Influences of the antidepressant fluoxetine on stream ecosystem function and aquatic insect emergence at environmentally realistic concentrations

References

• Arthur JW, Zischke JA, Allen KN, Hermanutz RO. 1983. Effects of diazinon on macroinvertebrates and insect emergence in outdoor experimental channels. Aquat Toxicol. 4(4):283–302.
   Web of Science ®Google Scholar
• Barranguet C, van den Ende FP, Rutgers M, Breure AM, Greijdanus M, Sinke JJ, Admiraal W. 2003. Copper-induced modifications of the trophic relations in riverine algal-bacterial biofilms. Environ Toxicol Chem. 22(6):1340–1349.
   PubMed Web of Science ®Google Scholar
• Baxter CV, Fausch KD, Saunders CW. 2005. Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol. 50(2):201–220.
   Web of Science ®Google Scholar
• Benke AC, Huryn AD, Smock LA, Wallace JB. 1999. Length-mass relationships for freshwater macroinvertebrates in north america with particular reference to the southeastern United States. J N Am Benthol Soc. 18(3):308–343.
   Web of Science ®Google Scholar
• Besemer K, Peter H, Logue JB, Langenheder S, Lindström ES, Tranvik LJ, Battin TJ. 2012. Unraveling assembly of stream biofilm communities. ISME J. 6(8):1459–1468.
   PubMed Web of Science ®Google Scholar
• Boxall ABA, Rudd MA, Brooks BW, Caldwell DJ, Choi K, Hickmann S, Innes E, Ostapyk K, Staveley JP, Verslycke T, et al. 2012. Pharmaceuticals and personal care products in the environment: what are the big questions? Environ Health Perspect. 120(9):1221–1229.
   PubMed Web of Science ®Google Scholar
• Brooks BW, Kevin Chambliss C, Stanley JK, Ramirez A, Banks KE, Johnson RD, Lewis RJ. 2005. Determination of select antidepressants in fish from an effluant dominated stream. Environ Toxicol Chem. 24(2):464–469.
   PubMed Web of Science ®Google Scholar
• Brooks BW, Foran CM, Richards SM, Weston J, Turner PK, Stanley JK, Solomon KR, Slattery M, La Point TW. 2003. Aquatic ecotoxicology of fluoxetine. Toxicol Lett. 142(3):169–183.
   PubMed Web of Science ®Google Scholar
• Bruner KA, Fisher SW, Landrum PF. 1994. The role of the zebra mussel, Dreissena polymorpha, in contaminant cycling: I. The effect of body size and lipid content on the bioconcentration of PCBs and PAHs. J Great Lakes Res. 20(4):725–734.
   Web of Science ®Google Scholar
• Bundy JG, Paton GI, Campbell CD. 2004. Combined microbial community level and single species biosensor responses to monitor recovery of oil polluted soil. Soil Biol Biochem. 36(7):1149–1159.
   Web of Science ®Google Scholar
• Campos B, Rivetti C, Kress T, Barata C, Dircksen H. 2016. Depressing antidepressant: fluoxetine affects serotonin neurons causing adverse reproductive responses in Daphnia magna. Environ Sci Technol. 50(11):6000–6007.
   PubMed Web of Science ®Google Scholar
• Champely S. 2007. PWR: Basic functions for power analysis. R Package Version 1.1. [Computer software]. Available from https://cran.r-project.org/web/packages/pwr/pwr.pdf.
   Google Scholar
• Christian BW, Lind OT. 2006. Key issues concerning biolog use for aerobic and anaerobic freshwater bacterial community-level physiological profiling. Int Rev Hydrobiol. 91(3):257–268.
   Web of Science ®Google Scholar
• Clarke K, Gorley R. 2006. User manual/tutorial. Plymouth: PRIMER-E Ltd.
   Google Scholar
• Cummins KW. 1974. Structure and function of stream ecosystems. BioScience. 24(11):631–641.
   Web of Science ®Google Scholar
• Daughton CG. 2003. Cradle-to-cradle stewardship of drugs for minimizing their environmental disposition while promoting human health. I. Rationale for and avenues toward a green pharmacy. Environ Health Perspect. 111(5):757–774.
   PubMed Web of Science ®Google Scholar
• Daughton CG, Ternes TA. 1999. Pharmaceuticals and personal care products in the environment: agents of subtle change? Environ Health Perspect. 107(suppl 6):907–938.
   PubMed Web of Science ®Google Scholar
• Dewey SL. 1986. Effects of the herbicide atrazine on aquatic insect community structure and emergence. Ecology. 67(1):148–162.
   Web of Science ®Google Scholar
• Drury B, Scott J, Rosi-Marshall EJ, Kelly JJ. 2013. Triclosan exposure increases triclosan resistance and influences taxonomic composition of benthic bacterial communities. Environ Sci Technol. 47(15):8923–8930.
   PubMed Web of Science ®Google Scholar
• Duan M, Gu J, Wang X, Li Y, Li P, Yin Y. 2018. Combined effects of compost containing sulfamethazine and zinc on pakchoi (Brassica chinensis L.) growth, soil sulfonamide resistance genes, and microbial communities. Arch Agron Soil Sci. 64(2):231–243.
   Web of Science ®Google Scholar
• El-Merahbi R, Löffler M, Mayer A, Sumara G. 2015. The roles of peripheral serotonin in metabolic homeostasis. FEBS Lett. 589(15):1728–1734.
   PubMed Web of Science ®Google Scholar
• Ellis RJ, Neish B, Trett MW, Best JG, Weightman AJ, Morgan P, Fry JC. 2001. Comparison of microbial and meiofaunal community analyses for determining impact of heavy metal contamination. J Microbiol Methods. 45(3):171–185.
   PubMed Web of Science ®Google Scholar
• Fisher SG, Likens GE. 1973. Energy flow in Bear Brook, New Hampshire: an integrative approach to stream ecosystem metabolism. Ecol Monogr. 43(4):421–439.
   Web of Science ®Google Scholar
• Fong PP. 1998. Zebra mussel spawning is induced in low concentrations of putative serotonin reuptake inhibitors. Biol Bull. 194(2):143.
   PubMed Web of Science ®Google Scholar
• Ford AT, Fong PP. 2015. The effects of antidepressants appear to be rapid and at environmentally relevant concentrations. Environ Toxicol Chem. 35(4):794–798.
   PubMed Web of Science ®Google Scholar
• Garland JL. 1997. Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol. 24(4):289–300.
   Web of Science ®Google Scholar
• Garland JL, Mills AL. 1991. Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol. 57(8):2351–2359.
   PubMed Web of Science ®Google Scholar
• Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S. 2010. Diversity meets decomposition. Trends Ecol Evol. 25(6):372–380.
   PubMed Web of Science ®Google Scholar
• Grace MR, Giling DP, Hladyz S, Caron V, Thompson RM, Mac Nally R. 2015. Fast processing of diel oxygen curves: estimating stream metabolism with BASE (BAyesian Single-station Estimation). Limnol Oceanogr: Methods. 13(3):103–114.
   Web of Science ®Google Scholar
• Hieber M, Gessner MO. 2002. Contribuitions of stream detrivores, fungi and bacteria to leaf breakdown based on biomass estimates. Ecology. 83(4):1026.
   Web of Science ®Google Scholar
• Hill BH, Herlihy AT, Kaufmann PR. 2002. Benthic microbial respiration in Appalachian Mountain, Piedmont, and Coastal Plains streams of the eastern U.S.A. Freshw Biol. 47(2):185–194.
   Web of Science ®Google Scholar
• Hoppe PD, Rosi-Marshall EJ, Bechtold HA. 2012. The antihistamine cimetidine alters invertebrate growth and population dynamics in artificial streams. Freshw Sci. 31(2):379–388.
   Web of Science ®Google Scholar
• Jonsson M, Ershammar E, Fick J, Brodin T, Klaminder J. 2015. Effects of an antihistamine on carbon and nutrient recycling in streams. Sci Total Environ. 538:240–245.
   PubMed Web of Science ®Google Scholar
• Kalaycı S, Demirci S, Sahin F. 2014. Antimicrobial properties of various psychotropic drugs against broad range microorganisms. Curr Psychopharmacol. 3(3):195–202.
   Google Scholar
• Kiffney PM, Clements WH. 1993. Bioaccumulation of heavy metals by benthic invertebrates at the Arkansas River, Colorado. Environ Toxicol Chem. 12(8):1507–1517.
   Web of Science ®Google Scholar
• Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT. 2002. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. Streams, 1999 − 2000: a national reconnaissance. Environ Sci Technol. 36(6):1202–1211.
   PubMed Web of Science ®Google Scholar
• Krams I, Trakimas G, Kecko S, Elferts D, Krams R, Luoto S, Rantala MJ, Mänd M, Kuusik A, Kekäläinen J, et al. 2018. Linking organismal growth, coping styles, stress reactivity, and metabolism via responses against a selective serotonin reuptake inhibitor in an insect. Sci Rep. 8(1):8599.
   PubMed Web of Science ®Google Scholar
• Kreutzweiser DP, Capell SS. 2003. Benthic microbial utilization of differential dissolved organic matter sources in a forest headwater stream. Can J For Res. 33(8):1444–1451.
   Web of Science ®Google Scholar
• Kwon J-W, Armbrust KL. 2006. Laboratory persistance and fate of fluoxetine in aquatic environments. Environ Toxicol Chem. 25(10):2561–2568.
   PubMed Web of Science ®Google Scholar
• Kwon J-W, Armbrust KL. 2008. Aqueous solubility, n-octanol-water partition coefficient, and sorption of five selective serotonin reuptake inhibitors to sediments and soils. Bull Environ Contam Toxicol. 81(2):128–135.
   PubMed Web of Science ®Google Scholar
• Lass-Flörl C, Fuchs D, Ledochowski M, Speth C, Dierich MP, Würzner R. 2003. Antifungal properties of 5-hydroxytryptamine (serotonin) against Candida species in vitro. J Med Microbiol. 52(2):169–171.
   PubMed Web of Science ®Google Scholar
• Lawrence JR, Swerhone GDW, Wassenaar LI, Neu TR. 2005. Effects of selected pharmaceuticals on riverine biofilm communities. Can J Microbiol. 51(8):655–669.
   PubMed Web of Science ®Google Scholar
• Laws J, Heppell K, Sheahan D, Liu C-F, Grey J. 2016. No such thing as a free meal: organotin transfer across the freshwater–terrestrial interface. Freshw Biol. 61(12):2051–2062.
   Web of Science ®Google Scholar
• Lazzara R, Blázquez M, Porte C, Barata C. 2012. Low environmental levels of fluoxetine induce spawning and changes in endogenous estradiol levels in the zebra mussel Dreissena polymorpha. Aquat Toxicol. 106–107:123–130.
   PubMed Web of Science ®Google Scholar
• Lee SS, Paspalof AM, Snow D, Richmond EK, Rosi-Marshall EJ, Kelly JJ. 2016. Occurrence and potential biological effects of amphetamine on stream communities. Environ Sci Technol. 50(17):9727–9735.
   PubMed Web of Science ®Google Scholar
• Martin JM, Saaristo M, Bertram MG, Lewis PJ, Coggan TL, Clarke BO, Wong BBM. 2017. The psychoactive pollutant fluoxetine compromises antipredator behaviour in fish. Environ Pollut. 222:592–599.
   PubMed Web of Science ®Google Scholar
• Mennigen JA, Stroud P, Zamora JM, Moon TW, Trudeau VL. 2011. Pharmaceuticals as neuroendocrine disruptors: lessons learned from fish on Prozac. J Toxicol Environ Health B. 14(5–7):387–412.
   PubMed Web of Science ®Google Scholar
• Merritt RW, Cummins KW. 1996. An introduction to the aquatic insects of North America. Dubuque, IA: Kendall Hunt.
   Google Scholar
• Minshall GW. 1978. Autotrophy in stream ecosystems. BioScience. 28(12):767–771.
   Web of Science ®Google Scholar
• Monteiro S, Boxall AA. 2010. Occurrence and fate of human pharmaceuticals in the environment reviews of environmental contamination and toxicology. In: Reviews of environmental contamination and toxicology. Vol. 202. New York: Springer; p. 53–154.
   Google Scholar
• Munoz-Bellido JL, Munoz-Criado S, Garcı̀a-Rodrı̀guez JA. 2000. Antimicrobial activity of psychotropic drugs: selective serotonin reuptake inhibitors. Int J Antimicrob Agents. 14(3):177–180.
   PubMed Web of Science ®Google Scholar
• Pelli M, Connaughton VP. 2015. Chronic exposure to environmentally-relevant concentrations of fluoxetine (Prozac) decreases survival, increases abnormal behaviors, and delays predator escape responses in guppies. Chemosphere. 139:202–209.
   PubMed Web of Science ®Google Scholar
• Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., R Core Team. 2009 nlme: linear and nonlinear mixed effects models. R package version 3.1 – 96. [Computer software]
   Google Scholar
• Proia L, Morin S, Peipoch M, Romaní AM, Sabater S. 2011. Resistance and recovery of river biofilms receiving short pulses of Triclosan and Diuron. Sci Total Environ. 409(17):3129–3137.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2014. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.
   Google Scholar
• Rasband W. 1997. ImageJ 2012. Bethesda (MD): US National Institutes of Health.
   Google Scholar
• Reisinger AJ, Rosi EJ, Bechtold HA, Doody TR, Kaushal SS, Groffman PM. 2017. Recovery and resilience of urban stream metabolism following Superstorm Sandy and other floods. Ecosphere. 8(4):e01776.
   Web of Science ®Google Scholar
• Richmond EK, Grace MR, Kelly JJ, Reisinger AJ, Rosi EJ, Walters DM. 2017. Pharmaceuticals and personal care products (PPCPs) are ecological disrupting compounds (EcoDC). Elem Sci Anth. 5:66.
   Web of Science ®Google Scholar
• Richmond EK, Rosi EJ, Walters DM, Fick J, Hamilton SK, Brodin T, Sundelin A, Grace MR. 2018. A diverse suite of pharmaceuticals contaminates stream and riparian food webs. Nat Commun. 9(1):4491.
   PubMed Web of Science ®Google Scholar
• Richmond EK, Rosi-Marshall EJ, Lee SS, Grace MR, Thompson RM. 2016. Antidepressants in stream ecosystems: influence of selective serotonin reuptake inhibitors (SSRIs) on algal production and insect emergence. Freshw Sci. 35(3):845–855.
   Web of Science ®Google Scholar
• Rosi-Marshall EJ, Kincaid DW, Bechtold HA, Royer TV, Rojas M, Kelly JJ. 2013. Pharmaceuticals suppress algal growth and microbial respiration and alter bacterial communities in stream biofilms. Ecol Appl. 23(3):583–593.
   PubMed Web of Science ®Google Scholar
• Rosi-Marshall EJ, Royer TV. 2012. Pharmaceutical compounds and ecosystem function: an emerging research challenge for aquatic ecologists. Ecosystems. 15(6):867–880.
   Web of Science ®Google Scholar
• Schmidt TS, Kraus JM, Walters DM, Wanty RB. 2013. Emergence flux declines disproportionately to larval density along a stream metals gradient. Environ Sci Technol. 47(15):8784–8792.
   PubMed Web of Science ®Google Scholar
• Silva LJG, Pereira AMPT, Meisel LM, Lino CM, Pena A. 2015. Reviewing the serotonin reuptake inhibitors (SSRIs) footprint in the aquatic biota: Uptake, bioaccumulation and ecotoxicology. Environ Pollut. 197:127–143.
   PubMed Web of Science ®Google Scholar
• Stefanowicz A. 2006. The Biolog plates technique as a tool in ecological studies of microbial communities. Pol J Environ Stud. 15(5):669.
   Web of Science ®Google Scholar
• Steinman AD, Lamberti GA, Leavitt PR. 1996. Biomass and pigments of benthic algae. In: FR. Hauer, GA. Lamberti (Eds.), Methods in stream ecology. Vol. 2, (pp. 357–379). Oxford, UK: Elsevier. doi:10.1016/B978-012332908-0.50024-3
   Google Scholar
• Styrishave B, Halling-Sørensen B, Ingerslev F. 2011. Environmental risk assessment of three selective serotonin reuptake inhibitors in the aquatic environment: a case study including a cocktail scenario. Environ Toxicol Chem. 30(1):254–261.
   PubMed Web of Science ®Google Scholar
• Tank JL, Rosi-Marshall EJ, Griffiths NA, Entrekin SA, Stephen ML. 2010. A review of allochthonous organic matter dynamics and metabolism in streams. J N Am Benthol Soc. 29(1):118–146.
   Google Scholar
• Tierney AJ, Hanzlik KN, Hathaway RM, Powers C, Roy M. 2016. Effects of fluoxetine on growth and behavior in the crayfish Orconectes rusticus. Mar Freshw Behav Physiol. 49(2):133–145.
   Web of Science ®Google Scholar
• Webster J, Benfield E. 1986. Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst. 17(1):567–594.
   Google Scholar
• Wetzel RG, Likens GE. 1991. Limnological analyses. New York: Springer Verlag; p. 391.
   Google Scholar
• Wiggins GB. 1996. Larvae of the North American caddisfly genera (Trichoptera). Toronto: University of Toronto Press.
   Google Scholar
• Wong DT, Bymaster FP, Engleman EA. 1995. Prozac (fluoxetine, Lilly 110140), the first selective serotonin uptake inhibitor and an antidepressant drug: twenty years since its first publication. Life Sci. 57(5):411–441.
   PubMed Web of Science ®Google Scholar