Fluoxetine alters adult freshwater mussel behavior and larval metamorphosis.

We used acute and partial-lifecycle tests to examine the effects of the pharmaceutical fluoxetine on freshwater mussels (Unionida). In acute tests lasting 24-48 h, we determined median effective concentrations (EC50s) for fluoxetine with larval (glochidia viability) and juvenile (survival) life-stages of fatmucket (Lampsilis siliquoidea) and black sandshell (Ligumia recta). In a 28-d behavioral test we exposed brooding adult female wavy-rayed lampmussels (Lampsilis fasciola) to 0.37 and 29.3 μg/L fluoxetine to determine effects on adult behavior (foot protrusion, mantle lure display and glochidia parturition). We also assessed the effects of 24-h exposure of 1 and 100 μg/L fluoxetine on glochidia viability duration and metamorphosis success for the wavy-rayed lampmussel. Fluoxetine EC50s ranged from 62 μg/L for juveniles (96 h) to 293 μg/L for glochidia (24 h). In adults, statistically significant increases were observed in foot protrusion at 0.37 and 29.3 μg/L fluoxetine and lure display rates at 29.3 μg/L; glochidia parturition was not significantly affected at any test concentration. Twenty-four hour exposure of glochidia to fluoxetine did not affect viability duration, but likelihood of metamorphosis to the juvenile stage significantly increased with 1 and 100 μg/L treatments. Our results demonstrated effects of fluoxetine to unionid mussels at concentrations less than previously reported and approaching concentrations measured in surface waters.

[1]  T. Newton,et al.  Environmental occurrence and reproductive effects of the pharmaceutical fluoxetine in native freshwater mussels , 2010, Environmental toxicology and chemistry.

[2]  T. Ternes,et al.  Pharmaceuticals and personal care products in the environment: agents of subtle change? , 1999, Environmental health perspectives.

[3]  R. Croll,et al.  Serotonergic responses of the siphons and adjacent mantle tissue of the zebra mussel, Dreissena polymorpha. , 1999, Comparative biochemistry and physiology. Part C, Pharmacology, toxicology & endocrinology.

[4]  P. Fong,et al.  Norfluoxetine Induces Spawning and Parturition in Estuarine and Freshwater Bivalves , 2008, Bulletin of environmental contamination and toxicology.

[5]  S. Mosher,et al.  Partial life‐cycle and acute toxicity of perfluoroalkyl acids to freshwater mussels , 2012, Environmental toxicology and chemistry.

[6]  J. Garric,et al.  Effects of fluoxetine on the reproduction of two prosobranch mollusks: Potamopyrgus antipodarum and Valvata piscinalis. , 2009, Environmental pollution.

[7]  C. Arellano,et al.  Upper thermal tolerances of early life stages of freshwater mussels , 2010, Journal of the North American Benthological Society.

[8]  M. Slattery,et al.  Waterborne and sediment toxicity of fluoxetine to select organisms. , 2003, Chemosphere.

[9]  A R R Péry,et al.  Fluoxetine effects assessment on the life cycle of aquatic invertebrates. , 2008, Chemosphere.

[10]  J. Downing,et al.  Suspects and evidence: a review of the causes of extirpation and decline in freshwater mussels , 2010, Animal Biodiversity and Conservation.

[11]  M. Barnhart.  Buckets of muckets: A compact system for rearing juvenile freshwater mussels , 2006 .

[12]  P. Sacerdote,et al.  Fluoxetine reduces inflammatory edema in the rat: involvement of the pituitary-adrenal axis. , 1994, European journal of pharmacology.

[13]  B. Campos,et al.  Mechanisms of action of selective serotonin reuptake inhibitors in Daphnia magna. , 2012, Environmental science & technology.

[14]  Jacob K Stanley,et al.  Aquatic ecotoxicology of fluoxetine. , 2003, Toxicology letters.

[15]  G. Duca,et al.  Pharmaceuticals and Personal Care Products in the Environment , 2009 .

[16]  C. Barata,et al.  Low environmental levels of fluoxetine induce spawning and changes in endogenous estradiol levels in the zebra mussel Dreissena polymorpha. , 2012, Aquatic toxicology.

[17]  F. J. Dwyer,et al.  Standard guide for conducting laboratory toxicity tests with freshwater mussels , 2006 .

[18]  Alejandro J. Ramirez,et al.  Occurrence of pharmaceuticals and personal care products in fish: Results of a national pilot study in the united states , 2009, Environmental toxicology and chemistry.

[19]  E. Leise,et al.  Induction of Metamorphosis in the Marine Gastropod Ilyanassa Obsoleta: 5HT, No and Programmed Cell Death , 2004, Acta biologica Hungarica.

[20]  Wendell R. Haag,et al.  Adaptations to host infection and larval parasitism in Unionoida , 2008, Journal of the North American Benthological Society.

[21]  William A. Brenneman.  Statistics for Research , 2005, Technometrics.

[22]  J. Allan.  Landscapes and Riverscapes: The Influence of Land Use on Stream Ecosystems , 2004 .

[23]  F. J. Dwyer,et al.  Differential exposure, duration, and sensitivity of unionoidean bivalve life stages to environmental contaminants , 2008, Journal of the North American Benthological Society.

[24]  Mollie E. Brooks,et al.  Generalized linear mixed models: a practical guide for ecology and evolution. , 2009, Trends in ecology & evolution.

[25]  F. J. Dwyer,et al.  Advances and opportunities in assessing contaminant sensitivity of freshwater mussel (unionidae) early life stages , 2007, Environmental toxicology and chemistry.

[26]  W. Weerachatyanukul,et al.  Localization of serotonin in neuronal ganglia of the freshwater pearl mussel, Hyriopsis (Hyriopsis) bialata , 2010 .

[27]  T. Henry,et al.  Acute and Chronic Toxicity of Fluoxetine (Selective Serotonin Reuptake Inhibitor) in Western Mosquitofish , 2008, Archives of environmental contamination and toxicology.

[28]  H Silverman,et al.  Musculature Associated with the Water Canals in Freshwater Mussels and Response to Monoamines In Vitro. , 1991, The Biological bulletin.

[29]  Adriano Joss,et al.  Scrutinizing pharmaceuticals and personal care products in wastewater treatment. , 2004, Environmental science & technology.

[30]  E. Leise,et al.  Serotonin Injections Induce Metamorphosis in Larvae of the Gastropod Mollusc Ilyanassa obsoleta. , 1996, The Biological bulletin.

[31]  R. Neves,et al.  Case Study: Sensitivity of Mussel Glochidia and Regulatory Test Organisms to Mercury and a Reference Toxicant , 2006 .

[32]  Kristin A Connors,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. , 2012, Environmental science & technology.

[33]  F. Galvez,et al.  Influence of Cortisol on the Attachment and Metamorphosis of Larval Utterbackia imbecillis on Bluegill Sunfish (Lepomis macrochirus) , 2011, The Biological Bulletin.

[34]  P. Fong,et al.  Zebra Mussel Spawning Is Induced in Low Concentrations of Putative Serotonin Reuptake Inhibitors. , 1998, The Biological bulletin.

[35]  K. Armbrust,et al.  Acute and chronic toxicity of five selective serotonin reuptake inhibitors in Ceriodaphnia dubia , 2004, Environmental toxicology and chemistry.

[36]  DAVID L. STRAYER,et al.  Changing Perspectives on Pearly Mussels, North America's Most Imperiled Animals , 2004 .

[37]  K. Kyozuka,et al.  Serotonergic Ligands Induce Spawning but not Oocyte Maturation in the Bivalve Mactra chinensis from Central Japan. , 1996, The Biological bulletin.

[38]  Kevin S. Cummings,et al.  Conservation Status of Freshwater Mussels of the United States and Canada , 1993 .

[39]  N. L. Johnson,et al.  Multivariate Analysis , 1958, Nature.

[40]  W. Cope,et al.  Acute and chronic toxicity of technical‐grade pesticides to glochidia and juveniles of freshwater mussels (unionidae) , 2007, Environmental toxicology and chemistry.

[41]  J. Machado,et al.  Parturition in Anodonta cygnea induced by selective serotonin reuptake inhibitors (SSRIs) , 2001 .

[42]  A. Panerai,et al.  Antidepressant drugs and experimental inflammation. , 1996, Pharmacological research.

[43]  J. Brausch,et al.  A review of personal care products in the aquatic environment: environmental concentrations and toxicity. , 2011, Chemosphere.