Abstract
Batrachochytrium dendrobatidis, a chytrid fungus infecting amphibians’ cutaneous layer, is responsible for the greatest contemporary loss of amphibian biodiversity. In South America, Suriname is one of the only three countries where B. dendrobatidis infections of anurans (frogs and toads) have not been documented. To further examine this apparent gap in pathogen occurrence, frogs were sampled for B. dendrobatidis spores at eight disparate geographic locations in Suriname, including locations with high and low levels of anthropogenic activities, and near Suriname’s border with Brazil and French Guiana, countries where B. dendrobatidis infections have been documented. None of the 347 frogs sampled, representing 37 species from eight families, tested positive for B. dendrobatidis. Our results provide the baseline data for future comparative testing and one of the last opportunities for a country in South America to proactively plan mitigation measures to protect amphibians from B. dendrobatidis’ presumed eventual incursion into Suriname.
Similar content being viewed by others
Data Availability
The dataset generated during the current study are available in the figshare repository, https://doi.org/10.6084/m9.figshare.16615981.
References
Arellano ML, Ferraro DP, Steciow MM, Lavilla EO (2009) Infection by the chytrid fungus Batrachochytrium dendrobatidis in the yellow belly frog (Elachistocleis bicolor) from Argentina. The Herpetological Journal 19(4):217–220
Barrionuevo JS, Aguayo R, Lavilla EO (2008) First record of chytridiomycosis in Bolivia (Rhinella quechua; Anura: Bufonidae). Diseases of Aquatic Organisms 82(2):161–163
Becker MH, Harris RN, Minbiole KP, Schwantes CR, Rollins-Smith LA, Reinert LK, Brucker RM, Domangue RJ, Gratwicke B (2011) Towards a better understanding of the use of probiotics for preventing chytridiomycosis in Panamanian golden frogs. Ecohealth 8(4):501–506
Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, Mcdonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95:9031–9036
Bower DS, Lips KR, Amepou Y, Richards S, Dahl C, Nagombi E, Supuma M, Dabek L, Alford RA, Schwarzkopf L, Ziembicki M, Noro JN, Hamidy A, Gillespie GR, Berger L, Eisemberg C, Li Y, Liu X, Jennings CK, Tjaturadi B, Peters A, Krockenberger AK, Nason D, Kusrini MD, Webb RJ, Skerratt LF, Banks C, Mack AL, Georges A, Clulow S (2019) Island of opportunity: can New Guinea protect amphibians from a globally emerging pathogen? Frontiers of Ecology Environment 17(6):348–354
Burrowes PA, De la Riva I (2017) Detection of the amphibian chytrid fungus Batrachochytrium dendrobatidis in museum specimens of Andean aquatic birds: implications for pathogen dispersal. Journal of Wildlife Diseases 53(2):349–355
Courtois EA, Pineau K, Villette B, Schmeller DS, Gaucher P (2012) Population estimates of Dendrobates tinctorius (Anura: Dendrobatidae) at three sites in French Guiana and first record of chytrid infection. Phyllomedusa: Journal of Herpetology 11(1):63–70
Courtois EA, Gaucher P, Chave J, Schmeller DS (2015) Widespread occurrence of Bd in French Guiana, South America. Plos ONE 10(4):1–14
De Dijn BPE, Molgo IE, Norconk MA, Gregory LT, O’Shea B, Marty C, Luger M, Ringler M, Crothers S, Noonan B, Fitzgerald K (2007) The biodiversity of the Brownsberg. CI Rapid Assessment Program Bulletin of Biological Assessment 43:135–155
de Queiroz Carnaval ACO, Puschendorf R, Peixoto OL, Verdade VK, Rodrigues MT (2006) Amphibian chytrid fungus broadly distributed in the Brazilian Atlantic rain forest. EcoHealth 3(1):41–48
d’Orgeix CA, Hardy D, Witiak SM, Robinson LR, Jairam R (2019) The blue dyeing poison-dart frog, Dendrobates tinctorius (Dendrobates azureus, Hoogmoed 1969): extant in Suriname based on a rapid survey. Amphibian & Reptile Conservation 13(2):259–264
Fisher MC, Garner TW (2007) The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews 21(1):2–9
Flechas SV, Sarmiento C, Amézquita A (2012) Bd on the beach: high prevalence of Batrachochytrium dendrobatidis in the lowland forests of Gorgona Island (Colombia, South America). EcoHealth 9(3):298–302
Flechas SV, Medina EM, Crawford AJ, Sarmiento C, Cárdenas ME, Amézquita A, Restrepo S (2013) Characterization of the First Batrachochytrium dendrobatidis Isolate from the Colombian Andes, an Amphibian Biodiversity Hotspot. EcoHealth 10:72–76
Flechas SV, Paz A, Crawford AJ, Sarmiento C, Acevedo AA, Arboleda A, Bolívar-García W, Echeverry-Sandoval CL, Franco R, Mojica C, Munoz A (2017) Current and predicted distribution of the pathogenic fungus Batrachochytrium dendrobatidis in Colombia, a hotspot of amphibian biodiversity. Biotropica 49(5):685–694
Garmyn A, Van Rooij P, Pasmans F, Hellebuyck T, Van Den Broek W, Haesebrouck F, Martel A (2012) Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PloS ONE 7(4):1–5
Gold KK, Reed PD, Bemis DA, Miller DL, Gray MJ, Souza MJ (2013) Efficacy of common disinfectants and terbinafine in inactivating the growth of Batrachochytrium dendrobatidis in culture. Diseases of Aquatic Organisms 107:77–81
Gower DJ, Doherty-Bone T, Loader SP, Wilkinson M, Kouete MT, Tapley B, Orton F, Daniel OZ, Wynne F, Flach E, Müller H, Menegon M, Stephen I, Browne RK, Fisher MC, Cunningham AA, Garner TWJ (2013) Batrachochytrium dendrobatidis infection and lethal chytridiomycosis in caecilian amphibians (Gymnophiona). EcoHealth 10:173–183
Harris RN, Brucker RM, Walke JB, Becker MH, Schwantes CR, Flaherty DC, Lam BA, Woohams DC, Briggs CJ, Vredenburg VT, Minbiole KPC (2009) Skin microbes on frogs prevent morbidity and mortality caused by a lethal skin fungus. ISME Journal 3:818–824
Hoogmoed MS (1969) Notes on the herpetofauna of Surinam III. A new species of Dendrobates (Amphibia, Salientia, Dendrobatidae) from Surinam. Zoologische Mededelingen Leiden 44(9):133–141
Hoogmoed MS (2019) Unpublished population data of Dendrobates azureus Hoogmoed 1969 obtained in 1968 and 1970, and its historical and current taxonomic status. Amphibian Reptile Conservation 13(2):95–101
Jairam R (2020) A historical overview of Batrachochytrium dendrobatidis infection from specimens at the National Zoological Collection Suriname. PloS ONE 15(10):e0239220
Johnson ML, Speare R (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Diseases of Aquatic Organisms 65(3):181–186
Julian JT, Henry PF, Drasher JM, Michell K, Smith SA (2020) Minimizing the spread of aquatic herpetofaunal pathogens by decontaminating construction equipment. Herpetological Review 51(3):472–483
Kolby JE, Ramirez SD, Berger L, Griffin DW, Jocque M, Skerratt LF (2015) Presence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) in rainwater suggests aerial dispersal is possible. Aerobiologia 31(3):411–419
Kosch TA, Morales V, Summers K (2012) Batrachochytrium Dendrobatidis in Peru. Herpetological Review 43(2):288–293
La Marca E, Lips KR, Lötters S, Puschendorf R, Ibáñez R, Rueda-Almonacid JV, Schulte R, Marty C, Castro F, Manzanilla-Puppo J, García-Pérez JE (2005) Catastrophic population declines and extinctions in Neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica: the Journal of Biology and Conservation 37(2):190–201
Lambertini C, Becker CG, Bardier C, da Silva Leite D, Toledo LF (2017) Spatial distribution of Batrachochytrium dendrobatidis in South American caecilians. Diseases of Aquatic Organisms 124(2):109–116
Lampo M, Barrio-Amoró C, Han B (2006a) Batrachochytrium dendrobatidis infection in the recently rediscovered Atelopus mucubajiensis (Anura, Bufonidae), a critically endangered frog from the Venezuelan Andes. EcoHealth 3:299–302
Lampo M, Rodriguez-Contreras A, La Marca E, Daszak P (2006b) A chytridiomycosis epidemic and a severe dry season precede the disappearance of Atelopus species from the Venezuelan Andes. Herpetological Journal 16(4):395–402
Lampo MA, Sánchez DI, Nicolás AN, Márquez MA, Nava-González FR, García CZ, Rinaldi MI, Rodriguez-Contreras AR, León F, Han B, Chacón-Ortiz AN (2008) Batrachochytrium Dendrobatidis in Venezuela. HerpetoLogical Review 39(4):449–454
Laufer G, Gobel N, Borteiro C, Soutullo A, Martínez-Debat C, de Sá RO (2018) Current status of American bullfrog, Lithobates catesbeianus, invasion in Uruguay and exploration of chytrid infection. Biological Invasions 20(2):285–291
Laurance W, McDonald KR, Speare R (1997) In defense of the epidemic disease hypothesis. Conservation Biology 11:1030–1034
Lips KR, Burrowes PA, Mendelson JR III, Parra-Olea G (2005) Amphibian Declines in Latin America: Widespread Population Declines, Extinctions, and Impacts. Biotropica: the Journal of Biology and Conservation 37(2):163–165
Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227
Luger M, Garner TW, Ernst R, Hödl W, Lötters S (2008) No evidence for precipitous declines of harlequin frogs (Atelopus) in the Guyanas. Studies on Neotropical Fauna and Environment 43(3):177–180
Mathie AH, Jarrett C, Jhaveri L, Hoskisson PA, Downie JR (2018) The first assessment of Batrachochytrium dendrobatidis in amphibian populations in the Kanuku Mountains Protected Area of Guyana. Herpetological Bulletin 146:18–24
McCracken S, Gaertner JP, Forstner MR, Hahn D (2009) Detection of Batrachochytrium dendrobatidis in amphibians from the forest floor to the upper canopy of an Ecuadorian Amazon lowland rainforest. Herpetological Review 40(2):190–195
O’Hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, Kosch TA, Murray KA, Brankovics B, Fumagalli M, Martin MD, Wales N, Alvarado-Rybak M, Bates KA, Berger L, Böll S, Brookes L, Clare F, Courtois EA, Cunningham AA, Doherty-Bone TM, Ghosh P, Gower DJ, Hintz WE, Höglund J, Jenkinson TS, Lin CF, Laurila A, Loyau A, Martel A, Meurling S, Miaud C, Minting P, Pasmans F, Schmeller DS, Schmidt BR, Shelton JMG, Skerratt LF, Smith F, Soto-Azat C, Spagnoletti M, Tessa G, Toledo LF, Valenzuela-Sánchez A, Verster R, Vörös J, Webb RJ, Wierzbicki C, Wombwell E, Zamudio KR, Aanensen DM, James TY, Gilbert MTP, Weldon C, Bosch J, Balloux F, Garner TWJ, Fisher MC (2018) Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360(6389):621–627
Olson D, Haman KH, Gray M, Harris R, Thompson T, Iredale M, Christman M, Williams J, Adams MJ, Ballard J (2021) Enhanced between-site biosecurity to minimize herpetofaunal disease-causing pathogen transmission. Herpetological Review 52(1):29–39
Ouboter PE, Jairam R (2012) Amphibians of Suriname. Leiden: Brill
Phillott AD, Speare R, Hines HB, Skerratt LF, Meyer E, McDonald KR, Cashins SD, Mendez D, Berger L (2010) Minimising exposure of amphibians to pathogens during field studies. Diseases of Aquatic Organisms 25:175–185
Ruiz A, Rueda-Almonacid JV (2008) Batrachochytrium dendrobatidis and chytridiomycosis in anuran amphibians of Colombia. EcoHealth 5(1):27–33
Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A, Beukema W, Acevedo AA, Burrowes PA, Carvalho T, Catenazzi A, De la Riva I (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363(6434):1459–1463
Solís R, Lobos G, Walker SF, Fisher M, Bosch J (2010) Presence of Batrachochytrium dendrobatidis in feral populations of Xenopus laevis in Chile. Biological Invasions 12(6):1641–1646
Soto-Azat C, Clarke BT, Poynton JC, Cunningham AA (2010) Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Diversity and Distributions 16(1):126–131
Stockwell MP, Clulow S, Clulow J, Mahony M (2008) The impact of chytrid fungus Batrachochytrium dendrobatidis on a Green and Golden Bell Frog Litoria aurea reintroduction program at the Hunter Wetlands Centre Australia in the Hunter Region of NSW. Zoologist 34(3):379–386
Van Rooij P, Martel A, Haesbrouck F, Pasmans F (2015) Amphibian chytridiomycosis: a review with focus on fungus-host interactions. Veterinary Research 46(1):137
Venesky MD, Wassersug RJ, Parris MJ (2010) Fungal pathogen changes the feeding kinematics of larval anurans. The Journal of Parasitology 96(3):552–557
Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proceedings of the Royal Society London B Biological Sciences 105:11466–11473
Weldon C, du Preez LH, Hyatt AD, Muller R, Spears R (2004) Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10(12):2100–2105
www.bd-maps.net. Accessed December 2019
Young BE, Lips KR, Reaser JK, Ibáñez R, Salas AW, Cedeño JR, Coloma LA, Ron S, La Marca E, Meyer JR, Muñoz A (2001) Population declines and priorities for amphibian conservation in Latin America. Conservation Biology 15(5):1213–1223
Acknowledgements
We would like to thank Paul Ouboter, from the National Zoological Collection of Suriname for support and advice during the time spent in Suriname. Kirsten Curran, Dallas Davidson, Christian H. d’Orgeix, Sabria Greiner, De’Jah Hardy, Raissa Kemajou, Cameron Lockett, Alyssia Velez, Ahnaia White, and Sarah Melissa Witiak participated in surveying frogs. The Trio indigenous people granted us permission to work in the Sipaliwini savanna and provided lodging, transportation and guides to the forest island sites. We thank the anonymous reviewers from this journal, and William R. Jones whose comments have improved this manuscript. All applicable institutional and/or national guidelines for the care and use of animals were followed. Permits for the fieldwork were granted by the Nature Conservation Department of Suriname. This work was supported in part by the HBCU-UP of the National Science Foundation under NSF Cooperative Agreement No. HRD-1036286 to C.A. d’Orgeix. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect those of the National Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jairam, R., Harris, A. & d’Orgeix, C.A. The Last South American Redoubt? Tested Surinamese Anurans Still Chytrid Free. EcoHealth 18, 465–474 (2021). https://doi.org/10.1007/s10393-021-01566-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-021-01566-4