Batrachochytrium dendrobatidis infection in amphibians predates first known epizootic in Costa Rica


Autoři: Marina E. De León aff001;  Héctor Zumbado-Ulate aff002;  Adrián García-Rodríguez aff003;  Gilbert Alvarado aff003;  Hasan Sulaeman aff006;  Federico Bolaños aff003;  Vance T. Vredenburg aff006
Působiště autorů: Department of Microbiology and Molecular genetics, University of California, Davis, United States of America aff001;  Department of Biological Sciences, Purdue University, West Lafayette, IN, United States of America aff002;  Escuela de Biología, Universidad de Costa Rica, San Pedro, Costa Rica aff003;  Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico aff004;  Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, Brazil aff005;  Department of Biology, San Francisco State University, San Francisco, California, United States of America aff006;  Museum of Vertebrate Zoology, University of California Berkeley, Berkeley, California, United States of America aff007
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0208969

Souhrn

Emerging infectious diseases are a growing threat to biodiversity worldwide. Outbreaks of the infectious disease chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), are implicated in the decline and extinction of numerous amphibian species. In Costa Rica, a major decline event occurred in 1987, more than two decades before this pathogen was discovered. The loss of many species in Costa Rica is assumed to be due to Bd-epizootics, but there are few studies that provide data from amphibians in the time leading up to the proposed epizootics. In this study, we provide new data on Bd infection rates of amphibians collected throughout Costa Rica, in the decades prior to the epizootics. We used a quantitative PCR assay to test for Bd presence in 1016 anuran museum specimens collected throughout Costa Rica. The earliest specimen that tested positive for Bd was collected in 1964. Across all time periods, we found an overall infection rate (defined as the proportion of Bd-positive individuals) of 4%. The number of infected individuals remained relatively low across all species tested and the range of Bd-positive specimens was shown to be geographically constrained up until the 1980s; when epizootics are hypothesized to have occurred. After that time, infection rate increased three-fold, and the range of specimens tested positive for Bd increased, with Bd-positive specimens collected across the entire country. Our results suggest that Bd dynamics in Costa Rica are more complicated than previously thought. The discovery of Bd’s presence in the country preceding massive declines leads to a number of different hypotheses: 1) Bd invaded Costa Rica earlier than previously known, and spread more slowly than previously reported; 2) Bd invaded multiple times and faded out; 3) an endemic Bd lineage existed; 4) an earlier Bd lineage evolved into the current Bd lineage or hybridized with an invasive lineage; or 5) an earlier Bd lineage went extinct and a new invasion event occurred causing epizootics. To help visualize areas where future studies should take place, we provide a Bd habitat suitability model trained with local data. Studies that provide information on genetic lineages of Bd are needed to determine the most plausible spatial-temporal, host-pathogen dynamics that could best explain the epizootics resulting in amphibian declines in Costa Rica and throughout Central America.

Klíčová slova:

Amphibians – Costa Rica – Epizootics – Frogs – Fungal pathogens – Museum collections – Pathogens


Zdroje

1. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. Status and trends of amphibian declines and extinctions worldwide. Science (80-). 2004;306(5702):1783–6.

2. Wake DB, Vredenburg VT. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci. 2008;105(Supplement 1):11466–73.

3. Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, et al. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth. 2007;4(2):125–34.

4. Longcore JE, Pessier AP, Nichols DK. Batrachochytrium Dendrobatidis gen. et sp. nov., a Chytrid Pathogenic to Amphibians. Mycologia. 1999 Mar;91(2):219.

5. Berger L, Roberts AA, Voyles J, Longcore JE, Murray KA, Skerratt LF. History and recent progress on chytridiomycosis in amphibians. Fungal Ecol. 2016;19:89–99.

6. Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F, Clare F, et al. Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Natl Acad Sci. 2011;108(46):18732–6. doi: 10.1073/pnas.1111915108 22065772

7. Becker CG, Greenspan SE, Tracy KE, Dash JA, Lambertini C, Jenkinson TS, et al. Variation in phenotype and virulence among enzootic and panzootic amphibian chytrid lineages. Fungal Ecol. 2017 Apr 1;26:45–50.

8. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, et al. Pathogenesis of Chytridiomycosis, a Cause of Catastrophic Amphibian Declines. Science (80-). 2009 Oct 22;326(5952):582 LP– 585.

9. Voyles J, Vredenburg VT, Tunstall TS, Parker JM, Briggs CJ, Rosenblum EB. Pathophysiology in mountain yellow-legged frogs (Rana muscosa) during a chytridiomycosis outbreak. PLoS One. 2012;7(4).

10. Fong JJ, Cheng TL, Bataille A, Pessier AP, Waldman B, Vredenburg VT. Early 1900s detection of Batrachochytrium dendrobatidis in Korean amphibians. PLoS One. 2015;10(3).

11. Rodriguez D, Becker CG, Pupin NC, Haddad CFB, Zamudio KR. Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic Forest of Brazil. Mol Ecol. 2014;23(4):774–87. doi: 10.1111/mec.12615 24471406

12. Tarrant J, Cilliers D, du Preez LH, Weldon C. Spatial Assessment of Amphibian Chytrid Fungus (Batrachochytrium dendrobatidis) in South Africa Confirms Endemic and Widespread Infection. PLoS One. 2013;8(7).

13. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc Natl Acad Sci. 2010;107(21):9689–94. doi: 10.1073/pnas.0914111107 20457913

14. Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, et al. Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Mol Ecol. 2012 Nov;21(21):5162–77. doi: 10.1111/j.1365-294X.2012.05710.x 22857789

15. O’Hanlon SJ, Rieux A, Farrer RA, Rosa GM. Recent Asian origin of chytrid fungi causing global amphibian declines. Science (80-). 2018;360(6389):621–7.

16. Cheng TL, Rovito SM, Wake DB, Vredenburg VT. Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc Natl Acad Sci. 2011;108(23):9502–7. doi: 10.1073/pnas.1105538108 21543713

17. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, et al. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci. 1998;95(15):9031–6. doi: 10.1073/pnas.95.15.9031 9671799

18. Rachowicz LJ, Hero JM, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, et al. The novel and endemic pathogen hypotheses: Competing explanations for the origin of emerging infectious diseases of wildlife. Vol. 19, Conservation Biology. 2005. p. 1441–8.

19. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Vol. 439, Nature. 2006. p. 161–7. doi: 10.1038/nature04246 16407945

20. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, et al. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci. 2006;103(9):3165–70. doi: 10.1073/pnas.0506889103 16481617

21. Lips KR. Decline of a Tropical Montane Amphibian Fauna. Vol. 12, Conservation Biology. 1998.

22. Lips KR, Green DE, Papendick R. Chytridiomycosis in Wild Frogs from Southern Costa Rica. J Herpetol. 2003;37(1):215–8.

23. Puschendorf R, Bolaños F, Chaves G. The amphibian chytrid fungus along an altitudinal transect before the first reported declines in Costa Rica. Biol Conserv. 2006;132(1):136–42.

24. Pounds JA, Crump ML. Amphibian Declines and Climate Disturbance: The Case of the Golden Toad and the Harlequin Frog. Soc Conserv Biol. 1994;8(1):72–85.

25. Whitfield SM, Alvarado G, Abarca J, Zumbado H, Zuñiga I, Wainwright M, et al. Differential patterns of Batrachochytrium dendrobatidis infection in relict amphibian populations following severe disease-associated declines. Dis Aquat Organ. 2017;126(1):33–41. doi: 10.3354/dao03154 28930083

26. Campbell JA, Savage JM. Taxonomic Reconsideration of Middle American Frogs of the Eleutherodactylus rugulosus Group (Anura: Leptodactylidae): A Reconnaissance of Subtle Nuances among Frogs. Herpetol Monogr. 2000;14:186.

27. Hedges SB, Hedges SB, Duellman WE, Duellman WE, Heinicke MP, Heinicke MP. Zootaxa 1737. Vol. 1737, Zootaxa. 2008. 1–182 p.

28. Savage JM. The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago Press; 2002. 934 p.

29. Jiménez R, Alvarado G. Craugastor escoces (Anura: Craugastoridae) reappears after 30 years: Rediscovery of an “extinct” Neotropical frog. Amphib Reptil. 2017;38(2):257–9.

30. Chaves G, Zumbado-Ulate H, García-Rodríguez A, Gómez E, Vredenburg VT, Ryan MJ. Rediscovery of the Critically Endangered Streamside Frog, Craugastor Taurus (Craugastoridae), in Costa Rica. Trop Conserv Sci. 2014;7(4):628–38.

31. Nishida K. Encounter with Hyla angustilineata Taylor, 1952 (Anura: Hylidae) in a cloud forest of Costa Rica. Brenesia. 2006;66Douglas(May 2005):78–81.

32. Gonzalez-Maya JF, Escobedo-Galvan AH, Wyatt SA, Schipper J, Belant JL, Fischer A, et al. Renewing hope: The rediscovery of Atelopus varius in Costa Rica. Amphib Reptil. 2013 Jan 1;34(4):573–8.

33. Mutnale MC, Anand S, Eluvathingal LM, Roy JK, Reddy GS, Vasudevan K. Enzootic frog pathogen Batrachochytrium dendrobatidis in Asian tropics reveals high ITS haplotype diversity and low prevalence. Sci Rep. 2018;8(1).

34. DeLeón ME, Vredenburg VT, Piovia-Scott J. Recent Emergence of a Chytrid Fungal Pathogen in California Cascades Frogs (Rana cascadae). Ecohealth. 2017;14(1):155–61. doi: 10.1007/s10393-016-1201-1 27957606

35. Talley BL, Muletz CR, Vredenburg VT, Fleischer RC, Lips KR. A century of Batrachochytrium dendrobatidis in Illinois amphibians (1888–1989). Biol Conserv. 2015;182:254–61.

36. Chaukulkar S, Sulaeman H, Zink AG, Vredenburg VT. Pathogen invasion and non-epizootic dynamics in Pacific newts in California over the last century. PLoS One. 2018;13(7).

37. Soto-Azat C, Clarke BT, Fisher MC, Walker SF, Cunningham AA. Non-invasive sampling methods for the detection of Batrachochytrium dendrobatidis in archived amphibians. Dis Aquat Organ. 2009;84(2):163–6. doi: 10.3354/dao02029 19476287

38. Ryan MJ, Bolanos F, Chaves G. Museums Help Prioritize Conservation Goals. Science (80-). 2010;1272:1273.

39. Garcia-Rodriguez A, Chaves G, Benavides-Varela C, Puschendorf R. Where are the survivors? Tracking relictual populations of endangered frogs in Costa Rica. Divers Distrib. 2012;18(2):204–12.

40. Young BE, Lips KR, Reaser JK, Ibáñez R, Salas AW, Cedeño JR, et al. Population Declines and Priorities for Amphibian Conservation in Latin America. Conserv Biol. 2001 Jul 7;15(5):1213–23.

41. IUCN 2018. The IUCN Red List of Threatened Species. Version 2018–2. http://www.iucnredlist.org. Downloaded on 09 October 2018. 2018.

42. AmphibiaWeb. 2018. University of California, Berkeley, CA, USA. Accessed 18 Oct 2018. [Internet]. 2018. Available from: https://amphibiandisease.org/

43. Boyle DG, Boyle DB, Olsen V, Morgan J a T, Hyatt AD. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Organ. 2004;60(2):141–8. doi: 10.3354/dao060141 15460858

44. Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendorf D, et al. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Vol. 73, Diseases of Aquatic Organisms. 2007. p. 175–92. doi: 10.3354/dao073175 17330737

45. Schloegel LM, Picco AM, Kilpatrick AM, Davies AJ, Hyatt AD, Daszak P. Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biol Conserv. 2009;142(7):1420–6.

46. Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, et al. Mapping the Global Emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus. Stajich JE, editor. PLoS One. 2013 Feb 27;8(2):e56802. doi: 10.1371/journal.pone.0056802 23463502

47. Phillips SJ, Dudík M, Schapire RE. A maximum entropy approach to species distribution modeling. In: Proceedings, Twenty-First Int Conf Mach Learn ICML 2004. 2004. p. 655–62.

48. Jenkinson TS, Betancourt Román CM, Lambertini C, Valencia-Aguilar A, Rodriguez D, Nunes-De-Almeida CHL, et al. Amphibian-killing chytrid in Brazil comprises both locally endemic and globally expanding populations. Mol Ecol. 2016 Jul;25(13):2978–96. doi: 10.1111/mec.13599 26939017

49. Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, et al. Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proc Natl Acad Sci. 2013;110(23):9385–90. doi: 10.1073/pnas.1300130110 23650365

50. Burrowes PA, De la Riva I. Detection of the Amphibian Chytrid Fungus Batrachochytrium dendrobatidis in Museum Specimens of Andean Aquatic Birds: Implications for Pathogen Dispersal. J Wildl Dis. 2017 Apr;53(2):349–55. doi: 10.7589/2016-04-074 28094607

51. Bataille A, Fong JJ, Cha M, Wogan GOU, Baek HJ, Lee H, et al. Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Mol Ecol. 2013;22(16):4196–209. doi: 10.1111/mec.12385 23802586

52. Parris MJ, Cornelius TO. Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology. 2004 Dec;85(12):3385–95.

53. Davidson C, Knapp RA. Multiple stressors and amphibian declines: Dual impacts of pesticides and fish on yellow-legged frogs. Ecol Appl. 2007 Mar;17(2):587–97. doi: 10.1890/06-0181 17489262

54. Bielby J, Fisher MC, Clare FC, Rosa GM, Garner TWJ. Host species vary in infection probability, sub-lethal effects, and costs of immune response when exposed to an amphibian parasite. Sci Rep. 2015;5.

55. Daszak P, Berger L, Cunningham AA, Hyatt AD, Earl Green D, Speare R. Emerging infectious diseases and amphibian population declines. Emerg Infect Dis. 1998;5(6):735–48.

56. Woodhams DC, Bosch J, Briggs CJ, Cashins S, Davis LR, Lauer A, et al. Mitigating amphibian disease: Strategies to maintain wild populations and control chytridiomycosis. Vol. 8, Frontiers in Zoology. 2011.

57. Voyles J, Rosenblum EB, Berger L. Interactions between Batrachochytrium dendrobatidis and its amphibian hosts: A review of pathogenesis and immunity. Vol. 13, Microbes and Infection. 2011. p. 25–32. doi: 10.1016/j.micinf.2010.09.015 20951224

58. Rollins-Smith LA. Amphibian immunity–stress, disease, and climate change. Dev Comp Immunol. 2017;66:111–9. doi: 10.1016/j.dci.2016.07.002 27387153

59. Ron SR. Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the new world. Biotropica. 2005 Jun;37(2):209–21.

60. Brem FMR, Lips KR. Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats and elevations during epizootic and enzootic stages. Dis Aquat Organ. 2008;81(3):189–202. doi: 10.3354/dao01960 18998584

61. Walls S, Barichivich W, Brown M. Drought, Deluge and Declines: The Impact of Precipitation Extremes on Amphibians in a Changing Climate. Biology (Basel). 2013;2(1):399–418.

62. Cayuela H, Arsovski D, Bonnaire E, Duguet R, Joly P, Besnard A. The impact of severe drought on survival, fecundity, and population persistence in an endangered amphibian. Ecosphere. 2016;7(2).

63. Scheele BC, Hunter DA, Banks SC, Pierson JC, Skerratt LF, Webb R, et al. High adult mortality in disease-challenged frog populations increases vulnerability to drought. J Anim Ecol. 2016;85(6):1453–60. doi: 10.1111/1365-2656.12569 27380945

64. Adams AJ, Kupferberg SJ, Wilber MQ, Pessier AP, Grefsrud M, Bobzie S, et al. Extreme drought, host density, sex, and bullfrogs influence fungal pathogen infection in a declining lotic amphibian. Ecosphere. 2017;8(3).

65. Catenazzi A, Lehr E, Rodriguez LO, Vredenburg VT. Batrachochytrium dendrobatidis and the collapse of anuran species richness and abundance in the Upper Manu National Park, southeastern Peru. Conserv Biol. 2011;25(2):382–91. doi: 10.1111/j.1523-1739.2010.01604.x 21054530

66. Langhammer PF, Burrowes PA, Lips KR, Bryant AB, Collins JP. Susceptibility to the amphibian chytrid fungus varies with ontogeny in the direct-developing frog, Eleutherodactylus coqui. J Wildl Dis. 2014;50(3):438–46. doi: 10.7589/2013-10-268 24807186

67. Lips K, Reeve J, Witters L. Ecological traits predicting amphibian population declines in Central America. Conserv Biol. 2003;17(4):1078–88.

68. La Marca E, Lips KR, Lötters S, Puschendorf R, Ibáñez R, Rueda-Almonacid JV, et al. Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Vol. 37, Biotropica. 2005. p. 190–201.

69. Ryan MJ, Lips KR, Eichholz MW. Decline and extirpation of an endangered Panamanian stream frog population (Craugastor punctariolus) due to an outbreak of chytridiomycosis. Biol Conserv. 2008;141(6):1636–47.

70. Puschendorf R, Carnaval AC, Vanderwal J, Zumbado-Ulate H, Chaves G, Bolaños F, et al. Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: Proposing climatic refuges as a conservation tool. Divers Distrib. 2009;15(3):401–8.

71. Yap TA, Koo MS, Ambrose RF, Vredenburg VT. Introduced bullfrog facilitates pathogen invasion in the western United States. Fisher MC, editor. PLoS One. 2018 Apr 16;13(4):e0188384. doi: 10.1371/journal.pone.0188384 29659568

72. Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A, Beukema W, et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science (80-). 2019 Mar 29;363(6434):1459–63.

73. Sette CM, Vredenburg VT, Zink AG. Reconstructing historical and contemporary disease dynamics: A case study using the California slender salamander. Biol Conserv. 2015;192:20–9.

74. Anderson RM, May RM. The Population Dynamics of Microparasites and Their Invertebrate Hosts. Philos Trans R Soc B Biol Sci. 1981;291(1054):451–524.

75. Swinton J, Woolhouse M, Begon M, Dobson A, Ferroglio E, Grenfell B, et al. “Microparasite transmission and persistence.” In: The ecology of wildlife diseases. 2002. p. 83–101.


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