DETECTION OF Batrachochytrium dendrobatidis IN AMPHIBIANS FROM A PET MARKET AND TWO WILD POPULATIONS IN MEXICO

Andrea Angeles-Vázquez; Mirna G. García-Castillo; Eria A. Rebollar; Gabriela Parra-Olea; María Delia Basanta

doi:10.22201/fc.25942158e.2025.3.1267

Autores/as

Andrea Angeles-Vázquez Facultad de Ciencias UNAM
Mirna G. García-Castillo Facultad de Ciencias UNAM
Eria A. Rebollar Centro de Ciencias Genómicas UNAM
Gabriela Parra-Olea
María Delia Basanta

DOI:

https://doi.org/10.22201/fc.25942158e.2025.3.1267

Palabras clave:

Declives de anfibios, enfermedades infecciosas, quitridiomicosis, patógenos fúngicos

Resumen

La quitridiomicosis, causada por los hongos Batrachochytrium dendrobatidis (Bd) y Batrachochytrium salamandrivorans (Bsal), es una de las principales causas de declives de anfibios a nivel mundial. En este estudio, se analizó la presencia de Bd y Bsal en 16 especies de anfibios de tres localidades de México, incluyendo el mercado de mascotas Emilio Carranza en Ciudad de México, y las localidades de Tenango de Doria, Hidalgo, y Cuetzalan, Puebla. Bsal no fue detectado en ninguna muestra. El mercado de mascotas presentó los valores más altos de infección por Bd con un 60 % de prevalencia y un promedio de 3.45x10¹² copias de ITS Bd. Tenango de Doria presentó 50 % de prevalencia de Bd, mientras que en Cuetzalan Bd no fue detectado. Estos resultados resaltan el riesgo potencial de dispersión de patógenos por parte del comercio de anfibios, y la importancia del monitoreo continuo para la conservación de los anfibios en México.

Citas

Angeles-Vázquez, A. P., García-Castillo, M. G., Parra-Olea, G., Solano de la Cruz, M. T., & Basanta, M. D. (2025). Influence of environmental temperature on the phenotypic variation of Batrachochytrium dendrobatidis isolates from Mexico. Fungal Genetics and Biology, 180, 104017. https://doi.org/10.1016/j.fgb.2025.104017

Basanta, M. D., Byrne, A. Q., Rosenblum, E. B., Piovia-Scott. J., & Parra-Olea, G. (2021). Early presence of Batrachochytrium dendrobatidis in Mexico with a contemporary dominance of the global panzootic lineage. Molecular Ecology, 30(2), 424–437. https://doi.org/10.1111/mec.15733

Basanta, M. D., Avila-Akerberg V., Byrne, A. Q., Castellanos-Morales, G., González Martínez, T. M., Maldonado-López, Y., Rosenblum, E. B., Suazo-Ortuño, I., Parra Olea, G., & Rebollar E. A. (2022). The fungal pathogen Batrachochytrium salamandrivorans is not detected in wild and captive amphibians from Mexico. PeerJ, 10, e14117. https://doi.org/10.7717/peerj.14117

Bates, K. A., Shelton, J. M. G., Mercier, V. L., Hopkins, K. P., Harrison, X. A., Petrovan, S. O., & Fisher, M. C. (2019). Captivity and infection by the fungal pathogen Batrachochytrium salamandrivorans perturb the amphibian skin microbiome. Frontiers in Microbiology, 10, 1834. https://doi.org/10.3389/fmicb.2019.01834

Berger, L., Marantelli, G., Skerratt, L., & Speare, R. (2005). Virulence of the amphibian chytrid fungus Batrachochytrium dendrobatidis varies with the strain. Diseases of Aquatic Organisms, 68(1), 47–50. https://doi.org/10.3354/dao068047

Boyle, D. G., Olsen, V., Morgan, J. A., & Hyatt, A. D. (2004). Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms, 60(2), 141–148. https://doi.org/10.3354/dao060141

Chomel, B. B., Belotto, A., & Meslin, F. X. (2007). Wildlife, exotic pets, and emerging zoonoses. Emerging Infectious Diseases, 13(1), 6–11. https://doi.org/10.3201/eid1301.060480

Daszak, P., Strieby, A., Cunningham, A. A., Longcore, J. E., Brown, C. C., & Porter, D. (2004). Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. The Herpetological Journal, 14, 201–207.

Fisher, M. C., Bosch, J., Yin, Z., et al. (2009). Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Molecular Ecology, 18(3), 415–429. https://doi.org/10.1111/j.1365-294X.2008.04041.x

Fisher, M. C., & Garner, T. W. J. (2020). Chytrid fungi and global amphibian declines. Nature Reviews. Microbiology, 18(6), 332–343. https://doi.org/10.1038/s41579-020-0335-x

Galindo-Bustos, M. A., Hernandez-Jauregui, D. M., Cheng, T., Vredenburg, V., & Parra-Olea, G. (2014). Presence and prevalence of Batrachochytrium dendrobatidis in commercial amphibians in Mexico City. Journal of zoo and wildlife medicine: official publication of the American Association of Zoo Veterinarians, 45(4), 830–835. https://doi.org/10.1638/2014-0023.1.

García-Feria, L., Brousset, D., Vallejo, D., & Cervantes-Olivares, R. (2017). El comercio de anfibios y la presencia de Batrachochytrium dendrobatidis en vida libre: ¿dispersión en círculo vicioso? Neotropical Biology and Conservation, 12(1), 30–36. https://doi.org/10.4013/nbc.2017.121.04

Gray, M. J., Carter, E. D., Piovia-Scott, J., et al. (2023). Broad host susceptibility of North American amphibian species to Batrachochytrium salamandrivorans suggests high invasion potential and biodiversity risk. Nature Communications, 14, 3270. https://doi.org/10.1038/s41467-023-38979-4

IUCN. 2024. The IUCN Red List of Threatened Species. Version 2024–21. https://www.iucnredlist.org. [Accessed in November 2024].

Karesh, W. B., Cook, R. A., Bennett, E. L., & Newcomb, J. (2005). Wildlife trade and global disease emergence. Emerging Infectious Diseases, 11(7), 1000–1002. https://doi.org/10.3201/eid1107.050194

Lambert, M. R., Womack, M. C., Byrne, A. Q., et al. (2020). Comment on "Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity". Science, 367(6484), eaay1838. https://doi.org/10.1126/science.aay1838

López–Velázquez, A. (2018). Ocurrencia de la quitridiomicosis en México. In López–Velázquez, A., Basanta, M. D., & Ochoa–Ochoa, L. (Eds.), Quitridiomicosis en México (pp. 35-52). Sociedad Herpetológica Mexicana A.C.

Martel, A., Spitzen-van der Sluijs, A., Blooi, M., et al. (2013). Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America, 110(38), 15325–15329. https://doi.org/10.1073/pnas.1307356110.

Martel, A., Blooi, M., Adriaensen, C., et al. (2014). Wildlife disease. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders. Science, 346(6209), 630–631. https://doi.org/10.1126/science.1258268.

North American Bsal Task Force (2022). A North American strategic plan to prevent and control invasions of the lethal salamander pathogen Batrachochytrium salamandrivorans. Bsal Task Force https://salamanderfungus.org/wp-content/uploads/sites/62/2022/03/Bsal-Strategic-Plan_March-2022_FINAL.pdf

O'Hanlon, S. J., Rieux, A., Farrer, R. A., et al. (2018). Recent Asian origin of chytrid fungi causing global amphibian declines. Science, 360(6389), 621–627. https://doi.org/10.1126/science.aar1965

Peralta-García, A., Valdez-Villavicencio, J. H. & P. Galina-Tessaro. 2014. African clawed frog (Xenopus laevis) in Baja California: a confirmed population and possible ongoing invasion in Mexican watersheds. The Southwestern Naturalist, 59(3):431–434.

Peterson, J. D., Steffen, J. E., Reinert, L. K., Cobine, P. A., Appel, A., Rollins-Smith, L., & Mendonça, M. T. (2013). Host stress response is important for the pathogenesis of the deadly amphibian disease, chytridiomycosis, in Litoria caerulea. PLoS ONE 8(4), e62146. https://doi.org/10.1371/journal.pone.0062146

Ramsey, J. P., Reinert, L. K., Harper, L. K., Woodhams, D. C., & Rollins-Smith, L. A. (2010). Immune defenses against Batrachochytrium dendrobatidis, a fungus linked to global amphibian declines, in the South African clawed frog, Xenopus laevis. Infection and immunity, 78(9), 3981–3992. https://doi.org/10.1128/IAI.00402-10

Rollins-Smith, L. A., & Conlon, J. M. (2005). Antimicrobial peptide defenses against chytridiomycosis, an emerging infectious disease of amphibian populations. Developmental and comparative immunology, 29(7), 589–598. https://doi.org/10.1016/j.dci.2004.11.004.

Scheele, B. C., Pasmans, F., Skerratt, L. F., et al. Science, 363(6434), 1459–1463. https://doi.org/10.1126/science.aav0379

Schloegel, L. M., Picco, A. M., Kilpatrick, A. M., Davies, A. J., Hyatt, A. D., Daszak, P. (2009). Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs Rana catesbeiana. Biological Conservation, 142(7),1420–1426. https://doi.org/10.1016/j.biocon.2009.02.007

Searle, C. L., Gervasi, S. S., Hua, J., Hammond, J. I., Relyea, R. A., Olson, D. H., & Blaustein, A. R. (2011). Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conservation biology: the journal of the Society for Conservation Biology, 25(5), 965–974. https://doi.org/10.1111/j.1523-1739.2011.01708.x

Van Rooij, P., Martel, A., Nerz, J., Voitel, S., Van Immerseel, F., Haesebrouck, F., & Pasmans, F. (2011). Detection of Batrachochytrium dendrobatidis in Mexican bolitoglossine salamanders using an optimal sampling protocol. EcoHealth, 8(2), 237–243. https://doi.org/10.1007/s10393-011-0704-z

Winzeler, M. E. & Grear, D. A. (2024). Student Network for Amphibian Pathogen Surveillance Data (ver. 2.0, April 2024). U.S. Geological Survey data release. https://doi.org/10.5066/P9F6OCWG.

World Organisation for Animal Health (2019) OIE - Aquatic Animal Health Code. https://rr-europe.woah.org/app/uploads/2020/08/oie-aqua-code_2019_en.pdf