Ecological effects of pharmaceuticals in aquatic systems—impacts through behavioural alterations

The study of animal behaviour is important for both ecology and ecotoxicology, yet research in these two fields is currently developing independently. Here, we synthesize the available knowledge on drug-induced behavioural alterations in fish, discuss potential ecological consequences and report results from an experiment in which we quantify both uptake and behavioural impact of a psychiatric drug on a predatory fish (Perca fluviatilis) and its invertebrate prey (Coenagrion hastulatum). We show that perch became more active while damselfly behaviour was unaffected, illustrating that behavioural effects of pharmaceuticals can differ between species. Furthermore, we demonstrate that prey consumption can be an important exposure route as on average 46% of the pharmaceutical in ingested prey accumulated in the predator. This suggests that investigations of exposure through bioconcentration, where trophic interactions and subsequent bioaccumulation of exposed individuals are ignored, underestimate exposure. Wildlife may therefore be exposed to higher levels of behaviourally altering pharmaceuticals than predictions based on commonly used exposure assays and pharmaceutical concentrations found in environmental monitoring programmes.

[1]  Karen A Kidd,et al.  Collapse of a fish population after exposure to a synthetic estrogen , 2007, Proceedings of the National Academy of Sciences.

[2]  E. Furlong,et al.  Selective uptake and biological consequences of environmentally relevant antidepressant pharmaceutical exposures on male fathead minnows. , 2011, Aquatic toxicology.

[3]  Kirsty J. Park,et al.  Detection of endocrine disrupting chemicals in aerial invertebrates at sewage treatment works. , 2009, Chemosphere.

[4]  A. Sih,et al.  Behavioral Syndromes: An Integrative Overview , 2004, The Quarterly Review of Biology.

[5]  V. Trudeau,et al.  Waterborne fluoxetine disrupts feeding and energy metabolism in the goldfish Carassius auratus. , 2010, Aquatic toxicology.

[6]  Jess G. Kohlert,et al.  Decreased Aggressive and Locomotor Behaviors in Betta Splendens after Exposure to Fluoxetine , 2012, Psychological reports.

[7]  Despo Fatta-Kassinos,et al.  Pharmaceutical residues in environmental waters and wastewater: current state of knowledge and future research , 2011, Analytical and bioanalytical chemistry.

[8]  Karen A Kidd,et al.  Biochemical and histopathological effects in pearl dace (Margariscus margarita) chronically exposed to a synthetic estrogen in a whole lake experiment , 2006, Environmental toxicology and chemistry.

[9]  O. Berglund,et al.  Ecological implications of altered fish foraging after exposure to an antidepressant pharmaceutical. , 2014, Aquatic toxicology.

[10]  F. Johansson,et al.  Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae , 2006, Oecologia.

[11]  Pierre-Olivier Montiglio,et al.  Contaminants as a neglected source of behavioural variation , 2014, Animal Behaviour.

[12]  C. Lillesaar The serotonergic system in fish , 2011, Journal of Chemical Neuroanatomy.

[13]  D. Réale,et al.  Predator-induced natural selection on temperament in bighorn ewes , 2003, Animal Behaviour.

[14]  J. Trumble,et al.  Trophic Transfer of Arsenic from an Aquatic Insect to Terrestrial Insect Predators , 2013, PloS one.

[15]  S. Rodrigues,et al.  Short-term effects of neuroactive pharmaceutical drugs on a fish species: biochemical and behavioural effects. , 2013, Aquatic toxicology.

[16]  Jerker Fick,et al.  Risks of hormonally active pharmaceuticals to amphibians: a growing concern regarding progestagens , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  S. Paul,et al.  Receptors for the age of anxiety: pharmacology of the benzodiazepines. , 1980, Science.

[18]  Marcus Östman,et al.  Occurrence and behaviour of 105 active pharmaceutical ingredients in sewage waters of a municipal sewer collection system. , 2014, Water research.

[19]  L. Rowe,et al.  LIFE HISTORY PLASTICITY IN A DAMSELFLY: EFFECTS OF COMBINED TIME AND BIOTIC CONSTRAINTS , 2001 .

[20]  L. Fahrig,et al.  Conservation of fragmented populations , 1994 .

[21]  A. Sih,et al.  Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis) , 2010, Proceedings of the Royal Society B: Biological Sciences.

[22]  Beverley Stinson,et al.  Pharmaceutical Formulation Facilities as Sources of Opioids and Other Pharmaceuticals to Wastewater Treatment Plant Effluents , 2010, Environmental science & technology.

[23]  Tomas Brodin,et al.  The conceptual imperfection of aquatic risk assessment tests: highlighting the need for tests designed to detect therapeutic effects of pharmaceutical contaminants , 2014 .

[24]  Erik Kristiansson,et al.  Evolutionary conservation of human drug targets in organisms used for environmental risk assessments. , 2008, Environmental science & technology.

[25]  Mats Tysklind,et al.  Contamination of surface, ground, and drinking water from pharmaceutical production , 2009, Environmental toxicology and chemistry.

[26]  Sun-Kyoung Shin,et al.  Occurrence and distribution of pharmaceuticals in wastewater from households, livestock farms, hospitals and pharmaceutical manufactures. , 2011, Chemosphere.

[27]  Masanori Seki,et al.  Acute effects of triclosan, diclofenac and carbamazepine on feeding performance of Japanese medaka fish (Oryzias latipes). , 2010, Chemosphere.

[28]  C. Tyler,et al.  Endocrine disrupting chemicals and sexual behaviors in fish – a critical review on effects and possible consequences , 2012, Critical reviews in toxicology.

[29]  Guy Woodward,et al.  Biodiversity, ecosystem functioning and food webs in fresh waters: assembling the jigsaw puzzle , 2009 .

[30]  J. Fick,et al.  Antihistamines and aquatic insects: bioconcentration and impacts on behavior in damselfly larvae (Zygoptera). , 2014, The Science of the total environment.

[31]  Francesca Prestinaci,et al.  Bioaccumulation and biomagnification potential of pharmaceuticals with a focus to the aquatic environment. , 2014, Journal of environmental management.

[32]  F. Johansson,et al.  Condition-dependent behaviour among damselfly populations , 2004 .

[33]  P. S. Lake,et al.  Energy and nutrient fluxes from rivers and streams into terrestrial food webs , 2006 .

[34]  Brigitte Poulin,et al.  Red flag for green spray: adverse trophic effects of Bti on breeding birds , 2010 .

[35]  Jan-Åke Nilsson,et al.  To boldly go: individual differences in boldness influence migratory tendency. , 2011, Ecology letters.

[36]  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.

[37]  F. Johansson,et al.  Conflicting selection pressures on the growth/predation risk trade-off in a damselfly , 2004 .

[38]  C. Chambliss,et al.  Bioaccumulation and trophic dilution of human pharmaceuticals across trophic positions of an effluent-dependent wadeable stream , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[39]  S. Peacor,et al.  A REVIEW OF TRAIT-MEDIATED INDIRECT INTERACTIONS IN ECOLOGICAL COMMUNITIES , 2003 .

[40]  D. Dietrich,et al.  Physiological Endpoints for Potential SSRI Interactions in Fish , 2008, Critical reviews in toxicology.

[41]  M. Vaswani,et al.  Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review , 2003, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[42]  J. Terborgh,et al.  Oddity and the ‘confusion effect’ in predation , 1986, Animal Behaviour.

[43]  Alejandro J. Ramirez,et al.  Enantiospecific sublethal effects of the antidepressant fluoxetine to a model aquatic vertebrate and invertebrate. , 2007, Chemosphere.

[44]  G. Bidoglio,et al.  EU-wide survey of polar organic persistent pollutants in European river waters. , 2009, Environmental pollution.

[45]  Terri Damstra,et al.  Global assessment of the state-of-the-science of endocrine disruptors , 2002 .

[46]  Jonathan M. Chase,et al.  Trophic cascades across ecosystems , 2005, Nature.

[47]  Diogo R. Lara,et al.  Effects of anxiolytics in zebrafish: Similarities and differences between benzodiazepines, buspirone and ethanol , 2011, Pharmacology Biochemistry and Behavior.

[48]  R. Nelson,et al.  Molecular basis of aggression , 2001, Trends in Neurosciences.

[49]  R. R. Krausz Living in Groups , 2013 .

[50]  S. Rodrigues,et al.  Effects of anticholinesterase drugs on biomarkers and behavior of pumpkinseed, Lepomis gibbosus (Linnaeus, 1758). , 2012, Journal of environmental monitoring : JEM.

[51]  K. Lesch,et al.  Impulsivity, aggression, and serotonin: a molecular psychobiological perspective. , 2000, Behavioral sciences & the law.

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

[53]  S. Klaine,et al.  Effects of the antidepressant venlafaxine on fish brain serotonin and predation behavior. , 2014, Aquatic toxicology.

[54]  Joanne A Harrold,et al.  Serotonin (5-HT) drugs: effects on appetite expression and use for the treatment of obesity. , 2005, Current drug targets.

[55]  S. Lawler,et al.  Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. , 2010, Ecology.

[56]  D. Larsson,et al.  Does waterborne citalopram affect the aggressive and sexual behaviour of rainbow trout and guppy? , 2011, Journal of hazardous materials.

[57]  S. Liggett,et al.  Pharmacology and physiology of human adrenergic receptor polymorphisms. , 2003, Annual review of pharmacology and toxicology.

[58]  J. F. Gilliam,et al.  Explaining Leptokurtic Movement Distributions: Intrapopulation Variation in Boldness and Exploration , 2001, The American Naturalist.

[59]  M. Ramenofsky,et al.  Fish on Prozac: a simple, noninvasive physiology laboratory investigating the mechanisms of aggressive behavior in Betta splendens. , 2007, Advances in physiology education.

[60]  P. Balvanera,et al.  Quantifying the evidence for biodiversity effects on ecosystem functioning and services. , 2006, Ecology letters.

[61]  J. Fick,et al.  Dilute Concentrations of a Psychiatric Drug Alter Behavior of Fish from Natural Populations , 2013, Science.

[62]  T. Brodin Behavioral syndrome over the boundaries of life - carryovers from larvae to adult damselfly. , 2009 .

[63]  S. Meriç,et al.  Occurrence patterns of pharmaceuticals in water and wastewater environments , 2007, Analytical and bioanalytical chemistry.

[64]  Lee E. Brown,et al.  Global Synthesis and Critical Evaluation of Pharmaceutical Data Sets Collected from River Systems , 2012, Environmental science & technology.

[65]  S. Dodson,et al.  Predation, Body Size, and Composition of Plankton. , 1965, Science.

[66]  M. Gessner,et al.  Antibiotics as a chemical stressor affecting an aquatic decomposer–detritivore system , 2009, Environmental toxicology and chemistry.

[67]  E. Kristiansson,et al.  Assessing variation in the potential susceptibility of fish to pharmaceuticals, considering evolutionary differences in their physiology and ecology , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  C. Chambliss,et al.  Effects of the antihistamine diphenhydramine on selected aquatic organisms , 2011, Environmental toxicology and chemistry.

[69]  P. Verlicchi,et al.  Occurrence of pharmaceutical compounds in urban wastewater: removal, mass load and environmental risk after a secondary treatment--a review. , 2012, The Science of the total environment.

[70]  C. Meston,et al.  The neurobiology of sexual function. , 2000, Archives of general psychiatry.

[71]  B. Bateman An integrative overview. , 1976 .

[72]  Åke Bergman,et al.  State of the Science of Endocrine Disrupting Chemicals - 2012 , 2012 .

[73]  J. Godwin,et al.  Fluoxetine treatment decreases territorial aggression in a coral reef fish , 2003, Physiology & Behavior.

[74]  R. Stoks Effect of lamellae autotomy on survival and foraging success of the damselfly Lestes sponsa (Odonata: Lestidae) , 1998, Oecologia.

[75]  V. Trudeau,et al.  Pharmaceuticals as Neuroendocrine Disruptors: Lessons Learned from Fish on Prozac , 2011, Journal of toxicology and environmental health. Part B, Critical reviews.

[76]  M. C. Ferrari,et al.  Evolution and behavioural responses to human-induced rapid environmental change , 2011, Evolutionary applications.

[77]  T. Backhaus Medicines, shaken and stirred: a critical review on the ecotoxicology of pharmaceutical mixtures , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[78]  S. Wilson,et al.  The utility of behavioral studies for aquatic toxicology testing: a meta-analysis. , 2013, Chemosphere.

[79]  R. Colwill,et al.  On the edge: Pharmacological evidence for anxiety-related behavior in zebrafish larvae , 2012, Behavioural Brain Research.

[80]  A. Soto,et al.  Developmental effects of endocrine-disrupting chemicals in wildlife and humans. , 1993, Environmental health perspectives.

[81]  D. Schlenk,et al.  Effects of exposure to the β-blocker propranolol on the reproductive behavior and gene expression of the fathead minnow, Pimephales promelas. , 2012, Aquatic toxicology.

[82]  A. Soto,et al.  Developmental effects of endocrine-disrupting chemicals in wildlife and humans , 1994 .

[83]  Donald J. Hall,et al.  Ontogenetic Habitat Shifts in Bluegill: The Foraging Rate‐Predation Risk Trade‐off , 1988 .

[84]  J. Fick,et al.  EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents. , 2013, Water research.

[85]  Karen A. Kidd,et al.  Direct and indirect responses of a freshwater food web to a potent synthetic oestrogen , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[86]  C. Gagnon,et al.  Review of the Occurrence of Anti-infectives in Contaminated Wastewaters and Natural and Drinking Waters , 2009, Environmental health perspectives.

[87]  A. Sih,et al.  Personality-dependent dispersal in the invasive mosquitofish: group composition matters , 2011, Proceedings of the Royal Society B: Biological Sciences.

[88]  E. Perkins,et al.  II: Effects of a dopamine receptor antagonist on fathead minnow dominance behavior and ovarian gene expression in the fathead minnow and zebrafish. , 2010, Ecotoxicology and environmental safety.

[89]  Andrew Sih,et al.  Predation: direct and indirect impacts on aquatic communities , 1988 .

[90]  Blaise Tymen,et al.  Personality-dependent dispersal cancelled under predation risk , 2013, Proceedings of the Royal Society B: Biological Sciences.

[91]  Kirsty J. Park,et al.  Use of sewage treatment works as foraging sites by insectivorous bats , 2006 .

[92]  K. Fent,et al.  Effects of diazepam on gene expression and link to physiological effects in different life stages in zebrafish Danio rerio. , 2010, Environmental science & technology.

[93]  T. L. Dzieweczynski,et al.  Fluoxetine alters behavioral consistency of aggression and courtship in male Siamese fighting fish, Betta splendens , 2012, Physiology & Behavior.

[94]  Daniel T. Blumstein,et al.  Fitness consequences of personality: a meta-analysis , 2008 .

[95]  M. Gross The Evolution of Parental Care , 2005, The Quarterly Review of Biology.

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

[97]  Jacob Gibs,et al.  Efficiency of conventional drinking-water-treatment processes in removal of pharmaceuticals and other organic compounds. , 2007, The Science of the total environment.

[98]  M. J. Barry Effects of fluoxetine on the swimming and behavioural responses of the Arabian killifish , 2013, Ecotoxicology.