Environmental Science and Pollution Research

, Volume 26, Issue 11, pp 11326–11335 | Cite as

Combined effects of NaCl and fluoxetine on the freshwater planarian, Schmidtea mediterranea (Platyhelminthes: Dugesiidae)

  • Pearl U. OfoegbuEmail author
  • Diana Campos
  • Amadeu M. V. M. Soares
  • Joāo L. T. Pestana
Research Article


Increasing salinity levels in freshwaters due to natural and anthropogenic sources pose risk to exposed aquatic organisms. However, there is a paucity of information on how salinity may influence the effects of other chemical stressors especially psychiatric pharmaceuticals. Freshwater planarians which have been suggested as bioindicator species in aquatic habitats were used in this study to evaluate toxic effects of sodium chloride (NaCl) used here as a surrogate for increasing salinity, and its influence on the effects of the antidepressant, fluoxetine. Effects of NaCl on Schmidtea mediterranea were evaluated using survival, regeneration, locomotion, feeding, and reproduction as endpoints. Subsequently, combined effects of NaCl and fluoxetine on planarians’ locomotion and reproduction were also evaluated. Result showed that exposure to increased NaCl concentrations is toxic to planarians with 48 and 96 h LC50 of 9.15 and 7.55 g NaCl L−1 respectively and exposure to sub-lethal concentrations led to reductions in feeding (LOEC of 0.75 g NaCl L−1 or 1906 μS cm−1 at 20 °C) and reproduction (LOEC 3.0 g NaCl L−1 or 5530 μS cm−1 at 20 °C), delayed head regeneration (LOEC of 1.5 g NaCl L−1 or 3210 μS cm−1 at 20 °C), and also slight decreases in locomotor activity. Moreover, some developmental malformations were observed in regenerating planarians, as well as delayed or inhibition of wound healing and degeneration after fissioning and during head regeneration. A significant interaction between fluoxetine and NaCl was observed for locomotor activity and unlike planarians exposed to fluoxetine alone, fissioned planarians and their pieces from the combined exposure treatments were also unable to regenerate missing portions. Results show that S. mediterranea can be highly sensitive to low NaCl concentrations and that this stressor can alter the effects of fluoxetine. The implication of these effects for planarian populations in the natural habitat is discussed as well as the need for more research on the effects of neuroactive pharmaceuticals under relevant exposure scenarios.


Psychiatric pharmaceuticals Freshwater salinization Toxicity Sub-lethal endpoints 



We thank FCT and POPH/FSE (Programa Operacional Potencial Humano/Fundo Social Europeu) for the research contract under the program “Investigador FCT 2015” of João L. T. Pestana (IF/01420/2015). Pearl U. Ofoegbu acknowledges Tertiary Education Trust Fund (TETFUND), Nigeria through the Federal University of Technology, Owerri, Nigeria for doctoral grant. Also, we acknowledge the Portuguese Foundation for Science and Technology (FCT) for the individual grant to Diana Campos (SFRH/BD/87370/2012). Prof. Francesc Cebrià and Prof. Néstor J. Oviedo are acknowledged for providing S. mediterranea with which we established our laboratory culture and useful information for establishing the cultures, respectively.

Funding information

This study received financial support from CESAM (UID/AMB/50017 - POCI-01-0145-FEDER-007638), from FCT/MCTES through national funds (PIDDAC), and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.

Supplementary material

11356_2019_4532_MOESM1_ESM.docx (1.3 mb)
ESM 1 (DOCX 1381 kb)


  1. Algeri S, Carolei A, Ferrett P, Gallone C (1983) Effects of dopaminergic agents on monoamine levels and motor behavior in planaria. Comp Biochem Physiol C 74:27–29Google Scholar
  2. ASTM (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E – 729-80. American Standards for Testing and Materials, Philadelphia, P.A. USAGoogle Scholar
  3. Buttarelli FR, Pellicano C, Pontieri FE (2008) Neuropharmacology and behavior in planarians: translations to mammals. Comp Biochem Physiol C 147:399–408Google Scholar
  4. Bymaster FP, Zhang W, Carter PA, Shaw J, Chernet E, Phebus L, Wong DT, Perry KW (2002) Fluoxetine, but not other selective serotonin uptake inhibitors, increases norepinephrine and dopamine extracellular levels in prefrontal cortex. Psychopharmacology 160:353–361CrossRefGoogle Scholar
  5. Cañedo-Argüelles M, Kefford BJ, Piscart C, Prat N, Schäfer RB, Schulz C–J (2013) Salinisation of rivers: an urgent ecological issue. Environ Pollut 173:157–167CrossRefGoogle Scholar
  6. Cartier V, Claret C, Garnier R, Franquet E (2011) How salinity affects life cycle of a brackish water species, Chironomus salinarius Kieffer (Diptera: Chironomidae). J Exp Mar Biol Ecol 405:93–98CrossRefGoogle Scholar
  7. Chand BK, Trivedi RK, Dubey SK, Rout SK, Beg MM, Das UK (2015) Effect of salinity on survival and growth of giant freshwater prawn Macrobrachium rosenbergii (de Man). Aquac Rep 2:26–33CrossRefGoogle Scholar
  8. Collins SJ, Russell RW (2009) Toxicity of road salt to Nova Scotia amphibians. Environ Pollut 157:320–324CrossRefGoogle Scholar
  9. Donner E, Kosjek T, Qualmann S, Kusk OK, Heath E, Revitt DM, Ledin A, Andersen HR (2013) Ecotoxicity of carbamazepine and its photolysis transformation products. Sci Total Environ 443:870–876CrossRefGoogle Scholar
  10. Dugan HA, Bartlett SL, Burke SM, Doubek JP, Krivak-Tetley FE, Skaff NK, Summers JC, Farrell KJ, McCullough IM, Morales-Williams AM, Roberts DC, Ouyang Z, Scordo F, Hanson PC, Weathers KC (2017) Salting our freshwater lakes. Proc Natl Acad Sci U S A 114:4453–4458CrossRefGoogle Scholar
  11. Ebele AJ, Abdallah MA, Harrad S (2017) Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg Contam 3:1–16CrossRefGoogle Scholar
  12. Fent K, Weston AA, Caminada D (2006) Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122–159CrossRefGoogle Scholar
  13. Fong PP, Ford AT (2014) The biological effects of antidepressants on the molluscs and crustaceans: a review. Aquat Toxicol 151:4–13Google Scholar
  14. Freitas R, Pires A, Velez C, Almeida A, Wrona FJ, Soares AMVM, Figueira E (2015) The effects of salinity changes on the polychaete Diopatra neapolitana: impacts on regenerative capacity and biochemical markers. Aquat Toxicol 163:167–176CrossRefGoogle Scholar
  15. Ghazy MMED, Habashy MM, Kossa FI, Mohammady EY (2009) Effects of salinity on survival, growth and reproduction of the water flea, Daphnia magna. Nat Sci 7:28–41Google Scholar
  16. Gonçalves AMM, Castro BB, Pardal MA, Gonçalves F (2007) Salinity effects on survival and life history of two freshwater cladocerans (Daphnia magna and Daphnia longispina). Ann Limnol Int J Limnol 43:13–20CrossRefGoogle Scholar
  17. Grzesiuk M, Mikulski A (2006) The effects of salinity on freshwater crustaceans. Pol J Ecol 54:669–674Google Scholar
  18. Hagstrom D, Cochet-Escartin O, Collins EMS (2016) Planarian brain regeneration as a model system for developmental neurotoxicology. Regeneration 3:65–77CrossRefGoogle Scholar
  19. Harrath A, Charni M, Sluys R, Zghal F, Tekaya S (2004) Ecology and distribution of the freshwater planarian Schmidtea mediterranea in Tunisia. Ital J Zool 71:233–236Google Scholar
  20. Hart BT, Bailey P, Edwards R, Hortle K, James K, McMahon A, Meredith C, Swadling K (1991) A review of the salt sensitivity of the Australian freshwater biota. Hydrobiologia 210:105–144CrossRefGoogle Scholar
  21. Kaushal SS, Groffman PM, Likens GE, Belt KT, Stack WP, Kelly VR, Band LE, Fisher GT (2005) Increased salinization of fresh water in the northeastern United States. Proc Natl Acad Sci USA 102:13517–13520CrossRefGoogle Scholar
  22. Kirecci SL, Simsek A, Gurbuz ZG, Mimaroglu S, Yuksel A, Vural P, Degirmencioglu S (2014) Relationship between plasma melatonin levels and the efficacy of selective serotonin reuptake inhibitors treatment on premature ejaculation. Int J Urol 21:917–920CrossRefGoogle Scholar
  23. Knakievicz T (2014) Planarians as invertebrate bioindicators in freshwater environmental quality: the biomarkers approach. Ecotoxicol Environ Contam 9:1–12Google Scholar
  24. Kwon JW, Armbrust KL (2006) Laboratory persistence and fate of fluoxetine in aquatic environments. Environ Toxicol Chem 25:2561–2568CrossRefGoogle Scholar
  25. Legner EF, Tsai TC, Medved RA (1976) Environmental stimulants to asexual reproduction in the planarian, Dugesia dorotocephala. Entomophaga 21:415–423CrossRefGoogle Scholar
  26. Manenti R, Bianchi B (2014) Distribution of the triclad Polycelis felina (Planariidae) in Aezkoa mountains: effects of stream biotic features. Acta Zool Bulg 66:271–275Google Scholar
  27. Morita M, Best JB (1993) The occurrence and physiological functions of melatonin in the most primitive eumetazoans, the planarians. Experimentia 49:623–626CrossRefGoogle Scholar
  28. Nakamura Y, Yamamoto H, Sekizawa J, Kondo T, Hirai N, Tatarazako N (2008) The effects of pH on fluoxetine in Japanese medaka (Oryzias latipes): acute toxicity in fish larvae and bioaccumulation in juvenile fish. Chemosphere 70:865–873CrossRefGoogle Scholar
  29. Nentwig G (2008) Another example of effects of pharmaceuticals on aquatic invertebrates: fluoxetine and ciprofloxacin. In: Kümmerer K (ed) Pharmaceuticals in the environment: sources, fate, effects and risks. Springer-Verlag, Berlin, pp 205–222CrossRefGoogle Scholar
  30. Ofoegbu PU, Simão FC, Cruz A, Mendo S, Soares AMVM, Pestana JLT (2016) Toxicity of tributyltin (TBT) to the freshwater planarian Schmidtea mediterranea. Chemosphere 148:61–67Google Scholar
  31. Ofoegbu PU, Lourenco J, Mendo S, Soares AMVM, Pestana JLT (2019) Effects of low concentrations of psychiatric drugs (carbamazepine and fluoxetine) on the freshwater planarian, Schmidtea mediterranea. Chemosphere 217:542–549CrossRefGoogle Scholar
  32. Rivera VR, Perich MJ (1994) Effects of water quality on survival and reproduction of four species of planaria (Turbellaria: Tricladida). Invertebr Reprod Dev 25:1–7CrossRefGoogle Scholar
  33. Rivetti C, Campos B, Barata C (2016) Low environmental levels of neuroactive pharmaceuticals alter phototactic behaviour and reproduction in Daphnia magna. Aquat Toxicol 170:289–296CrossRefGoogle Scholar
  34. Sanzo D, Hecnar SJ (2006) Effects of road de-icing salt (NaCl) on larval wood frogs (Rana sylvatica). Environ Pollut 140:247–256CrossRefGoogle Scholar
  35. Sarma SSS, Nandini S, Morales-Ventura J, Delgado-Martínez I, González-Valverde L (2006) Effects of NaCl salinity on the population dynamics of freshwater zooplankton (rotifers and cladocerans). Aquat Ecol 40:349–360CrossRefGoogle Scholar
  36. Schultz MA, Furlong ET, Kolpin DW, Werner SL, Schoenfuss HL, Barber LB, Blazer VS, Norris DO, Vajda AM (2010) Antidepressant pharmaceuticals in two U.S. effluent-impacted streams: occurrence and fate in water and sediment, and selective uptake in fish neural tissue. Environ Sci Technol 44:1918–1925CrossRefGoogle Scholar
  37. Schürmann W, Peter R (1998) Inhibition of regeneration in the planarian Dugesia polychroa (Schmidt) by treatment with magnesium chloride: a morphological study of wound closure. Inhibition of regeneration in planarian. Hydrobiologia 383:111–116CrossRefGoogle Scholar
  38. Searle CL, Shaw CL, Hunsberger KK, Prado M, Duffy MA (2016) Salinization decreases population densities of the freshwater crustacean, Daphnia dentifera. Hydrobiologia 770:165–172CrossRefGoogle Scholar
  39. Shock BC, Foran CM, Stueckle TA (2009) Effects of salinity stress on survival, metabolism, limb regeneration, and ecdysis in Uca pugnax. J Crustac Biol 29:293–301CrossRefGoogle Scholar
  40. Squires ZE, Bailey PCE, Reina RD, Wong BM (2008) Environmental deterioration increases tadpole vulnerability to predation. Biol Lett 4:392–394CrossRefGoogle Scholar
  41. Venãncio CAR (2017) Salinization effects on coastal terrestrial and freshwater ecosystems. PhD Thesis, Department of Biology, University of Aveiro, 278 pp.Google Scholar
  42. Weston, J. J., Huggett, D. B., Rimoldi, J., Foran, C. M., Stattery, M., 2001. Determination of fluoxetine (“Prozac”) and norfluoxetine in the aquatic environment. In: Annual Meeting of the Society of Environmental Toxicology and Chemistry, Baltimore, MD.Google Scholar
  43. Wong DT, Bymaster FP, Engleman EA (1995) Prozac (fluoxetine, Lilly 110,140), the first selective serotonin uptake inhibitor and an antidepressant drug: twenty years since its first publication. Life Sci 57:411–441CrossRefGoogle Scholar
  44. Wu JP, Li MH (2018) The use of freshwater planarians in environmental toxicology studies: advantages and potential. Ecotoxicol Environ Saf 161:45–56CrossRefGoogle Scholar
  45. Zinchenko TD, Golovatyuk LV (2013) Salinity tolerance of macroinvertebrates in stream waters. Arid Ecosyst 3:113–121CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Pearl U. Ofoegbu
    • 1
    • 2
    Email author
  • Diana Campos
    • 1
  • Amadeu M. V. M. Soares
    • 1
  • Joāo L. T. Pestana
    • 1
  1. 1.Department of Biology & CESAMUniversity of Aveiro, Campus Universitário de SantiagoAveiroPortugal
  2. 2.Department of BiologyFederal University of TechnologyOwerriNigeria

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