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The effects of atrazine on spotted salamander embryos and their symbiotic alga

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Abstract

Worldwide amphibian declines have been a concern for biologists for the past several decades. The causes of such declines may include habitat loss, invasive species, pathogens, and man-made chemicals. Agricultural herbicides, in particular, are known to interfere with reproduction in amphibians and are likely contributing to population declines. We tested the effects of the herbicide atrazine on developing spotted salamanders (Ambystoma maculatum) and their symbiotic green alga Oophila amblystomatis. We exposed spotted salamander egg masses to atrazine at concentrations of 0 μg/L (control), 50, 100, 200, and 400 μg/L. Algae were eliminated in all atrazine treatments. Hatching success was significantly lower for atrazine-treated egg masses than for the controls, and was inversely related to atrazine concentration. The highest developmental stage reached by the embryos was significantly lower in the atrazine treatments than in the controls, and was inversely related to atrazine concentration. These results indicate that atrazine exposure affected spotted salamanders both directly by causing pathologies and mortality in embryos and indirectly by eliminating their symbiotic alga.

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References

  • Adolph EF (1979) Development of dependence on oxygen in embryo salamanders. Am J Physiol 236:R282–R291

    CAS  Google Scholar 

  • Allran JW, Karasov WH (2001) Effects of atrazine on embryos, larvae, and adults of anuran amphibians. Environ Toxicol Chem 20:769–775

    Article  CAS  Google Scholar 

  • Bachmann MD, Carlton RG, Burkholder JM, Wetzel RG (1986) Symbiosis between salamander eggs and green algae: microelectrode measurements inside eggs demonstrate effect of photosynthesis on oxygen concentration. Can J Zool 64:1586–1588

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Butler GL, Deason TR, O’Kelley J (1975) The effect of atrazine, 2, 4-d, methoxychlor, carbaryl, and diazion on the growth of planktonic algae. Br Phycol J 10:371–376

    Article  Google Scholar 

  • Capel PD, Larson SJ (2001) Effect of scale on the behavior of atrazine in surface waters. Environ Sci Technol 35:648–657

    Article  CAS  Google Scholar 

  • Chivers DP, Kiesecker JM, De Marco A, Vito J, Anderson MT, Blaustein AR (2001) Predator-induced life history changes in amphibians: egg predation induces hatching. Oikos 92:135–142

    Article  Google Scholar 

  • Davidson C, Shafer HB, Jennings MR (2002) Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conserv Biol 16:1588–1601

    Article  Google Scholar 

  • Detwiler SR, Copenhaver WM (1940) The developmental behavior of Ambystoma eggs subjected to atmospheres of low oxygen and high carbon dioxide. Am J Anat 66:393–410

    Article  CAS  Google Scholar 

  • Forson D, Storfer A (2006a) Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecol Appl 16:2325–2332

    Article  Google Scholar 

  • Forson D, Storfer A (2006b) Effects of atrazine and iridovirus infection on survival and life-history traits of the long-toed salamander (Ambystoma macrodactylum). Environ Toxicol Chem 25:168–173

    Article  CAS  Google Scholar 

  • Freeman JL, Rayburn AL (2005) Developmental impact of atrazine on metamorphosing Xenopus laevis as revealed by nuclear analysis and morphology. Environ Toxicol Chem 24:1648–1653

    Article  CAS  Google Scholar 

  • Gatz AJ (1973) Algal entry into the eggs of Ambystoma maculatum. J Herpetol 7:137–138

    Article  Google Scholar 

  • Gilbert PW (1942) Observations on the eggs of Ambystoma maculatum with especial reference to the green algae found within the egg envelopes. Ecology 23:215–227

    Article  Google Scholar 

  • Gilbert PW (1944) The alga–egg relationship in Ambystoma maculatum, a case of symbiosis. Ecology 25:366–369

    Article  Google Scholar 

  • Harrison RG (1969) Harrison stages and description of the normal development of the spotted salamander, Ambystoma punctatum (Linn.). In: Harrison RG (ed) Organization and development of the embryo. Yale University Press, New Haven, pp 44–66

    Google Scholar 

  • Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, Vonk A (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci 99:5476–5480

    Article  CAS  Google Scholar 

  • Hayes TB, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A (2003) Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana pipiens): laboratory and field evidence. Environ Health Perspect 111:568–575

    CAS  Google Scholar 

  • Hutchison VH, Hammen CS (1958) Oxygen utilization in the symbiosis of embryos of the salamander, Ambystoma maculatum and the alga, Oophila amblystomatis. Biol Bull 155:483–489

    Article  Google Scholar 

  • Isensee AR, Nash RG, Helling CS (1990) Effect of conventional vs no-tillage on pesticide leaching to shallow groundwater. J Environ Qual 19:434–440

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lannoo M (ed) (2005) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley

    Google Scholar 

  • Larson DL, McDonald S, Fivizzani AJ, Newton WE, Hamilton SJ (1998) Effects of herbicide atrazine on Ambystoma tigrinum metamorphosis: duration, larval growth, and hormonal response. Physiol Zool 71:671–679

    CAS  Google Scholar 

  • Marco A, Blaustein AR (2000) Symbiosis with green algae affects survival and growth of northwestern salamander embryos. J Herpetol 34:617–621

    Article  Google Scholar 

  • Miller SM, Sweet CW, Depinto JV, Hornbuckle KC (2000) Atrazine and nutrients in precipitation: results from the Lake Michigan mass balance study. Environ Sci Technol 34:55–61

    Article  CAS  Google Scholar 

  • Mills NE, Barnhart MC (1999) Effects of hypoxia on embryonic development in two Ambystoma and two Rana species. Physiol Biochem Zool 72:179–188

    Article  CAS  Google Scholar 

  • Muller SR, Berg M, Ulrich MM, Schwarzenbach RP (1997) Atrazine and its primary metabolites in Swiss lakes: input characteristics and long-term behavior in the water column. Environ Sci Technol 31:2104–2113

    Article  Google Scholar 

  • Orr H (1888) Note on the development of amphibians, chiefly concerning the central nervous system; with additional observations on the hypophysis, mouth, and the appendages and skeleton of the head. Q J Microsc Sci 29:295–324

    Google Scholar 

  • Pinder AW, Friet SC (1994) Oxygen transport in egg masses of the amphibians Rana sylvatica and Ambystoma maculatum: convection, diffusion, and oxygen production by algae. J Exp Biol 197:17–30

    Google Scholar 

  • Rehage JS, Lynn SG, Hammond JI, Palmer BD, Sih A (2002) Effects of larval exposure to triphenyltin on the survival, growth, and behavior of larval and juvenile Ambystoma barbouri salamanders. Environ Toxicol Chem 21:807–815

    CAS  Google Scholar 

  • Relyea RA (2004) Growth and survival of five amphibian species exposed to combinations of pesticides. Environ Toxicol Chem 23:1737–1742

    Article  CAS  Google Scholar 

  • Relyea RA (2005a) The lethal impacts of roundup and predatory stress on six species of North American tadpoles. Arch Environ Contam Toxicol 48:351–357

    Article  CAS  Google Scholar 

  • Relyea RA (2005b) The lethal impact of roundup on aquatic and terrestrial amphibians. Ecol Appl 15:1118–1124

    Article  Google Scholar 

  • Relyea RA (2006) The effects of pesticides, pH, and predatory stress on amphibians under mesocosm conditions. Ecotoxicology 15:503–511

    Article  CAS  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 98:2491–2496

    Article  CAS  Google Scholar 

  • Relyea RA, Schoeppner NM, Hoverman JT (2005) Pesticides and amphibians: the importance of community context. Ecol Appl 15:1125–1134

    Article  Google Scholar 

  • Rohr JR, Palmer BD (2005) Aquatic herbicide exposure increases salamander desiccation risk eight months later in a terrestrial environment. Environ Toxicol Chem 24:1253–1258

    Article  CAS  Google Scholar 

  • Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy TM, Niedzwiecki JH, Sager T, Sih A, Palmer BD (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  Google Scholar 

  • Rohr JR, Elskus AA, Shepherd BS, Crowley PH, McCarthy 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

    Article  Google Scholar 

  • Savage WK, Zamudio KR (2005) Ambystoma maculatum (Shaw 1802) spotted salamander. In: Lannoo M (ed) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley, pp 621–627

    Google Scholar 

  • 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 306:1783–1786

    Article  CAS  Google Scholar 

  • Valls JH, Mills NE (2007) Intermittent hypoxia in eggs of Ambystoma maculatum: embryonic development and egg capsule conductance. J Exp Biol 210:2430–2435

    Article  Google Scholar 

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Acknowledgments

We conducted this study with IACUC approval (No. 2008-8717-015). For help, facilities, and supplies, we thank Cory Birdsong, Joey Bennett, Dr. Jeff Boundy, Dr. Paul Leberg, Dr. Paul Klerks, Wayne Olivier, and the Center for Ecology and Environmental Technology at UL Lafayette. For funding we thank the Louisiana Department of Wildlife and Fisheries and the UL Lafayette Graduate Student Organization.

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Correspondence to Heather M. Olivier.

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Olivier, H.M., Moon, B.R. The effects of atrazine on spotted salamander embryos and their symbiotic alga. Ecotoxicology 19, 654–661 (2010). https://doi.org/10.1007/s10646-009-0437-8

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  • DOI: https://doi.org/10.1007/s10646-009-0437-8

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