Abstract
The amphibian disease chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis (Bd), has been linked to significant amphibian declines over the past three decades. The most severe effects of the pathogen have been primarily observed in relatively pristine areas that are not affected by many anthropogenic factors.
One hypothesis concerning improved amphibian persistence with Bd in disturbed landscapes is that contaminants may abate the effects of Bd on amphibians. Recent laboratory studies have shown that pesticides, specifically the fungicide thiophanate-methyl (TM), can kill Bd outside of hosts and clear Bd infections within hosts. Using aquatic mesocosms, we tested the hypothesis that TM (0.43 mg/L) would alter growth and development of Lithobates sphenocephalus (southern leopard frog) tadpoles and Bd-infection loads in infected individuals. We hypothesized that the scope of such alterations and infection clearing would be affected by aquatic community variables, specifically zooplankton. TM altered zooplankton diversity (reduced cladoceran and increased copepod and ostracod abundances) and caused mortality to all tadpoles in TM-exposed tanks. In TM-free tanks, Bd-exposed tadpoles in high-density treatments metamorphosed smaller than Bd-unexposed, effects that were reversed in low-density treatments. Our study demonstrates the potential adverse effects of a fungicide and Bd on tadpoles and aquatic systems.
Similar content being viewed by others
References
Berger L, Speare R, Daszak P, Green DE, Cunningham AA (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci U S A 95:9031–9036
Boyle DG, Boyle DB, Olsen V, Morgan JA, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60:141–148
Briggs JA, Riley MB, Whitwell T (1998) Quantification and remediation of pesticides in runoff water from containerized plant production. J Environ Qual 27(4):814–820
Briggs J, Whitwell T, Fernandez RT, Riley MB (2002) Effect of integrated pest management strategies on chlorothalonil, metalaxyl, and thiophanate-methyl runoff at a container nursery. J Am Soc Hortic Sci 127(6):1018–1024
Buck JC, Scheessele EA, Relyea RA, Blaustein AR (2012) The effects of multiple stressors on wetland communities: pesticides, pathogens and competing amphibians. Freshwater Biol 57:61–73
Carter A (2000) How pesticides get into water-and proposed reduction measures. Pestic Outlook 11:149–156
Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9:141–150
Davidson C, Benard MF, Shaffer HB, Parker JM, O’Leary C, Conlon JM, Rollins-Smith LA (2007) Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ Sci Tech 41:1771–1776
Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill
Earl JE, Castello PO, Cohagen KE, Semlitsch RD (2014) Effects of subsidy quality on reciprocal subsidies: how leaf litter species changes frog biomass export. Oecologia 175(1):209–218
Earl JE, Semlitsch RD (2012) Reciprocal subsidies in ponds: Does leaf input increase frog biomass export? Oecologia 170(4):1077–1087
Egea-Serrano A, Relyea RA, Tejedo M, Torralva M (2012) Understanding of the impact of chemicals on amphibians: a meta-analytic review. Ecol Evol 2:1382–1397
Gahl MK, Pauli BD, Houlahan JE (2011) Effects of chytrid fungus and a glyphosate-based herbicide on survival and growth of wood frogs (Lithobates sylvaticus). Ecol Appl 21:2521–2529
Giesy J, Dobson S, Solomon K (2000) Ecotoxicological risk assessment for Roundup® herbicide. Rev Environ Contam Toxicol 167:35–120
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
Hamilton PT, Richardson JM, Anholt BR (2012) Daphnia in tadpole mesocosms: trophic links and interactions with Batrachochytrium dendrobatidis. Freshwater Biol 57(4):676–683
Hanlon SM, Parris MJ (2012) The impact of pesticides on the pathogen Batrachochytrium dendrobatidis independent of potential hosts. Arch Environ Contam Toxicol 63:137–143
Hanlon SM, Parris MJ (2014) The interactive effects of chytrid fungus, pesticides, and exposure timing on gray treefrog (Hyla versicolor) larvae. Environ Toxicol Chem 33(1):216–222
Hanlon SM, Kerby JL, Parris MJ (2012) Unlikely remedy: Fungicide clears infection from pathogenic fungus in larval southern leopard frogs (Lithobates sphenocephalus). PLoS One 7:43573
Hua J, Relyea RA (2012) East Coast vs West Coast: effects of an insecticide in communities containing different amphibian assemblages. Freshwat Sci 31(3):787–799
Hua J, Relyea RA (2014) Chemical cocktails in aquatic systems: pesticide effects on the response and recovery of > 20 animal taxa. Environ Pollut 189:18–26
Hyatt AD, Boyle DG, Olsen V, Bolye DB, Berger L, Obendorf D, Dalton A, Kriger K, Heros M, Hines H, Phillot R, Campbell R, Marantelli G, Gleason F, Coiling A (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis Aquat Organ 73:175–192
IPCS (2012) Carbandazim, Benomyl, and Thiophanate-methyl. Geneva, Switzerland, World Health Organization, International Programme on Chemical Safety
Johnson ML, Speare R (2003) Survival of Batrachochytrium dendrobatidis in water: quarantine and disease control implications. Emerg Infect Dis 9:922–925
Johnson ML, Berger L, Phillips L, Speare R (2003) Fungicidal effects of chemical disinfectants, UV light, desiccation and heat on the amphibian chytrid, Batrachochytrium dendrobatidis. Dis Aquat Organ 57:255–260
Jones DK, Hammond JI, Relyea RA (2011) Competitive stress can make the herbicide Roundup® more deadly to larval amphibians. Environ Toxicol Chem 30(2):446–454
Kerby JL, Schieffer A, Brown JR, Whitfield S (2013) Utilization of fast qPCR techniques to detect the amphibian chytrid fungus: a cheaper and more efficient alternative method. Methods Ecol Evol 4:162–166
Kriger KM, Hines HB, Hyatt AD, Boyle DG, Hero JM (2006) Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Dis Aquat Org 71:141–148
Külköylüoğlu O (2004) On the usage of ostracods (Crustacea) as bioindicator species in different aquatic habitats in the Bolu region, Turkey. Ecol Indic 4(2):139–147
Kyriakopoulou K, Anastasiadou P, Machera K (2009) Comparative toxicities of fungicide and herbicide formulations on freshwater and marine species. Bull Environ Contam Toxicol 82(3):290–295
Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227
Maderik R, Gagno SR II, Makuch JR III (2006) Wetlands in agricultural landscapes: A Conservation Effects Assessment Project (CEAP) bibliography. Special reference briefs
Mann RM, Hyne RV, Choung CB, Wilson SP (2009) Amphibians and agricultural chemicals: review of the risks in a complex environment. Environ Pollut 157(11):2903–2927
McMahon TA, Halstead NT, Johnson S, Raffel TR, Romansic JM, Crumrine PW, Rohr JR (2012) Fungicide‐induced declines of freshwater biodiversity modify ecosystem functions and services. Ecol Lett 15(7):714–722
McMahon TA, Romansic JM, Rohr JR (2013) Nonmonotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on tadpoles. Environ Sci Tech 47(14):7958–7964
Miller S, Zieger U, Ganser C, Satterlee SA, Bankovich B, Amadi V, Hariharan H, Stone D, Wisely SM (2015) Influence of land use and climate on salmonella carrier status in the small Indian mongoose (Herpestes auropunctatus) in Grenada, West Indies. J Wild Dis 51(1):60–68
Morin PJ (1983) Predation, competition, and the composition of larval anuran guilds. Ecol Mono 53:119–138
OECD (2007) OECD guidelines for the testing of chemicals. OECD Publishing, Vol. Section 5
Parris MJ, Cornelius TO (2004) Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385–3395
Payne NJ, Feng JC, Reynolds PE (1990) Off-target deposits and buffer zones required around water for aerial glyphosate applications. Pest Manage Sci 30:183–198
Pieri V, Caserini C, Gomarasca S, Martens K, Rossetti G (2007) Water quality and diversity of the Recent ostracod fauna in lowland springs from Lombardy (northern Italy). In Ostracodology—Linking Bio-and Geosciences (pp. 79-87). Springer Netherlands
R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/
Relyea RA, Diecks N (2008) An unforeseen chain of events: Lethal effects of pesticides on frogs at sublethal concentrations. Ecol Appl 18:1728–1748
Roossinck MJ, García-Arenal F (2015) Ecosystem simplification, biodiversity loss and plant virus emergence. Curr Opin Virol 10:56–62
Schmeller DS, Blooi M, Martel A, Garner TW, Fisher MC, Azemar F, Clare FC, Leclerc C, Jäger L, Guevara-Nieto M, Loyau A, Pasmans F (2014) Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr Biol 24(2):176–180
Schultz TW, Douglas A (2003) Housing and husbandry of Xenopus for oocyte production. Lab Anim 32(2):34–39
Searle CL, Mendelson JR, Green LE, Duffy MA (2013) Daphnia predation on the amphibian chytrid fungus and its impacts on disease risk in tadpoles. Ecol Evol 3(12):4129–4138
Skelly DK (1997) Tadpole communities: pond permanence and predation are powerful forces shaping the structure of tadpole communities. Am Sci 85(1):36–45
Skelly DK, Kiesecker JM (2001) Venue and outcome in ecological experiments: manipulations of larval anurans. Oikos 94(1):198–208
Smalling KL, Orlando JL, Calhoun D, Battaglin WA, Kuivila KM (2012) Occurrence of Pesticides in Water and Sediment Collected from Amphibian Habitats Located Throughout the United States, 2009–2010
Sparling DW, Linder G, Bishop CA, Krest SK (2010) Ecotoxicology of amphibians and reptiles, 2nd edn. SETAC/Taylor & Francis, Boca Raton, FL
Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306(5702):1783–1786
Van den Brink PJ, Hattink J, Bransen F, Van Donk E, Brock T (2000) Impact of the fungicide carbendazim in freshwater microcosms. II. Zooplankton, primary producers and final conclusions. Aquat Toxicol 48(2):251–264
Venesky MD, Parris MJ, Storfer A (2009) Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. EcoHealth 6:565–575
Venesky MD, Wassersug RJ, Parris MJ (2010) Fungal pathogen changes the feeding kinematics of larval anurans. J Parisitol 3:552–557
Venesky MD, Hanlon SM, Lynch K, Parris MJ, Rohr JR (2013) Optimal digestion theory does not predict the effect of pathogens on intestinal plasticity. Biol Lett 9(2):20130038
Vincelli P (2004) Simulations of fungicide runoff following applications for turfgrass disease control. Plant Dis 88(4):391–396
Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc Natl Acad Sci U S A 107:9689–9694
Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci U S A 105:11466–11473
Wilson G, Williamson M (2008) Topsin-M: the new benomyl for mycorrhizal-suppression experiments. Mycologia 100:548–544
Acknowledgments
We would like to thank Jerad Henson, Nick Hobbs, Eron Raines, and Chris Vlautin for experimental assistance.
Compliance with Ethical Standards
TN collection permits were obtained prior to collecting the animals in these experiments. All experiments were conducted in accordance with approved IACUC protocols. The authors have no conflicts of interest to report. This project was funded in part by university funds awarded to MJP and a Sigma Xi Gant-in-Aid of Research awarded to SMH.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Cinta Porte
Rights and permissions
About this article
Cite this article
Hanlon, S.M., Lynch, K.J., Kerby, J.L. et al. The effects of a fungicide and chytrid fungus on anuran larvae in aquatic mesocosms. Environ Sci Pollut Res 22, 12929–12940 (2015). https://doi.org/10.1007/s11356-015-4566-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4566-8