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Pharmaceuticals May Disrupt Natural Chemical Information Flows and Species Interactions in Aquatic Systems: Ideas and Perspectives on a Hidden Global Change

  • Ellen Van Donk
  • Scott Peacor
  • Katharina Grosser
  • Lisette N. De Senerpont Domis
  • Miquel Lürling
Part of the Reviews of Environmental Contamination and Toxicology book series (RECT, volume 238)

Abstract

Pharmaceuticals consumption by humans and animals is increasing substantially, leading to unprecedented levels of these compounds in aquatic environments worldwide. Recent findings that concentrations reach levels that can directly have negative effects on organisms are important per se, but also sound an alarm for other potentially more pervasive effects that arise from the interconnected nature of ecological communities. Aquatic organisms use chemical cues to navigate numerous challenges, including the location of mates and food, and the avoidance of natural enemies. Low concentrations of pharmaceuticals can disrupt this “smellscape” of information leading to maladaptive responses. Furthermore, direct effects of pharmaceuticals on the traits and abundance of one species can cascade through a community, indirectly affecting other species. We review mechanisms by which pharmaceuticals in surface waters can disrupt natural chemical information flows and species interactions. Pharmaceuticals form a new class of chemical threats, which could have far-reaching implications for ecosystem functioning and conservation management.

Keywords

Fathead Minnow Realistic Concentration Pheromone Communication Gray Tree Frog Receiver Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We want to thank Wim van der Putten and two anonymous reviewers for constructive comments on an earlier draft of the manuscript. This is publication 5932 of the Netherlands Institute of Ecology (NIOO-KNAW).

References

  1. Barry MJ (2013) Effects of fluoxetine on the swimming and behavioural responses of the Arabian killifish. Ecotoxicology 22:425–432CrossRefGoogle Scholar
  2. Boeing WJ, Ramcharan CW (2010) Inducible defences are a stabilizing factor for predator and prey populations: a field experiment. Freshw Biol 55:2332–2338Google Scholar
  3. Boettcher AA, Target NM (1998) Role of chemical inducers in larval metamorphosis of queen conch, Strombus gigas Linnaeus: relationship to other marine invertebrate systems. Biol Bull 194:132–142CrossRefGoogle Scholar
  4. Boxall ABA, Rudd MA, Brooks BW et al (2012) Pharmaceuticals and personal care products in the environment: what are the big questions? Environ Health Perspect 120:1221–1229CrossRefGoogle Scholar
  5. Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36:46–58CrossRefGoogle Scholar
  6. Bringolf RB, Heltsley RM, Newton TJ et al (2010) Environmental occurrence and reproductive effects of the pharmaceutical fluoxetine in native freshwater mussels. Environ Toxicol Chem 29:1311–1318Google Scholar
  7. Brodin T, Fick J, Jonsson M et al (2013) Dilute concentrations of a psychiatric drug alter behavior of fish from natural populations. Science 339:814–815CrossRefGoogle Scholar
  8. Brodin T, Piovano S, Fick J, Klaminder J, Heynen M, Jonsson M (2014) Ecological effects of pharmaceuticals in aquatic systems-impacts through behavioural alterations. Philos Trans R Soc Lond B Biol Sci 369:20130580CrossRefGoogle Scholar
  9. Brönmark C, Hansson L-A (2012) Aquatic chemical ecology: new directions and challenges for the future. In: Brönmark C, Hansson L-A (eds) Chemical ecology in aquatic systems. Oxford University Press, New York, NYCrossRefGoogle Scholar
  10. Caldwell DJ, Mastrocco F, Margiotta-Casaluci L, Brooks BW (2014) An integrated approach for prioritizing pharmaceuticals found in the environment for risk assessment, monitoring and advanced research. Chemosphere 115:4–12CrossRefGoogle Scholar
  11. De Lange HJ, Lürling M, Van Den Borne B, Peeters ETHM (2005) Attraction of the amphipod Gammarus pulex to water-borne cues of food. Hydrobiologia 544:19–25CrossRefGoogle Scholar
  12. De Lange HJ, Noordhoven W, Murk AJ, Lürling M, Peeters ETHM (2006) Behavioural responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. Aquat Toxicol 78:209–216CrossRefGoogle Scholar
  13. De Lange HJ, Peeters ETHM, Lürling M (2009) Changes in ventilation and locomotion of Gammarus pulex (Crustacea, Amphipoda) in response to low concentrations of pharmaceuticals. Hum Ecol Risk Assess 15(1):111–120CrossRefGoogle Scholar
  14. De Voogt P, Janex-Habibi ML, Sacher F, Puijker L, Mons M (2009) Development of a common priority list of pharmaceuticals relevant for the water cycle. Water Sci Technol 59:39–46CrossRefGoogle Scholar
  15. Dodson SI, Crowl TA, Peckarsky BL et al (1994) Non-visual communication in freshwater benthos - an overview. J N Am Benthol Soc 13:268–282CrossRefGoogle Scholar
  16. EC. 2012. Directive of the European Parliament and of the Council amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. In: 2011/0429 (COD). http://eur-lex.europa.eu/legal-content/EN/NOT/?uri=CELEX:52011PC0876
  17. Fleeger JW, Carmana KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233CrossRefGoogle Scholar
  18. Fong PP (1998) Zebra mussel spawning is induced in low concentrations of putative serotonin reuptake inhibitors. Biol Bull 194:143–149CrossRefGoogle Scholar
  19. Fong PP, Hoy CM (2012) Antidepressants (venlafaxine and citalopram) cause foot detachment from the substrate in freshwater snails at environmentally relevant concentrations. Mar Environ Res 45:145–153Google Scholar
  20. Gross-Sorokin MY, Roast SD, Brighty GC (2006) Assessment of feminization of male fish in English rivers by the Environment Agency of England and Wales. Environ Health Perspect 114(suppl 1):147–151Google Scholar
  21. Guler Y, Ford AT (2010) Anti-depressants make amphipods see the light. Aquat Toxicol 99:397–404CrossRefGoogle Scholar
  22. Heberer T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131(1-2):5–17CrossRefGoogle Scholar
  23. Hedgespeth ML, Nilsson PA, Berglund O (2014) Ecological implications of altered fish foraging after exposure to an antidepressant pharmaceutical. Aquat Toxicol 151:84–87CrossRefGoogle Scholar
  24. Hellström G, Magnhagen C (2011) The influence of experience on risk taking: results from a common-garden experiment on populations of Eurasian perch. Behav Ecol Sociobiol 65:1917–1926CrossRefGoogle Scholar
  25. Jung C, Son A, Her N, Zoh KD, Cho J, Yoon Y (2015) Removal of endocrine disrupting compounds, pharmaceuticals, and personal care products in water using carbon nanotubes: a review. J Ind Eng Chem 27:1–11CrossRefGoogle Scholar
  26. Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchak JM, Flick RW (2007) Collapse of a fish population after exposure to a synthetic estrogen. Proc Natl Acad Sci U S A 104:8897–8901CrossRefGoogle Scholar
  27. Klaminder J, Jonsson M, Fick J, Sundelin A, Brodin T (2014) The conceptual imperfection of aquatic risk assessment tests: highlighting the need for tests designed to detect therapeutic effects of pharmaceutical contaminants. Environ Res Lett 9(8):084003CrossRefGoogle Scholar
  28. Klaminder J, Brodin T, Sundelin A, Anderson NJ, Fahlman J, Jonsson M, Fick J (2015) Long-term persistence of an anxiolytic drug (oxazepam) in a large freshwater lake. Environ Sci Tech 49(17):10406–10412CrossRefGoogle Scholar
  29. Klaschka U (2008) The infochemical effect—a new chapter in ecotoxicology. Environ Sci Pollut Res 15:452–462CrossRefGoogle Scholar
  30. Kolodziej EP, Gray JL, Sedlak DL (2003) Quantification of steroid hormones with pheromonal properties in municipal wastewater effluent. Environ Toxicol Chem 22:2622–2629CrossRefGoogle Scholar
  31. Kolpin DW, Furlong ET, Meyer MT et al (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999–2000: a National reconnaissance. Environ Sci Tech 36:1202–1211CrossRefGoogle Scholar
  32. Kümmerer K (2008) Pharmaceuticals in the environment. Sources, fate, effects and risks. Springer, BerlinGoogle Scholar
  33. Lamichhane K, Garcia SN, Huggett DB et al (2014) Exposures to a selective serotonin reuptake inhibitor (SSRI), sertraline hydrochloride, over multiple generations: changes in life history traits in Ceriodaphnia dubia. Ecotoxicol Environ Saf 101:124–130CrossRefGoogle Scholar
  34. Länge R, Hutchinson TH, Croudace CP, Siegmund F, Schweinfurth H, Hampe P, Panter GH, Sumpter JP (2001) Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ Toxicol Chem 20(6):1216–1227CrossRefGoogle Scholar
  35. Lazzara R, Blazquez 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 106:123–130CrossRefGoogle Scholar
  36. Lemmnitz G, Schuppe H, Wolff HG (1989) Neuromotor bases of the escape behavior of Nassa mutabilis. J Exp Biol 143:493–507Google Scholar
  37. Loos R, Gawlik BM, Locoro G et al (2009) EU-wide survey of polar organic persistent pollutants in European river waters. Environ Pollut 157:561–568CrossRefGoogle Scholar
  38. Luna TO, Plautz SC, Salice CJ (2013) Effects of 17α-ethynylestradiol, fluoxetine, and the mixture on life history traits and population growth rates in a freshwater gastropod. Environ Toxicol Chem 32(12):2771–2778CrossRefGoogle Scholar
  39. Lürling M (2012) Infodisruption: pollutants interfering with the natural chemical information conveyance in aquatic systems. In: Brönmark C, Hansson L-A (eds) Chemical ecology in aquatic systems. Oxford University Press, New York, NY, pp 250–271CrossRefGoogle Scholar
  40. Lürling M, Scheffer M (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol Evol 22:374–379CrossRefGoogle Scholar
  41. Lürling M, Van Donk E (1997) Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnol Oceanogr 42:783–788CrossRefGoogle Scholar
  42. Mehinto AC, Hill EM, Tyler CR (2010) Uptake and biological effects of environmentally relevant concentrations of the nonsteroidal anti-inflammatory pharmaceutical diclofenac in rainbow trout (Oncorhynchus mykiss). Environ Sci Tech 44:2176–2182CrossRefGoogle Scholar
  43. Mennigen JA, Martyniuk CJ, Crump K et al (2008) Effects of fluoxetine on the reproductive axis of female goldfish (Carassius auratus). Physiol Genomics 35:273–282CrossRefGoogle Scholar
  44. Mennigen JA, Lado WE, Zamora JM et al (2010) Waterborne fluoxetine disrupts the reproductive axis in sexually mature male goldfish, Carassius auratus. Aquat Toxicol 100:354–364CrossRefGoogle Scholar
  45. 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 Crit Rev 14(5-7):387–412CrossRefGoogle Scholar
  46. Oaks JL, Gilbert M, Virani MZ et al (2004) Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 427:630–633CrossRefGoogle Scholar
  47. Olsén KH (2011) Effects of pollutants on olfactory mediated behaviors in fish and crustaceans. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer Science + Business Media LLC, New York, NY, pp 507–529, Doi:  10.1007/978-0-387-77101-4-26 Google Scholar
  48. Orlando EF, Ellestad LE (2014) Sources, concentrations, and exposure effects of environmental gestagens on fish and other aquatic wildlife, with an emphasis on reproduction. Gen Comp Endocrinol 203:241–249CrossRefGoogle Scholar
  49. OSPAR Commission (2013) Background Document on Clotrimazole (2013 update). Publication Number: 595/2013. ISBN 978-1-909159-28-0.Google Scholar
  50. Overturf MD, Overturf CL, Baxter D et al (2012) Early life-stage toxicity of eight pharmaceuticals to the fathead minnow, Pimephales promelas. Arch Environ Contam Toxicol 62:455–464CrossRefGoogle Scholar
  51. Painter MM, Buerkley MA, Julius ML et al (2009) Antidepressants at environmentally relevant concentrations affect predator avoidance behavior of larval fathead minnows (Pimephales promelas). Environ Toxicol Chem 28:2677–2684CrossRefGoogle Scholar
  52. Paul VJ, Ritson-Williams R, Sharp K (2011) Marine chemical ecology in benthic environments. Nat Prod Rep 28:345–387CrossRefGoogle Scholar
  53. Pohnert G, Steinke M, Tollrian R (2007) Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends Ecol Evol 22:198–204CrossRefGoogle Scholar
  54. Quinlan EL, Nietch CT, Blocksom K, Lazorchak JM, Batt AL, Griffiths R, Klemm DJ (2011) Temporal dynamics of periphyton exposed to tetracycline in stream mesocosms. Environ Sci Tech 45:10684–10690CrossRefGoogle Scholar
  55. Rastogi T, Leder C, Kummerer K (2014) Designing green derivatives of beta-blocker metoprolol: a tiered approach for green and sustainable pharmacy and chemistry. Chemosphere 111:493–499CrossRefGoogle Scholar
  56. Relyea RA, Diecks N (2008) An unforeseen chain of events: lethal effects of pesticides on frogs at sublethal concentrations. Ecol Appl 18:1728–1742CrossRefGoogle Scholar
  57. Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171CrossRefGoogle Scholar
  58. Ringelberg J (2009) Diel vertical migration of zooplankton in lakes and oceans: causal explanations and adaptive significances. Springer, New York, NY. ISBN ISBN 978-90-481-3092-4Google Scholar
  59. Rolfe R, Barrett J, Perry R (2001) Electrophysiological analysis of responses of adult females of Brugia pahangi to some chemicals. Parasitology 122:347–357CrossRefGoogle Scholar
  60. Rosi-Marshall EJ, Royer TV (2012) Pharmaceutical compounds and ecosystem function: an emerging research challenge for aquatic ecologists. Ecosystems 15:867–880CrossRefGoogle Scholar
  61. Sacher F, Ehmann M, Gabriel S, Graf C, Brauch HJ (2008) Pharmaceutical residues in the river Rhine - results of a one-decade monitoring programme. J Environ Monit 10:664–670CrossRefGoogle Scholar
  62. Santos LHMLM, Araújo AN, Fachini A et al (2010) Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mater 175:45–95CrossRefGoogle Scholar
  63. Schultz MM, Painter MM, Bartell SE, Logue A, Furlong ET, Werner SL, Schoenfuss HL (2011) Selective uptake and biological consequences of environmentally relevant antidepressant pharmaceutical exposures on male fathead minnows. Aquat Toxicol 104:38–47CrossRefGoogle Scholar
  64. Stacey N (2011) Hormonally derived sex pheromones in fishes. In: Norris OD, Lopez KH (eds) Hormones and reproduction of vertebrates. Elsevier, Atlanta, GAGoogle Scholar
  65. Tollrian R, Harvell D (1999) The ecology and evolution of inducible defenses. The ecology and evolution of inducible defenses. Princeton University Press, New York, NYGoogle Scholar
  66. Troyer RR, Turner AM (2015) Chemosensory perception of predators by larval amphibians depends on water quality. PLoS One 10(6):e0131516CrossRefGoogle Scholar
  67. Van Buskirk J, Ferrari M, Kueng D, Napflin K, Ritter N (2011) Prey risk assessment depends on conspecific density. Oikos 120:1235–1239CrossRefGoogle Scholar
  68. Van Donk E, Ianora A, Vos M (2011) Induced defences in marine and freshwater phytoplankton: a review. Hydrobiologia 668:3–19CrossRefGoogle Scholar
  69. Vos M, Vet LEM, Wackers FL et al (2006) Infochemicals structure marine, terrestrial and freshwater food webs: implications for ecological informatics. Ecol Inform 1:23–32CrossRefGoogle Scholar
  70. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  71. Wiklund AE, Oskarsson H, Thorsn G et al (2011) Behavioural and physiological responses to pharmaceutical exposure in macroalgae and grazers from a Baltic Sea littoral community. Aquat Biol 14:29–39CrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  • Ellen Van Donk
    • 1
    • 2
  • Scott Peacor
    • 1
    • 3
  • Katharina Grosser
    • 1
    • 4
  • Lisette N. De Senerpont Domis
    • 1
    • 5
  • Miquel Lürling
    • 1
    • 5
  1. 1.Department of Aquatic EcologyNetherlands Institute of Ecology (NIOO-KNAW)WageningenNetherlands
  2. 2.Department of Ecology and BiodiversityUniversity of UtrechtUtrechtNetherlands
  3. 3.Department of Fisheries and WildlifeMichigan State UniversityEast LansingUSA
  4. 4.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  5. 5.Aquatic Ecology & Water Quality Management Group, Dept. Environmental SciencesWageningen UniversityWageningenNetherlands

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