A pesticide paradox: fungicides indirectly increase fungal infections.

Jason R Rohr, Jenise Brown, William A Battaglin, Taegan A McMahon, Rick A Relyea
Author Information
  1. Jason R Rohr: Department of Integrative Biology, University of South Florida, Tampa, Florida, 33620, USA.
  2. Jenise Brown: Department of Integrative Biology, University of South Florida, Tampa, Florida, 33620, USA.
  3. William A Battaglin: U.S. Geological Survey, Colorado Water Science Center, Lakewood, Colorado, 80225, USA.
  4. Taegan A McMahon: Department of Biology, University of Tampa, Tampa, Florida, 33606, USA.
  5. Rick A Relyea: Department of Biological Sciences, Darrin Fresh Water Institute, Rensselaer Polytechnic Institute, Troy, New York, 12180, USA.

Abstract

There are many examples where the use of chemicals have had profound unintended consequences, such as fertilizers reducing crop yields (paradox of enrichment) and insecticides increasing insect pests (by reducing natural biocontrol). Recently, the application of agrochemicals, such as agricultural disinfectants and fungicides, has been explored as an approach to curb the pathogenic fungus, Batrachochytrium dendrobatidis (Bd), which is associated with worldwide amphibian declines. However, the long-term, net effects of early-life exposure to these chemicals on amphibian disease risk have not been thoroughly investigated. Using a combination of laboratory experiments and analysis of data from the literature, we explored the effects of fungicide exposure on Bd infections in two frog species. Extremely low concentrations of the fungicides azoxystrobin, chlorothalonil, and mancozeb were directly toxic to Bd in culture. However, estimated environmental concentrations of the fungicides did not reduce Bd on Cuban tree frog (Osteopilus septentrionalis) tadpoles exposed simultaneously to any of these fungicides and Bd, and fungicide exposure actually increased Bd-induced mortality. Additionally, exposure to any of these fungicides as tadpoles resulted in higher Bd abundance and greater Bd-induced mortality when challenged with Bd post-metamorphosis, an average of 71 d after their last fungicide exposure. Analysis of data from the literature revealed that previous exposure to the fungicide itraconazole, which is commonly used to clear Bd infections, made the critically endangered booroolong frog (Litoria booroolongensis) more susceptible to Bd. Finally, a field survey revealed that Bd prevalence was positively associated with concentrations of fungicides in ponds. Although fungicides show promise for controlling Bd, these results suggest that, if fungicides do not completely eliminate Bd or if Bd recolonizes, exposure to fungicides has the potential to do more harm than good. To ensure that fungicide applications have the intended consequence of curbing amphibian declines, researchers must identify which fungicides do not compromise the pathogen resistance mechanisms of amphibians.

Keywords

References

  1. Sci Total Environ. 2016 Oct 1;566-567:320-332 [PMID: 27232962]
  2. Dis Aquat Organ. 2003 Dec 29;57(3):255-60 [PMID: 14960039]
  3. Toxicol Appl Pharmacol. 2006 Apr 15;212(2):89-98 [PMID: 16112155]
  4. Dis Aquat Organ. 2007 Jan 18;73(3):175-92 [PMID: 17330737]
  5. Environ Sci Technol. 2009 Oct 1;43(19):7556-63 [PMID: 19848176]
  6. Front Zool. 2011 Apr 18;8(1):8 [PMID: 21496358]
  7. Science. 2012 Jun 8;336(6086):1268-73 [PMID: 22674334]
  8. Dis Aquat Organ. 2012 Feb 17;98(1):11-25 [PMID: 22422126]
  9. J Anim Ecol. 2018 Mar;87(2):489-499 [PMID: 29030867]
  10. Environ Sci Technol. 2007 Mar 1;41(5):1771-6 [PMID: 17396672]
  11. Environ Health Perspect. 2011 Aug;119(8):1098-103 [PMID: 21463979]
  12. Dis Aquat Organ. 2009 Feb 25;83(3):257-60 [PMID: 19402457]
  13. Sci Total Environ. 2015 Jan 1;502:80-90 [PMID: 25244036]
  14. Science. 1971 Jan 29;171(3969):385-7 [PMID: 5538935]
  15. Science. 2009 Oct 23;326(5952):582-5 [PMID: 19900897]
  16. Environ Toxicol Chem. 2014 Oct;33(10):2358-62 [PMID: 25044296]
  17. Environ Sci Technol. 2017 Jan 3;51(1):671-679 [PMID: 28001054]
  18. Emerg Infect Dis. 2011 Dec;17(12):2383-4 [PMID: 22172594]
  19. Ecol Appl. 2008 Oct;18(7):1743-53 [PMID: 18839768]
  20. Toxicol Ind Health. 1999 Jan-Mar;15(1-2):119-32 [PMID: 10188195]
  21. Ecol Lett. 2006 Oct;9(10):1157-71 [PMID: 16972879]
  22. PLoS One. 2017 Jan 17;12(1):e0167882 [PMID: 28095428]
  23. Proc Natl Acad Sci U S A. 2012 May 1;109(18):6999-7003 [PMID: 22493237]
  24. Trends Ecol Evol. 2006 Nov;21(11):606-13 [PMID: 16843566]
  25. Nature. 2014 Jul 10;511(7508):224-7 [PMID: 25008531]
  26. Proc Natl Acad Sci U S A. 2013 Sep 17;110(38):15325-9 [PMID: 24003137]
  27. PLoS One. 2013;8(2):e56747 [PMID: 23451076]
  28. Ecol Lett. 2014 Aug;17(8):932-41 [PMID: 24811760]
  29. Annu Rev Entomol. 2007;52:81-106 [PMID: 16842032]
  30. Dis Aquat Organ. 2010 Nov;92(2-3):165-74 [PMID: 21268978]
  31. Ecol Appl. 2011 Oct;21(7):2521-9 [PMID: 22073641]
  32. Proc Biol Sci. 2013 Dec 7;280(1772):20131502 [PMID: 24266041]
  33. Ecol Appl. ;24(8):1945-53 [PMID: 29185664]
  34. Proc Natl Acad Sci U S A. 2011 Jan 11;108(2):662-7 [PMID: 21199943]
  35. Nature. 2008 Oct 30;455(7217):1235-9 [PMID: 18972018]
  36. Environ Health Perspect. 2006 Jan;114(1):46-50 [PMID: 16393657]
  37. Sci Total Environ. 2003 Dec 30;317(1-3):207-33 [PMID: 14630423]
  38. Appl Environ Microbiol. 2016 Aug 30;82(18):5653-60 [PMID: 27422829]
  39. Environ Toxicol Chem. 2005 May;24(5):1253-8 [PMID: 16111008]
  40. Environ Health Perspect. 2010 Jan;118(1):20-32 [PMID: 20056568]
  41. Arch Environ Contam Toxicol. 2012 Jul;63(1):137-43 [PMID: 22228138]
  42. Ecol Lett. 2013 Jun;16(6):807-20 [PMID: 23452227]
  43. Trends Ecol Evol. 2010 Feb;25(2):109-18 [PMID: 19836101]
  44. Environ Toxicol Chem. 2010 Nov;29(11):2477-80 [PMID: 20836054]
  45. Proc Natl Acad Sci U S A. 2015 Mar 10;112(10):3008-13 [PMID: 25713379]
  46. Ecohealth. 2015 Mar;12(1):188-93 [PMID: 25384612]
  47. Biol Lett. 2015 Nov;11(11): [PMID: 26582843]
  48. PLoS One. 2015 Jul 16;10(7):e0132832 [PMID: 26181492]
  49. Science. 1973 Nov 2;182(4111):443-9 [PMID: 17832454]
  50. Ann N Y Acad Sci. 2010 May;1195:129-48 [PMID: 20536821]
  51. Ecol Lett. 2012 Jul;15(7):714-22 [PMID: 22587750]
  52. PLoS One. 2012;7(8):e43573 [PMID: 22912890]
  53. J Parasitol. 1980 Apr;66(2):362-4 [PMID: 7391881]
  54. Nat Commun. 2017 Jul 20;8(1):86 [PMID: 28729558]
  55. Ecohealth. 2016 Mar;13(1):111-22 [PMID: 26911919]
  56. Environ Sci Technol. 2013 Jul 16;47(14):7958-64 [PMID: 23777241]
  57. Environ Sci Pollut Res Int. 2015 Sep;22(17):12929-40 [PMID: 25913318]
  58. Conserv Biol. 2013 Aug;27(4):741-51 [PMID: 23773091]
  59. Environ Toxicol Chem. 2009 Sep;28(9):1939-45 [PMID: 19358624]
  60. Arch Environ Health. 1996 Nov-Dec;51(6):445-51 [PMID: 9012323]
  61. Environ Toxicol Chem. 2014 Sep;33(9):2114-9 [PMID: 24934557]
  62. Ecol Appl. 2006 Oct;16(5):2022-7; author reply 2027-34 [PMID: 17069392]

Grants

  1. R01 GM109499/NIGMS NIH HHS
  2. R01 TW010286/FIC NIH HHS

MeSH Term

Animals
Anura
Chytridiomycota
Fungicides, Industrial
Mycoses

Chemicals

Fungicides, Industrial

Word Cloud

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