Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Effects of a pharmaceutical mixture at environmentally relevant concentrations on the amphipod Gammarus fossarum

Sabine Dietrich A C , Shana Dammel A , Florian Ploessl B , Franz Bracher B and Christian Laforsch A
+ Author Affiliations
- Author Affiliations

A Department of Biology II, Ludwig-Maximilians-University Munich, Großhaderner Straße 2, 82152 Planegg-Martinsried, Germany.

B Department of Pharmacy, Ludwig-Maximilians-University Munich, Butenandtstraße 5, 81377 Munich, Germany.

C Corresponding author. Email: dietrich@biologie.uni-muenchen.de

Marine and Freshwater Research 61(2) 196-203 https://doi.org/10.1071/MF09048
Submitted: 6 March 2009  Accepted: 30 July 2009   Published: 25 February 2010

Abstract

The continuous discharge of pharmaceuticals into the environment results in the chronic exposure of aquatic organisms to complex drug mixtures. We examined the influence of a mixture of pharmaceuticals (carbamazepine (CBZ), diclofenac (DIC), metoprolol (MET) and 17α-ethinylestradiol (EE2)) at environmentally relevant (‘env’) and artificially high (‘high’) concentrations on Gammarus fossarum. Different sublethal responses such as moulting, reproduction and the content of the energy-storage component glycogen were analysed. The drug mixture influenced the moulting behaviour of gammarids at both the ‘env’ and ‘high’ concentration levels, leading to a discontinuous increase of body length in successive moults, compared with the constant increase of body length in the control treatment. Moreover, the time between successive moults of animals exposed to the ‘env’ and ‘high’ pharmaceutical concentrations was decreased because of shortened intermoult periods. We observed no significant impact of the pharmaceuticals on reproduction. In addition, the content of glycogen was not significantly affected by the drug mixture. Permanent exposure of G. fossarum to a wider range of pharmaceuticals in natural aquatic systems may influence moulting behaviour and accompanied life-history parameters, followed by severe ecological consequences as gammarids play an important role in many freshwater ecosystems of the northern hemisphere.

Additional keywords: amphipoda, life-history traits, micropollutants.


Acknowledgements

This work was financially supported by a PhD scholarship from Studienstiftung des deutschen Volkes to Sabine Dietrich. We thank Jonathan Jeschke and Carola Winkelmann for advice, Mechthild Kredler for assistance in the laboratory, Jennifer Lohr for linguistic improvements and two anonymous reviewers for their helpful comments on the manuscript. The handling procedure of the amphipods was done in accordance with institutional guidelines.


References

Adler, P. , Steger-Hartmann, T. , and Kalbfus, W. (2001). Vorkommen natürlicher und synthetischer östrogener Steroide in Wässern des süd- und mitteldeutschen Raumes. Acta Hydrochimica et Hydrobiologica 29, 227–241.
CrossRef | CAS |

Altenburger, R. , Walter, H. , and Grote, M. (2004). What contributes to the combined effect of a complex mixture? Environmental Science and Technology 38, 6353–6362.
CrossRef | CAS | PubMed |

Baldwin, W. S. , Milam, D. L. , and LeBlanc, G. A. (1995). Physiological and biochemical perturbations in Daphnia magna following exposure to the model environmental estrogen diethylstilbestrol. Environmental Toxicology and Chemistry 14, 945–952.
CrossRef | CAS |

Bergmeyer H. U. (1985). ‘Methods of Enzymatic Analysis. Vol. VI.’ (Verlag Chemie: Weinheim, Germany.)

Blockwell, S. J. , Taylor, E. J. , Jones, I. , and Pascoe, D. (1998). The influence of fresh water pollutants and interaction with Asellus aquaticus (L.) on the feeding activity of Gammarus pulex (L.). Archives of Environmental Contamination and Toxicology 34, 41–47.
CrossRef | CAS | PubMed |

Borgmann, U. , Bennie, D. T. , Ball, A. L. , and Palabrica, V. (2007). Effect of a mixture of seven pharmaceuticals on Hyalella azteca over multiple generations. Chemosphere 66, 1278–1283.
CrossRef | CAS | PubMed |

Buikema, A. L. , and Benfield, E. F. (1979). Use of macroinvertebrate life-history information in toxicity tests. Journal of the Fisheries Research Board of Canada 36, 321–328.
CAS |

Chang, E. S. , Bruce, M. J. , and Tamone, S. L. (1993). Regulation of crustacean molting – a multi-hormonal system. American Zoologist 33, 324–329.
CAS |

Christensen, A. M. , Faaborg-Andersen, S. , Ingerslev, F. , and Baun, A. (2007). Mixture and single-substance toxicity of selective serotonin reuptake inhibitors toward algae and crustaceans. Environmental Toxicology and Chemistry 26, 85–91.
CrossRef | CAS | PubMed |

Cleuvers, M. (2003). Aquatic ecotoxicity of pharmaceuticals including the assessment of combination effects. Toxicology Letters 142, 185–194.
CrossRef | CAS | PubMed |

Cleuvers, M. (2004). Mixture toxicity of the anti-inflammatory drugs diclofenac, ibuprofen, naproxen, and acetylsalicylic acid. Ecotoxicology and Environmental Safety 59, 309–315.
CrossRef | CAS | PubMed |

Cold, A. , and Forbes, V. E. (2004). Consequences of a short pulse of pesticide exposure for survival and reproduction of Gammarus pulex. Aquatic Toxicology 67, 287–299.
CrossRef | CAS | PubMed |

Daughton, C. G. , and Ternes, T. A. (1999). Pharmaceuticals and personal care products in the environment: Agents of subtle change? Environmental Health Perspectives 107, 907–938.
CrossRef | CAS | PubMed |

Dick, J. T. A. , Faloon, S. E. , and Elwood, R. W. (1998). Active brood care in an amphipod: Influences of embryonic development, temperature and oxygen. Animal Behaviour 56, 663–672.
CrossRef | PubMed |

Dzialowski, E. M. , Turner, P. K. , and Brooks, B. W. (2006). Physiological and reproductive effects of beta adrenergic receptor antagonists in Daphnia magna. Archives of Environmental Contamination and Toxicology 50, 503–510.
CrossRef | CAS | PubMed |

Eggers T. O., and Martens A. (2001). ‘Bestimmungsschlüssel der Süßwasser-Amphipoda (Crustacea) Deutschlands.’ (Lauterbornia 42: Dinkelscherben, Germany.)

Elwood, R. , Gibson, J. , and Neil, S. (1987). The amorous Gammarus: size assortative mating in G. pulex. Animal Behaviour 35, 1–6.
CrossRef |

Fent, K. , Weston, A. A. , and Caminada, D. (2006). Ecotoxicology of human pharmaceuticals. Aquatic Toxicology 76, 122–159.
CrossRef | CAS | PubMed |

Ferrari, B. , Paxéus, N. , Lo Giudice, R. , Pollio, A. , and Garric, J. (2003). Ecotoxicological impact of pharmaceuticals found in treated wastewaters: study of carbamazepine, clofibric acid, and diclofenac. Ecotoxicology and Environmental Safety 55, 359–370.
CrossRef | CAS | PubMed |

Goto, T. , and Hiromi, J. (2003). Toxicity of 17α-ethynylestradiol and norethindrone, constituents of an oral contraceptive pill to the swimming and reproduction of cladoceran Daphnia magna, with special reference to their synergetic effect. Marine Pollution Bulletin 47, 139–142.
CrossRef | CAS | PubMed |

Greenwood, P. J. , and Adams, J. (1984). Sexual dimorphism in Gammarus pulex: the effect of current flow on pre-copula pair formation. Freshwater Biology 14, 203–209.
CrossRef |

Halling-Sørensen, B. , Nielsen, S. N. , Lanzky, P. F. , Ingerslev, F. , and Holten Lützhøft, H. C. , et al. (1998). Occurrence, fate and effects of pharmaceutical substances in the environment – A review. Chemosphere 36, 357–393.
CrossRef | PubMed |

Heberer, T. (2002). Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicology Letters 131, 5–17.
CrossRef | CAS | PubMed |

Henry, T. B. , and Black, M. C. (2007). Mixture and single-substance acute toxicity of selective serotonin reuptake inhibitors in Ceriodaphnia dubia. Environmental Toxicology and Chemistry 26, 1751–1755.
CrossRef | CAS | PubMed |

Hynes, H. B. N. (1955). The reproductive cycle of some British freshwater Gammaridae. Journal of Animal Ecology 24, 352–387.
CrossRef |

Kaushik, N. K. , and Hynes, H. B. N. (1971). Fate of dead leaves that fall into streams. Archiv für Hydrobiologie 68, 465–515.


Kolpin, D. W. , Furlong, E. T. , Meyer, M. T. , Thurman, E. M. , and Zaugg, S. D. , et al. (2002). Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams, 1999–2000: A national reconnaissance. Environmental Science and Technology 36, 1202–1211.
CrossRef | CAS | PubMed |

Kreuzinger, N. , Clara, M. , Strenn, B. , and Vogel, B. (2004). Investigation on the behaviour of selected pharmaceuticals in the groundwater after infiltration of treated wastewater. Water Science and Technology 50, 221–228.
CAS | PubMed |

Ladewig, V. , Jungmann, D. , Köhler, H. R. , Schirling, M. , and Triebskorn, R. , et al. (2006). Population structure and dynamics of Gammarus fossarum (Amphipoda) upstream and downstream from effluents of sewage treatment plants. Archives of Environmental Contamination and Toxicology 50, 370–383.
CrossRef | CAS | PubMed |

Laforsch, C. , Beccara, L. , and Tollrian, R. (2006). Inducible defenses: The relevance of chemical alarm cues in Daphnia. Limnology and Oceanography 51, 1466–1472.


Lawrence, J. R. , Swerhone, G. D. W. , Wassenaar, L. I. , and Neu, T. R. (2005). Effects of selected pharmaceuticals on riverine biofilm communities. Canadian Journal of Microbiology 51, 655–669.
CrossRef | CAS | PubMed |

Lawrence, J. R. , Swerhone, G. D. W. , Topp, E. , Korber, D. R. , and Neu, T. R. , et al. (2007). Structural and functional responses of river biofilm communities to the nonsteroidal anti-inflammatory diclofenac. Environmental Toxicology and Chemistry 26, 573–582.
CrossRef | CAS | PubMed |

Lürling, M. , Sargant, E. , and Roessink, I. (2006). Life-history consequences for Daphnia pulex exposed to pharmaceutical carbamazepine. Environmental Toxicology 21, 172–180.
CrossRef | PubMed |

MacNeil, C. , Dick, J. T. A. , and Elwood, R. W. (1999). The dynamics of predation on Gammarus spp. (Crustacea: Amphipoda). Biological Reviews of the Cambridge Philosophical Society 74, 375–395.
CrossRef |

MacNeil, C. , Platvoet, D. , and Dick, J. T. A. (2008). Potential roles for differential body size and microhabitat complexity in mediating biotic interactions within invasive freshwater amphipod assemblages. Fundamental and Applied Limnology 172, 175–182.
CrossRef |

Marques, C. R. , Abrantes, N. , and Gonçalves, F. (2004). Life-history traits of standard and autochthonous cladocerans: I. Acute and chronic effects of acetylsalicylic acid. Environmental Toxicology 19, 518–526.
CrossRef | CAS | PubMed |

McCahon, C. P. , and Pascoe, D. (1988a). Use of Gammarus pulex (L.) in safety evaluation tests: culture and selection of a sensitive life stage. Ecotoxicology and Environmental Safety 15, 245–252.
CrossRef | CAS | PubMed |

McCahon, C. P. , and Pascoe, D. (1988b). Cadmium toxicity to the freshwater amphipod Gammarus pulex (L.) during the molt cycle. Freshwater Biology 19, 197–203.
CrossRef | CAS |

McCahon, C. P. , and Pascoe, D. (1988c). Increased sensitivity to cadmium of the freshwater amphipod Gammarus pulex (L.) during the reproductive period. Aquatic Toxicology (Amsterdam, Netherlands) 13, 183–193.
CrossRef | CAS |

OECD (2004). OECD guidelines for the testing of chemicals, no. 219. Sediment-water Chironomid toxicity test using spiked water. Organization for Economic Cooperation and Development, Paris.

Oetken, M. , Nentwig, G. , Löffler, D. , Ternes, T. , and Oehlmann, J. (2005). Effects of pharmaceuticals on aquatic invertebrates. Part I. The antiepileptic drug carbamazepine. Archives of Environmental Contamination and Toxicology 49, 353–361.
CrossRef | CAS | PubMed |

Pöckl, M. (1992). Effects of temperature, age and body size on moulting and growth in the freshwater amphipods Gammarus fossarum and G. roeseli. Freshwater Biology 27, 211–225.
CrossRef |

Rohweder U. (2003). Arzneimittel in der Umwelt, Auswertung der Untersuchungsergebnisse. Bund/Länderausschuss für Chemikaliensicherheit (BLAC), Bericht an die 61. Umweltministerkonferenz, Hamburg, Gemany.

Schill, R. O. , and Köhler, H. R. (2004). Does the environment or the source of the population define stress status and energy supply in the freshwater amphipod, Gammarus fossarum? Ecotoxicology 13, 683–695.
CrossRef | CAS | PubMed |

Schirling, M. , Jungmann, D. , Ladewig, V. , Ludwichowski, K. U. , and Nagel, R. , et al. (2006). Bisphenol A in artificial indoor streams: II. Stress response and gonad histology in Gammarus fossarum (Amphipoda). Ecotoxicology (London, England) 15, 143–156.
CrossRef | CAS | PubMed |

Schwaiger, J. , Ferling, H. , Mallow, U. , Wintermayr, H. , and Negele, R. D. (2004). Toxic effects of the non-steroidal anti-inflammatory drug diclofenac Part 1: histopathological alterations and bioaccumulation in rainbow trout. Aquatic Toxicology 68, 141–150.
CrossRef | CAS | PubMed |

Schwarzenbach, R. P. , Escher, B. I. , Fenner, K. , Hofstetter, T. B. , and Johnson, C. A. , et al. (2006). The challenge of micropollutants in aquatic systems. Science 313, 1072–1077.
CrossRef | CAS | PubMed |

Sengl M., and Schüssler W. (2004). Arzneimittel in der Umwelt. Bayerisches Landesamt für Wasserwirtschaft, Schlußbericht, München, Germany.

Sheader, M. (1983). The reproductive biology and ecology of Gammarus duebeni (Crustacea: Amphipoda) in southern England. Journal of the Marine Biological Association of the United Kingdom 63, 517–540.
CrossRef |

Sheader, M. (1996). Factors influencing egg size in the gammarid amphipod Gammarus insensibilis. Marine Biology 124, 519–526.
CrossRef |

Sutcliffe, D. W. , Carrick, T. R. , and Willoughby, L. G. (1981). Effects of diet, body size, age and temperature on growth rates in the amphipod Gammarus pulex. Freshwater Biology 11, 183–214.
CrossRef |

Ternes, T. A. (1998). Occurrence of drugs in German sewage treatment plants and rivers. Water Research 32, 3245–3260.
CrossRef | CAS |

Triebskorn, R. , Casper, H. , Heyd, A. , Eikemper, R. , and Köhler, H. R. , et al. (2004). Toxic effects of the non-steroidal anti-inflammatory drug diclofenac Part II. Cytological effects in liver, kidney, gills and intestine of rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 68, 151–166.
CrossRef | CAS | PubMed |

Ward, P. I. (1983). Advantages and a disadvantage of large size for male Gammarus pulex (Crustacea: Amphipoda). Behavioral Ecology and Sociobiology 14, 69–76.
CrossRef |

Winkelmann, C. , and Koop, J. H. E. (2007). The management of metabolic energy storage during the life cycle of mayflies: a comparative field investigation of the collector-gatherer Ephemera danica and the scraper Rhithrogena semicolorata. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 177, 119–128.
CrossRef | PubMed |

Winkelmann, C. , Worischka, S. , Koop, J. H. E. , and Benndorf, J. (2007). Predation effects of benthivorous fish on grazing and shredding macroinvertebrates in a detritus-based stream food web. Limnologica 37, 121–128.
CrossRef |

Zou, E. M. , and Fingerman, M. (1997). Effects of estrogenic xenobiotics on molting of the water flea, Daphnia magna. Ecotoxicology and Environmental Safety 38, 281–285.
CrossRef | CAS | PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (6)