Fungal community on skin tissue of amphibians collected in the Santarém region, Pará, Brazil / Comunidade de fungos do tecido cutâneo de anfíbios coletados na região de Santarém, Pará, Brasil

Andreza da Silva Peixoto, Daniel de Sousa Guedes, Vanessa dos Santos Bentes, Nathan Sousa da Silva, Eveleise Samira Martins Canto, Ricardo Alexandre Kawashita-Ribeiro, Graciene do Socorro Taveira Fernandes


Among living beings, the Amphibia Class has unique characteristics. The cutaneous tissue of these animals has properties that provide ideal conditions for the establishment of microorganisms in their skin, which act in several important functions. The present study aimed to characterize the cultivable fungal microbiota of amphibians collected in the Santarém region, Western Pará, Brazil. Two species of toads were captured, totalling 25 individuals, being 15 specimens of Rhinella major and 10 individuals of R. marina. Collections were performed by active search at night, between the months of November 2017 to April 2019. Cutaneous samples were collected by smear in the dorsoventral region of the animal, using a swab soaked in sterile 0.85% saline solution with 10-3 dilution, and grown in Petri dishes containing Potato Dextrose Agar culture medium. The animals were euthanized and deposited in the herpetological collection of Federal University of Western Pará. For identification, isolation, morphological characterization and microculture of fungal colonies were used. In total, 75 fungal colonies representative of 11 genera were identified. Penicillium and Aspergillus have been identified as the most representative genera in both amphibian species. There were differences in the composition of the cutaneous mycobiota between R. major and R. marina, but not related to seasonality, which may be linked to the environment they inhabit, as well as to the physiological factors inherent to each species. The present work presents the taxa Absidia, Curvularia, Scopulariopsis and the group mycelia sterilia as new records of fungi associated with the skin tissue of adult anurans. Thus, it is suggested that further studies be carried out in Amazonian environments, with a larger sample size, as well as the use of molecular tools, for a better identification and understanding of the composition of the anuran skin microbiota.


Anurans, Microbiota, Fungi, Amazonia


ABDEL-WARETH, M. T. A.; GHAREEB, M. A.; ABDEL-AZIZ, M. S.; EL-HAGRASSI, A. M. Snailicidal, antimicrobial, antioxidant and anticancer activities of Beauveria bassiana, Metarhizium anisopliae and Paecilomyces lilacinus fungal extracts. Egyptian Journal of Aquatic Biology and Fisheries, v. 23, n. 2, p. 195-212, 2019.

ACEVEDO, A. A.; LAMPO, M.; CIPRIANI, R. The cane or marine toad, Rhinella marina (Anura, Bufonidae): two genetically and morphologically distinct species. Zootaxa, v. 4103, n. 6, p. 574-586, 2016.

AMPHIBIAWEB. Rhinella marina: South American Cane Toad. Accessible at University of California, Berkley, USA. Accessed in July 30, 2020.

ASSIS, A. B. Microbiota, secreções cutâneas e microclima: consequências para os anfíbios. Revista da Biologia, v. 8, p. 45-48, 2012.

ATANASOVA, L. Ecophysiology of Trichoderma in genomic perspective. In: GUPTA, V.; SCHMOLL, M.; HERRERA-ESTRELLA, A.; UPADHYAY, R. S.; DRUZHININA, I.; TUOHY, M. (Ed.), Biotechnology and Biology of Trichoderma (p. 25-40). Elsevier, 2014.

ÁVILA-PIRES, T. C. S.; HOOGMOED, M. S.; VITT, L. J. Herpetofauna da Amazônia. In: NASCIMENTO, L. B.; OLIVEIRA, M. E. (Ed.), Herpetologia no Brasil II (p. 13-43). Belo Horizonte, MG: Sociedade Brasileira de Herpetologia, 2007.

BALLHAUSEN, B. D.; GEISWEID, K.; HARTMANN, K.; HIRSCHBERGER, J.; MAJZOUB, M.; SCHULZ, B. Systemic Acremonium species infection in a dog. Tierärztliche Praxis Ausgabe K: Kleintiere/Heimtiere, v. 44, n. 06, p. 424-428, 2016.

BANIK, A.; HALDER, S. K.; GHOSH, C.; MONDAL, K. C. Fungal Probiotics: Opportunity, Challenge, and Prospects. In: YADAV, A. N.; SINGH, S.; MISHRA, S.; GUPTA, A. (Ed.), Recent Advancement in White Biotechnology Through Fungi (p. 101-117). Cham, SWI: Springer, 2019.

BENNY, G. L. Methods used by Dr. RK Benjamin, and other mycologists, to isolate zygomycetes. Aliso: A Journal of Systematic and Evolutionary Botany, v. 26, n. 1, p. 37-61, 2008.

BENSCH, K.; BRAUN, U.; GROENEWALD, J. Z.; CROUS, P. W. The Genus Cladosporium. Studies in Mycology, v. 72, p. 1-401, 2012.

BIZJAK-MALI, L.; ZALAR, P.; TURK, M.; BABIČ, M. N.; KOSTANJSEK, R.; GUNDE-CIMERMAN, N. Opportunistic fungal pathogens isolated from a captive individual of the European blind cave salamander Proteus anguinus. Diseases of Aquatic Organisms, v. 129, n. 1, p. 15-30, 2018.

BLETZ, M. C.; PERL, R. B.; VENCES, M. Skin microbiota differs drastically between co-occurring frogs and newts. Royal Society Open Science, v. 4, n. 4, p. 170107, 2017a.

BLETZ, M. C.; ARCHER, H.; HARRIS, R. N.; MCKENZIE, V. J.; RABEMANANJARA, F. C.; RAKOTOARISON, A.; VENCES, M. Host ecology rather than host phylogeny drives amphibian skin microbial community structure in the biodiversity hotspot of Madagascar. Frontiers in Microbiology, v. 8, n. 1530, 2017b.

BOS, J. D.; LUITEN, R. M. Skin Immune System. In: STOCKFLETH, E.; ULRICH, C. (Ed.), Skin Cancer after Organ Transplantation (p. 45-62). Springer US, 2009.

BRIGHT, M.; BULGHERESI, S. A complex journey: transmission of microbial symbionts. Nature Reviews Microbiology, v. 8, n. 3, p. 218-230, 2010.

CAPRILES, C. H.; MATA, S.; MIDDELVEEN, M. Preservation of fungi in water (Castellani): 20 years. Mycopathologia, v. 106, n. 2, p. 73-79, 1989.

CHUONG, C. M., NICKOLOFF, B. J., ELIAS, P. M., GOLDSMITH, L. A., MACHER, E., MADERSON, P. A., SUNDBERG, J. P.; TAGAMI, H.; PLONKA, P. M.; THESTRUP-PEDERSON, K.; BERNARD, B. A.; SCHÖDER, J. M.; DOTTO, P.; CHANG, C. M.; WILLIAMS, M. L.; FEINGOLD, K. R.; KING, L. E.; KLINGMAN, A. M.; REES, J. L.; CHRISTOPHERS, E. What is the 'true' function of skin?. Experimental Dermatology, v. 11, n. 2, p. 159-187, 2002.

COLOMBO, B. M.; SCALVENZI, T.; BENLAMARA, S.; POLLET, N. Microbiota and mucosal immunity in amphibians. Frontiers in Immunology, v. 6, n. 111, 2015.

CONNOLLY, J. H. Mucormycosis in the platypus and amphibians caused by Mucor amphibiorum. Microbiology Australia, v. 36, n. 2, p. 83-87, 2015.

CONSTANTINIDES, J.; MISRA, A.; NASSAB, R.; WILSON, Y. Absidia corymbifera fungal infection in burns: a case report and review of the literature. Journal of Burn Care & Research, v. 29, n. 2, p. 416-419, 2008.

CRAMP, R. L.; MCPHEE, R. K.; MEYER, E. A.; OHMER, M. E.; FRANKLIN, C. E. First line of defence: the role of sloughing in the regulation of cutaneous microbes in frogs. Conservation Physiology, v. 2, n. 1, p. cou012, 2014.

CROUS, P. W.; BRAUN, U.; SCHUBERT, K.; GROENEWALD, J. Z. Delimiting Cladosporium from morphologically similar genera. Studies in Mycology, v. 58, p. 33-56, 2007.

CULP, C. E.; FALKINHAM III, J. O.; BELDEN, L. K. Identification of the natural bacterial microflora on the skin of eastern newts, bullfrog tadpoles and redback salamanders. Herpetologica, v. 63, n. 1, p. 66-71, 2007.

DA CUNHA, K. C.; SUTTON, D. A.; FOTHERGILL, A. W.; CANO, J.; GENÉ, J.; MADRID, H.; DE HOOG, S.; CROUS, P. W.; GUARRO, J. Diversity of Bipolaris species in clinical samples in the United States and their antifungal susceptibility profiles. Journal of Clinical Microbiology, v. 50, n. 12, p. 4061-4066, 2012.

DA CUNHA, K. C.; SUTTON, D. A.; FOTHERGILL, A. W.; GENÉ, J.; CANO, J.; MADRID, H.; DE HOOG, S.; CROUS, P. W.; GUARRO, J. In vitro antifungal susceptibility and molecular identity of 99 clinical isolates of the opportunistic fungal genus Curvularia. Diagnostic Microbiology and Infectious Disease, v. 76, n. 2, p. 168-174, 2013.

DAS, S.; SAHA, R.; DAR, S. A.; RAMACHANDRAN, V. G. Acremonium species: a review of the etiological agents of emerging hyalohyphomycosis. Mycopathologia, v. 170, n. 6, p. 361-375, 2010.

DENSMORE, C. L.; GREEN, D. E. Diseases of amphibians. Ilar Journal, v. 48, n. 3, p. 235-254, 2007.

DOUGLAS, S. I.; AMUZIE, C. C. Microbiological quality of Hoplobatrachus occipitalis (Amphibia, Anura) used as meat. International Journal of Current Microbiology and Applied Sciences, v. 6, n. 6, p. 3192-3200, 2017.

EZENWA, V. O.; GERARDO, N. M.; INOUYE, D. W.; MEDINA, M.; XAVIER, J. B. Animal behavior and the microbiome. Science, v. 338, n. 61041, p. 98-199, 2012.

FLÓREZ, L. V.; BIEDERMANN, P. H.; ENGL, T.; KALTENPOTH, M. Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Natural Product Reports, v. 32, n. 7, p. 904-936, 2015.

FREIRE, F. D. C. O.; VIEIRA, I. G. P.; GUEDES, M. I. F.; MENDES, F. N. P. Micotoxinas: importância na alimentação e na saúde humana e animal. Embrapa Agroindústria Tropical, v. 48, 2007.

FROST, D. R. Amphibian Species of the World: An Online Reference. Version 6.1 Electronic Database accessible at American Museum of Natural History, New York, USA, 2020.

GARCIA‐HERMOSO, D.; ALANIO, A.; CABARET, O.; OLIVI, M.; FOULET, F.; CORDONNIER, C.; COSTA, J-M.; BRETAGNE, S. High diversity of non‐sporulating moulds in respiratory specimens of immunocompromised patients: should all the species be reported when diagnosing invasive aspergillosis?. Mycoses, v. 58, n. 9, p. 557-564 2015.

GARCÍA-PAJARES, F.; SÁNCHEZ-ANTOLÍN, G.; ALVÁREZ, C. A.; RUBIALES, B. M.; NÚÑEZ-RODRÍGUEZ, H.; DEL VAL, L. S.; RUIZ-ZORRILLA, R.; BARRERA, A.; GÓMEZ-NIETO, A.; HERRERO, I. P.; GARCÍA, A. V.; CARO-PATÓN, A. Cutaneous mucormycosis infection by Absidia in two consecutive liver transplant patients. Transplantation Proceedings, v. 44, n. 6, p. 1562-1564, 2012.

GONZÁLEZ-BERNAL, E.; GREENLEES, M. J.; BROWN, G. P.; SHINE, R. Toads in the backyard: why do invasive cane toads (Rhinella marina) prefer buildings to bushland?. Population Ecology, v. 58, n. 2, p. 293-302, 2016.

GUERRA, V.; JARDIM, L.; LLUSIA, D.; MÁRQUEZ, R.; BASTOS, R. P. Knowledge status and trends in description of amphibian species in Brazil. Ecological Indicators, v. 18, n. 2020, p. 106754, 2020.

HAMANN, M. I.; GONZÁLEZ, C. E. Helminth parasites in the toad Rhinella major (Bufonidae) from Chaco region, Argentina. Acta Herpetologica, v. 10, n. 2, p. 93-101, 2015.

HERMET, A.; MÉHEUST, D.; MOUNIER, J.; BARBIER, G.; JANY, J.-L. Molecular systematics in the genus Mucor with special regards to species encountered in cheese. Fungal Biology, v. 116, n. 6, p. 692–705, 2012.

HOFFMANN, K.; DISCHER, S.; VOIGT, K. Revision of the genus Absidia (Mucorales, Zygomycetes) based on physiological, phylogenetic, and morphological characters; thermotolerant Absidia spp. form a coherent group, Mycocladiaceae fam. nov. Mycological Research, v. 111, n. 10, p. 1169-1183, 2007.

HOFFMANN, K. Identification of the genus Absidia (Mucorales, Zygomycetes): a comprehensive taxonomic revision. In: GHERBAWY, Y.; VOIGT, K. (Ed.), Molecular Identification of Fungi (p. 439-460). Berlin: Springer, 2010.

HOFFMANN, K.; PAWŁOWSKA, J.; WALTHER, G.; WRZOSEK, M.; DE HOOG, G. S.; BENNY, G. L.; KIRK, P. M.; VOIGT, K. The family structure of the Mucorales: a synoptic revision based on comprehensive multigene-genealogies. Persoonia: Molecular Phylogeny and Evolution of Fungi, v. 30, p. 57-76, 2013.

HOLDEN, W. M.; HANLON, S. M.; WOODHAMS, D. C.; CHAPPELL, T. M.; WELLS, H. L.; GLISSON, S. M.; MCKENZIE, V. J.; KNIGHT, R.; PARRIS, M. J.; ROLLINS-SMITH, L. A. Skin bacteria provide early protection for newly metamorphosed southern leopard frogs (Rana sphenocephala) against the frog-killing fungus, Batrachochytrium dendrobatidis. Biological Conservation, v. 187, p. 91-102, 2015.

HUANG, L.; LI, J.; ANBOUKARIA, H.; LUO, Z.; ZHAO, M.; WU, H. Comparative transcriptome analyses of seven anurans reveal functions and adaptations of amphibian skin. Scientific Reports, v. 6, n. 1, p. 1-11, 2016.

IWEN, P. C.; SCHUTTE, S. D.; FLORESCU, D. F.; NOEL-HURST, R. K.; SIGLER, L. Invasive Scopulariopsis brevicaulis infection in an immunocompromised patient and review of prior cases caused by Scopulariopsis and Microascus species. Medical Mycology, v. 50, n. 6, p. 561-569, 2012.

KEARNS, P. J.; FISCHER, S.; FERNÁNDEZ-BEASKOETXEA, S.; GABOR, C. R.; BOSCH, J.; BOWEN, J. L.; TLUSTY, M. F.; WOODHAMS, D. C. Fight fungi with fungi: antifungal properties of the amphibian mycobiome. Frontiers in Microbiology, v. 8, n. 2494, 2017.

KELLY, D.; MULDER, I. E. Microbiome and immunological interactions. Nutrition Reviews, 70(suppl_1), p. S18-S30, 2012.

KHAN, N. T. Cephalosporin C Production from Acremonium chrysogenum. Enzyme Engineering, v. 6, n. 1, 2017.

KHIRALLA, A.; SPINA, R.; SALIBA, S.; LAURAIN-MATTAR, D. Diversity of natural products of the genera Curvularia and Bipolaris. Fungal Biology Reviews, v. 33, n. 2, p. 101-122, 2019.

KIM, S.; EOM, A. H.; PARK, D.; RA, N. Y. Detection of infectious fungal diseases of frogs inhabiting in Korea. Mycobiology, v. 36, n. 1, p. 10-12, 2008.

KLIMKO, N. N.; KHOSTELIDI, S. N.; MELEKHINA, Y. E.; GORNOSTAEV, D. A.; SEMELEV, V. N. Acremonium Pneumonia Successfully Treated in Patient with Acute Myeloid Leukemia: A Case Report. Journal of Bacteriology & Mycology: Open Access, v. 2, n. 5, p. 116-119, 2016.

KRIZSÁN, K.; PAPP, T.; MANIKANDAN, P.; SHOBANA, C. S.; CHANDRASEKARAN, M.; VÁGVÖLGYI, C.; KREDICS, L. Clinical Importance of the Genus Curvularia. In: RAZZAGHI-ABYANEH, M.; SHAMS-GHAHFAROKHI, M.; RAI, M. (Ed.), Medical Mycology: Current Trends and Future Prospects (p. 147-204). CRC Press, 2015.

KUENEMAN, J. G.; PARFREY, L. W.; WOODHAMS, D. C.; ARCHER, H. M.; KNIGHT, R.; MCKENZIE, V. J. The amphibian skin‐associated microbiome across species, space and life history stages. Molecular Ecology, v. 23, n. 6, p. 1238-1250, 2014.

KUENEMAN, J. G.; WEISS, S.; MCKENZIE, V. J. Composition of micro-eukaryotes on the skin of the cascades Frog (Rana cascadae) and patterns of correlation between skin microbes and Batrachochytrium dendrobatidis. Frontiers in Microbiology, v. 8, n. 2350, 2017.

KUENEMAN, J. G.; WOODHAMS, D. C.; HARRIS, R.; ARCHER, H. M.; KNIGHT, R.; MCKENZIE, V. J. Probiotic treatment restores protection against lethal fungal infection lost during amphibian captivity. Proceedings of the Royal Society B: Biological Sciences, v. 283, n. 1839, 20161553, 2016.

LACAP, D. C.; HYDE, K. D.; LIEW, E. C. Y. An evaluation of the fungal 'morphotype' concept based on ribosomal DNA sequences. Fungal Diversity, v. 12, p. 53-66, 2003.

LACAZ, C. S.; PORTO, E.; MARTINS, J. E. C.; HEINS-VACCARI, E. M.; MELO, N. T. Tratado de Micologia Médica. São Paulo: Sarvier, 2002.

LAM, B. A.; WALKE, J. B.; VREDENBURG, V. T.; HARRIS, R. N. Proportion of individuals with anti-Batrachochytrium dendrobatidis skin bacteria is associated with population persistence in the frog Rana muscosa. Biological Conservation, v. 143, n. 2, p. 529-531, 2010.

LARONE, D. H. Medically Important Fungi: A Guide to Identification. Washington, D.C.: American Society for Microbiology, 1993.

LAUER, A.; SIMON, M. A.; BANNING, J. L.; ANDRÉ, E.; DUNCAN, K.; HARRIS, R. N. Common cutaneous bacteria from the eastern red-backed salamander can inhibit pathogenic fungi. Copeia, v. 2007, n. 3, p. 630-640, 2007.

LI, X. Q.; XU, K.; LIU, X. M.; ZHANG, P. A Systematic Review on Secondary Metabolites of Paecilomyces Species: Chemical Diversity and Biological Activity. Planta Medica, 2020.

LIANG, Z. Q.; HAN, Y. F.; CHU, H. L.; LIU, A. Y. Studies on the genus Paecilomyces in China I. Fungal Diversity, v. 20, p. 83-101, 2005.

MANAMGODA, D. S.; CAI, L.; MCKENZIE, E. H. C.; CHUKEATIROTE, E.; HYDE, K. D. Two new Curvularia species from northern Thailand. Sydowia, v. 64, n. 2, p. 255-266, 2012a.

MANAMGODA, D. S.; CAI, L.; MCKENZIE, E. H. C.; CROUS, P. W.; MADRID, H.; CHUKEATIROTE, E.; SHIVAS, R. G.; TAN, Y. P.; HYDE, K. D. A phylogenetic and taxonomic re-evaluation of the Bipolaris-Cochliobolus-Curvularia complex. Fungal Diversity, v. 56, n. 1, p. 131-144, 2012b.

MANAMGODA, D. S.; ROSSMAN, A. Y.; CASTLEBURY, L. A.; CHUKEATIROTE, E.; HYDE, K. D. A taxonomic and phylogenetic re-appraisal of the genus Curvularia (Pleosporaceae): human and plant pathogens. Phytotaxa, v. 212, n. 3, p. 175-198, 2015.

MCKENZIE, V. J.; BOWERS, R. M.; FIERER, N.; KNIGHT, R.; LAUBER, C. L. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. The ISME Journal, v. 6, n. 3, p. 588-596, 2012.

MEDINA, D.; HUGHEY, M. C.; WALKE, J. B.; BECKER, M. H.; PONTARELLI, K.; SUN, S.; BADGLEY, B.; BELDEN, L. K. Amphibian skin fungal communities vary across host species and do not correlate with infection by a pathogenic fungus. Environmental Microbiology, v. 21, n. 8, p. 2905-2920, 2019.

MENDOZA, Á. M.; AGUIRRE-ROJAS, L.; SARRIA, M.; GIRALDO, A. Hongos dérmico saprófitos de Dendropsophus columbianus (Hylidae) en Caloto, Colombia. Boletín Científico, v. 16, n. 1, p. 33-40, 2012.

MUKHERJEE, P. K., HORWITZ, B. A., SINGH, U. S., MUKHERJEE, M., & SCHMOLL, M. Trichoderma in agriculture, industry and medicine: an overview. In: MUKHERJEE, P. K.; HORWITZ, B. A.; SINGH, U. S.; MUKHERJEE, M.; SCHMOLL, M. (Ed.), Trichoderma Biology and Applications (p. 1-9). Boston: CAB International, 2013.

NARVAES, P.; RODRIGUES, M. T. Taxonomic revision of Rhinella granulosa species group (Amphibia, Anura, Bufonidae), with description of a new species. Arquivos de Zoologia, v. 40, n. 1, p. 1-73, 2009.

NICKERSON, C. A.; OTT, C. M.; CASTRO, S. L.; GARCIA, V. M.; MOLINA, T. C.; BRIGGLER, J. T.; PITT, A. L.; TAVANO, J. J.; BYRAM, J. K.; BARRILA, J.; NICKERSON, M. A. Evaluation of microorganisms cultured from injured and repressed tissue regeneration sites in endangered giant aquatic Ozark hellbender salamanders. PLoS ONE, v. 6, n. 12, p. e28906, 2011.

OGOANAH, O. S.; OKAFOR, A. E.; EYONG, M. M. Effect of different preparatory methods on microbial load of the edible frog Hoplobatrachus occipitalis from Aguleri, Anambra State, Nigeria. NISEB Journal, v. 17, n. 3, p. 91-95, 2017.

OLSON, D. H.; AANENSEN, D. M.; RONNENBERG, K. L.; POWELL, C. I.; WALKER, S. F.; BIELBY, J.; GARNER, T. W. J.; WEAVER, G.; The Bd Mapping Group.; FISHER, M. C. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PloS ONE, v. 8, n. 2, p. e56802, 2013.

PEAY, K. G.; KENNEDY, P. G.; TALBOT, J. M. Dimensions of biodiversity in the Earth mycobiome. Nature Reviews Microbiology, v. 14, n. 7, p. 434, 2016.

PELOSO, P. L. V.; MACHADO, I.; BECKER, G. Fotografia da conservação na herpetologia: um ensaio sobre anfíbios ameaçados de extinção no Brasil. Herpetologia Brasileira, v. 8, n. 1, p. 26-29, 2019.

PERDOMO, H.; SUTTON, D. A.; GARCÍA, D.; FOTHERGILL, A. W.; CANO, J.; GENÉ, J.; SUMMERBELL, R. C.; RINALDI, M. G.; GUARRO, J. Spectrum of clinically relevant Acremonium species in the United States. Journal of Clinical Microbiology, v. 49, n. 1, p. 243-256, 2011.

PETRISKO, J. E.; PEARL, C. A.; PILLIOD, D. S.; SHERIDAN, P. P.; WILLIAMS, C. F.; PETERSON, C. R.; BURY, R. B. Saprolegniaceae identified on amphibian eggs throughout the Pacific Northwest, USA, by internal transcribed spacer sequences and phylogenetic analysis. Mycologia, v. 100, n. 2, p. 171-180, 2008.

PÉREZ-CANTERO, A.; GUARRO, J. Current knowledge on the etiology and epidemiology of Scopulariopsis infections. Medical Mycology, v. 58, n. 2, p. 145-155m 2020.

POUGH, F. H.; JANIS, C. M.; HEISER, J. B. A Vida dos Vertebrados. São Paulo: Atheneu, 2008.

POUNDER, J. I.; SIMMON, K. E.; BARTON, C. A.; HOHMANN, S. L.; BRANDT, M. E.; PETTI, C. A. Discovering potential pathogens among fungi identified as nonsporulating molds. Journal of Clinical Microbiology, v. 45, n. 2, p. 568-571, 2007.

PROKSCH, E.; BRANDNER, J. M.; JENSEN, J. M. The skin: an indispensable barrier. Experimental Dermatology, v. 17, n. 12, p. 1063-1072, 2008.

REAVILL, D. R. Amphibian skin diseases. Veterinary Clinics of North America: Exotic Animal Practice, v. 4, n. 2, p. 413-440, 2001.

REBOLLAR, E. A.; HARRIS, R. Ecology of amphibian-microbial symbioses. Frontiers in Microbiology, v. 10, p. 766, 2019.

REBOLLAR, E. A.; MARTÍNEZ-UGALDE, E.; ORTA, A. H. The amphibian skin microbiome and its protective role against chytridiomycosis. Herpetologica, v. 76, n. 2, p. 167-177, 2020.

RIDDELL, R. W. Permanent stained mycological preparations obtained by slide culture. Mycologia, v. 42, n. 2, p. 265-270, 1950.

SANDOVAL-DENIS, M.; SUTTON, D. A.; FOTHERGILL, A. W.; CANO-LIRA, J.; GENÉ, J.; DECOCK, C. A.; DE HOOG, G. S.; GUARRO, J. Scopulariopsis, a poorly known opportunistic fungus: spectrum of species in clinical samples and in vitro responses to antifungal drugs. Journal of Clinical Microbiology, v. 51, n. 12, p. 3937-3943, 2013.

SANDOVAL-DENIS, M.; SUTTON, D. A.; CANO-LIRA, J. F.; GENÉ, J.; FOTHERGILL, A. W.; WIEDERHOLD, N. P.; GUARRO, J. Phylogeny of the clinically relevant species of the emerging fungus Trichoderma and their antifungal susceptibilities. Journal of Clinical Microbiology, v. 52, n. 6, p. 2112-2125, 2014.

SANDOVAL-DENIS, M.; GENÉ, J.; SUTTON, D. A.; WIEDERHOLD, N. P.; CANO-LIRA, J. F.; GUARRO, J. New species of Cladosporium associated with human and animal infections. Persoonia: Molecular Phylogeny and Evolution of Fungi, v. 36, p. 281-298, 2016.

SCHUSTER, A.; SCHMOLL, M. Biology and biotechnology of Trichoderma. Applied Microbiology and Biotechnology, v. 87, n. 3, p. 787-799, 2010.

SEBBEN, A. Microdissecação fisiológica a fresco: uma nova visão sobre a anatomia de anfíbios e répteis. In: NASCIMENTO, L. B.; OLIVEIRA, M. E. (Ed.), Herpetologia no Brasil II (p. 311-325). Belo Horizonte, MG: Sociedade Brasileira de Herpetologia, 2007.

SEGALLA, M. V.; CARAMASCHI, U.; CRUZ, C. A. G.; GRANT, T.; HADDAD, C. F. B.; LANGONE, J. A.; GARCIA, P. C. A. Brazilian amphibians: List of species. Herpetologia Brasileira, v. 5, n. 2, p. 34-46, 2016.

SHEEBA, H., ALI, M. S.; ANURADHA, V. Bioactive compounds and antimicrobial activity of fungal crude extract from medicinal plants. Journal of Pharmaceutical Sciences and Research, v. 11, n. 5, p. 1826-1833, 2019.

SINGH, P. K.; KATHURIA, S.; AGARWAL, K.; GAUR, S. N.; MEIS, J. F.; CHOWDHARY, A. Clinical significance and molecular characterization of nonsporulating molds isolated from the respiratory tracts of bronchopulmonary mycosis patients with special reference to basidiomycetes. Journal of Clinical Microbiology, v. 51, n. 10, p. 3331-3337, 2013.

SOUCHIE, E. L.; AZCÓN, R.; BAREA, J. M.; SAGGIN-JÚNIOR, O. J.; SILVA, E. M. R. Solubilização de fosfatos em meios sólido e líquido por bactérias e fungos do solo. Pesquisa Agropecuária Brasileira, v. 40, n. 11, p. 1149-1152, 2005.

SUMMERBELL, R. C. Aspergillus, Fusarium, Sporothrix, Piedraia, and their relatives. In: HOWARD, D. H. (Ed.), Pathogenic Fungi in Humans and Animals (p. 237-498). New York: CRC Press, 2003.

THIRION‐DELALANDE, C.; GUILLOT, J.; JENSEN, H. E.; CRESPEAU, F. L.; BERNEX, F. Disseminated acute concomitant aspergillosis and mucormycosis in a pony. Journal of Veterinary Medicine Series A, v. 52, n. 3, p. 121-124, 2005.

VAN ROOIJ, P.; MARTEL, A.; HAESEBROUCK, F.; PASMANS, F. Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Veterinary Research, v. 46, n. 1, p. 137, 2015.

VARELA, B. J.; LESBARRÈRES, D.; IBÁÑEZ, R.; GREEN, D. M. Environmental and host effects on skin bacterial community composition in panamanian frogs. Frontiers in Microbiology, v. 9, n. 298, 2018.

VILLA, J. Two fungi lethal to frog eggs in Central America. Copeia, v. 1979, n. 4, p. 650-655, 1979.

VITT, L. J.; CALDWELL, J. P. Herpetology: An Introductory Biology of Amphibians and Reptiles. Academic Press, 2013.

WALKE, J. B.; BECKER, M. H.; LOFTUS, S. C.; HOUSE, L. L.; CORMIER, G.; JENSEN, R. V.; BELDEN, L. K. Amphibian skin may select for rare environmental microbes. The ISME Journal, v. 8, n. 11, p. 2207-2217, 2014.

WALKE, J. B.; BECKER, M. H.; HUGHEY, M. C.; SWARTWOUT, M. C.; JENSEN, R. V.; BELDEN, L. K. Most of the dominant members of amphibian skin bacterial communities can be readily cultured. Applied and Environmental Microbiology, v. 81, n. 19, p. 6589-6600, 2015.

XU, X.; LAI, R. The chemistry and biological activities of peptides from amphibian skin secretions. Chemical Reviews, v. 115, n. 4, p. 1760-1846, 2015.

ZAIN, M. E. Impact of mycotoxins on humans and animals. Journal of Saudi Chemical Society, v. 15, n. 2, p. 129-144, 2011.



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