Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-14T04:20:15.081Z Has data issue: false hasContentIssue false
  • English
  • Français

Pollution-induced heat shock protein expression in the amphipod Gammarus roeseli is affected by larvae of Polymorphus minutus (Acanthocephala)

Published online by Cambridge University Press:  01 June 2007

B. Sures  and
H. Radszuweit
B. Sures*
Affiliation:
Angewandte Zoologie/Hydrobiologie, Universität Duisburg-Essen, 45117 Essen, Germany:
H. Radszuweit
Affiliation:
Zoologisches Institut I – Ökologie/Parasitologie, Universität Karlsruhe, Kaiserstr. 12, Geb. 07.01, 76128 Karlsruhe, Germany
*
*Fax: +49-201/183 2179 E-mail: bernd.sures@uni-due.de
Get access Rights & Permissions [Opens in a new window]

Abstract

The relationship between the exposure of organisms to chemicals and subsequent alterations in various biochemical processes (commonly referred to as biomarkers) is of growing importance in environmental and ecotoxicological research. However, parasites which also affect the physiological homeostasis of their hosts, and thus may alter biomarker reactions, are usually ignored in environmental research. To address this deficit, we have used the host–parasite system Gammarus roeseli naturally infected with cystacanths of the acanthocephalan Polymorphus minutus to investigate whether infection of gammarids with parasites alters their heat shock protein response following exposure to palladium (Pd). After 24 days of metal exposure relative levels of heat shock protein hsp70 were analysed in the tissues of parasites and intermediate hosts. Simultaneously, the metal accumulation in gammarids and parasites was determined. As none of the infected gammarids showed hsp70 levels at the end of the Pd exposure (either exposed or not), infected and unparasitized G. roeseli were exposed to heat. Again, only uninfected gammarids showed a temperature-dependent increase in hsp70 levels. Interestingly, although the intermediate hosts showed no hsp70 response, exposure to Pd and heat results in increasing hsp70 in the parasites within in the haemocoel of G. roeseli. Heat experiments with isolated cystacanths also showed increasing hsp70 levels in P. minutus with temperature. Concerning uninfected G. roeseli, exposure to Pd and heat causes a hsp70 response. Pd concentrations were found to be higher in the larval parasites than in the gammarids. This result clearly contradicts previous results, as high metal accumulation was so far only described from adult acanthocephalans. Our findings provide experimental evidence that parasites alter the biomarker responses of their host and that the infection status of test animals is extremely important for ecotoxicological studies.

Type
ICOPAXI Papers
Information
Journal of Helminthology , Volume 81 , Issue 2: Special Issue , June 2007 , pp. 191 - 197
Copyright
Copyright © Cambridge University Press 2007

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

Bakker, T.C.M., Mazzi, D. & Zala, S. (1997) Parasite-induced changes in behaviour and color make Gammarus pulex more prone to fish predation. Ecology 78, 1098–1104.CrossRefGoogle Scholar
Bauer, A., Trouve, A., Gregoire, A., Bollache, L. & Cezilly, F. (2000) Differential influence of Pomphorhynchus laevis (Acanthocephala) on the behaviour of native and invader gammarid species. International Journal for Parasitology 30, 1453–1457.CrossRefGoogle ScholarPubMed
Braunbeck, T., Hinton, D.E. & Streit, B. (1998) Fish ecotoxicology. Basel, Birkhäuser Verlag.CrossRefGoogle Scholar
Brown, A.F. & 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
Dezfuli, B.S. & Giari, L. (1999) Amphipod intermediate host of Polymorphus minutus (Acanthocephala), parasite of water birds, with notes on ultrastructure of host-parasite interface. Folia Parasitologica 46, 117–122.Google Scholar
Dezfuli, B.S., Franzoi, P., Trisolini, R. & Rossi, R. (1989) On the crustacean hosts of larval acanthocephalan parasites of fishes from a coastal lagoon of River Po delta. Parassitologia 31, 51–57.Google ScholarPubMed
Directive 2000/60/EC of the European parliament and of the council of 23 October 2000 establishing a framework for Community action in the field of water policy. Official Journal of the European Communities, 72 pp.Google Scholar
Greenstein, D., Tiefenthaler, L. & Bay, S. (2004) Toxicity of parking lot runoff after application of simulated rainfall. Archives of Environmental Contamination and Toxicology 47, 199–206.CrossRefGoogle ScholarPubMed
Harrison, R.M. & Wilson, S.J. (1985a) The chemical-composition of highway drainage waters 1. Major ions and selected trace-metals. Science of the Total Environment 43, 63–77.CrossRefGoogle Scholar
Harrison, R.M. & Wilson, S.J. (1985b) The chemical-composition of highway drainage waters 2. Associations of metals in the suspended sediment. Science of the Total Environment 43, 79–83.CrossRefGoogle Scholar
Köhler, H.R., Bartussek, C., Eckwert, H., Farian, K., Gränzer, S., Knigge, T. & Kunz, N. (2001) The hepatic stress protein (hsp 70) response to interacting abiotic parameters in fish exposed to various levels of pollution. Journal of Aquatic Ecosystem Stress and Recovery 8, 261–279.CrossRefGoogle Scholar
Lewis, S., Handy, D., Cordi, B., Billinghurst, Z. & Depledge, M.H. (1999) Stress proteins (HSP's): Methods of detection and their use as an environmental biomarker. Ecotoxicology 8, 351–368.CrossRefGoogle Scholar
Maltby, L., Forrow, D.M., Boxall, A.B.A., Calow, P. & Betton, C.I. (1995a) The effects of motorway runoff on fresh-water ecosystems, 1. Field-Study. Environmental Toxicology and Chemistry 14, 1079–1092.CrossRefGoogle Scholar
Maltby, L., Boxall, A.B.A., Forrow, D.M., Calow, P. & Betton, C.I. (1995b) The effects of motorway runoff on fresh-water ecosystems, 2. Identifying major toxicants. Environmental Toxicology and Chemistry 14, 1093–1101.CrossRefGoogle Scholar
Merian, E., Anke, M., Ihnat, M. & Stoeppler, M. (2004) Elements and their compounds in the environment. Weinheim, Wiley-VCH.CrossRefGoogle Scholar
Oetinger, D.F. (1987) Effects of Acanthocephalus dirus (Acanthocephala) on morphometrics and reproduction of Caecideotea intermedius (Crustacea: Isopoda). Transactions of the American Microscopical Society 106, 240–248.CrossRefGoogle Scholar
Perceval, O., Pinel-Alloul, B., Méthot, G., Couillard, Y., Giguère, A., Campbell, P.G.C. & Hare, L. (2001) Cadmium accumulation and metallothionein synthesis in freshwater bivalves (Pyganodon grandis): relative influence of the metal exposure gradient versus limnological variability. Environmental Pollution 118, 5–17.CrossRefGoogle Scholar
Radlowska, M. & Pempkowiak, J (2002) Stress-70 as indicator of heavy metals accumulation in blue mussel Mytilus edulis. Environment International 27, 605–608.CrossRefGoogle ScholarPubMed
Rumpus, A.E. & Kennedy, C.R. (1974) The effect of the acanthocephalan Pomphorhynchus laevis upon the respiration of its intermediate host, Gammarus pulex. Parasitology 68, 271–284.CrossRefGoogle ScholarPubMed
Sanders, B. (1993) Stress proteins in aquatic organisms: an environmental perspective. Critical Reviews in Toxicology 23, 49–75.CrossRefGoogle ScholarPubMed
Scherer, U., Fuchs, S., Behrendt, H. & Hillenbrand, T. (2003) Emissions of heavy metals into river basins of Germany. Water Science and Technology 47, 251–257.CrossRefGoogle ScholarPubMed
Schirling, M., Jungmann, D., Ladewig, V., Ludwichowski, K.-U., Nagel, R., Köhler, H.-R. & Triebskorn, R. (2006) Bisphenol A in artificial indoor streams: II. Stress response and gonad histology in Gammarus fossarum (Amphipoda). Ecotoxicology 15, 143–156.CrossRefGoogle ScholarPubMed
Schröder, H.C., Batel, R., Hassanein, H.M.A., Lauenroth, S., Jenke, H.S.T., Simat, T., Steinhart, H. & Müller, W.E.G. (1999) Correlation between the level of the potential biomarker, heat shock protein, and the occurrence of DNA damage in the dab, Limanda limanda: a field study in the North Sea and the English Channel. Marine Environmental Research 49, 201–215.CrossRefGoogle Scholar
Segner, H. & Braunbeck, T. (1998) Cellular response profile to chemical stress. pp. 521–570 in Schüürmann, G. & Markert, B. (Eds) Ecotoxicology: ecological fundamentals, chemical exposure, and biological effects. New York, Wiley.Google Scholar
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 ScholarPubMed
Singer, C., Zimmermann, S. & Sures, B. (2005) Induction of heat shock proteins (hsp70) in the Zebra mussel (Dreissena polymorpha) following exposure to platinum group metals (platinum, palladium and rhodium): comparison with lead and cadmium exposures. Aquatic Toxicology 75, 65–75.CrossRefGoogle ScholarPubMed
Sures, B. (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, S53–S60.CrossRefGoogle Scholar
Sures, B. (2004) Environmental parasitology: relevancy of parasites in monitoring environmental pollution. Trends in Parasitology 20, 170–177.CrossRefGoogle ScholarPubMed
Sures, B. (2006) How parasitism and pollution affect the physiological homeostasis of aquatic hosts. Journal of Helminthology 80, 151–157.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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 ScholarPubMed
Sures, B. & Taraschewski, H. (1995) Cadmium concentrations in two adult acanthocephalans, Pomphorhynchus laevis and Acanthocephalus lucii, as compared with their fish hosts and cadmium and lead levels in larvae of A. lucii as compared with their crustacean host. Parasitology Research 81, 494–497.CrossRefGoogle ScholarPubMed
Sures, B. & Zimmermann, S. (2007) Impact of humic substances on the aqueous solubility, uptake and bioaccumulation of platinum, palladium and rhodium in exposure studies with Dreissena polymorpha. Environmental Pollution 146, 444–451.CrossRefGoogle ScholarPubMed
Sures, B., Siddall, R. & Taraschewski, H. (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 16–21.CrossRefGoogle ScholarPubMed
Sures, B., Taraschewski, H. & Haug, C. (1995) Determination of trace metals (Cd, Pb) in fish by electrothermal atomic absorption spectrometry after microwave digestion. Analytica Chimica Acta 311, 135–139.CrossRefGoogle Scholar
Tain, L., Perrot-Minnot, M.J. & Cezilly, F. (2006) Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proceedings of the Royal Society B 273, 3039–3045.CrossRefGoogle ScholarPubMed
Tokalov, S.V. & Gutzeit, H.O. (2003) Weak electromagnetic fields (50 Hz) elicit a stress response in human cells. Environmental Research 94, 145–151.CrossRefGoogle Scholar
Ward, N.I. (1990) Multielement contamination of British motorway environments. Science of the Total Environment 93, 393–401.CrossRefGoogle Scholar
Werner, I. & Hinton, D.E. (1999) Spatial profiles of hsp70 proteins in Asian clam (Potamocorbula amurensis) in northern San Francisco Bay may be linked to natural rather than anthropogenic stressors. Marine Environmental Research 50, 379–384.CrossRefGoogle Scholar
Zimmermann, S., Messerschmidt, J., von Bohlen, A. & Sures, B. (2003) Determination of the platinum group metals Pt, Pd and Rh in biological samples by electrothermal atomic absorption spectrometry as compared with adsorptive cathodic stripping voltammetry and total reflection X-ray fluorescence analysis. Analytica Chimica Acta 498, 93–104.CrossRefGoogle Scholar