Anti-depressants make amphipods see the light.

The effects of serotonin altering parasites, serotonin, the anti-depressant fluoxetine, plus two other highly prescribed pharmaceuticals (carbamazepine and diclofenac) on the behaviour of the marine amphipod, Echinogammarus marinus were investigated. Acanthocephalan parasites are known to alter the swimming behaviour in their amphipod hosts through changes in serotonergic activity resulting in increased predation. Behavioural assays were adapted to record changes in phototaxis and geotaxis behaviour in male E. marinus following 7, 14 and 21 days exposure to serotonin and each pharmaceutical compound at 4 concentrations compared to a control (between 10 ng/L and 10 microg/L). E. marinus infected with acanthocephalans parasites had both significantly higher phototaxis and geotaxis scores than those of uninfected specimens. Phototaxis and geotaxis behaviour increased significantly in a concentration-dependent manner with exposure to serotonin. Fluoxetine significantly altered phototaxis and geotaxis activity in what appeared to be a non-monotonic concentration response curve with the greatest behavioural changes observed at 100 ng/L. The main patterns of these behavioural responses were consistent between two trials and the 3 weeks exposure with specimens spending more time within the light and occurring higher in the water column. No obvious trends could be concluded in the phototaxis and geotaxis scores from individuals exposed to carbamazepine or diclofenac as might be expected from their known mode of action. From this study phototaxis and geotaxis behaviour have been observed to be affected by exposure to serotonin modulators. Parasite studies have shown strong links between changes in behaviour and increased predation risk correlating with changes in serotonergic activity. This study has highlighted the potential for highly prescribed anti-depressant drugs to change the behaviour of an ecologically relevant marine species in ways which could conceivably lead to population level effects.

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

[2]  R. Poulin,et al.  Host sharing and host manipulation by larval helminths in shore crabs: cooperation or conflict? , 2003, International journal for parasitology.

[3]  M. J. Hazen,et al.  Ecotoxicological evaluation of carbamazepine using six different model systems with eighteen endpoints. , 2003, Toxicology in vitro : an international journal published in association with BIBRA.

[4]  F. Gagné,et al.  Occurrence of pharmaceutical products in a municipal effluent and toxicity to rainbow trout (Oncorhynchus mykiss) hepatocytes. , 2006, Ecotoxicology and environmental safety.

[5]  J. Vane,et al.  Mechanism of action of nonsteroidal anti-inflammatory drugs. , 1998, The American journal of medicine.

[6]  C. Wang,et al.  Short-term responses of Oryzias latipes (Pisces: Adrianichthyidae) and Macrobrachium nipponense (Crustacea: Palaemonidae) to municipal and pharmaceutical waste water in Beijing, China: survival, behaviour, biochemical biomarkers. , 2002, Chemosphere.

[7]  R. Satterlie,et al.  Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. I. Serotonin immunoreactivity in the central nervous system and wings. , 1995, The Journal of experimental biology.

[8]  Almut Gerhardt,et al.  Behavioural responses of indigenous benthic invertebrates (Echinogammarus meridionalis, Hydropsyche pellucidula and Choroterpes picteti) to a pulse of Acid Mine Drainage: a laboratorial study. , 2008, Environmental pollution.

[9]  Klaus Kümmerer,et al.  Pharmaceuticals in the environment : sources, fate, effects and risks , 2008 .

[10]  R. Blust,et al.  Analysis of the swimming velocity of cadmium-stressed Daphnia magna , 1999 .

[11]  C. Eades,et al.  The effects of diclofenac on the physiology of the green shore crab Carcinus maenas. , 2010, Marine environmental research.

[12]  L. Lanfumey,et al.  Early desensitization of somato-dendritic 5-HT1A autoreceptors in rats treated with fluoxetine or paroxetine , 1995, Naunyn-Schmiedeberg's Archives of Pharmacology.

[13]  K. Fent,et al.  Ecotoxicology of human pharmaceuticals. , 2006, Aquatic toxicology.

[14]  F. Cézilly,et al.  Increased susceptibility to predation and altered anti-predator behaviour in an acanthocephalan-infected amphipod. , 2007, International journal for parasitology.

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

[16]  P. Benjamin,et al.  Modulatory role for the serotonergic cerebral giant cells in the feeding system of the snail, Lymnaea. I. Fine wire recording in the intact animal and pharmacology. , 1994, Journal of neurophysiology.

[17]  M. Perrot-Minnot,et al.  The acanthocephalan parasite Polymorphus minutus alters the geotactic and clinging behaviours of two sympatric amphipod hosts: the native Gammarus pulex and the invasive Gammarus roeseli , 2005 .

[18]  D. Zaremba,et al.  Non-epilepsy uses of antiepileptic drugs , 2006 .

[19]  K. Dams-O’Connor,et al.  Behavioral effects of serotonin and serotonin agonists in two crayfish species, Procambarus clarkii and Orconectes rusticus. , 2004, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

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

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

[22]  Roberto Andreozzi,et al.  Pharmaceuticals in STP effluents and their solar photodegradation in aquatic environment. , 2003, Chemosphere.

[23]  E. Furlong,et al.  Pharmaceuticals and Personal Care Products in the Environment ANTIDEPRESSANTS AT ENVIRONMENTALLY RELEVANT CONCENTRATIONS AFFECT PREDATOR AVOIDANCE BEHAVIOR OF LARVAL FATHEAD MINNOWS (PIMEPHALES PROMELAS) , 2009 .

[24]  S. Dodson,et al.  Effects of pharmaceuticals on Daphnia survival, growth, and reproduction. , 2005, Chemosphere.

[25]  P. Fong,et al.  Effects of the serotonin receptor ligand methiothepin on reproductive behavior of the freshwater snail Biomphalaria glabrata: reduction of egg laying and induction of penile erection. , 2001, The Journal of experimental zoology.

[26]  R. Lincoln British Marine Amphipoda: Gammaridea , 1979 .

[27]  H. Kaiser,et al.  Monitoring Behavioral Responses to the Heavy Metal Cadmium in the Marine Shrimp Hippolyte inermis Leach (Crustacea: Decapoda) with Video Imaging , 2005 .

[28]  J N Lester,et al.  Human pharmaceuticals in the aquatic environment a review. , 2001, Environmental technology.

[29]  F. Cézilly,et al.  Differential influence of Pomphorhynchus laevis (Acanthocephala) on brain serotonergic activity in two congeneric host species , 2007, Biology Letters.

[30]  F. Cézilly,et al.  Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity , 2006, Proceedings of the Royal Society B: Biological Sciences.

[31]  T. Heberer Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. , 2002, Toxicology letters.

[32]  G. Charmantier,et al.  Physiological and behavioural responses of Gammarus pulex (Crustacea: Amphipoda) exposed to cadmium. , 2008, Aquatic toxicology.

[33]  E. Peeters,et al.  Development of a feeding behavioural bioassay using the freshwater amphipod Gammarus pulex and the Multispecies Freshwater Biomonitor. , 2009, Chemosphere.

[34]  Cora J Young,et al.  Aquatic persistence of eight pharmaceuticals in a microcosm study , 2004, Environmental toxicology and chemistry.

[35]  R. Satterlie,et al.  Serotonergic modulation of swimming speed in the pteropod mollusc Clione limacina. III. Cerebral neurons. , 1995, The Journal of experimental biology.

[36]  L. Bollache,et al.  Modification of hosts' behavior by a parasite: field evidence for adaptive manipulation. , 2007, Ecology.

[37]  D. Kolpin,et al.  Transport of chemical and microbial compounds from known wastewater discharges: potential for use as indicators of human fecal contamination. , 2005, Environmental science & technology.

[38]  C. Metcalfe,et al.  Pharmaceuticals and Endocrine Disruptors in Wastewater Treatment Effluents and in the Water Supply System of Calgary, Alberta, Canada , 2006 .

[39]  S. Jørgensen,et al.  Occurrence, fate and effects of pharmaceutical substances in the environment--a review. , 1998, Chemosphere.

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

[41]  T. Poiger,et al.  Occurrence and Fate of the Pharmaceutical Drug Diclofenac in Surface Waters: Rapid Photodegradation in a Lake , 1998 .

[42]  A. Nogueira,et al.  Behavioural and feeding responses of Echinogammarus meridionalis (Crustacea, Amphipoda) to acid mine drainage. , 2007, Chemosphere.

[43]  S. Klaine,et al.  Behavioral and biochemical responses of hybrid striped bass during and after fluoxetine exposure. , 2008, Aquatic toxicology.

[44]  R. E. Gosselin,et al.  The cilioexcitatory activity of serotonin. , 1961, Journal of cellular and comparative physiology.

[45]  M. Servos,et al.  Occurrence of neutral and acidic drugs in the effluents of Canadian sewage treatment plants , 2003, Environmental toxicology and chemistry.

[46]  S. Czuczwar,et al.  Non-epilepsy uses of antiepilepsy drugs. , 2006, Pharmacological reports : PR.

[47]  M. Lürling,et al.  Changes in Ventilation and Locomotion of Gammarus pulex (Crustacea, Amphipoda) in Response to Low Concentrations of Pharmaceuticals , 2009 .

[48]  J. Holmes,et al.  Altered Evasive Behavior and Responses to Light in Amphipods Harboring Acanthocephalan Cystacanths , 1973 .

[49]  P. Chapman Integrating toxicology and ecology: putting the "eco" into ecotoxicology. , 2002, Marine pollution bulletin.

[50]  M. Gu,et al.  Analysis of the effects diclofenac has on Japanese medaka (Oryzias latipes) using real-time PCR. , 2007, Chemosphere.

[51]  J. Vane,et al.  Mechanism of action of antiinflammatory drugs. , 1998, International journal of tissue reactions.

[52]  M. Lürling,et al.  Behavioural responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. , 2006, Aquatic toxicology.

[53]  M. Benotti,et al.  Microbial degradation of pharmaceuticals in estuarine and coastal seawater. , 2009, Environmental pollution.

[54]  K. Sloman,et al.  The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. , 2004, Aquatic toxicology.

[55]  E. Kravitz,et al.  Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[56]  W. Wallace,et al.  Differential susceptibility of horizontal and vertical swimming activity to cadmium exposure in a gammaridean amphipod (Gammarus lawrencianus). , 2004, Aquatic toxicology.

[57]  E. Thurman,et al.  Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. , 2002, Environmental science & technology.

[58]  E. Thurman,et al.  Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. , 2002 .

[59]  F. Cézilly,et al.  Conflict between co-occurring manipulative parasites? An experimental study of the joint influence of two acanthocephalan parasites on the behaviour of Gammarus pulex , 2000, Parasitology.

[60]  F. Thomas,et al.  Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) on serotonergic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda) , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.