Fluoxetine alters adult freshwater mussel behavior and larval metamorphosis

Science of the Total Environment

Volumn 445-446, Issue , 2013, Pages 94-100

  Hazelton, Peter D ^a   Cope, W Gregory ^b   Mosher, Shad ^b   Pandolfo, Tamara J ^b   Belden, Jason B ^c   Barnhart, M Christopher ^d   Bringolf, Robert B ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c OKLAHOMA STATE UNIVERSITY   (United States)

^d MISSOURI STATE UNIVERSITY   (United States)

Author keywords

Behavior; Emerging contaminants; Metamorphosis; Pharmaceuticals; PPCP; Toxicity

Indexed keywords

ADULT FEMALES; BEHAVIOR; EFFECTIVE CONCENTRATION; EMERGING CONTAMINANT; FLUOXETINE; FRESHWATER MUSSELS; METAMORPHOSIS; PPCP;

DRUG PRODUCTS; TOXICITY; WATER;

SHELLFISH;

FLUOXETINE; SURFACE WATER;

BEHAVIORAL RESPONSE; BIVALVE; CONCENTRATION (COMPOSITION); DRUG; LARVAL DEVELOPMENT; METAMORPHOSIS; POLLUTION EFFECT; POLLUTION EXPOSURE; SURVIVAL; TOXICITY;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BIRTH; CONCENTRATION (PARAMETERS); CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EXPOSURE; EMBRYO; FEMALE; FOOT; GLOCHIDIUM; LAMPSILIS FASCIOLA; LAMPSILIS SILIQUOIDEA; LARVA; LIFE CYCLE; LIGUMIA RECTA; MALE; METAMORPHOSIS; MUSSEL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; FLUOXETINE; LARVA; TOXICITY TESTS, ACUTE; UNIONIDAE; WATER POLLUTANTS, CHEMICAL;

GLOCHIDIA; LAMPSILIS FASCIOLA; LAMPSILIS SILIQUOIDEA; LIGUMIA RECTA; UNIONIDAE;

EID: 84872378287     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2012.12.026     Document Type: Article

References (49)

1. Allan J.D. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu Rev Ecol Evol Syst 2004, 35:257-284.
2. ASTM Standard guide for conducting acute toxicity tests on test materials with fishes, macroinvertebrates, and amphibians. Annual Book of ASTM Standards 2006, 729-796. American Society for Testing and Materials, Philadelphia, PA.
3. ASTM Standard guide for conducting laboratory toxicity tests with freshwater mussels. Annual Book of ASTM Standards 2006, 1393-2028. American Society for Testing and Materials, Philadelphia, PA.
4. Augspurger T., Dwyer F.J., Ingersoll C.G., Kane C.M. Advances and opportunities in assessing contaminant sensitivity of freshwater mussel (Unionidae) early life stages. Environ Toxicol Chem 2007, 26:2025-2028.
5. Barnhart M.C. Buckets of muckets: A compact system for rearing juvenile freshwater mussels. Aquaculture 2006, 254:227-233.
6. Barnhart M.C., Haag W.R., Roston W.N. Adaptations to host infection and larval parasitism in Unionoida. J N Am Benthol Soc 2008, 27:370-394.
7. Bates D., Sarkar D. lme4: linear mixed-effects models using S4 classes. R package version 2.14.0 2007.
8. Bianchi M., Panerai A.E. Antidepressant drugs and experimental inflammation. Pharmacol Res 1996, 33:235-238.
9. Bianchi M., Sacerdote P., Panerai A.E. Fluoxetine reduces inflammatory edema in the rat - involvement of the pituitary-adrenal axis. Eur J Pharmacol 1994, 263:81-84.
10. Bolker B.M., Brooks M.E., Clark C.J., Geange S.W., Poulsen J.R., Stevens M.H.H., et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 2009, 24:127-135.
11. Brausch J.M., Rand G.M. A review of personal care products in the aquatic environment: environmental concentrations and toxicity. Chemosphere 2011, 82:1518-1532.
12. Bringolf R.B., Cope W.G., Eads C.B., Lazaro P.R., Barnhart M.C., Shea D. Acute and chronic toxicity of technical-grade pesticides to glochidia and juveniles of freshwater mussels (Unionidae). Environ Toxicol Chem 2007, 26:2086-2093.
13. Bringolf R.B., Heltsley R.M., Newton T.J., Eads C.B., Fraley S.J., Shea D., et al. Environmental occurrence and reproductive effects of the pharmaceutical fluoxetine in native freshwater mussels. Environ Toxicol Chem 2010, 29:1311-1318.
14. Brooks B.W., Foran C.M., Richards S.M., Weston J., Turner P.K., Stanley J.K., et al. Aquatic ecotoxicology of fluoxetine. Toxicol Lett 2003, 142:169-183.
15. Brooks B.W., Turner P.K., Stanley J.K., Weston J.J., Glidewell E.A., Foran C.M., et al. Waterborne and sediment toxicity of fluoxetine to select organisms. Chemosphere 2003, 52:135-142.
16. Campos B., Piña B., Barata C.C. Mechanisms of action of selective serotonin reuptake inhibitors in Daphnia magna. Environ Sci Technol 2012, 46:2943-2950.
17. Cope W.G., Bringolf R.B., Buchwalter D.B., Newton T.J., Ingersoll C.G., Wang N., et al. Differential exposure, duration, and sensitivity of Unionoidean bivalve life stages to environmental contaminants. J N Am Benthol Soc 2008, 27:451-462.
18. Couper J.M., Leise E.M. Serotonin injections induce metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta. Biol Bull 1996, 191:178-186.
19. Cunha E.M., Machado J. Parturition in Anodonta cygnea induced by selective serotonin reuptake inhibitors (SSRIs). Can J Zool 2001, 79:95-100.
20. Daughton C.G. Pharmaceuticals and personal care products in the environment: overarching issues and overview. Pharmaceuticals and care products in the environment 2001, 2-38. American Chemical Society, Washington, DC. C.G. Daughton, T.L. Jones-Lepp (Eds.).
21. Daughton C.G., Ternes T.A. Pharmaceuticals and personal care products in the environment: agents of subtle change?. Environ Health Perspect 1999, 107:907-938.
22. Dowdy S., Weardon S., Chilko S. Statistics for research 2004, Third, Wiley Interscience, Hoboken, NJ.
23. Downing J.A., Van Meter P., Woolnough D.A. Suspects and evidence: a review of the causes of extirpation and decline in freshwater mussels. Anim Biodivers Conserv 2010, 33:151-185.
24. Dubansky B., Whitaker B., Galvez F. Influence of cortisol on the attachment and metamorphosis of larval Utterbackia imbecillis on bluegill sunfish (Lepomis macrochirus). Biol Bull 2011, 220:97-106.
25. Fong P.P. Zebra mussel spawning is induced in low concentrations of putative serotonin reuptake inhibitors. Biol Bull 1998, 194:143-149.
26. Fong P., Molnar N. Norfluoxetine induces spawning and parturition in estuarine and freshwater bivalves. Bull Environ Contam Toxicol 2008, 81:535-538.
27. Fong P.P., Deguchi R., Kyozuka K. Serotonergic ligands induce spawning but not oocyte maturation in the bivalve Mactra chinensis from central Japan. Biol Bull 1996, 191:27-32.
28. Gagne F., Andre C., Blaise C. Increased vitellogenin gene expression in the mussel Elliptio complanata exposed to estradiol-17 beta. Fresenius Environ Bull 2005, 14:861-866.
29. Gardiner D.B., Silverman H., Dietz T.H. Musculature associated with the water canals in fresh-water mussels and response to monoamines in vitro. Biol Bull 1991, 180:453-465.
30. Gust M., Buronfosse T., Giamberini L., Ramil M., Mons R., Garric J. Effects of fluoxetine on the reproduction of two prosobranch mollusks: Potamopyrgus antipodarum and Valvata piscinalis. Environ Pollut 2009, 157:423-429.
31. Hair J.F., Black B., Babin B., Anderson R., Tatham R.L. Multivariate analysis 1998, Prentice Hall, Fifth, Saddle River, NJ.
32. Hazelton P.D., Cope W.G., Pandolfo T.J., Mosher S., Strynar M.J., Barnhart M.C., et al. Partial life-cycle and acute toxicity of perfluoroalkyl acids to freshwater mussels. Environ Toxicol Chem 2012, 31:1611-1620.
33. Henry T.B., Black M.C. Acute and chronic toxicity of fluoxetine (selective serotonin reuptake inhibitor) in western mosquitofish. Arch Environ Contam Toxicol 2008, 54:325-330.
34. Henry T.B., Kwon J.W., Armbrust K.L., Black M.C. Acute and chronic toxicity of five selective serotonin reuptake inhibitors in Ceriodaphnia dubia. Environ Toxicol Chem 2004, 23:2229-2233.
35. Lazzara R., Blazquez M., Porte C., Barata C. Low environmental levels of fluoxetine induce spawning and changes in endogenous estradiol levels in the zebra mussel Dreissena polymorpha. Aquat Toxicol 2012, 106:123-130.
36. Leise E.M., Thavaradhara K., Durham N.R., Turner B.E. Serotonin and nitric oxide regulate metamorphosis in the marine snail Ilyanassa obsoleta. Am Zool 2001, 41:258-267.
37. Leise E.M., Kempf S.C., Durham N.R., Gifondorwa D.J. Induction of metamorphosis in the marine gastropod Ilyanassa obsoleta: 5HT, NO and programmed cell death. Acta Biol Hung 2004, 55:293-300.
38. McMahon R.F., Bogan A.E. Mollusca: bivalvia. Ecology and classification of North American freshwater invertebrates, 2nd 2001, 331-429. Academic Press, San Diego. J.H. Thorp, A.P. Covich (Eds.).
39. Meechonkit P., Kovitvadhi U., Chatchavalvanich K., Sretarugsa P., Weerachatyanukul W. Localization of serotonin in neuronal ganglia of the freshwater pearl mussel, Hyriopsis bialata. J Molluscan Stud 2010, 76:267-274.
40. Pandolfo T.J., Cope W.G., Arellano C., Bringolf R.B., Barnhart M.C., Hammer E. Upper thermal tolerances of early life stages of freshwater mussels. J N Am Benthol Soc 2010, 29:959-969.
41. Péry A.R.R., Gust M., Vollat B., Mons R., Ramil M., Fink G., et al. Fluoxetine effects assessment on the life cycle of aquatic invertebrates. Chemosphere 2008, 73:300-304.
42. R: A language and environment for statistical computing. R package version 2.14.0 2010, R Foundation for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austia.
43. Ram J.L., Moore D., Putchakayala S., Paredes A.A., Ma D., Croll R.P. Serotonergic responses of the siphons and adjacent mantle tissue of the zebra mussel, Dreissena polymorpha. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1999, 124:211-220.
44. Ramirez A.J., Brain R.A., Usenko S., Mottaleb M.A., O'Donnell J.G., Stahl L.L., et al. Occurrence of pharmaceuticals and personal care products in fish: results of a national pilot study in the United States. Environ Toxicol Chem 2009, 28:2587-2597.
45. Strayer D.L., Downing J.A., Haag W.R., King T.L., Layzer J.B., Newton T.J., et al. Changing perspectives on pearly mussels, North America's most imperiled animals. Bioscience 2004, 54:429-439.
46. Ternes T.A., Joss A., Siegrist H. Scrutinizing pharmaceuticals and personal care products in wastewater treatment. Environ Sci Technol 2004, 38:392A-399A.
47. Valenti T.W., Cherry D.S., Neves R.J., Locke B.A., Schmerfeld J.J. Case study: sensitivity of mussel glochidia and regulatory test organisms to mercury and a reference toxicant. Freshwater bivalve ecotoxicology 2007, 351-367. SETAC press, Pensacola, FL. J.L. Farris, J.H. Van Hassel (Eds.).
48. Valenti T.W., Gould G.G., Berninger J.P., Connors K.A., Keele N.B., Prosser K.N., et al. Human therapeutic plasma levels of the selective serotonin reuptake inhibitor (SSRI) sertraline decrease serotonin reuptake transporter binding and shelter-seeking behavior in adult male fathead minnows. Environ Sci Technol 2012, 46:2427-2435.
49. Williams J.D., Warren M.L., Cummings K.S., Harris J.L., Neves R.J. Conservation status of fresh-water mussels of the United States and Canada. Fisheries 1993, 18:6-22.