The interactive effects of chytrid fungus, pesticides, and exposure timing on gray treefrog (Hyla versicolor) larvae

Environmental Toxicology and Chemistry

Volumn 33, Issue 1, 2014, Pages 216-222

  Hanlon, Shane M ^a   Parris, Matthew J ^a  

^a University of Memphis   (United States)

Author keywords

Acetylcholinesterase inhibitors; Amphibians; Aquatic toxicology; Organophosphate; Pathology

Indexed keywords

ACETYLCHOLINESTERASE INHIBITORS; AMPHIBIANS; AQUATIC TOXICOLOGY; CHEMICAL CONTAMINANTS; FACTORIAL DESIGN; INTERACTIVE EFFECT; LARVAL DEVELOPMENT; ORGANOPHOSPHATE;

FORESTRY; MEDICINE; PATHOGENS; PATHOLOGY;

PESTICIDE EFFECTS;

CARBARIL; GLYPHOSATE;

AQUATIC ORGANISM; CHEMICAL POLLUTANT; FROG; FUNGUS; HOST-PATHOGEN INTERACTION; INFECTIVITY; INHIBITOR; LARVA; LARVAL DEVELOPMENT; METAMORPHOSIS; ORGANOPHOSPHATE; PATHOLOGY; POLLUTION EXPOSURE; SURVIVAL; TOXICOLOGY;

ANIMAL EXPERIMENT; ARTICLE; BATRACHOCHYTRIUM DENDROBATIDIS; CHYTRIDIOMYCOSIS; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FACTORIAL DESIGN; HOST PATHOGEN INTERACTION; HYLA; HYLA VERSICOLOR; LARVAL DEVELOPMENT; METAMORPHOSIS; NONHUMAN; PRIORITY JOURNAL; SURVIVAL; TADPOLE;

AMPHIBIA; BATRACHOCHYTRIUM DENDROBATIDIS; FUNGI; HYLA VERSICOLOR; METAMORPHA;

ACETYLCHOLINESTERASE INHIBITORS; AMPHIBIANS; AQUATIC TOXICOLOGY; ORGANOPHOSPHATE; PATHOLOGY;

ANIMALS; ANURA; CARBARYL; CHYTRIDIOMYCOTA; GLYCINE; HOST-PATHOGEN INTERACTIONS; LARVA; METAMORPHOSIS, BIOLOGICAL; PESTICIDES;

EID: 84890789400     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.2419     Document Type: Article

References (63)

1. Van Dyke F. 2008. Conservation Biology: Foundations, Concepts, Applications, 2nd ed. Springer, New York, NY, USA.
2. Newman MC. 2009. Fundamentals of Ecotoxicology, 3rd ed. CRC Press, Boca Raton, FL, USA.
3. Sparling DW, Linder G, Bishop CA, Krest S. 2010. Ecotoxicology of Amphibians and Reptiles, 2nd ed. SETAC/Taylor & Francis, Pensacola, FL, USA.
4. Cypser JR, Johnson TE. 2002. Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J Gerontol A-Biol 57:B109-B114.
5. Relyea RA, Mills N. 2001. Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc Natl Acad Sci U S A 98:2491-2496.
6. Norris LA, Lorz HW, Gregory SV. 1983. Influence of forest and range land management on anadromous fish habitat in Western North America: Forest chemicals. Technical Report. PW-149. US Department of Agriculture Forest Service, Portland, OR.
7. 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. Data Series 707. US Geological Survey, Reston, VA.
8. Collins JP, Crump ML, Lovejoy TE III. 2009. Extinction in Our Times: Global Amphibian Decline. Oxford University Press, New York, NY, USA.
9. Jones DK, Hammond JI, Relyea RA. 2011. Competitive stress can make the herbicide Roundup® more deadly to larval amphibians. Environ Toxicol Chem 30:446-454.
10. Rohr JR, Raffel TR, Sessions SK, Hudson PJ. 2008. Understanding the net effects of pesticides on amphibian trematode infections. Ecol Appl 18:1743-1753.
11. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Gogging CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H. 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.
12. Longcore JE, Pesser AP, Nichols DK. 1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219-227.
13. Daszak P, Cunningham AA, Hyatt AD. 2003. Infectious disease and amphibian population declines. Divers Distrib 9:141-150.
14. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R. 2009. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582-585.
15. Venesky MD, Parris MJ, Storfer A. 2009. Impacts of Batrachochytrium dendrobatidis infection on tadpole foraging performance. EcoHealth 6:565-575.
16. Parris MJ. 2004. Hybrid response to pathogen infection in interspecific crosses between two amphibian species (Anura: Ranidae). Evol Ecol Res 6:457-471.
17. Carey C, Bruzgul JE, Livo LJ, Walling ML, Kuehl KA, Dixon BF, Pessier AP, Alford RA, Rogers KB. 2006. Experimental exposures of boreal toads (Bufo boreas) to a pathogenic chytrid fungus (Batrachochytrium dendrobatidis). EcoHealth 3:5-21.
18. Searle CL, Xie GY, Blaustein AR. 2013. Development and infectious disease in hosts with complex life cycles. PLoS ONE 8:e60920.
19. Mann RM, Hyne RV, Choung CB, Wilson SP. 2009. Amphibians and agricultural chemicals: Review of the risks in a complex environment. Environ Pollut 157:2903-2927.
20. 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.
21. Buck JC, Scheessele EA, Relyea RA, Blaustein AR. 2012. The effects of multiple stressors on wetland communities: Pesticides, pathogens and competing amphibians. Fresh Biol 57:61-73.
22. Kleinhenz P, Boone MD, Fellers G. 2012. Effects of the amphibian chytrid fungus and four insecticides on Pacific treefrogs (Pseudacris regilla). J Herpetol 46:625-631.
23. Kiesecker JM. 2002. Synergism between trematode infection and pesticides exposure: A link to amphibian limb deformities in nature? Proc Natl Acad Sci U S A 99:9900-9904.
24. Rohr JR, Schotthoefer AM, Raffel TR, Carric HJ, Halstead N, Hoverman HT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR. 2008. Agrochemicals increase trematode infections in a declining amphibian species. Nature 455:1235-1239.
25. Martin LB, Hopkins WA, Mydlarz LD, Rohr JR. 2010. The effects of anthropogenic global changes on immune functions and disease resistance. Ann N Y Acad Sci 1195:129-148.
26. 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.
27. Hanlon SM, Kerby JR, Parris MJ. 2012. Unlikely remedy: Fungicide clears pathogenic fungus in larval southern leopard frogs (Lithobates sphenocephalus). PLoS ONE 7:e43573.
28. McMahon TA, Romansic JM, Rohr JR. 2013. Non-monotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on tadpoles. Environ Sci Technol 47:7958-7964.
29. Bunn TL, Parsons PJ, Kao E, Dietert RR. 2001. Exposure to lead during critical windows of embryonic development: Differential immunotoxic outcome based on stage of exposure and gender. Toxicol Sci 64:57-66.
30. Tchounwou PB, Patlolla AK, Centeno JA. 2003. Invited reviews: Carcinogenic and systemic health effects associated with arsenic exposure-A critical review. Toxicol Pathol 31:575-588.
31. Johnson PTJ, Kellermanns E, Bowerman J. 2011. Critical windows of disease risk: Amphibian pathology driven by developmental changes in host resistance and tolerance. Funct Ecol 25:726-734.
32. Rachoqicz LJ, Vredenburg VT. 2004. Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Dis Aquat Org 61:75-83.
33. Garner TWJ, Walker S, Bosch J, Leech S, Rowcliffe JM, Cunningham AA, Fisher M. 2009. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783-791.
34. Boone MD, Bridges CM, Rothermel BB. 2001. Growth and development of larval green frogs (Rana clamitans) exposed to multiple doses of an insecticide. Oecologia 129:518-524.
35. Greulich K, Pflugmacher S. 2003. Differences in susceptibility of various life stages of amphibians to pesticide exposure. Aquat Toxicol 65:329-336.
36. Gosner KL. 1960. A simplified key for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183-190.
37. Davis MJ, Kleinhenz P, Boone MD. 2011. Juvenile green frog (Rana clamitans) predatory ability not affected by exposure to carbaryl at different times during larval development. Environ Toxicol Chem 30:1618-1620.
38. Boone MD, Hammond SA, Veldhoen N, Youngquist M, Helbing CC. 2013. Specific time of exposure during tadpole development influences biological effects of the insecticide carbaryl in green frogs (Lithobates clamitans). Aquat Toxicol 130:139-148.
39. Relyea RA. 2009. A cocktail of contaminants: How mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 159:363-376.
40. Donaldson D, Kiely T, Grube A. 2002. Pesticides industry sales and usage: 1998 and 1999 market estimates. EPA 733/R-02/001. US Environmental Protection Agency, Washington, DC.
41. Aly OM, El-Dib MA. 1971. Studies on the persistence of some carbamate insecticides in the aquatic environment-I: Hydrolysis of Sevin®, Baygon®, Pyrolan® and Dimetilan® in waters. Water Res 5:1191-1205.
42. Wauchope RD, Haque R. 1973. Effects of pH, light and temperature on carbaryl in aqueous media. Bull Environ Contam Toxicol 9:257-260.
43. Baylis A. 2000. Why glyphosate is a global herbicide: Strengths, weaknesses and prospects. Pest Manag Sci 56:299-308.
44. Giesy J, Dobson S, Solomon KR. 2000. Ecotoxicological risk assessment for Roundup® herbicide. Rev Environ Contam Toxicol 167:35-120.
45. Howe CM, Berrill M, Pauli Bd, Helbing CC, Werry K, Welhoen N. 2004. Toxicity of glyphosate-based pesticides to four North American frog species. Environ Toxicol Contam 23:1928-1938.
46. Edwards W. 1980. A watershed study of glyphosate transport in runoff. J Environ Qual 9:661-665.
47. Bridges CM. 1997. Tadpole swimming performance and activity affected by acute exposure to sublethal levels of carbaryl. Arch Environ Con Toxicol 16:1935-1939.
48. 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.
49. 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 Org 6073:175-192.
50. Kriger KM, Hero J. 2006. Survivorship in wild frogs infected with chytridiomycosis. EcoHealth 3:171-177.
51. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ. 2010. Large-scale amphibian die-offs driven by the dynamics of an emerging infectious disease. Proc Natl Acad Sci U S A 107:9689-9694.
52. 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 9:20130038.
53. R Core Development Team. Package 'car', Ver 2.0-19. R Project for Statistical Computing. [cited 2013 July 11]. Available from: http://cran.r-project.org/web/packages/car/car.pdf.
54. Rohr JR, Elskus AA, Sheperd BS, Crowley PH, McCathy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD. 2004. Multiple stressors and salamanders: Effects of an herbicide, food limitation, and hydroperiod. Ecol Appl 14:1028-1040.
55. Boone MD, Semlitsch RD, Little EE, Dolye MC. 2007. Multiple stressors in amphibian communities: Effects of chemical contamination, bullfrogs, and fish. Ecol Appl 17:291-301.
56. Davidson C, Benard MF, Shaffer HB, Parker JM, O'Leary C, Conlon JM, Rollins-Smith LA. 2007. Effects of chytrid infection and carbaryl exposure on survival, growth and antimicrobial peptide defenses in foothill yellow-legged frogs (Rana boylii). Environ Sci Tech 41:1771-1776.
57. Parris MJ, Beaudoin JG. 2004. Chytridiomycosis impacts predator-prey interactions in larval amphibian communities. Oecologia 140:626-632.
58. Parris MJ, Cornelius TO. 2004. Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85:3385-3395.
59. McDiarmid RW, Altig RA. 1999. Tadpoles: The Biology of Anuran Larvae. University of Chicago Press, Chicago, II, USA.
60. Luquet E, Garner TWJ, Lena J-P, Bruel C, Joly Pierre, Lengagne, Grolet O, Plenet S. 2012. Genetic erosion in wild populations makes resistance to a pathogen more costly. Evolution 66:1942-1952.
61. McMahon TA, Brannelly LA, Chatfield MWH, Johnson PTJ, Joseph MB, McKenzie VJ, Richards-Zawacki CL, Venesky MD, Rohr JR. 2013. Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proc Natl Acad Sci U S A 110:210-215.
62. Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ. 2008. Evaluating the links between climate, disease spread, and amphibian declines. Proc Natl Acad Sci U S A 105:17436-17441.
63. Ron SR. 2005. Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the new world. Biotropica 37:209-221.