Abstract

Our understanding of fungal diseases in reptiles has evolved significantly over the last 20 years. Mycoses have risen to occupy the top of the list of differential diagnoses for reptiles with cutaneous lesions. Molecular studies of fungi that were once lumped in the Chrysosporium anamorph of Nannizziopsis vriesii (CANV) complex resulted in the reassignment of isolates to novel Nannizziopsis species, and to two novel genera: Paranannizziopsis and Ophidiomyces.¹³ These are accommodated inside a novel family of fungi in the Onygenales, the Nannizziopsiacaea.¹⁴ Nannizziopsiacaean fungi grow on agar as white powdery to cottony colonies with a beige to yellow reverse, similar to dermatophytes.^13,14 The combined presence of aleurioconidia in clusters and arthroconidia is typical, and most demonstrate limited thermotolerance.^13,14 Nannizziopsiacean fungi grow slowly, and will quickly and invariably be overgrown and concealed by contaminants or saprophytes such as Aspergilli and Penicillium unless selective, cycloheximide-containing agars are used. All nannizziopsiacaean fungi are practically morphologically identical and can only be distinguished using molecular tools. Each species appears to associate with a reptile taxon, and hosts span all four taxonomical reptilian orders.¹³ These fungi appear to be primary pathogens, able to produce disease in wild reptiles and in captive reptiles housed under adequate husbandry parameters. Similarly, fungi involved in a clinical syndrome of chameleons consisting of a fulminant and conspicuous disseminated granulomatous disease first reported in the early 1960s have been molecularly characterized as two morphologically identical species, Metarhizium granulomatis and M. viride.^10,11

Former CANV isolates recovered from humans, usually immunosuppressed individuals, were found to differ from reptile isolates and were assigned to three species: Nannizziopsis obscura, N. hominis, and N. infrequens.¹³ Reptile isolates were different. Those from lizards mostly fell into novel species in the genus Nannizziopsis. Nannizziopsis guarroi causes Yellow Fungus Disease (YFD) in bearded dragons, green iguanas, and in other lizards.^6,13 YFD, one of the most common infectious disease of bearded dragons, manifests as a contagious progressive dermatomycosis with discoloration, sloughing and/or hyperkeratosis of the skin.⁶ Although infection rarely disseminates, skin lesions lead to debilitation and the course is often fatal. A number of related species, such as N. barbata, N. chlamydospora, will cause very similar lesions in agamids, and likely other lizards.⁶ A related species, N. dermatitidis, causes dermatomycosis in chameleons and geckos but infection is aggressive and typically quickly extends to deeper tissue, or disseminates.⁶

Paranannizziopsis crustacea, P. californiense, P. longispora, and P. tardicrescens infect captive tentacled snakes.^7,13,14 A tree viper and a rhinoceros snake housed in tanks in the same room as tentacled snakes with P. tardicrescens infection also developed cutaneous lesions.⁷ The fifth Paranannizziopsis species, P. australasiensis, caused chronic, recurrent superficial dermatomycosis in tuataras.² It also has been recovered from skin lesions in a file snake and a bearded dragon.¹³ Cases were all from Australia and New Zealand until it was recently recovered from yet another captive tentacled snake in New York (unpublished data).

Finally, Ophidiomyces ophiodiicola is a nannizziopsiacean fungus that seems to only infect snakes.^13,14 It has been recovered from lesions in captive snakes in North America, Europe, and Australia, and likely occurs worldwide. It also infects wild snakes in the USA, and was just recently identified in wild snakes in Europe.¹ It is by far, the most common fungal pathogen of snakes, captive or wild. A typical presentation consists of multiple swellings, crusts, scabs, and ulcers over the head, and less so the body. In some species, infection may extend to deeper tissues to cause disfigurement.

In Paris, in the early 1960s, four carpet chameleons recently imported from Madagascar all succumbed to a systemic mycosis, then attributed to Paecilomyces viridis.¹² Necropsy revealed conspicuous disseminated granulomatous disease, very similar to those seen 40 years later in several captive Jackson’s chameleons in a New Zealand zoo (unpublished data). Recently, a disease with practically identical lesions has been documented in captive veiled chameleons in Europe and the USA and was attributed to the novel fungus Chamaeleomyces granulomatis.^10,11 Miliary to clustered spherical granulomas are seen on the skin, tongue, pharynx, lungs, and liver of infected animals. This fungus was renamed Metarhizium granulomatis and P. viridis was renamed Metarhizium viride.¹⁰ These can only be distinguished using molecular tools. Both are uncommon but serious pathogens of chameleons, and maybe other lizards.

Fungi are omnipresent on the skin of reptiles. Ubiquitous saprophytic fungi, such as Aspergilla and Penicillium, are much more likely to be recovered from intact reptile skin than not.⁴ These typically irrelevant contaminants will misleadingly overgrow and conceal the presence of fungal pathogens if selective agars are not used. A variety of fungal organisms that are better known as insect pathogens, such as Metarhizium anisopliae, Purpureocillium (formerly Paecilomyces) lilacinum, and Beauveria bassiana, occasionally cause severe disease in reptiles, almost always in immunocompromised animals.⁵ Several fusaria are reptile pathogens. Fusarium incarnatum (formerly F. semitectum) has been repeatedly linked with epidermal necrosis and discoloration of the shell in tortoises (Necrotic Scute Disease),^3,8 and members of the Fusarium solani complex, F. falciforme and F. keratoplasticum, are potent pathogens of sea turtle eggs.⁹

A number of other fungi have been solidly incriminated in cases of reptile mycoses, and more are likely to be discovered and documented. For causality to be established, a putative fungus needs to be recovered or molecularly detected from a lesion, tissue sections need to identify fungal elements as the cause of lesions, and the morphology of fungal structures (hyphae, conidia, etc.) in tissue needs to be consistent with that of the fungus isolated from that lesion. Case reports in which such criteria are not met may well be misleading and contribute little to our expanding understanding of mycoses in reptiles. Molecular tools have now become practically indispensable for identification of reptile pathogens to species, and sequencing ideally should be carried out on all isolates causing reptile lesions or disease. Preservation of such isolates in microfungus collections is highly desirable, as it will then allow for further characterization and studies to be performed at a later time.

Acknowledgments

The author would like to thank medical mycologist and professor emeritus Lynne Sigler, MSc, for meticulously collecting, preserving, and studying reptile fungal isolates over 50 years and, in doing so, providing a better understanding of fungal pathogens of reptiles.

Literature Cited

1.  Franklinos LHV, Lorch JM, Bohuski E, Rodriguez-Ramos Fernandez J, Wright ON, Fitzpatrick L, et al. Emerging fungal pathogen Ophidiomyces ophiodiicola in wild European snakes. Sci Rep. 2017;7(1):3844.

2.  Masters NJ, Alexander S, Jackson B, Sigler L, Chatterton J, Harvey C, et al. Dermatomycosis caused by Paranannizziopsis australasiensis in five tuatara (Sphenodon punctatus) and a coastal bearded dragon (Pogona barbata) in a zoological collection in New Zealand. N Z Vet J. 2016;64:301–307.

3.  Nardoni S, Lungonelli P, Papini R, Mugnaini L, Mancianti F. Shell mycosis in a group of Hermann’s tortoises (Testudo hermanni). Vet Rec. 2012;170:76.

4.  Paré JA, Sigler L, Rypien KL, Gibas CF. Cutaneous mycobiota of captive squamate reptiles with notes on the scarcity of Chrysosporium anamorph of Nannizziopsis vriesii. J Herpetol Med Surg. 2003;13:10–15.

5.  Paré JA, Sigler L, Rosenthal KL, Mader DR. Microbiology: Fungal and Bacterial Diseases of Reptiles, in Reptile Medicine and Surgery, 2nd ed. Mader DR ed. St. Louis, MO: Saunders Elsevier; 2006:217–238.

6.  Paré JA, Sigler L. An overview of reptile fungal pathogens in the genera Nannizziopsis, Paranannizziopsis, and Ophidiomyces. J Herpetol Med Surg. 2016;26:46–53.

7.  Rainwater KL, Wiederhold NP, Sutton DA, Garner MM, Maguire C, Sanders C, et al. Novel Paranannizziopsis species in a Wagler’s viper (Tropidolaemus wagleri) and tentacle snake (Erpeton tentaculatum) in a zoological collection. In: Proceedings of the Association of Reptile Amphibian Veterinarians. Dallas, TX: 2017.

8.  Rose FL, Koke J, Koehn R, Smith D. Identification of the etiological agent for necrotizing scute disease in the Texas tortoise. J Wildl Dis. 2001;37:223–228.

9.  Sarmiento-Ramirez JM, Abella-Pérez E, Phillott AD, Sim J, van West P, Martin MP, et al. 2010. Global distribution of two fungal pathogens threatening endangered sea turtles. PLoS ONE. 2014;9(1):e85853.

10.  Schmidt V, Klasen L, Schneider J, Hübel J, Pees M. Characterization of Metarhizium viride mycosis in veiled chameleons (Chamaeleo calyptratus), panther chameleons (Furcifer pardalis) and inland bearded dragons (Pogona vitticeps). J Clin Microbiol. 2017a;55:832–843.

11.  Schmidt V, Klasen L, Schneider J, Hübel J, Pees M. Fungal dermatitis, glossitis, and disseminated visceral mycosis caused by different Metarhizium granulomatis genotypes in veiled chameleons (Chamaeleo calyptratus) and first isolation in healthy lizards. Vet Microbiol. 2017;207:74–82.

12.  Segretain G, Fromntin H, Destombes P, Brygoo Er, Dodin A. Paecilomyces viridis nov. sp., dimorphic fungus agent of a generalized mycosis in Chamaeleo lateralis Gray. Compt Rend Acad Sci (Paris). 1964;259:258–261.

13.  Sigler L, Hambleton S, Paré J. Molecular characterization of reptile pathogens currently known as members of the Chrysosporium anamorph of Nannizziopsis vriesii complex and relationship with some human-associated isolates. J Clin Microbiol. 2013;52:3338–3357.

14.  Stchigel AM, Sutton DA, Cano-Lira JF, Cabanes FJ, Abarca L, Tintelnot K, et al. Phylogeny of chrysosporia infecting reptiles: proposal of the new family Nannizziopsiaceae and five new species. Persoonia. 2013;31:86–100.