Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-23T17:05:26.960Z Has data issue: false hasContentIssue false
  • English
  • Français

Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective

Published online by Cambridge University Press:  10 November 2003

B. SURES
B. SURES
Affiliation:
Zoologisches Institut – Ökologie/Parasitologie, Geb. 07.01, Universität Karlsruhe, Kornblumenstr. 13, 76128 Karlsruhe, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

Intestinal helminths of fish are of increasing interest as potential bioindicators for heavy metal contamination in aquatic habitats. Among these parasites cestodes and acanthocephalans in particular have an enormous heavy metal accumulation capacity exceeding that of established free living sentinels. Metal concentrations several thousand times higher in acanthocephalans than in host tissues were described from field and laboratory studies. Whereas larval stages inside their intermediate hosts are not able to take up high quantities of metals, young worms begin to take up metals immediately after infection of the final host. After four to five weeks of exposure, the parasites reach a steady-state concentration orders of magnitude higher than the ambient water level. Thus, acanthocephalans are not only very effective in taking up metals, but they can also respond very rapidly to changes in environmental exposure. The mechanism which enable acanthocephalans to take up metals from the intestinal lumen of the host appears to be based on the presence of bile acids, which form organo-metallic complexes that are easily absorbed by the worms due to their lipophilicity. Investigations of the environmental conditions affecting metal uptake have shown that the parasites are more consistent and reliable indicators for metal pollution than the host tissues as metal levels of the latter are much more dependent on the water chemistry. Thus, after some years of research on the uptake of metals by acanthocephalans and on the factors affecting metal accumulation in intestinal parasites it should be asked if acanthocephalans meet the criteria commonly accepted for sentinels. If parasites can be considered as promising sentinels, we need reasons for the establishment of ‘new’ indicators. Therefore, this review summarises the present knowledge about parasites as bioindicators and compares the accumulation properties of parasites and established free living indicators. Finally, this review presents possible answers to the question why it could be advantageous to have new and even more sensitive indicators for environmental monitoring purposes.

Keywords

Parasitesacanthocephalanscestodesbioindicatorspollution
Type
Research Article
Information
Parasitology , Volume 126 , Issue 7 , March 2003 , pp. S53 - S60
Copyright
© 2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AMLACHER, E. (1992). Taschenbuch der Fischkrankheiten. Jena Stuttgart, Gustav Fischer Verlag.
BARUš, V., TENORA, F. & KRÁČMAR, S. (2000 a). Heavy metal (Pb, Cd) concentrations in adult tapeworms (Cestoda) parasitizing birds (Aves). Helminthologia 37, 131–136.Google Scholar
BARUš, V., TENORA, F., KRÁČMAR, S. & DVOŘÁČEK, J. (1999 a). Contents of several inorganic substances in European eel infected and uninfected by Anguillicola crassus (Nematoda). Diseases of Aquatic Organisms 37, 135–137.Google Scholar
BARUš, V., TENORA, F., KRÁČMAR, S., HEDVÁBNÝ, J., PROKEš, M. & SITKO, J. (2000 b). Heavy metal (Pb, Cd) concentrations in the Ligula intestinalis (Cestoda) and the host Phalacocorax carbo (Aves). Helminthologia 37, 178–179.Google Scholar
BARUš, V., TENORA, F., KRÁČMAR, S., PROKEš, M. & DVOŘÁČEK, J. (1999 b). Microelement contents in males and females of Anguillicola crassus (Nematoda: Dracunculoidea). Helminthologia 36, 283–285.Google Scholar
BEEBY, A. (2001). What do sentinels stand for? Environmental Pollution 112, 285–298.Google Scholar
BROWN, A. P. & PASCOE, D. (1989). Parasitism and host sensitivity to cadmium: an acanthocephalan infection of the freshwater amphipod Gammarus pulex. Journal of Applied Ecology 26, 473–487.CrossRefGoogle Scholar
COPE, W. G., BARTSCH, M. R., RADA, R. G., BALOGH, S. J., RUPPRECHT, J. E., YOUNG, R. D. & JOHNSON, D. K. (1999). Bioassessment of mercury, cadmium, polychlorinated biphenyls, and pesticides in the Upper Mississippi River with zebra mussels (Dreissena polymorpha). Environmental Science and Technology 33, 4385–4390.CrossRefGoogle Scholar
DALLINGER, R. (1994). Invertebrate organisms as biological indicators of heavy metal pollution. Applied Biochemistry and Biotechnology 48, 27–31.CrossRefGoogle Scholar
DOBSON, A. P. & KEYMER, A. E. (1985). Life history models. In Biology of the Acanthocephala (ed. Crompton, D. W. T. & Nickol, B. B.), pp. 347–384. Cambridge, Cambridge University Press.
DUšEK, L., GELNAR, M. & šEBELOVÁ, š. (1998). Biodiversity of parasites in a freshwater environment with respect to pollution: metazoan parasites of chub (Leuciscus cephalus L.) as a model for statistical evaluation. International Journal for Parasitology 28, 1555–1571.Google Scholar
GUNKEL, G. (1994). Bioindikation in aquatischen Ökosystemen. Jena, Stuttgart, Gustav Fischer Verlag.
HOPPSTOCK, K. & SURES, B. (2003). Platinum group metals. In Elements and their Compounds in the Environment (ed. Merian, E., Anke, M., Ihnat, M. & Stoeppler, M.) Weinheim, WILEY-VCH, in press.
KENNEDY, C. R. (1985). Regulation and dynamics of acanthocephalan populations. In Biology of the Acanthocephala (ed. Crompton, D. W. T. & Nickol, B. B.), pp. 385–416. Cambridge, Cambridge University Press.
KENNEDY, C. R. (1997). Freshwater fish parasites and environmental quality: an overview and caution. Parassitologia 39, 249–254.Google Scholar
LAFFERTY, K. D. (1997). Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.Google Scholar
LAFFERTY, K. D. & KURIS, A. M. (1999). How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925–931.CrossRefGoogle Scholar
MACKENZIE, K., WILLIAMS, H. H., WILLIAMS, B., McVICAR, A. H. & SIDDALL, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85–144.CrossRefGoogle Scholar
MARTIN, M. H. & COUGHTREY, P. J. (1982). Biological Monitoring of Heavy Metal Pollution: Land and Air. London, Applied Science.CrossRef
MERIAN, E. (1991). Metals and their Compounds in Environment and Life. Occurence, Analysis and Biological Relevance. New York, Verlag Chemie Weinheim.
MORLEY, N. J., CRANE, M. & LEWIS, J. W. (2001 a). Toxicity of cadmium and zinc to Diplostomum spathaceum (Trematoda: Diplostomidae) cercarial survival. International Journal for Parasitology 31, 1211–1217.Google Scholar
MORLEY, N. J., CRANE, M. & LEWIS, J. W. (2001 b). Toxicity of cadmium and zinc to miracidia of Schistosoma mansoni. Parasitology 122, 81–85.Google Scholar
OVERSTREET, R. M. (1997). Parasitological data as monitors of environmental health. Parassitologia 39, 169–175.Google Scholar
PALACIOS, M. A., GÓMEZ, M. M., MOLDOVAN, M., MORRISON, G., RAUCH, S., McLEOD, C., MA, R., LASERNA, J., LUCENA, P., CAROLI, S., ALIMONTI, A., PETRUCCI, F., BOCCA, B., SCHRAMEL, P., LUSTIG, S., ZISCHKA, M., WASS, U., STENBOM, B., LUNA, M., SAENZ, J. C., SANTAMARÍA, J. & TORRENS, J. M. (2000). Platinum-group elements: quantification in collected exhaust fumes and studies of catalyst surfaces. The Science of the Total Environment 257, 1–15.CrossRefGoogle Scholar
PHILLIPS, D. J. H. & RAINBOW, P. S. (1993). Biomonitoring of Trace Aquatic Contaminants. London, Elsevier.
PHILLIPS, D. J. H. & SEGAR, D. A. (1986). Use of bio-monitors in monitoring conservative contaminants: programme design imperatives. Marine Pollution Bulletin 17, 10–17.CrossRefGoogle Scholar
RIGGS, M. R., LEMLY, A. D. & ESCH, G. W. (1987). The growth, biomass and fecundity of Bothriocephalus acheilognathi in a North Carolina cooling reservoir. Journal of Parasitology 73, 893–900.CrossRefGoogle Scholar
RODITI, H. A. & FISHER, N. S. (1999). Rates and routes of trace element uptake in zebra mussels. Limnology and Oceanography 44, 1730–1749.CrossRefGoogle Scholar
RODITI, H. A., FISHER, N. S. & SANUDO-WILHELMY, S. A. (2000). Field testing a metal bioaccumulation model for zebra mussels. Environmental Science and Technology 34, 2817–2825.CrossRefGoogle Scholar
ROSENBERG, D. M. & RESH, V. H. (1993). Freshwater Biomonitoring and Benthic Macroinvertebrates. New York, Chapman & Hall.
SANCHEZ-HERNANDEZ, J. C. (2000). Trace element contamination in Antarctic ecosystems. Reviews in Environmental Contamination and Toxicology 166, 83–127.Google Scholar
SCHEEF, G., SURES, B. & TARASCHEWSKI, H. (2000). Cadmium accumulation in Moniliformis moniliformis (Acanthocephala) from experimentally infected rats. Parasitology Research 86, 688–691.CrossRefGoogle Scholar
SCHLUDERMANN, C., KONECNY, R., LAIMGRUBER, S., CHOVANEC, A., LEWIS, J. W., SCHIEMER, F. & SURES, B. (2003). Fish macroparasites as potential indicators of pollution in the river Danube. Parasitology (in press).CrossRefGoogle Scholar
SEGNER, H. (1998). Fish cell lines as a tool in aquatic toxiclogy. In Fish Ecotoxicology (ed. Braunbeck, T., Hinton, D. E. & Streit, B.), pp. 1–38. Basel, Birkhäuser Verlag.
SEGNER, H. & BRAUNBECK, T. (1998). Cellular response profile to chemical stress. In Ecotoxicology: Ecological Fundamentals, Chemical Exposure, and Biological Effects (ed. Schüürmann, G. & Markert, B.), pp. 521–570. New York, Wiley.
SIDDALL, R. & SURES, B. (1998). Uptake of lead by Pomphorhynchus laevis cystacanths in Gammarus pulex and immature worms in chub (Leuciscus cephalus). Parasitology Research 84, 573–577.CrossRefGoogle Scholar
SPRY, D. J. & WIENER, J. G. (1991). Metal bioavailability and toxicity to fish in low-alkalinity lakes: a critical review. Environmental Pollution 71, 243–304.CrossRefGoogle Scholar
SURES, B. (2001). The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review. Aquatic Ecology 35, 245–255.CrossRefGoogle Scholar
SURES, B. (2002 a). Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis). International Journal for Parasitology 32, 1117–1122.Google Scholar
SURES, B. (2002 b). Charakterisierung aquatischer Wirt-Parasit-Interaktionen aus ökologischer und (öko-)toxikologischer Sicht. Habilitationsschrift, Universität Karlsruhe.
SURES, B., FRANKEN, M. & TARASCHEWSKI, H. (2000 a). Element concentrations in the archiacanthocephalan Macracanthorhynchus hirudinaceus compared with those in the porcine host from a slaughterhouse in La Paz, Bolivia. International Journal for Parasitology 30, 1071–1076.Google Scholar
SURES, B., GRUBE, K. & TARASCHEWSKI, H. (2002 a). Experimental studies on the lead accumulation in the cestode Hymenolepis diminuta and its final host, Rattus norvegicus. Ecotoxicology 11, 365–368.Google Scholar
SURES, B., JÜRGES, G. & TARASCHEWSKI, H. (1998). Relative concentrations of heavy metals in the parasites Ascaris suum (Nematoda) and Fasciola hepatica (Digenea) and their respective porcine and bovine definitive hosts. International Journal for Parasitology 28, 1173–1178.CrossRefGoogle Scholar
SURES, B., JÜRGES, G. & TARASCHEWSKI, H. (2000 b). Accumulation and distribution of lead in the acanthocephalan Moniliformis moniliformis from experimental infected rats. Parasitology 121, 427–433.Google Scholar
SURES, B. & REIMANN, N. (2003). Analysis of trace metals in the Antarctic host-parasite system Notothenia coriiceps and Aspersentis megarhynchus (Acanthocephala) caught at King George Island, South Shetland Islands. Polar Biology (in press).CrossRefGoogle Scholar
SURES, B. & SIDDALL, R. (1999). Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Experimental Parasitology 93, 66–72.CrossRefGoogle Scholar
SURES, B. & SIDDALL, R. (2001). Comparison between lead accumulation of Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) and in the body cavity of goldfish (Carassius auratus auratus). International Journal for Parasitology 31, 669–673.CrossRefGoogle Scholar
SURES, B. & SIDDALL, R. (2003). Uptake and accumulation of lead by the parasitic worm Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus). International Journal for Parasitology 33, 65–70.CrossRefGoogle Scholar
SURES, B., SIDDALL, R. & TARASCHEWSKI, H. (1999 a). Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 16–21.Google Scholar
SURES, B., STEINER, W., RYDLO, M. & TARASCHEWSKI, H. (1999 b). Concentrations of 17 elements in the zebra mussel (Dreissena polymorpha), in different tissues of perch (Perca fluviatilis), and in perch intestinal parasites (Acanthocephalus lucii) from the subalpin lake Mondsee (Austria). Environmental Toxicology and Chemistry 18, 2574–2579.Google Scholar
SURES, B. & TARASCHEWSKI, H. (1995). Cadmium concentrations of two adult acanthocephalans (Pomphorhynchus laevis, Acanthocephalus lucii) compared to their fish hosts and cadmium and lead levels in larvae of A. lucii compared to their crustacean host. Parasitology Research 81, 494–497.Google Scholar
SURES, B., TARASCHEWSKI, H. & JACKWERTH, E. (1994 a). Lead content of Paratenuisentis ambiguus (Acanthocephala), Anguillicola crassus (Nematodes) and their host Anguilla anguilla. Diseases of Aquatic Organisms 19, 105–107.Google Scholar
SURES, B., TARASCHEWSKI, H. & JACKWERTH, E. (1994 b). Lead accumulation in Pomphorhynchus laevis and its host. Journal of Parasitology 80, 355–357.Google Scholar
SURES, B., TARASCHEWSKI, H. & JACKWERTH, E. (1994 c). Comparative study of lead accumulation in different organs of perch (Perca fluviatilis) and its intestinal parasite Acanthocephalus lucii. Bulletin of Environmental Contamination and Toxicology 52, 269–273.Google Scholar
SURES, B., TARASCHEWSKI, H. & ROKICKI, J. (1997 b). Lead and cadmium content of two cestodes Monobothrium wageneri and Bothriocephalus scorpii, and their fish hosts. Parasitology Research 83, 618–623.Google Scholar
SURES, B., TARASCHEWSKI, H. & RYDLO, M. (1997 c). Intestinal fish parasites as heavy metal bioindicators: a comparison between Acanthocephalus lucii (Palaeacanthocephala) and the zebra mussel, Dreissena polymorpha. Bulletin of Environmental Contamination and Toxicology 59, 14–21.Google Scholar
SURES, B., TARASCHEWSKI, H. & SIDDALL, R. (1997 a). Heavy metal concentrations in adult acanthocephalans and cestodes compared to their fish hosts and to established free-living bioindicators. Parasitologia 39, 213–218.Google Scholar
SURES, B., ZIMMERMANN, S., MESSERSCHMIDT, J. & VON BOHLEN, A. (2002 b). Relevance and analysis of traffic related platinum group metals (Pt, Pd, Rh) in the aquatic biosphere, with emphasis on Palladium. Ecotoxicology 11, 385–392.Google Scholar
SURES, B., ZIMMERMANN, S., MESSERSCHMIDT, J., VON BOHLEN, A. & ALT, F. (2001). First report on the uptake of automobile catalyst emitted Palladium by European eels (Anguilla anguilla) following experimental exposure to road dust. Environmental Pollution 113, 341–345.CrossRefGoogle Scholar
SURES, B., ZIMMERMANN, S., SONNTAG, C., STÜBEN, D. & TARASCHEWSKI, H. (2003). The acanthocephalan Paratenuisentis ambiguus as a sensitive indicator of the precious metals Pt and Rh emitted from automobile catalytic converters. Environmental Pollution 122, 401–405.CrossRefGoogle Scholar
SZEFER, P., ROKICKI, J., FRELEK, K., SKÓRA, K. & MALINGA, M. (1998). Bioaccumulation of selected trace elements in lung nematodes, Pseudalius inflexus, of harbor porpoise (Phocoena phocoena) in a Polish zone of the Baltic Sea. The Science of the Total Environment 220, 19–24.CrossRefGoogle Scholar
TARASCHEWSKI, H. (2000). Host-parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1–179.CrossRefGoogle Scholar
TENORA, F., BARUš, V., KRÁČMAR, S. & DVOŘÁČEK, J. (2000). Concentrations of some heavy metals in Ligula intestinalis plerocercoids (Cestoda) and Philometra ovata (Nematoda) compared to some of their hosts (Osteichthyes). Helminthologia 37, 15–18.Google Scholar
TENORA, F., KRÁČMAR, S., BARUš, V. & DVOŘÁČEK, J. (1997). Some inorganic substances in plerocercoids of Ligula intestinalis (Pseudophyllidea). Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 45, 23–30.Google Scholar
TENORA, F., BARUš, V., KRÁČMAR, S., DVOŘÁČEK, J. & SRNKOVÁ, J. (1999 b). Parallel analysis of some heavy metals concentrations in the Anguillicola crassus (Nematoda) and the European eel Anguilla anguilla (Osteichthyes). Helminthologia 36, 79–81.Google Scholar
TENORA, F., KRÁČMAR, S., BARUš, V. & DVOŘÁČEK, J. (1999 a). Content of microelements of heavy metals in males and females of Toxocara canis and Protospirura muricola (Nematoda). Helminthologia 36, 127.Google Scholar
TURČEKOVÁ, L. & HANZELOVÁ, V. (1996). Concentrations of heavy metals in the cestode Proteocephalus percae, parasite of perch. Helminthologia 37, 162–163.Google Scholar
VALTONEN, E. T., HOLMES, J. C. & KOSKIVAARA, M. (1997). Eutrophication, pollution, and fragmentation: effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Canadian Journal of Fisheries and Aquatic Sciences 54, 572–585.CrossRefGoogle Scholar
ZIMMERMANN, S., ALT, F., MESSERSCHMIDT, J., VON BOHLEN, A., TARASCHEWSKI, H. & SURES, B. (2002 b). Bioavailability of traffic related platinum group elements (Pd, Pt, Rh) and other metals to the zebra mussel (Dreissena polymorpha) in water containing road dust. Environmental Toxicology and Chemistry 21, 2713–2718.Google Scholar
ZIMMERMANN, S., MENZEL, C. M., STÜBEN, D., TARASCHEWSKI, H. & SURES, B. (2002 a). Lipid solubility of the platinum group metals Pt, Pd and Rh in dependence on the presence of complexing agents. Environmental Pollution 124, 1–5.Google Scholar
ZIMMERMANN, S., SURES, B. & TARASCHEWSKI, H. (1999). Experimental studies on lead accumulation in the eel specific endoparasites Anguillicola crassus (Nematoda) and Paratenuisentis ambiguus (Acanthocephala) as compared with their host, Anguilla anguilla. Archives of Environmental Contamination and Toxicology 37, 190–195.CrossRefGoogle Scholar