Shifts in temperature influence how Batrachochytrium dendrobatidis infects amphibian larvae

English version

Autoři: Paul W. Bradley ^aff001; Michael D. Brawner ^aff002; Thomas R. Raffel ^aff003; Jason R. Rohr ^aff004; Deanna H. Olson ^aff005; Andrew R. Blaustein ^aff002
Působiště autorů: Environmental Sciences Graduate Program, Oregon State University, Corvallis, Oregon, United States of America ^aff001; Department of Integrative Biology, Oregon State University, Corvallis, OR, United States of America ^aff002; Department of Biology, Oakland University, Rochester, MI, United States of America ^aff003; Department of Integrative Biology, University of South Florida, Tampa, FL, United States of America ^aff004; USDA Forest Service, Pacific Northwest Research Station, Corvallis, OR, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0222237

Souhrn

Many climate change models predict increases in frequency and magnitude of temperature fluctuations that might impact how ectotherms are affected by disease. Shifts in temperature might especially affect amphibians, a group with populations that have been challenged by several pathogens. Because amphibian hosts invest more in immunity at warmer than cooler temperatures and parasites might acclimate to temperature shifts faster than hosts (creating lags in optimal host immunity), researchers have hypothesized that a temperature shift from cold-to-warm might result in increased amphibian sensitivity to pathogens, whereas a shift from warm-to-cold might result in decreased sensitivity. Support for components of this climate-variability based hypothesis have been provided by prior studies of the fungus Batrachochytrium dendrobatidis (Bd) that causes the disease chytridiomycosis in amphibians. We experimentally tested whether temperature shifts before exposure to Batrachochytrium dendrobatidis (Bd) alters susceptibility to the disease chytridiomycosis in the larval stage of two amphibian species–western toads (Anaxyrus boreas) and northern red legged frogs (Rana aurora). Both host species harbored elevated Bd infection intensities under constant cold (15° C) temperature in comparison to constant warm (20° C) temperature. Additionally, both species experienced an increase in Bd infection abundance after shifted from 15° C to 20° C, compared to a constant 20° C but they experienced a decrease in Bd after shifted from 20° C to 15° C, compared to a constant 15° C. These results are in contrast to prior studies of adult amphibians highlighting the potential for species and stage differences in the temperature-dependence of chytridiomycosis.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Mycology – Animals – Developmental biology – Medicine and health sciences – Microbiology – Medical microbiology – Microbial pathogens – Pathology and laboratory medicine – Pathogens – Vertebrates – Fungal pathogens – Earth sciences – Amphibians – Frogs – Atmospheric science – Life cycles – Larvae – Pathogenesis – Euthanasia – Climatology – Climate change – Toads – Host-pathogen interactions

Zdroje

1. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB. Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci U S A. 2010 August 24, 2010;107(34):15135–9. doi: 10.1073/pnas.1006422107 20696913

2. Paaijmans KP, Read AF, Thomas MB. Understanding the link between malaria risk and climate. Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13844–9. doi: 10.1073/pnas.0903423106 19666598. Pubmed Central PMCID: 2720408.

3. Horton RM, Mankin JS, Lesk C, Coffel E, Raymond C. A Review of Recent Advances in Research on Extreme Heat Events. Current Climate Change Reports. 2016;2(4):242–59.

4. Schar C, Vidale PL, Luthi D, Frei C, Haberli C, Liniger MA, et al. The role of increasing temperature variability in European summer heatwaves. Nature. 2004;427(6972):332–6. doi: 10.1038/nature02300 14716318

5. Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO. Climate extremes: observations, modeling, and impacts. Science. 2000 September 22, 2000;289(5487):2068–74. doi: 10.1126/science.289.5487.2068 11000103

6. Rummukainen M. Changes in climate and weather extremes in the 21st century. Wiley Interdiscip Rev: Clim Change. 2012;3(2):115–29.

7. Teskey R, Wertin T, Bauweraerts I, Ameye M, McGuire MA, Steppe K. Responses of tree species to heat waves and extreme heat events. Plant Cell Environ. 2015 Sep;38(9):1699–712. doi: 10.1111/pce.12417 25065257.

8. Hoover DL, Knapp AK, Smith MD. Resistance and resilience of a grassland ecosystem to climate extremes. Ecology. 2014;95(9):2646–56.

9. Anderegg WRL, Kane JM, Anderegg LDL. Consequences of widespread tree mortality triggered by drought and temperature stress. Nature Clim Change. 2013 01//print;3(1):30–6.

10. Ben-Horin T, Lenihan HS, Lafferty KD. Variable intertidal temperature explains why disease endangers black abalone. Ecology. 2012 2013/01/01;94(1):161–8.

11. Bannerman JA, Roitberg BD. Impact of extreme and fluctuating temperatures on aphid-parasitoid dynamics. Oikos. 2014;123(1):89–98.

12. Raffel TR, Halstead NT, McMahon TA, Davis AK, Rohr JR. Temperature variability and moisture synergistically interact to exacerbate an epizootic disease. Proceedings of the Royal Society B: Biological Sciences. 2015;282(1801):20142039. doi: 10.1098/rspb.2014.2039 25567647

13. Lawler JJ, Shafer SL, Bancroft BA, Blaustein AR. Projected climate impacts for the amphibians of the Western hemisphere. Conserv Biol. 2010 Feb;24(1):38–50. doi: 10.1111/j.1523-1739.2009.01403.x 20121840.

14. Blaustein AR, Walls SC, Bancroft BA, Lawler JJ, Searle CL, Gervasi SS. Direct and indirect effects of climate change on amphibian populations. Diversity. 2010;2(2):281–313. doi: 10.3390/d2020281

15. Li Y, Cohen JM, Rohr JR. Review and synthesis of the effects of climate change on amphibians. Integr Zool. 2013 Jun;8(2):145–61. doi: 10.1111/1749-4877.12001 23731811.

16. Shoo LP, Olson DH, McMenamin SK, Murray KA, Van Sluys M, Donnelly MA, et al. Engineering a future for amphibians under climate change. J Appl Ecol. 2011;48(2):487–92.

17. McCallum ML. Amphibian decline or extinction? Current declines dwarf background extinction rate. J Herpetol. 2007 September 01, 2007;41(3):483–91.

18. Wake DB. Facing extinction in real time. Science. 2012 March 2, 2012;335(6072):1052–3. doi: 10.1126/science.1218364 22383836

19. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. Status and trends of amphibian declines and extinctions worldwide. Science. 2004 December 3, 2004;306(5702):1783–6. doi: 10.1126/science.1103538 15486254

20. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ. Evaluating the links between climate, disease spread, and amphibian declines. Proc Natl Acad Sci U S A. 2008;105(45):17436. doi: 10.1073/pnas.0806368105 18987318

21. Longcore J, Pessier A, Nichols D. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia. 1999;91(2):219–27.

22. 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. PLoS ONE. 2013;8(2):e56802. doi: 10.1371/journal.pone.0056802 23463502

23. Liu X, Rohr JR, Li Y. Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society B: Biological Sciences. 2013 February 22, 2013;280(1753):20122506. doi: 10.1098/rspb.2012.2506 23256195

24. Skerratt L, Berger L, Speare R, Cashins S, McDonald K, Phillott A, et al. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth. 2007;4(2):125–34.

25. Xie GY, Olson DH, Blaustein AR. Projecting the global distribution of the emerging amphibian fungal pathogen, Batrachochytrium dendrobatidis, based on IPCC climate futures. PLoS ONE. 2016;11(8):e0160746. doi: 10.1371/journal.pone.0160746 27513565. Pubmed Central PMCID: 4981458.

26. Gervasi S, Gondhalekar C, Olson DH, Blaustein AR. Host identity matters in the amphibian-Batrachochytrium dendrobatidis system: Fine-scale patterns of variation in responses to a multi-host pathogen. PLoS ONE. 2013;8(1):e54490. doi: 10.1371/journal.pone.0054490 23382904. Pubmed Central PMCID: 3554766.

27. Blaustein AR, Romansic JM, Scheessele EA, A. Han B, Pessier AP, Longcore JE. Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv Biol. 2005;19(5):1460–8.

28. Garner TWJ, Walker S, Bosch J, Leech S, Rowcliffe JM, Cunningham AA, et al. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos. 2009 May;118(5):783–91. WOS:000265711500016. English.

29. Gervasi SS, Stephens PR, Hua J, Searle CL, Xie GY, Urbina J, et al. Linking ecology and epidemiology to understand predictors of multi-host responses to an emerging pathogen, the amphibian chytrid fungus. PLoS ONE. 2017;12(1):e0167882. doi: 10.1371/journal.pone.0167882 28095428

30. Marantelli G, Berger L, Speare R, Keegan L. Distribution of the amphibian chytrid Batrachochytrium dendrobatidis and keratin during tadpole development. Pac Conserv Biol. 2004;10(3):173–9.

31. McMahon TA, Rohr JR. Transition of chytrid fungus infection from mouthparts to hind limbs during amphibian metamorphosis. EcoHealth. 2015 Mar;12(1):188–93. 25384612. doi: 10.1007/s10393-014-0989-9 25384612

32. Han BA, Bradley PW, Blaustein AR. Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, Batrachochytrium dendrobatidis. Behav Ecol Sociobiol. 2008;63(2):241–50.

33. Buck JC, Scheessele EA, Relyea RA, Blaustein AR. The effects of multiple stressors on wetland communities: pesticides, pathogens and competing amphibians. Freshwat Biol. 2012 Jan;57(1):61–73. WOS:000297468100006. English.

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

35. Rohr JR, Raffel TR. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proc Natl Acad Sci U S A. 2010 May 4;107(18):8269–74. doi: 10.1073/pnas.0912883107 20404180. Pubmed Central PMCID: 2889522.

36. Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR. Disease and thermal acclimation in a more variable and unpredictable climate. Nat Clim Change. 2013;3(2):146–51.

37. Woodhams DC, Alford RA, Briggs CJ, Johnson M, Rollins-Smith LA. Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen. Ecology. 2008;89(6):1627–39. doi: 10.1890/06-1842.1 18589527

38. 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 Apr 19:1–11. doi: 10.1007/s00442-017-3866-8 28424893.

39. McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM, Deutsch K, et al. Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature. 2014 Jul 10;511(7508):224–7. doi: 10.1038/nature13491 25008531.

40. Voyles J, Johnson LR, Briggs CJ, Cashins SD, Alford RA, Berger L, et al. Temperature alters reproductive life history patterns in Batrachochytrium dendrobatidis, a lethal pathogen associated with the global loss of amphibians. Ecology and Evolution. 2012;2(9):2241–9. doi: 10.1002/ece3.334 23139882

41. 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. Dis Aquat Org. 2007 January 18, 2007;73(3):175–92.

42. Rohr JR, Raffel TR, Blaustein AR, Johnson PTJ, Paull SH, Young S. Using physiology to understand climate-driven changes in disease and their implications for conservation. Conserv Physiol. 2013 January 1, 2013;1(1):cot022. doi: 10.1093/conphys/cot022 27293606

43. Blaustein AR, Gervasi SS, Johnson PTJ, Hoverman JT, Belden LK, Bradley PW, et al. Ecophysiology meets conservation: understanding the role of disease in amphibian population declines. Philos Trans R Soc, B. 2012 June 19, 2012;367(1596):1688–707.

44. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. Toward a metabolic theory of ecology. Ecology. 2004 2012/03/19;85(7):1771–89.

45. Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ. Negative effects of changing temperature on amphibian immunity under field conditions. Funct Ecol. 2006;20(5):819–28.

46. Pearl CA, Bull EL, Green DE, Bowerman J, Adams MJ, Hyatt A, et al. Occurrence of the amphibian pathogen Batrachochytrium dendrobatidis in the Pacific Northwest. J Herpetol. 2007 March 01, 2007;41(1):145–9.

47. Muths E, Pilliod DS, Livo LJ. Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA. Biol Conserv. 2008;141(6):1484–92.

48. Piovia-Scott J, Pope KL, Lawler SP, Cole EM, Foley JE. Factors related to the distribution and prevalence of the fungal pathogen Batrachochytrium dendrobatidis in Rana cascadae and other amphibians in the Klamath Mountains. Biol Conserv. 2011;144(12):2913–21.

49. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org. 2004 August 09, 2004;60(2):141–8. doi: 10.3354/dao060141 15460858

50. Utltsch GR, Bradford DF, Freda J. Physiology: coping with the environment. In: Altig R, McDiarmid RW, editors. Tadpoles: the biology of anuran larvae. Chicago; London: The University of Chicago Press; 1999. p. 189–214.

51. Beiswenger RE. Responses of Bufo tadpoles (Amphibia, Anura, Bufonidae) to laboratory gradients of temperature. J Herpetol. 1978:499–504.

52. Karlstrom EL. The toad genus Bufo in the Sierra Nevada of California: ecological and systematic relationships: Berkeley: University of California Press.; 1962.

53. Bancroft BA, Baker NJ, Searle CL, Garcia TS, Blaustein AR. Larval amphibians seek warm temperatures and do not avoid harmful UVB radiation. Behav Ecol. 2008 July 1, 2008;19(4):879–86.

54. Raffel TR, Michel PJ, Sites EW, Rohr JR. What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. EcoHealth. 2010 Dec;7(4):526–36. doi: 10.1007/s10393-010-0358-2 21125308.

55. IPCC. Climate Change 2007: Synthesis Report. Geneva: IPCC, 2007.

56. Searle CL, Gervasi SS, Hua J, Hammond JI, Relyea RA, Olson DH, et al. Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conserv Biol. 2011;25(5):965–74. doi: 10.1111/j.1523-1739.2011.01708.x 21732979

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

58. Rachowicz LJ, Vredenburg VT. Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis Aquat Org. 2004 October 21, 2004;61(1–2):75–83.

59. Berger L, Speare R, Hines HB, Marantelli G, Hyatt AD, McDonald KR, et al. Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Aust Vet J. 2004;82(7):434–9. doi: 10.1111/j.1751-0813.2004.tb11137.x 15354853

60. Kilpatrick AM, Briggs CJ, Daszak P. The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol. 2010;25(2):109–18. doi: 10.1016/j.tree.2009.07.011 19836101

61. Venesky MD, Raffel TR, McMahon TA, Rohr JR. Confronting inconsistencies in the amphibian-chytridiomycosis system: implications for disease management. Biol Rev Camb Philos Soc. 2013 Oct 4;89(2):477–83. doi: 10.1111/brv.12064 24118903.

62. Cohen JM, Venesky MD, Sauer EL, Civitello DJ, McMahon TA, Roznik EA, et al. The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecol Lett. 2017 Feb;20(2):184–93. doi: 10.1111/ele.12720 28111904.

Shifts in temperature influence how Batrachochytrium dendrobatidis infects amphibian larvae

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz