Widespread chytrid infection across frogs in the Peruvian Amazon suggests critical role for low elevation in pathogen spread and persistence


Autoři: Imani D. Russell aff001;  Joanna G. Larson aff001;  Rudolf von May aff001;  Iris A. Holmes aff001;  Timothy Y. James aff001;  Alison R. Davis Rabosky aff001
Působiště autorů: Department of Ecology and Evolutionary Biology and Museum of Zoology (UMMZ), University of Michigan, Ann Arbor, Michigan, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222718

Souhrn

Outbreaks of emerging infectious diseases are becoming more frequent as climate changes wildlife communities at unprecedented rates, driving population declines and raising concerns for species conservation. One critical disease is the global pandemic of chytridiomycosis in frogs, which can be caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Although there is clear evidence for Bd-induced mortality across high-elevation frog communities, little attention is given to the role of lowlands in Bd’s persistence and spread because low elevations are assumed to be too warm to harbor significant levels of Bd. Here, we report widespread Bd infection across 80 frog species from three sites in the lowland Peruvian Amazon, an area with no documented Bd-related amphibian declines. Despite observing no clinical signs of infection in the field, we found that 24–46% of individuals were infected per site (up to ≈105,000 zoospore equivalents per frog) by three Bd strains from the global pandemic lineage (Bd-GPL). We also found collection site and seasonal effects to be only weak predictors of Bd prevalence and load, with lower elevation and drier habitats marginally decreasing both prevalence and load. We found no further effect of host phylogeny, ecotype, or body size. Our results showing high and widespread prevalence across a lowland tropical ecosystem contradict the expectations based on the global pattern of pathogenicity of Bd that is largely restricted to higher elevations and colder temperatures. These findings imply that the lowlands may play a critical role in the spread and persistence of Bd over time and space.

Klíčová slova:

Amphibians – Body temperature – Frogs – Fungal pathogens – Phylogenetics – Polymerase chain reaction – Disease dynamics – Comparative sequence analysis


Zdroje

1. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, et al. Emerging fungal threats to animal, plant and ecosystem health. Nature. 2012;484:186. doi: 10.1038/nature10947 22498624

2. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, et al. Climate warming and disease risks for terrestrial and marine biota. Science. 2002;296(5576):2158–62. doi: 10.1126/science.1063699 12077394

3. Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, et al. An emerging disease causes regional population collapse of a common North American bat species. Science. 2010;329(5992):679–82. doi: 10.1126/science.1188594 20689016

4. 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.

5. Longcore JE, Pessier AP, Nichols DK. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia. 1999:219–27.

6. 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. P Natl Acad Sci USA. 1998;95(15):9031–6.

7. Rachowicz LJ, Knapp RA, Morgan JA, Stice MJ, Vredenburg VT, Parker JM, et al. Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology. 2006;87(7):1671–83. doi: 10.1890/0012-9658(2006)87[1671:eidaap]2.0.co;2 16922318

8. 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

9. Scheele BC, Hunter DA, Brannelly LA, Skerratt LF, Driscoll DA. Reservoir‐host amplification of disease impact in an endangered amphibian. Conserv Biol. 2017;31(3):592–600. doi: 10.1111/cobi.12830 27594575

10. Brannelly L, Webb R, Hunter D, Clemann N, Howard K, Skerratt L, et al. Non‐declining amphibians can be important reservoir hosts for amphibian chytrid fungus. Anim Conserv. 2018;21(2):91–101.

11. Bosch J, Martínez-Solano I, García-París M. Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biol Conserv. 2001;97(3):331–7.

12. Savage AE, Zamudio KR. MHC genotypes associate with resistance to a frog-killing fungus. P Natl Acad Sci USA. 2011;108(40):16705–10.

13. Grogan LF, Robert J, Berger L, Skerratt LF, Scheele BC, Castley JG, et al. Review of the amphibian immune response to chytridiomycosis, and future directions. Front Immunol. 2018;9:2536. doi: 10.3389/fimmu.2018.02536 30473694

14. Woodhams D, Ardipradja K, Alford R, Marantelli G, Reinert L, Rollins‐Smith L. Resistance to chytridiomycosis varies among amphibian species and is correlated with skin peptide defenses. Anim Conserv. 2007;10(4):409–17.

15. Kriger KM, Hero JM. The chytrid fungus Batrachochytrium dendrobatidis is non‐randomly distributed across amphibian breeding habitats. Divers Distrib. 2007;13(6):781–8.

16. Piotrowski JS, Annis SL, Longcore JE. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia. 2004;96(1):9–15. 21148822

17. Voyles J, Johnson LR, Rohr J, Kelly R, Barron C, Miller D, et al. Diversity in growth patterns among strains of the lethal fungal pathogen Batrachochytrium dendrobatidis across extended thermal optima. Oecologia. 2017;184(2):363–73. Epub 2017/04/21. doi: 10.1007/s00442-017-3866-8 28424893; PubMed Central PMCID: PMC5487841.

18. O’hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science. 2018;360(6389):621–7. doi: 10.1126/science.aar1965 29748278

19. Becker C, Greenspan S, Tracy K, Dash J, Lambertini C, Jenkinson T, et al. Variation in phenotype and virulence among enzootic and panzootic amphibian chytrid lineages. Fungal Ecology. 2017;26:45–50.

20. Ron SR. Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica. 2005;37(2):209–21.

21. Stevenson LA, Alford RA, Bell SC, Roznik EA, Berger L, Pike DA. Variation in thermal performance of a widespread pathogen, the amphibian chytrid fungus Batrachochytrium dendrobatidis. PLoS One. 2013;8(9):e73830. doi: 10.1371/journal.pone.0073830 24023908

22. James TY, Toledo LF, Rödder D, Silva Leite D, Belasen AM, Betancourt‐Román CM, et al. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecol Evol. 2015;5(18):4079–97. doi: 10.1002/ece3.1672 26445660

23. Kosch TA, Morales V, Summers K. Batrachochytrium dendrobatidis in Peru. Herpetol Rev. 2012;43(2):288.

24. von May R, Catenazzi A, Santa-Cruz R, Kosch TA, Vredenburg VT. Microhabitat Temperatures and Prevalence of the Pathogenic Fungus Batrachochytrium dendrobatidis in Lowland Amazonian Frogs. Trop Conserv Sci. 2018;11:1940082918797057.

25. Rödder D, Kielgast J, Bielby J, Schmidtlein S, Bosch J, Garner TW, et al. Global amphibian extinction risk assessment for the panzootic chytrid fungus. Diversity. 2009;1(1):52–66.

26. Kriger KM, Hines HB, Hyatt AD, Boyle DG, Hero J-M. Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Dis Aquat Organ. 2006;71(2):141–8. doi: 10.3354/dao071141 16956061

27. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ. Dynamics of an emerging disease drive large-scale amphibian population extinctions. P Natl Acad Sci USA. 2010;107(21):9689–94.

28. Whitfield SM, Kerby J, Gentry LR, Donnelly MA. Temporal variation in infection prevalence by the amphibian chytrid fungus in three species of frogs at La Selva, Costa Rica. Biotropica. 2012;44(6):779–84.

29. Rebollar EA, Hughey MC, Harris RN, Domangue RJ, Medina D, Ibáñez R, et al. The lethal fungus Batrachochytrium dendrobatidis is present in lowland tropical forests of far eastern Panamá. PLoS One. 2014;9(4):e95484. doi: 10.1371/journal.pone.0095484 24740162

30. Kilburn VL, Ibáñez R, Sanjur O, Bermingham E, Suraci JP, Green DM. Ubiquity of the pathogenic chytrid fungus, Batrachochytrium dendrobatidis, in anuran communities in Panamá. EcoHealth. 2010;7(4):537–48. doi: 10.1007/s10393-010-0634-1 21225313

31. DiRenzo GV, Campbell Grant EH, Longo AV, Che‐Castaldo C, Zamudio KR, Lips KR. Imperfect pathogen detection from non‐invasive skin swabs biases disease inference. Methods Ecol Evol. 2018;9(2):380–9.

32. Seimon TA, Seimon A, Daszak P, Halloy SR, Schloegel LM, Aguilar CA, et al. Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Global Change Biology. 2007;13(1):288–99.

33. Fisher MC, Garner TW, Walker SF. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual review of microbiology. 2009;63:291–310. doi: 10.1146/annurev.micro.091208.073435 19575560

34. Zumbado‐Ulate H, García‐Rodríguez A, Vredenburg VT, Searle C. Infection with Batrachochytrium dendrobatidis is common in tropical lowland habitats: Implications for amphibian conservation. Ecol Evol. 2019.

35. Venesky MD, Mendelson JR III, Sears BF, Stiling P, Rohr JR. Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conserv Biol. 2012;26(4):586–92. doi: 10.1111/j.1523-1739.2012.01854.x 22809350

36. Daszak P, Strieby A, Cunningham AA, Longcore J, Brown C, Porter D. Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetol J. 2004;14:201–8.

37. Yap TA, Koo MS, Ambrose RF, Wake DB, Vredenburg VT. Averting a North American biodiversity crisis. Science. 2015;349(6247):481–2. doi: 10.1126/science.aab1052 26228132

38. Morgan JA, Vredenburg VT, Rachowicz LJ, Knapp RA, Stice MJ, Tunstall T, et al. Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis. P Natl Acad Sci USA. 2007;104(34):13845–50.

39. James TY, Litvintseva AP, Vilgalys R, Morgan JA, Taylor JW, Fisher MC, et al. Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathog. 2009;5(5):e1000458. doi: 10.1371/journal.ppat.1000458 19478871

40. 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;21(21):5162–77. doi: 10.1111/j.1365-294X.2012.05710.x 22857789

41. Jenkinson T, Román B, Lambertini C, Valencia‐Aguilar A, Rodriguez D, Nunes‐de‐Almeida C, et al. Amphibian‐killing chytrid in Brazil comprises both locally endemic and globally expanding populations. Mol Ecol. 2016;25(13):2978–96. doi: 10.1111/mec.13599 26939017

42. Morehouse EA, James TY, Ganley AR, Vilgalys R, Berger L, Murphy PJ, et al. Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Mol Ecol. 2003;12(2):395–403. doi: 10.1046/j.1365-294x.2003.01732.x 12535090

43. Palumbi S. Simple fool's guide to PCR. 1991.

44. Jetz W, Pyron RA. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol. 2018;2(5):850. doi: 10.1038/s41559-018-0515-5 29581588

45. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol. 2012;3(2):217–23.

46. Tung Ho Ls, Ané C. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst Biol. 2014;63(3):397–408. doi: 10.1093/sysbio/syu005 24500037


Článek vyšel v časopise

PLOS One


2019 Číslo 10