Burrowing in the Freshwater Mussel Elliptio complanata is Sexually Dimorphic and Feminized by Low Levels of Atrazine

REFERENCES

• Amyot , J.-P. and Downing , J. A. 1991 . Endo- and epibenthic distribution of the Unionid mollusc Elliptio complanata . J. North Am. Benthol. Soc , 10 : 280 – 285 .
   Web of Science ®Google Scholar
• Amyot , J.-P. and Downing , J. A. 1997 . Seasonal variation in vertical and horizontal movement of the freshwater bivalve Elliptio complanata (Mollusca: Unionidae) . Freshwater Biol , 37 : 345 – 354 .
   Web of Science ®Google Scholar
• Balfour , D. L. and Smock , L. A. 1995 . Distribution, age structure, and movements of the freshwater mussel Elliptio complanata (Mollusca: Unionidae) in a headwater stream . J. Freshwater Ecol. , 10 : 255 – 268 .
   Web of Science ®Google Scholar
• Bayley , M. , Nielsen , J. R. and Baatrup , E. 1999 . Guppy sexual behavior as an effect biomarker of estrogen mimics . Ecotoxicol. Environ. Safety , 43 : 68 – 73 .
   PubMed Web of Science ®Google Scholar
• Beresford , N. , Brian , J. V. , Runnalls , T. J. , Sumpter , J. P. and Jobling , S. 2011 . Estrogenic activity of tropical fish food can alter baseline vitellogenin concentrations in male fathead minnow (Pimephales promelas) . Environ. Toxicol. Chem. , 30 : 1139 – 1145 .
   PubMed Web of Science ®Google Scholar
• Bogan , A. E. 1993 . Freshwater bivalve extinctions (Mollusca: Unionoida): A search for causes . Am. Zool. , 33 : 599 – 609 .
   Google Scholar
• Bouchard , B. , Gagné , F. , Fortier , M. and Fournier , M. 2009 . An in-situ study of the impacts of urban wastewater on the immune and reproductive systems of the freshwater mussel Elliptio complanata . Comp. Biochem. Physiol. C Toxicol. Pharmacol. , 150 : 132 – 140 .
   PubMed Web of Science ®Google Scholar
• Central Pine Barrens Joint Planning and Policy Commission. 2013. New York State's Central Pine Barrens. July 22. http://pb.state.ny.us (http://pb.state.ny.us) (Accessed: 19 August 2013 ).
   Google Scholar
• Chen , W.-Y. , Jou , L.-J. , Chen , S.-H. and Liao , C.-M. 2012 . A real-time biomonitoring system to detect arsenic toxicity by valve movement in freshwater clam Corbicula fluminea . Ecotoxicology , 21 : 1177 – 1187 .
   PubMed Web of Science ®Google Scholar
• Ciocan , C. M. , Cubero-Leon , E. , Puinean , A. M. , Hill , E. M. , Minier , C. , Osada , M. , Fenlon , K. and Rotchell , J. M. 2010 . Effects of estrogen exposure in mussels, Mytilus edulis, at different stages of gametogenesis . Environ. Pollut. , 158 : 2977 – 2984 .
   PubMed Web of Science ®Google Scholar
• Clotfelter , E. D. , Bell , A. M. and Levering , K. R. 2004 . The role of animal behaviour in the study of endocrine-disrupting chemicals . Anim. Behav. , 68 : 665 – 676 .
   Web of Science ®Google Scholar
• Coady , K. K. , Murphy , M. M. , Villeneuve , D. L. , Hecker , M. , Jones , P. D. , Carr , J. A. , Solomon , K. R. , Smith , E. E. , van der Kraak , G. , Kendall , R. J. and Giesy , J. P. 2004 . Effects of atrazine on metamorphosis, growth, and gonadal development in the green frog (Rana clamitans) . J. Toxicol. Environ. Health A , 67 : 941 – 957 .
   PubMed Web of Science ®Google Scholar
• Corvi , M. M. , Stanle , K. A. , Peterson , T. S. , Kent , M. L. , Feist , S. W. , La Du , J. K. , Volz , D. C. , Hosmer , A. J. and Tanguay , R. L. 2012 . Investigating the impact of chronic atrazine exposure on sexual development in zebrafish . Birth Defects Res. B Dev. Reprod. Toxicol. , 95 : 276 – 288 .
   PubMed Web of Science ®Google Scholar
• de Campos Ventura , B. , de Fransceschi de Angelis , D. and Aparecida Marin-Morales , M. 2008 . Mutagenic and genotoxic effects of the atrazine herbicide in Oreochromis niloticus (Perciformes, Cichlidae) detected by the micronuclei test and the comet assay . Pestic. Biochem. Physiol. , 90 : 42 – 51 .
   Web of Science ®Google Scholar
• del Carmen Alvarez , M. and Fuiman , L. A. 2005 . Environmental levels of atrazine and its degradation products impair survival skills and growth of red drum larvae . Aquat. Toxicol. , 74 : 229 – 241 .
   PubMed Web of Science ®Google Scholar
• Downing , J. A. , Amyot , J.-P. , Pérusse , M. and Rochon , Y. 1989 . Visceral sex, hermaphroditism and protandry in a population of the freshwater bivalve Elliptio complanata . J. North Am. Benthol. Soc. , 8 : 92 – 99 .
   Web of Science ®Google Scholar
• Fan , W. , Yanase , T. , Morinaga , H. , Gondo , S. , Okabe , T. , Nomura , M. , Komatsu , T. , Morohashi , K. , Hayes , T. B. , Takayanagi , R. and Nawata , H. 2007 . Atrazine-induced aromatase expression is SF-1 dependent: Implications for endocrine disruption in wildlife and reproductive cancers in humans . Environ. Health Perspect. , 115 : 720 – 727 .
   PubMed Web of Science ®Google Scholar
• Flynn , K. and Spellman , T. 2009 . Environmental levels of atrazine decrease spatial aggregation in the freshwater mussel, Elliptio complanata . Ecotoxicol. Environ. Safety , 72 : 1228 – 1233 .
   PubMed Web of Science ®Google Scholar
• Gagné , F. , André , C. and Blaise , C. 2005 . Increased vitellogenin gene expression in the mussel Elliptio complanata exposed to estradiol-17β . Fresenius Environ. Bull. , 14 : 861 – 866 .
   Web of Science ®Google Scholar
• Gagné , F. and Blaise , C. 2003 . “ Biomarkers to assess endocrine disruption or reproduction in bivalves ” . In In vitro methods in aquatic toxicology , Edited by: Mothensill , C. and Austin , B. 221 – 240 . Chichester , , UK : Praxis Publishing .
   Google Scholar
• Gagné , F. , Blaise , C. , Salazar , M. , Salazar , S. and Hansen , P. D. 2001 . Evaluation of estrogenic effects of municipal effluents to the freshwater mussel . Elliptio complanata. Comp. Biochem. Physiol. C Toxicol. Pharmacol , 128 : 213 – 225 .
   PubMed Web of Science ®Google Scholar
• Gagné , F. , Bouchard , B. , André , C. , Farcy , E. and Fournier , M. 2011 . Evidence of feminization in wild Elliptio complanata mussels in the receiving waters downstream of a municipal effluent outfall . Comp. Biochem. Physiol. C Toxicol. Pharmacol. , 153 : 99 – 106 .
   PubMed Web of Science ®Google Scholar
• Garden City Park Water District. 2006. 2006 Water quality report. May. http://www.gcpwater.org/wq.html (http://www.gcpwater.org/wq.html) (Accessed: 19 August 2013 ).
   Google Scholar
• Gioiosa , L. , Fissore , E. , Ghirardelli , G. , Parmigiani , S. and Palanza , P. 2007 . Developmental exposure to low-dose estrogenic endocrine disruptors alters sex differences in exploration and emotional responses in mice . Horm. Behav. , 52 : 307 – 316 .
   PubMed Web of Science ®Google Scholar
• Gluth , G. , Freitag , D. , Hanke , W. and Korte , F. 1985 . Accumulation of pollutants in fish . Comp. Biochem. Physiol. , 81 : 273 – 277 .
   Google Scholar
• Graymore , M. , Stagnitti , F. and Allinson , G. 2001 . Impacts of atrazine in aquatic ecosystems . Environ. Int. , 26 : 483 – 495 .
   PubMed Web of Science ®Google Scholar
• Griggs , J. L. and Belden , L. K. 2008 . Effects of atrazine and metolachlor on the survivorship and infectivity of Echinostoma trivolvis Trematode Cercariae . Arch. Environ. Contam. Toxicol. , 54 : 195 – 202 .
   PubMed Web of Science ®Google Scholar
• Hallgren , P. , Mårtensson , L. and Mathiasson , L. 2009 . Improved spectrophotometric vitellogenin determination via alkali-labile phosphate in fish plasma—A cost effective approach for assessment of endocrine disruption . Int. J. Environ. Anal. Chem. , 89 : 1023 – 1042 .
   Web of Science ®Google Scholar
• Hayes , T. B. , Collins , A. , Lee , M. , Mendoza , M. , Noriega , N. , Stuart , A. A. and Vonk , A. 2002 . Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses . Proc. Natl. Acad. Sci. USA , 99 : 5476 – 5480 .
   PubMed Web of Science ®Google Scholar
• Hayes , T. B. , Stuart , A. A. , Mendoza , M. , Collins , A. , Noriega , N. , Vonk , A. , Johnston , G. , Liu , R. and Kpodzo , D. 2006 . Characterization of atrazine-induced gonadal malformations in African clawed frogs (Xenopus laevis) and comparisons with effects of an androgen antagonist (cyproterone acetate) and exogenous estrogen (17β-estradiol): Support for the demasculinization/feminization hypothesis . Environ. Health Perspect. , 114 : 134 – 141 .
   PubMed Web of Science ®Google Scholar
• Hecker , M. , Kim , W. J. , Park , J.-W. , Murphy , M. B. , Villeneuve , D. , Coady , K. K. , Jones , P. D. , Solomon , K. R. , Van Der Kraak , G. , Carr , J. A. , Smith , E. E. , du Preez , L. , Kendall , R. J. and Giesy , J. P. 2005 . Plasma concentrations of estradiol and testosterone, gonadal aromatase activity and ultrastructure of the testis in Xenopus laevis exposed to estradiol or atrazine . Aquat. Toxicol. , 72 : 383 – 396 .
   PubMed Web of Science ®Google Scholar
• Herrel , A. , Gonwouo , L. N. , Fokam , E. B. , Ngundu , W. I. and Bonneaud , C. 2012 . Intersexual differences in body shape and locomotor performance in the aquatic frog . Xenopus tropicalis. J. Zool , 287 : 311 – 316 .
   Google Scholar
• Holloway , A. C. , Anger , D. A. , Crankshaw , D. J. , Wu , M. and Foster , W. G. 2008 . Atrazine-induced changes in aromatase activity in estrogen sensitive target tissues . J. Appl. Toxicol. , 28 : 260 – 270 .
   PubMed Web of Science ®Google Scholar
• Huber , W. 1993 . Ecological relevance of atrazine in aquatic systems . Environ. Toxicol. Chem. , 12 : 1865 – 1881 .
   Web of Science ®Google Scholar
• Jordaens , K. , Dillen , L. and Backeljau , T. 2009 . Shell shape and mating behaviour in pulmonate gastropods (Mollusca) . Biol. J. Linn. Soc. Lond. , 96 : 306 – 321 .
   Web of Science ®Google Scholar
• Kadar , E. , Salanki , J. , Jugdaohsingh , R. , Powell , J. J. , McCrohan , C. R. and White , K. N. 2001 . Avoidance responses to aluminum in the freshwater bivalve . Anodonta cygnea. Aquat Toxicol , 55 : 137 – 148 .
   PubMed Web of Science ®Google Scholar
• Kat , P. W. 1983 . Sexual selection and simultaneous hermaphroditism among the Unionidae (Bivalvia: Mollusca) . J. Zool. , 201 : 395 – 416 .
   Web of Science ®Google Scholar
• Kontreczky , C. , Farkas , A. , Nemcsok , J. and Salanki , J. 1997 . Short- and long-term effects of deltamethrin on filtering activity of freshwater mussel (Anodonta cygnea L) . Ecotoxicol. Environ. Safety , 38 : 195 – 199 .
   PubMed Web of Science ®Google Scholar
• LaFiandra , E. M. , Babbitt , K. J. and Sower , S. A. 2008 . Effects of atrazine on anuran development are altered by the presence of a nonlethal predator . J. Toxicol. Environ. Health A , 71 : 505 – 511 .
   PubMed Web of Science ®Google Scholar
• Martin , J.-R. 2004 . A portrait of locomotor behaviour in Drosophila determined by a video-tracking paradigm . Behav. Processes , 67 : 207 – 219 .
   PubMed Web of Science ®Google Scholar
• Mazzanti , L. , Rice , C. , Bialek , K. , Sparling , D. , Stevenson , C. , Johnson , W. E. , Kangas , P. and Rheinstein , J. 2003 . Aqueous-phase disappearance of atrazine, metolachor, and chlorpyrifos in laboratory aquaria and outdoor macrocosms . Arch. Environ. Contam. Toxicol. , 44 : 67 – 76 .
   PubMed Web of Science ®Google Scholar
• Myers , J. P. , Zoeller , R. T. and vom Saal , F. S . 2009 . A clash of old and new scientific concepts in toxicity, with important implications for public health . Environ. Health Perspect. , 117 : 1652 – 1655 .
   PubMed Web of Science ®Google Scholar
• Orlando , E. F. and Guillette , L. J. Jr. 2007 . Sexual dimorphic responses in wildlife exposed to endocrine disrupting chemicals . Environ. Res. , 104 : 163 – 173 .
   PubMed Web of Science ®Google Scholar
• Pampanin , D. M. , Maragon , I. , Volpato , E. , Campesan , G. and Nasci , C. 2005 . Stress biomarkers and alkali-labile phosphate level in mussels (Mytilus galloprovincialis) collected in the urban area of Venice (Venice Lagoon, Italy) . Environ. Pollut. , 136 : 103 – 107 .
   PubMed Web of Science ®Google Scholar
• Pandey , R. B. , Adams , G. L. and Warren , L. W. 2011 . Survival and precopulatory guarding behavior of Hyalella azteca (Amphipoda) exposed to nitrate in the presence of atrazine . Environ. Toxicol. Chem. , 30 : 1170 – 1177 .
   PubMed Web of Science ®Google Scholar
• Phelps , H. L. , Hardy , J. T. , Pearson , W. H. and Apts , C. W. 1983 . Clam burrowing behaviour: Inhibition by copper-enriched sediment . Mar. Pollut. Bull. , 14 : 452 – 455 .
   Web of Science ®Google Scholar
• Phyu , Y. L. , Warne , M. S. and Lim , R. P. 2005 . Toxicity and bioavailability of atrazine and molinate to the freshwater shrimp (Paratya australiensis) under laboratory and simulated field conditions . Ecotoxicol. Environ. Safety , 60 : 113 – 122 .
   PubMed Web of Science ®Google Scholar
• Quinn , B. , Gagné , F. , Costello , M. , McKenzie , C. , Wilson , J. and Mothersill , C. 2004 . The endocrine disrupting effect of municipal effluent on the zebra mussel (Dreissena polymorpha) . Aquat. Toxicol. , 66 : 279 – 292 .
   PubMed Web of Science ®Google Scholar
• Rochette , R. , Maltais , M. J. , Dill , L. M. and Himmelman , J. H. 1999 . Interpopulation and context-related differences in responses of a marine gastropod to predation risk . Anim. Behav. , 57 : 977 – 987 .
   PubMed Web of Science ®Google Scholar
• Rohr , J. R. and McCoy , K. A. 2010 . A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians . Environ. Health Perspect. , 118 : 20 – 32 .
   PubMed Web of Science ®Google Scholar
• Roper , D. S. and Hickey , C. W. 1994 . Behavioural responses of the marine bivalve Macoma liliana exposed to copper- and chlordane-dosed sediments . Mar. Biol. , 118 : 673 – 680 .
   Web of Science ®Google Scholar
• Saarinen , M. and Taskinen , J. 2003 . Burrowing and crawling behaviour of three species of Unionidae in Finland . J. Mollusk Stud. , 69 : 81 – 86 .
   Web of Science ®Google Scholar
• Schwalb , A. N. and Pusch , M. T. 2007 . Horizontal and vertical movements of unionid mussels in a lowland river . J. North Am. Benthol. Soc. , 26 : 261 – 272 .
   Web of Science ®Google Scholar
• Smale , L. , Nunes , S. and Holekamp , K. E. 1997 . Sexually dimorphic dispersal in mammals: Patterns, causes, and consequences . Adv. Study Behav. , 26 : 181 – 250 .
   Web of Science ®Google Scholar
• Stefano , G. B. , Cadet , P. , Mantione , K. , Cho , J. J. , Jones , D. and Zhu , W. 2003 . Estrogen signaling at the cell surface coupled to nitric oxide release in Mytilus edulis nervous system . Endocrinology , 144 : 1234 – 1240 .
   PubMed Web of Science ®Google Scholar
• Storrs , S. I. and Kiesecker , J. M. 2004 . Survivorship patterns of larval amphibians exposed to low concentrations of atrazine . Environ. Health Perspect. , 112 : 1054 – 1057 .
   PubMed Web of Science ®Google Scholar
• Tran , D. , Fournier , E. , Durrieu , G. and Massabuau , J.-C. 2003 . Copper detection in the Asiatic clam Corbicula fluminea: Optimum valve closure response . Aquat. Toxicol. , 65 : 317 – 327 .
   PubMed Web of Science ®Google Scholar
• Tran , D. , Haberkorn , H. , Soudant , P. , Ciret , P. and Massabuau , J.-C. 2010 . Behavioral responses of Crassostrea gigas exposed to the harmful algae . Alexandrium minutum. Aquaculture , 298 : 338 – 345 .
   Google Scholar
• U.S. Environmental Protection Agency . 2003 . Interim reregistration eligibility decision for atrazine Washington , DC. Case no. 0062
   Google Scholar
• Vaughn , C. C. and Hakenkamp , C. C. 2001 . “ The functional role of burrowing bivalves in freshwater ecosystems ” . In Freshwater Biol. Vol. 46 , 1431 – 1446 .
   Google Scholar
• Vaughn , C. C. , Nichols , S. J. and Spooner , D. E. 2008 . Community and foodweb ecology of freshwater mussels . J. North Am. Benthol. Soc. , 27 : 409 – 423 .
   Web of Science ®Google Scholar
• Watters , G. T. , O'Dee , S. H. and Chordas , S. 2001 . Patterns of vertical migration in freshwater mussels (Bivalvia: Unionoida) . J. Freshwater Ecol. , 16 : 541 – 549 .
   Web of Science ®Google Scholar
• Widarto , T. H. 2009 . Shell form variation of a freshwater mussel Velesunio ambiguus Philippi from the Ross River, Australia . HAYATI J. Biosci. , 14 : 98 – 104 .
   Google Scholar
• Won , S.-J. , Novillo , A. , Rie , M. T. , Fitzgerald , K. , Osada , M. and Callard , I. P. 2005 . The freshwater mussel (Elliptio complanata) as a sentinel species: Vitellogenin and steroid receptors . Int. Comp. Biol. , 45 : 72 – 80 .
   PubMed Web of Science ®Google Scholar
• Yang , L. , Zha , J. , Zhang , X. , Li , W. , Li , Z. and Wang , Z. 2010 . Alterations in mRNA expression of steroid receptors and heat shock proteins in the liver of rare minnow (Grobiocypris rarus) exposed to atrazine and p,p’-DDE . Aquat. Toxicol. , 98 : 381 – 387 .
   PubMed Web of Science ®Google Scholar
• Zieritz , A. and Aldridge , D. C. 2011 . Sexual, habitat-constrained and parasite-induced dimorphism in the shell of a freshwater mussel (Anodonta anatina, Unionidae) . J. Morphol. , 272 : 1365 – 1375 .
   PubMed Web of Science ®Google Scholar