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Pesticide alters oviposition site selection in gray treefrogs

  • Global Change and Conservation Ecology
  • Published:
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An Erratum to this article was published on 14 October 2008

Abstract

Understanding the impacts of pesticides on non-target organisms is an important issue for conservation biology. Research into the environmental consequences of pesticides has largely focused on pesticide toxicity. We have less understanding of the nonlethal effects of pesticides, and the consequences of nonlethal effects for species and communities. For example, we know very little about whether pesticides alter habitat selection behavior. Understanding whether pesticides alter habitat selection is important because pesticide-induced shifts in habitat selection could either magnify or reduce the toxic effects of contaminants by funneling organisms into or directing them away from contaminated sites. Here we present four field experiments that examine the effect of the commercial pesticide Sevin® and its active ingredient, carbaryl, on oviposition site selection by the gray treefrog (Hyla chrysoscelis). Our results show that uncontaminated pools consistently received 2–3 times more eggs than contaminated pools; that treefrogs appeared to respond to Sevin® directly, not indirectly via its effects on the aquatic food web, and that this preference persisted across a range of temporal and spatial scales. Both Sevin® and carbaryl per se reduced oviposition, while other volatile chemicals (e.g., our solvent control, acetone) had no effect. These findings suggest that in order to understanding the consequences of contaminants in aquatic systems we will need to consider not only toxicity, but also how contaminant effects on habitat selection alter the way organisms distribute themselves in the environment.

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References

  • 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 demetilan in waters. Water Res 5:1191–1205

    Article  CAS  Google Scholar 

  • Binckley CA, Resetarits WJ (2005) Habitat selection determines abundance, richness and species composition of beetles in aquatic communities. Biol Lett 1:370–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Blaustein L, Kotler BP (1993) Oviposition habitat selection by the mosquito, Culiseta longiareolata-effects of conspecifics, food and green toad tadpoles. Ecol Entomol 18:104–108

    Article  Google Scholar 

  • Boone MD, James SM (2003) Interactions of an insecticide, herbicide, and natural stressors in amphibian community mesocosms. Ecol Appl 13(3):829–841

    Article  Google Scholar 

  • Boone MD, Semlitsch RD (2001) Interactions of an insecticide with larval density and predation in experimental amphibian communities. Conserv Biol 15:228–238

    Article  Google Scholar 

  • Boone MD, Semlitsch RD (2002) Interactions of an insecticide with competition and pond drying in amphibian communities. Ecol Appl 12:307–316

    Article  Google Scholar 

  • Bosch J, Martinez-Solano I (2003) Factors influencing occupancy of breeding ponds in a Montane amphibian assemblage. J Herpetol 37:410–413

    Article  Google Scholar 

  • Charnov EL (1976) Optimal foraging: the marginal value theorem. Theor Popul Biol 9:129–136

    Article  CAS  PubMed  Google Scholar 

  • Chesson J (1984) Effect of Notonecta (Hemiptera: Notonectidae) on mosquitoes (Diptera: Culicidae): predation or selective oviposition? Environ Entomol 13:531–538

    Article  Google Scholar 

  • Fegraus EH, Marsh DM (2000) Are newer ponds better? Pond chemistry, oviposition site selection, and tadpole performance in the tungara frog, Physalaemus pustulosus. J Herpetol 34:455–459

    Article  Google Scholar 

  • Fretwell SD, Lucas HL (1970) On the territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Biotheoretica 19:16–36

    Article  Google Scholar 

  • Hayes TB, Collins A, Lee M, et al. (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476–5480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755

    Article  CAS  PubMed  Google Scholar 

  • Johnson JR (2005) Multi-scale investigations of gray treefrog movements: patterns or migration, dispersal, and gene flow. Dissertation, Department of Biology. University of Missouri, Columbia, MO, pp i–246

  • Kats LB, Sih A (1992) Oviposition site selection and avoidance of fish by streamside salamanders (Ambystoma barbouri). Copeia:468–473

  • Kiesecker JM (2002) Synergism between trematode infection and pesticide exposure: a link to amphibian limb deformities in nature? Proc Natl Acad Sci USA 99:9900–9904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsh DM, Borrell BJ (2001) Flexible oviposition strategies in tungara frogs and their implications for tadpole spatial distributions. Oikos 93:101–109

    Article  Google Scholar 

  • Moe SJ, Stenseth NC, Smith RH (2001) Effects of a toxicant on population growth rates: sublethal and delayed responses in blowfly populations. Funct Ecol 15:712–721

    Article  Google Scholar 

  • Osenberg CW, Shima JS, St Mary CM (2006) Habitat degradation and settlement behavior: effects on fish settlement, survival, and recruitment. In: Suzuki Y, Nakamori T, Hidaka M, et al. (eds) Proceedings of the 10th International Coral Reef Symposium. Japanese Coral Reef Society, Tokyo

  • Petranka JW, Fakhoury K (1991) Evidence of a chemically mediated avoidance response of ovipositing insects to blue gills and green frog tadpoles. Copeia 234–239

  • Rajkumar S, Jebanesan A (2005) Oviposition deterrent and skin repellent activities of Solanum trilobatum leaf extract against the malarial vector Anopheles stephensi. J Insect Sci 5:15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Relyea RA (2003) Predator cues and pesticides: a double dose of danger for amphibians. Ecol Appl 13:1515–1521

    Article  Google Scholar 

  • Relyea RA (2004) Synergistic impacts of malathion and predatory stress on six species of North American tadpoles. Environ Toxicol Chem 23:1080–1084

    Article  CAS  PubMed  Google Scholar 

  • Relyea R, Hoverman JT (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171

    Article  PubMed  Google Scholar 

  • Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proc Natl Acad Sci USA 98:2491–2496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Resetarits WJ (2001) Colonization under threat of predation: avoidance of fish by an aquatic beetle, Tropisternus lateralis (Coleoptera : Hydrophilidae). Oecologia 129:155–160

    Article  Google Scholar 

  • Resetarits WJ (2005) Habitat selection behavior links local and regional scales in aquatic systems. Ecol Lett 8:480–486

    Article  PubMed  Google Scholar 

  • Resetarits WJ, Wilbur HM (1989) Choice of oviposition site by Hyla chrysoscelis: Role of predators and competitors. Ecology 70:220–228

    Article  Google Scholar 

  • Resetarits WJ, Binckley CA, Chalcraft DR (2005) Habitat selection, species interactions, and processes of community assembly in complex landscapes: a metacommunity perspective. In: Holyoak M, Leibold M, Holt RD (eds) Metacommunities: Spatial dynamics and ecological communities. The University of Chicago Press, Chicago, IL, pp 374–398

  • Rohr JR, Elskus AA, Shepherd BS, et al. (2003) Lethal and sublethal effects of atrazine, carbaryl, endosulfan, and octylphenol on the streamside salamander (Ambystoma barbouri). Environ Toxicol Chem 22:2385–2392

    Article  CAS  PubMed  Google Scholar 

  • Rohr JR, Kerby J, Sih A (2006a) Community ecology as a framework for predicting contaminant effects. Trends Ecol Evol 21:606–613

    Article  PubMed  Google Scholar 

  • Rohr JR, Sager T, Sesterhenn TM, Palmer BD (2006b) Exposure, post-exposure, and density-mediated effects of atrazine on amphibians: breaking down net effects into their parts. Environ Health Perspect 114:46–50

    Article  CAS  PubMed  Google Scholar 

  • Semlitsch RD, Bridges CM, Welch AM (2000) Genetic variation and a fitness tradeoff in the tolerance of gray treefrog (Hyla versicolor) tadpoles to the insecticide carbaryl. Oecologia 125:179–185

    Article  CAS  PubMed  Google Scholar 

  • Sharom MS, Miles JRW, Harris CR, McEwen FL (1980) Persistence of 12 insecticides in water. Water Res 14:1089–1093

    Article  CAS  Google Scholar 

  • Skelly DK (2001) Distributions of pond-breeding anurans: an overview of mechanisms. Isr J Zool 47:313–332

    Article  Google Scholar 

  • Spieler M, Linsenmair KE (1997) Choice of optimal oviposition sites by Hoplobatrachus occipitalis (Anura: Ranidae) in an unpredictable and patchy environment. Oecologia 109(2):184–199

    Article  CAS  PubMed  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Viertel B (1999) Salt tolerance of Rana temporaria: spawning site selection and survival during embyonic development. Amphib–Reptil 20:161–171

    Google Scholar 

  • Vonesh JR, De la Cruz O (2002) Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133:325–333

    Article  Google Scholar 

  • Wake DB (1991) Declining amphibian populations. Science 253:860–860

    Article  CAS  PubMed  Google Scholar 

  • Wauchope RD, Haque R (1973) Effects of pH, light and temperature on carbaryl in aqueous media. Bull Environ Contam Toxicol 9:257–260

    Article  CAS  PubMed  Google Scholar 

  • Wolfe NL, Zepp RG, Paris DF (1978) Carbaryl, propham and cholorpropham: a comparison of the rates of hydrolysis and photolysis with the rate of biolysis. Water Res 12:565–571

    Article  CAS  Google Scholar 

  • Xue RD, Barnard DR, Ali A (2001) Laboratory and field evaluation of insect repellents as oviposition deterrents against the mosquito Aedes albopictus. Med Vet Entomol 15:126–131

    Article  CAS  PubMed  Google Scholar 

  • Xue RD, Barnard DR, Ali A (2006) Laboratory evaluation of 21 insect repellents as larvicides and as oviposition deterrents of Aedes albopictus (Diptera: Culicidae). J Am Mosq Control Assoc 22:126–130

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Thanks to S. Gallitano, T. Giarla, S. Rosenberg, R. Shulman, M. Sobotka, and for assisting in experiments; M. Boone and R. Semlitsch for sharing original data; B. Allen, L. Blaustein, J. Chase, P. Crumrine, T. Knight, A. Randle, W. Resetarits, J. Rohr, W. Ryberg, T. Steury, and R. Shulman for discussions that helped shape this research and/or for providing comments on the manuscript; and the staff at Tyson Research Center for logistical support. This research was funded by HHMI/SURF and Crescent Hills Research Fund support to JCB and a Tyson Research Center, Washington University in St. Louis postdoctoral fellowship to JRV. Research was conducted according to Washington University IACUC/EH&S protocol # 20050173.

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Authors and Affiliations

  1. Tyson Research Center, Washington University in Saint Louis, One Brookings Drive, Campus Box 1229, St. Louis, MO, 63130-4899, USA

    James R. Vonesh & Julia C. Buck

  2. Department of Biology, Virginia Commonwealth Univesity, 1000 West Cary Street, P.O. Box 842012, Richmond, VA, 23284-2012, USA

    James R. Vonesh

Authors
  1. James R. Vonesh
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  2. Julia C. Buck
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Corresponding author

Correspondence to James R. Vonesh.

Additional information

Communicated by William Resetarits.

An erratum to this article can be found at http://dx.doi.org/10.1007/s00442-008-1166-z

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Below is the link to the electronic supplementary material.

Fig. S1A–D

Arial view of Tyson Research Center illustrating spatial layout of Experiments 1–4. A Overview of Tyson hollow with small circles indicating approximate placement of pools in Experiment 3. Location of real ponds is also indicated (P). Experimental pools were isolated from each other and other ponds by a minimum of 100 m. B Overview of laboratory building and ponds (P) showing placement of five blocks of experimental pools (Exp. 1: blocks 1–5; Exp. 2: blocks 2–3; Exp. 4: blocks 1–3). Each block included an equal number of pools, although the number per block varied among experiments. C Close-up of block 4 during Experiment 1 showing pools and predator enclosures. D Pair of gray treefrogs in amplexus with eggs in an experimental pool (DOC 171 kb)

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Vonesh, J.R., Buck, J.C. Pesticide alters oviposition site selection in gray treefrogs. Oecologia 154, 219–226 (2007). https://doi.org/10.1007/s00442-007-0811-2

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  • DOI: https://doi.org/10.1007/s00442-007-0811-2

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