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Size-dependent bioaccumulation of metals in the amphipod Gammarus zaddachi (Sexton 1912) from the River Hunte (Germany) and its relationship to the permeable body surface area

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Abstract

The present study aims to evaluate and verify toxicokinetic models for the bioaccumulation of Cd, Pb, Cu and Zn in the gammaridean amphipod Gammarus zaddachi (Sexton 1912) from the River Hunte (Germany). The bioaccumulation experiment was performed in a static system, taking into account the effect of body size on bioaccumulation and the relationship between toxicokinetic model parameters and the permeable body surface area of gammarids. A modified two-compartment model was employed, which was not limited to changes in both biomass of gammarids in the experiments and metal exposure concentrations; the result was a significant model fit. The parameters k 1 and BCF decreased with increasing body length (BL) of G. zaddachi, while no such trend was observed for k 2 among BLs ranging from 8.1 to 24.1 mm. The nonlinear relationship was successfully quantified using an inverse-sigmoid logistic model as a basis for subsequent adjustment of the toxicokinetic uptake models. Moreover, k 1 and BCF increased with increasing specific surface area (SSA, i.e., the ratio of permeable body surface area to body volume) of gammarids. This relationship was successfully quantified using an extended Langmuir equation, which was derived by combining the inversely sigmoid logistic relationship between k 1, BCFExp and BL with a single-exponential-decay relationship between SSA and BL reported previously, implying that the size-dependent bioconcentration was dominated by the SSA-related uptake. Thus, with increasing SSA, k1 and BCF at first increased sharply, for smaller SSAs with larger BLs, but then approached saturation for larger SSAs with smaller BLs. In addition, field-to-experimental BCF ratios (BCFField/BCFExp) were determined, yielding values around 1 (indicating equality of the two BCFs) for Pb and Cd for smaller amphipods, but much higher values for larger sizes. The BCF ratios for Cu and Zn were much larger than 1 for both smaller and larger sizes. However, when seasonal changes in BL distribution of gammarids were considered, no significant differences were observed between annual ranges of BCFField and BCFExp for Pb and Cd. Considering the seasonal changes in BL distribution as well as the Cu and Zn metabolic requirements, no significant difference was observed for Cu, but still a significant one for Zn. From an ecotoxicological perspective we suggest that in the verification of toxicokinetic models not only field-to-experimental BCF ratios should be taken into account, but also several ecological factors such as the size distribution of the animal populations under study as well as, if applicable, metabolic requirements for essential elements.

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References

  • Amiard-Triquet, C., F. Rainglet, C. Larroux, F. Regoli & H. Hummel, 1998. Metallothioneins in Arctic bivalves. Ecotoxicology and Environmental Safety 41: 96–102.

    PubMed  Google Scholar 

  • Anonymous, 1999. Chemikaliengesetz: Gesetz zum Schutz vor gefährlichen Stoffen. Anhang 1 (zu §19a Abs. 1)-Grundsätze der guten Laborpraxis (GLP). In Steinberg, C., H. Bernhardt, W. Calmano, H. Klapper & R.-D. Wilken (eds), Handbuch angewandte Limnologie, Chapter IX-5, 7. Erg.Lfg. 4/99. ecomed, Landsberg am Lech.

  • Bäumer, H.-P., A. van der Linde & G.-P. Zauke, 1991. Structural equation models, applications in biological monitoring. Biometrie und Informatik in Medizin und Biologie 22: 156–178.

    Google Scholar 

  • Bernds, D., D. Wübben & G.-P. Zauke, 1998. Bioaccumulation of trace metals in polychaetes from the German Wadden Sea: Evaluation and verification of toxicokinetic models. Chemosphere 37: 2573–2587.

    Google Scholar 

  • Brody, S., 1945. Bioenergetics and Growth. Reinhold Publishing Corporation, New York: 1023.

    Google Scholar 

  • Büttner, J. R., R. Borth, H. J. Boutwell, P. M. G. Broughton & R. C. Bowyer, 1980. Approved recommendation (1978) on quality control in clinical chemistry. Journal of Clinical Chemistry and Clinical Biochemistry 18: 78–88.

    Google Scholar 

  • Caltran, H. & P. Silan, 1996. Gill filaments of Liza ramada, a biotope for ectoparasites: Surface area acquisition using image analysis and growth models. Journal of Fish Biology 49: 1267–1279.

    Google Scholar 

  • Chiaravalle, K., J. Hughes, R. Javonillo & L. Deegan, 1997. Tidal river riffle habitats support high diversity and abundance of gammaridean amphipods. Biological Bulletin 193: 283–285.

    Google Scholar 

  • Clason, B., 2002. Toxicokinetik von Schwermetallen in marinen Gammariden auf großer geografischer Maßstabsebene (Chaetogammarus marinus-Südengland, Gammarus oceanicus-Nordnorwegen und Paramoera walkeri-Casey, Antarktis). PhD thesis, Fachbereich Bio-, Geo und Umweltwissenschaften. Oldenburg, Carl von Ossietzky Universität: 117 pp.

    Google Scholar 

  • Clason, B., S. Duquesne, M. Liess, R. Schulz & G.-P. Zauke, 2003. Bioaccumulation of trace metals in the Antarctic amphipod Paramoera walkeri (Stebbing, 1906): Comparison of two-compartment and hyperbolic toxicokinetic models. Aquatic Toxicology 65: 117–140.

    PubMed  Google Scholar 

  • Clason, B., B. Gulliksen & G. P. Zauke, submitted. Assessment of two-compartment models as predictive tools for the bioaccumulation of trace metals in the amphipod Gammarus oceanicus Segerstråle, 1947 from Grunnfjord (Northern Norway): Science of the Total Environment.

  • Clason, B., W. J. Langston & G. P. Zauke, in press. Bioaccumulation of trace metals in the amphipod Chaetogammarus marinus (Leach, 1815) from the Avon-and Tamar-estuary (Devon, UK): Comparison of two-compartment and hyperbolic toxicokinetic models. Marine Environmental Research.

  • Clason, B. & G.-P. Zauke, 2000. Bioaccumulation of trace metals in marine and estuarine amphipods: Evaluation and verification of toxicokinetic models. Canadian Journal of Fisheries and Aquatic Sciences 57: 1410–1422.

    Google Scholar 

  • Dallinger, R., 1995. Mechanisms of metal incorporation into cells. In Cajaraville, M. P. (ed), Cell Biology in Environmental Toxicology. Universidad del Pais Vasco, Bilbao: 135–154.

    Google Scholar 

  • Dos Santos, J. & M. Jobling, 1995. Test of a food consumption model for the Atlantic cod. ICES Journal of Marine Science 52: 209–219.

    Google Scholar 

  • Fisher, N. S., P. Bjerregaard & S. W. Fowler, 1983a. Interaction of marine plankton with transuranic elements. 1. Biokinetics of neptunium, americium, and californium in phytoplankton. Limnology and Oceanography 28: 432–447.

    Google Scholar 

  • Fisher, N. S., P. Bjerregaard & S. W. Fowler, 1983b. Interaction of marine plankton with transuranic elements. 3. Biokinetics of americium in euphausiids. Marine Biology 75: 261–268.

    Google Scholar 

  • Fisher, N. S., J. L. Teyssie, S. Krishnaswami & M. Baskaran, 1987. Accumulation of Th, Pb, U, and Ra in marine phytoplankton and its geochemical significance. Limnology and Oceanography 32: 131–142.

    Google Scholar 

  • Gilek, M., N. Bjork & C. Naf, 1996. Influence of body size on the uptake, depuration, and bioaccumulation of polychlorinated biphenyl congeners by Baltic Sea blue mussels, Mytilus edulis. Marine Biology 125: 499–510.

    Google Scholar 

  • Hendrickx, M. E., F. Paezosuna & H. M. Zazuetpadilla, 1998. Biology and biochemical composition of the deep-water shrimp Heterocarpus vicarius Faxon (Crustacea: Decapoda: Caridea: Pandalidae) from the southeastern Gulf of California, Mexico. Bulletin of Marine Science 63: 265–275.

    Google Scholar 

  • Hoffer, S. A., 1972. Some aspects of the life cycle of Parathemisto abyssorum (Amphipoda: Hyperiidea) in the Gulf of St. Lawrence. Canadian Journal of Zoology 50: 1175–1178.

    Google Scholar 

  • Jeckel, W. H., R. R. Roth & L. Ricci, 1996. Patterns of tracemetal distribution in tissues of Pleoticus muelleri (Crustacea: Decapoda: Solenoceridae). Marine Biology 125: 297–306.

    Google Scholar 

  • Kahle, J., B. Clason & G.-P. Zauke, 2003. Sequential determination of Cd, Cu, Pb, Co and Ni in marine invertebrates by graphite furnace atomic absorption spectroscopy and Zeeman background correction. Varian AA at Work No. 129: 1–15.

    Google Scholar 

  • Kahle, J. & G.-P. Zauke, 2002. Bioaccumulation of trace metals in the copepod Calanoides acutus from the Weddell Sea (Antarctica): Comparison of two-compartment and hyperbolic toxicokinetic models. Aquatic Toxicology 59: 115–135.

    PubMed  Google Scholar 

  • Klerks, P. L. & J. S. Levinton, 1989. Effects of heavy metals in a polluted aquatic ecosystem. In Levin, S. A., M. A. Harwell, J. R. Kelly & K. D. Kimball (eds), Ecotoxicology. Problems and Approaches. Springer Verlag, New York: 41–67.

    Google Scholar 

  • Klerks, P. L. & J. S. Weis, 1987. Genetic adaptation to heavy metals in aquatic organisms. A review. Environmental Pollution 45: 173–205.

    PubMed  Google Scholar 

  • Meurs, H.-G. & G.-P. Zauke, 1996. Populationsbiologische Untersuchungen an Gammariden als Grundlage zur Abschätzung von Eingriffen (UVS) in Flußmündungen. Zeitschrift für Ökologie und Naturschutz 5: 107–113.

    Google Scholar 

  • Mulvey, M. & S. A. Diamond, 1991. Genetic factors and tolerance acquisiton in populations exposed to metals and metalloids. In Newmann, M. C. M., A. W. McIntosh (eds), Metal Ecotoxicology-Concepts & Applications. Lewis Publishers, Chelsea: 301–321.

    Google Scholar 

  • Nagel, R. & R. Loskill, 1991. Bioaccumulation in Aquatic Systems. VCH Verlagsgesellschaft, Weinheim.

    Google Scholar 

  • Newman, M. C. & S. V. Mitz, 1988. Size dependence of zinc elimination and uptake from water by mosquitofish Gambusia affinis (Baird and Girard). Aquatic Toxicology 12: 17–32.

    Google Scholar 

  • Nugegoda, D. & P. S. Rainbow, 1988. Zinc Uptake and Regulation by the Sublittoral Prawn Pandalus montagui (Crustacea, Decapoda). Estuarine Coastal and Shelf Science 26: 619–632.

    Google Scholar 

  • Rainbow, P. S., 1993. The significance of trace Metal concentration in marine Invertebrates. In Dallinger, R. & P. S. Rainbow (eds), Ecotoxicology of metals in invertebrates. Lewis Publishers, Boca Raton: 4–23.

    Google Scholar 

  • Rainbow, P. S., 1995. Physiology, physicochemistry and metal uptake-A crustacean perspective. Marine Pollution Bulletin 31: 55–59.

    Google Scholar 

  • Rainbow, P. S., W. Fialkowski & B. D. Smith, 1998. The sandhopper Talitrus saltator as a trace metal biomonitor in the Gulf of Gdansk, Poland. Marine Pollution Bulletin 36: 193–200.

    Google Scholar 

  • Rinderhagen, M., J. Ritterhoff & G.-P. Zauke, 2000. Crustaceans as bioindicators. In Gerhardt, A. (ed.), Biomonitoring of Polluted Water-Reviews on Actual Topics. Trans Tech Publications-Scitech Publications, Environmental Research Forum, Vol. 9. Uetikon, Zürich: 161–194.

    Google Scholar 

  • Ritterhoff, J. & G.-P. Zauke, 1997a. Bioaccumulation of trace metals in Greenland Sea copepod and amphipod collectives on board ship: verification of toxicokinetic model parameters. Aquatic Toxicology 40: 63–78.

    Google Scholar 

  • Ritterhoff, J. & G.-P. Zauke, 1997b. Evaluation of trace metal toxicokinetics in Greenland Sea copepod and amphipod collectives from semi-static experiments on board ship. Polar Biology 17: 242–250.

    Google Scholar 

  • Ritterhoff, J. & G.-P. Zauke, 1997c. Influence of body length, life-history status and sex on trace metal concentrations in selected zooplankton collectives from the Greenland Sea. Marine Pollution Bulletin 34: 614–621.

    Google Scholar 

  • Ritterhoff, J. & G.-P. Zauke, 1998. Potential role of metal-binding proteins in cadmium detoxification in Themisto libellula (Mandt) and Themisto abyssorum Boeck from the Greenland sea. Marine Environmental Research 45: 179–191.

    Google Scholar 

  • Ritterhoff, J., G.-P. Zauke & R. Dallinger, 1996. Calibration of the estuarine amphipods, Gammarus zaddachi Sexton (1912), as biomonitors: toxicokinetics of cadmium and possible role of inducible metal binding proteins in Cd detoxification. Aquatic Toxicology 34: 351–369.

    Google Scholar 

  • Roesijadi, G., 1992. Metallothionein in metal regulation and toxicity in aquatic animals. Aquatic Toxicology 22: 81–114.

    Google Scholar 

  • Roesijadi, G., 1996. Metallothionein and its role in toxic metal regulation. Comparative Biochemistry and Physiology C-Toxicology 113C: 117–123.

    Google Scholar 

  • Skoglund, R. S. & D. L. Swackhamer, 1994. Fate of Hydrophobic Organic Contaminants-Processes Affecting Uptake by Phytoplankton. Environmental Chemistry of Lakes and Reservoirs 237: 559–573.

    Google Scholar 

  • Thomann, R. V., 1981. Equilibrium model of fate of microcontaminants in diverse aquatic food chains. Canadian Journal of Fisheries and Aquatic Sciences 38: 280–296.

    Google Scholar 

  • Timmermans, K. R., E. Spijkerman, M. Tonkes & H. Grovers, 1992. Cadmium and Zinc uptake by two species of aquatic invertebrate predators from dietary and aquaeous sources. Canadian Journal of Fisheries and Aquatic Sciences 49: 655–662.

    Google Scholar 

  • Viarengo, A. & J. A. Nott, 1993. Mini-review. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comparative Biochemistry and Physiology C-Toxicology 104C: 355–372.

    Google Scholar 

  • Wang, W. X. & N. S. Fisher, 1997. Modeling the influence of body size on trace element accumulation in the mussel Mytilus edulis. Marine Ecology-Progress Series 161: 103–115.

    Google Scholar 

  • Wang, W. X. & N. S. Fisher, 1998. Accumulation of trace elements in a marine copepod. Limnology and Oceanography 43: 273–283.

    Google Scholar 

  • Wang, W. X. & N. S. Fisher, 1999. Delineating metal accumulation pathways for marine invertebrates. Science of the Total Environment 238: 459–472.

    Google Scholar 

  • Wang, X. & G.-P. Zauke, 2002. Relationship between growth parameters of the amphipod Gammarus zaddachi (Sexton 1912) and the permeable body surface area determined by the acid-base titration method. Hydrobiologia 482: 179–189.

    Google Scholar 

  • Wang, X. L., S. Harada, M. Watanabe, H. Koshikawa & H. J. Geyer, 1996. Modelling the bioconcentration of hydrophobic organic chemicals in aquatic organisms. Chemosphere 32: 1783–1793.

    Google Scholar 

  • Wang, X. L., Y. J. Ma, W. J. Yu & H. J. Geyer, 1997. Twocompartment thermodynamic model for bioconcentration of hydrophobic organic chemicals by alga: Quantitative relationship between bioconcentration factor and surface area of marine algae or octanol/water partition coefficient. Chemosphere 35: 1781–1797.

    Google Scholar 

  • Wilkinson, L., 2000. Nonparametric statistics. In Anonymous (eds), SYSTAT 10: Statistics II. SPSS Inc, Chicago, IL: 197–218.

    Google Scholar 

  • Wright, D. A., 1986. Trace metal uptake and sodium regulation in Gammarus marinus from metal polluted estuaries in England. Journal of the Marine Biological Association of the United Kingdom 66: 83–92.

    Google Scholar 

  • Zauke, G.-P., M. Krause & A. Weber, 1996a. Trace metals in mesozooplankton of the North Sea: Concentrations in different taxa and preliminary results on bioaccumulation in copepod collectives (Calanus finmarchicus / C. helgolandicus). Internationale Revue der Gesamten Hydrobiologie 81: 141–160.

    Google Scholar 

  • Zauke, G.-P. & G. Petri, 1993. Metal concentrations in Antarctic Crustacea. The problem of background levels. In Dallinger, R. & P. S. Rainbow (eds), Ecotoxicology of Metals in Invertebrates. Lewis Publishers, Boca Raton: 73–101.

    Google Scholar 

  • Zauke, G.-P., G. Petri, J. Ritterhoff & H.-G. Meurs, 1996b. Theoretical background for the assessment of the quality status of ecosystems: lessons from studies of heavy metals in aquatic invertebrates. Senckenbergiana Maritima 27: 207–214.

    Google Scholar 

  • Zauke, G.-P., R. von Lemm, H.-G. Meurs & W. Butte, 1995. Validation of estuarine gammarid collectives (Amphipoda: Crustacea) as biomonitors for cadmium in semi-controlled toxicokinetic flow-through experiments. Environmental Pollution 90: 209–219.

    PubMed  Google Scholar 

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Wang, X., Zauke, GP. Size-dependent bioaccumulation of metals in the amphipod Gammarus zaddachi (Sexton 1912) from the River Hunte (Germany) and its relationship to the permeable body surface area. Hydrobiologia 515, 11–28 (2004). https://doi.org/10.1023/B:HYDR.0000027314.07061.b0

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