting the conservation of this population, the occurrence of this pathogen may serve as Methods and materials an additional threat to its conservation. In this report we describe the ecology of O. ophiodiicola in Four Illinois O. ophiodiicola isolates (isolated in 2014) from the laboratory and consider aspects of this disease that various infection sites located on free range snakes were require