Effects of the pharmaceutical fluoxetine in spiked-sediments on feeding activity and growth of the polychaete Capitella teleta
Introduction
Pharmaceuticals administered to patients are normally discharged into aquatic environments via the sewage treatment plant systems (Kwon and Armbrust, 2006), occurring thus in groundwater, lakes, oceans (Boyd et al., 2003; Buser et al., 1998) and sediment (Coyne et al., 1994). One of the apparently more persistent pharmaceuticals in the environment is fluoxetine (Nmethyl-3-phenyl-3[4′-trifluoromethyl-phenoxy] propan-1-amine HCl; e.g. Prozac®), which has been found in streams and sewage treatment works effluents and there are concerns about accumulation in the environment (Brooks et al., 2003a; Kolpin et al., 2002; Metcalfe et al., 2003). Fluoxetine is a selective serotonin reuptake inhibitor used for the treatment of clinical depression, obsessive-compulsive disorder, and bulimia in humans. It is one of the most heavily prescribed drugs in the United States (Wong et al., 1995). During 2003, it was ranked 34th among the top 200 dispensed prescriptions (http://www.rxlist.com/top200.htm).
Fluoxetine is primarily excreted as a parental compound in urine (Hiemke and Härtter, 2000), thus it is not surprising to find that compound in effluents and surface waters at low to mid ng/l concentrations (Kolpin et al., 2002; Weston et al., 2001). Fluoxetine residues were detected at a concentration of 0.012 μg/l in streams (Kolpin et al., 2002), at 0.099 μg/l in sewage treatment plant effluents (Metcalfe et al., 2003) and at 0.54 mg/l in municipal effluents (Weston et al., 2001). According to Kwon and Armbrust (2006), in water/sediment systems fluoxetine rapidly adsorbs in sediment, where it appears to be persistent. Fluoxetine degradation in sediments has been little studied. It has been found that its degradation mainly depends on light, pH, organic matter, and humic acid. Kwon and Armbrust's (2006) biodegradability experiments indicated that flouxetine did not degrade over 28 days at 20 °C in medium containing inoculum collected from a secondary wastewater treatment plant. Moreover, Redshaw et al. (2008) concluded that fluoxetine can resist more than 200 days in sewage sludge-amended soils.
Fluoxetine exposure may affect pelagic organisms (Fong, 2001) and may bind to sediments and affect benthic organisms (Brooks et al., 2003a). Very little information is available for fluoxetine exposure (Kolpin et al., 2002; Weston et al., 2001) and its effects in aquatic ecosystems (Brooks et al., 2003a,b; Fong, 2001). Changes in feeding patterns have been detected in freshwater amphipods at low fluoxetine exposure, whilst increased ventilation was apparent in some cases at 1–100 ng/l, and increased locomotion at doses reaching up to 106 ng/l (De Lange et al., 2005, 2009). De Lange et al. (2006) observed that lower doses of fluoxetine exhibited more deleterious effects in activity of the epibenthic amphipod Gammarus pulex than higher doses. Several abnormalities have been observed in developing embryos of the Japanese medaka Oryzias latipes exposed to 0.1–5 mg/l fluoxetine during four weeks, and it was reported that 56 μg/l fluoxetine enhanced fecundity of Ceriodaphnia dubia (Brooks et al., 2003a). Flaherty et al. (2001) observed a comparable reproductive stimulation when Daphnia magna specimens were exposed to 36 μg/l fluoxetine for 30 days. Recently, Campos et al. (2012a) reported that 10, 40 and 80 μg/l fluoxetine increased D. magna offspring production relative to control treatments.
Effects of sediment-spiked fluoxetine on benthic fauna have been little studied and have been only reported at mg/kg levels (Brooks et al., 2003a; Péry et al., 2008). Brooks et al. (2003a) found that a 10-day sediment fluoxetine exposure with Chironomus tentans revealed a LC50 value of 17 mg/kg and a LOEC on growth of 1.3 mg/kg and an EC50 > 43 mg/kg for Hyalella azteca. A 42 day study revealed that fecundity (young per female) was not significantly reduced by fluoxetine treatment levels. H. azteca survival was not affected by the highest treatment level tested (43 mg/kg). However, growth of this species was significantly reduced by fluoxetine levels comprised between 5.4 and 43.2 mg/kg, with a LOEC of 5.6 mg/kg.
The endobenthic deposit feeder Capitella capitata (Fabricius, 1780) is a cosmopolitan polychaete that has been considered a universal indicator of organically enriched marine sediments (e.g. Pearson and Rosenberg, 1978). This polychaete can dominate sediments located close to sewage sludge inputs (Chang et al., 1992), which can be subjected to the effect of many contaminants including fluoxetine. C. capitata consists of a complex of non-interbreeding but morphologically similar sibling species which are distinguishable by protein variation, developmental and reproductive features, ecophysiological characters, such as tolerance to abiotic factors (i.e., organic matter in sediments, anoxia), and respiration rate (Grassle and Grassle, 1976; Linke-Gamenick et al., 2000a,b). Among the described Capitella sibling species, Capitella sp I has been considered as the most opportunistic species due to its rapid growth rate and numerical dominance in organically enriched areas, thus it has been the subject of several ecological and experimental investigations around the world (Forbes et al., 1994; Grassle and Grassle, 1974; Tsutsumi, 1987). Recently, Blake et al. (2009) substituted the provisional designation “Capitella sp I” by the proper species name “Capitella teleta” (hereafter termed this way), which continues being an experimental polychaete in several laboratories.
Sediment processing by members of the Capitella species-complex may have important ecological implications in the recovery of polluted sediments via sediment turnover (Méndez et al., 2001, 2008; Méndez, 2006a; Méndez and Baird, 2002; Selck et al., 1998, 1999). It has been estimated that the C.teleta population as a whole, could process from 270 to 1368 g of sediment per day/m2 (Méndez, 2006a; Méndez and Baird, 2002; respectively). Effects of fluoxetine on C. teleta could reflect detrimental effects on natural invertebrate populations inhabiting sediments subjected to this compound, which has an important ecological significance. Thus, the purpose of this study was to determine the possible effects of fluoxetine spiked-sediments on feeding activity (through egestion rates and size-specific egestion rates) and growth (body weight) of adult males and females of C. teleta under laboratory conditions.
Section snippets
Test organisms
Specimens of C. teleta were obtained originally from organically polluted sediments in Setauket Harbor, Long Island, New York, U.S.A. They were first identified as Capitella sp I by Judith Grassle and have been successfully cultured in the Department of Life Sciences and Chemistry of the Roskilde University (Denmark) for many generations over more than 20 years (Ramskov et al., 2009). Worms were held in culture in the Department of Environmental Chemistry, Institute of Environmental Assessment
Results
The initial length of worms ranged from 5.8 to 17.0 mm (average: 10.3 ± 2.1 mm; n = 60). Males measured from 5.8 to 12.6 mm (average: 9.4 ± 2.0 mm; n = 30), while females, from 7.6 to 17.0 mm (average: 11.2 ± 1.9 mm; n = 30). Initial dry weight of worms varied from 0.25 to 2.37 mg (average: 0.71 ± 0.34; n = 60), from which males ranged from 0.25 to 1.29 mg (average: 0.67 ± 0.27; n = 30) and females, from 0.29 to 2.37 mg (average: 0.76 ± 0.40; n = 30). Mean initial dry weights between males and
Discussion
This is the first experimental study concerning the effects of fluoxetine spiked-sediments on the marine polychaete Capitella species-complex, which normally inhabits sediments of the vicinities of sewage sludge inputs. Experimental studies in the laboratory can contribute to the knowledge of the fate of fluoxetine in sediment which, according to Kwon and Armbrust (2006), is a greater issue than its fate in water, due to its high persistence (more than 200 days; Redshaw et al., 2008).
It has
Conclusion
Results found here have shown that fluoxetine per se at the studied concentrations did not impair sediment processing rates or growth of C. teleta but could be partly or completely responsible of the occurrence of proteroginous individuals and males with abnormal genital spines. Considering that fluoxetine tends to remain largely bound to sediment, with a maximal half-life of 102–385 days (Kwon and Armbrust, 2006), Capitella could play an important ecological role in the recovery of sediments
Acknowledgements
This study was supported by the Dirección General de Apoyo al Personal Académico, UNAM, Mexico. We want to thank Cristian García, Alejandro Delgado, Marcel Mesado and Denisse Fernandes for their help with fluoxetine extraction and HPLC analyses. Capitella teleta specimens were provided by Henriette Selck (Department of Life Sciences and Chemistry, University of Roskilde). Jim Marlatt revised the written English.
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