Advertisement

EcoHealth

, Volume 16, Issue 1, pp 128–140 | Cite as

The Chytrid Fungus, Batrachochytrium dendrobatidis, is Widespread Among Cuban Amphibians

  • Antonio CádizEmail author
  • Mey Ling Reytor
  • Luis M. Díaz
  • Tara Chestnut
  • John A. Burns
  • George Amato
Original Contribution

Abstract

The fungus Batrachochytrium dendrobatidis (Bd) is a generalist amphibian pathogen responsible for chytridiomycosis. It was documented for the first time in Cuba in 2007, the apparent cause of the decline in one species of toad. In a recent survey, Bd was reported only for the highlands of Central Cuba. In the present study, we reexamined the geographic distribution and level of impact of Bd in Cuba by conducting an island-wide sampling in 10 localities and collecting skin swabs from 18 species and 28 environmental samples. We report detection of Bd in 60% of sampled sites and in 58% of sampled taxa. We show that Bd is associated with riparian, arboreal and terrestrial species, and it was estimated to occur in approximately 30% of the aquatic habitats we sampled. In addition, we confirmed that a dying individual of the species Eleutherodactylus casparii was severely infected with Bd. We also rise concern about the endanger toad Peltophryne longinasus and about three species of endemic riparian frogs that were not detected during our surveys. This study demonstrates that this pathogen is widespread throughout Cuba and provides relevant evidence to advance our understanding of its detection in amphibians and the aquatic environment in Cuba and about the occurrence of Bd in species with different ecologies. We provide valuable baseline information for Bd risk assessment and decision-making processes to mitigate its negative impact on Cuban amphibians.

Keywords

Batrachochytrium dendrobatidis Cuba Eleutherodactylus Peltophryne longinasus Wildlife disease Aquatic 

Notes

Acknowledgements

This work was supported by the Rufford Small Grant Foundation (Project Number 18878-1 to Mey Ling Reytor and Antonio Cádiz) and The Mohamed bin Zayed Species Conservation Fund (Project Number 14259845 to Antonio Cádiz). A research grant from the American Society for Biochemistry and Molecular Biology (PROLAB Grant) to Antonio Cádiz allowed him to conduct laboratory experiments at The American Museum of Natural History. Our gratitude to Amphibian Ark for partial support of fieldwork, especially to Kevin Zippel and Kevin Johnson. We are very grateful to Rachel Batista, Rosana Gonzalez and Manuel Iturriaga for their assistance during fieldwork. Ariatna Linares helped during fieldwork coordination. Gricelia Calzada supported us with housing and hospitality. The Faculty of Biology and The Museum of Natural History of Cuba provided legal support for expeditions. David Bird and Darren Reynolds from the University of West of England, Wolfgang Feichtinger from the University of Wuerzburg, Masakado Kawata from Tohoku University and Jenny Urbina from Oregon State University kindly provided sampling equipment. Deanna H. Olson from Pacific Northwest Research Station provided Bd strain used for standards. Rebecca Hersch provided laboratory assistance. This manuscript was greatly improved thanks to two anonymous reviewers.

Supplementary material

10393_2018_1383_MOESM1_ESM.docx (77 kb)
Supplementary material 1 (DOCX 77 kb)

References

  1. Adams M J, Chelgren ND, Reinitz D, Cole RA, Rachowicz LJ, Galvan S, et al. (2010) Using occupancy models to understand the distribution of an amphibian pathogen, Batrachochytrium dendrobatidis. Ecological Applications 20(1):289–302.CrossRefGoogle Scholar
  2. Alemu JB, Cazabon-Mannette MN, Cunningham AA, Dempewolf L, Hailey A, Mannette RP, Naranjit KT, Perkins MW, Schmidt-Roach AC (2013) Presence of the chytrid fungus Batrachochytrium dendrobatidis in a Vulnerable frog in Trinidad, West Indies. Endangered Species Research 20:131–136.  https://doi.org/10.3354/esr00485.CrossRefGoogle Scholar
  3. Alonso R, Crawford AJ, Bermingham E (2012) Molecular phylogeny of an endemic radiation of Cuban toads (Bufonidae: Peltophryne) based on mitochondrial and nuclear genes. Journal of Biogeography 39:434–451.CrossRefGoogle Scholar
  4. Barbour T (1926) New amphibia. Occasional Papers of the Boston Society of Natural History 5: 1991-1994.Google Scholar
  5. Berger L, Hyatt AD, Speare R, Longcore JE (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 68:51–63.CrossRefGoogle Scholar
  6. Blaustein AR, Gervasi SS, Johnson PTJ, Hoverman JT, Belden LK, Bradley PW, Xie GY (2012) Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philosophical Transactions of the Royal Society B 367:1688–1707CrossRefGoogle Scholar
  7. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60:141–148.CrossRefGoogle Scholar
  8. Brem F, Mendelson J, Lips (2007) Field-Sampling Protocol for Batrachochytrium dendrobatidis from Living Amphibians, using Alcohol Preserved Swabs. http://www.amphibians.org
  9. Burrowes PA, Joglar RL, Green DE (2004) Potential causes for amphibian declines in Puerto Rico. Herpetologica 60: 141–154.CrossRefGoogle Scholar
  10. Burrowes PA, Longo AV, Joglar RL, Cunningham AA (2008) Geographic Distribution of Batrachochytrium dendrobatidis in Puerto Rico. Herpetological Review 39(3): 321–324.Google Scholar
  11. Chestnut T, Anderson C, Popa R, Blaustein AR, Voytek M, Olson DH, et al (2014) Heterogeneous Occupancy and Density Estimates of the Pathogenic Fungus Batrachochytrium dendrobatidis in Waters of North America. PLoS ONE 9(9).Google Scholar
  12. Daszak P, Strieby A, Cunningham AA, Longcore JE, Brown CC, Porter D (2004) Experimental evidence that the bullfrog (fRana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetological Journal 14:201–207.Google Scholar
  13. Díaz LM, Cádiz A, Chong A, and Silva A (2007) First report of chytridiomycosis in a dying toad (Anura: Bufonidae) from Cuba: a new conservation challenge for the island. Eco-Health 4:172–175.Google Scholar
  14. Díaz LM, Estrada AR, Hedges SB (2001) A new riparial frog of the genus Eleutherodactylus (Anura: Leptodactylidae) from Eastern Cuba. Caribbean Journal of Science 37: 63-71.Google Scholar
  15. Díaz LM, Cádiz A (2008) Guía taxonómica de los anfibios de Cuba. Abc Taxa Press.Google Scholar
  16. Forrest MJ, Schlaepfer MA (2011) Nothing a Hot Bath Won’t Cure: Infection Rates of Amphibian Chytrid Fungus Correlate Negatively with Water Temperature under Natural Field Settings. PLoS ONE 6(12): e28444;  https://doi.org/10.1371/journal.pone.0028444
  17. García G, Lopez J, Fa JE, Gray GAL (2009) Chytrid fungus strikes mountain chickens in Montserrat. Oryx 43: 323–324.CrossRefGoogle Scholar
  18. Hedges SB, González L, Estrada AR (1995) Rediscovery of the Cuban frogs Eleutherodactylus cubanus and E. turquinensis (Anura: Leptodactylidae). Caribbean Journal of Science 31: 327-332.Google Scholar
  19. Holmes I, McLaren K, Wilson B (2012) Surveys for frog diversity and Batrachochytrium dendrobatidis in Jamaica. Herpetological Review 43(2): 150–159.Google Scholar
  20. Johnson M, Berger L, Philips L, Speare L (2003) Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 57:255–260.CrossRefGoogle Scholar
  21. Kilpatrick AM, Briggs CJ, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends in Ecology and Evolution 25:109–118.CrossRefGoogle Scholar
  22. Kirshtein JD, Anderson CW, Wood JS, Longcore JE, Voytek MA (2007). Quantitative PCR detection of Batrachochytrium dendrobatidis DNA from sediments and water. Diseases of Aquatic Organisms 77:11.CrossRefGoogle Scholar
  23. Kolby JE, Ramirez SD, Berger L, Richards-Hrdlicka KL, Jocque M, Skerratt LF (2015) Terrestrial Dispersal and Potential Environmental Transmission of the Amphibian Chytrid Fungus (Batrachochytrium dendrobatidis). PLoS ONE 10(4): e0125386.  https://doi.org/10.1371/journal.pone.0125386 CrossRefPubMedCentralGoogle Scholar
  24. Langhammer PF (2013) Chytridiomycosis in the Direct-developing Frogs of Puerto Rico. A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy. 109 pp.Google Scholar
  25. Lips KR, Burrowes PA, Mendelson JR, Parra-Olea G (2005) Amphibian declines in Latin America: widespread population declines, extinctions, and impacts. Biotropica 37:163– 165.CrossRefGoogle Scholar
  26. Longo AV, Burrowes PA. 2010. Persistence with chytridiomycosis does not assure survival of direct-developing frogs. Ecohealth 7:185–195.CrossRefGoogle Scholar
  27. Longo AV, Burrowes PA, Joglar RL (2009) Seasonality of Batrachochytrium dendrobatidis infection in direct-developing frogs suggests a mechanism for persistence. Disease of Aquatic Organisms 92: 253–260.CrossRefGoogle Scholar
  28. Longo AV, Rodriguez D, da Silva Leite D, Toledo LF, Mendoza Almeralla C, et al. (2013) ITS1 Copy Number Varies among Batrachochytrium dendrobatidis Strains: Implications for qPCR Estimates of Infection Intensity from Field-Collected Amphibian Skin Swabs. PLoS ONE 8(3): e59499. doi:10.1371/journal.pone.0059499.CrossRefPubMedCentralGoogle Scholar
  29. Magin C (2003) Dominica’s frogs are croaking. Oryx 37:406.Google Scholar
  30. MacKenzie DI, Nichols JD, Lachman BG, Droege S, Royle JA, Langtimm CA (2002) Estimating site occupancy rates when detection probabilities are less than one. Ecology 83:2248-2255.CrossRefGoogle Scholar
  31. Malhotra A, Thorpe RS, Hypolite E, James A (2007) A report on the status of the herpetofauna of the Commonwealth of Dominica, West Indies. Applied Herpetology 4:177–194.CrossRefGoogle Scholar
  32. Nichols DK, Lamirande EW, Pessier AP, Longcore JE (2001) Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs. Journal of Wildlife Diseases. 37:1–11;  https://doi.org/10.7589/0090-3558-37.1.1
  33. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, et al (2013) Mapping the Global Emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus. PLoS ONE 8(2): e56802;  https://doi.org/10.1371/journal.pone.0056802
  34. Pessier, AP and Mendelson JR (2010) A Manual for Control of Infectious Diseases in Amphibian Survival Assurance Colonies and Reintroduction Programs. IUCN/SSC Conservation Breeding Specialist Group: Apple Valley, MN.Google Scholar
  35. Piotrowski SJ, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia, 96 (1):9–15.CrossRefGoogle Scholar
  36. Ramakers C, Ruijter JM, Deprez RHL, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience letters 339(1):62-66.CrossRefGoogle Scholar
  37. Rowley JJL, Alford RA (2013) Hot bodies protect amphibians against chytrid infection in nature. Scientific Reports 3:1515;  https://doi.org/10.1038/srep01515
  38. Sabino-Pinto J, Bletz CM, Iturriaga M, Vences M, Rodríguez A (2017). Low infection prevalence of the amphibian chytrid fungus Batrachochytrium dendrobatidis (Chytridiomycetes: Rhizophydiales) in Cuba. Amphibia-Reptilia 1-7;  https://doi.org/10.1163/15685381-00003100
  39. Schloegel LM, Toledo LF, Longcore J E, Greenspan SE, Vieira CA, Lee M, et al. (2012) Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21:5162–5177.CrossRefGoogle Scholar
  40. Valdés de la Osa A, Ruíz-García F (1980) Consideraciones sistemáticas sobre Bufo longinasus (Anura: Bufonidae) de Cuba y descripción de una nueva subespecie. Poeyana 206:1-34.Google Scholar
  41. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, et al (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582–585.CrossRefGoogle Scholar
  42. Vredenburg VT, Knapp RA, Tunstall TS, Briggs C (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences 107:9689–9694.CrossRefGoogle Scholar
  43. Whitfield SM, Geerdes E, Chacon I, Ballestero ER, Jimenez RR, Donnelly MA, Kerby JL (2013) Infection and co-infection by the amphibian chytrid fungus and ranavirus in wild Costa Rican frogs. Diseases of Aquatic Organisms 104:173–178.CrossRefGoogle Scholar

Copyright information

© EcoHealth Alliance 2018

Authors and Affiliations

  1. 1.Faculty of BiologyHavana UniversityLa HavanaCuba
  2. 2.National Museum of Natural History of CubaLa HavanaCuba
  3. 3.Mt Rainier National ParkWashingtonUSA
  4. 4.Sackler Institute for Comparative GenomicsAmerican Museum of Natural HistoryNew YorkUSA
  5. 5.WeehawkenUSA

Personalised recommendations