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How parasitism and pollution affect the physiological homeostasis of aquatic hosts

Published online by Cambridge University Press:  12 April 2024

B. Sures
B. Sures*
Affiliation:
Zoologisches Institut I - Ökologie/Parasitologie, Universität Karlsruhe, Kaiserstr. 12, Geb. 07.01, 76128 Karlsruhe, Germany
*
*Fax: +49 721 6087655 E-mail: [email protected]
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Abstract

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Parasitism poses a serious threat to hosts under certain circumstances, while the well-being of organisms is also negatively affected by environmental pollution. Little information is available on the simultaneous effects of parasites and pollutants on the physiological homeostasis of organisms. The present paper demonstrates that parasites: (i) may influence the metabolism of pollutants in infected hosts, (ii) interact with pollution in synergistic or antagonistic ways, and (iii) may induce physiological reactions in hosts which were thought to be pollutant-induced. Experimental studies on the uptake and accumulation of metals by fish reveal that fish infected with acanthocephalans have lower metal levels than uninfected hosts; e.g. Pomphorhynchus laevis reduces lead levels in fish bile, thereby diminishing or impeding the hepatic intestinal cycling of lead, which may reduce the quantity of metals available for fish. Alterations in pollutant uptake and accumulation in different intermediate and final hosts due to parasites are thus very important in the field of ecotoxicology. In addition to such alterations, there is a close interaction between the effects of pollutants and parasites which seems to be mediated at least partly by the endocrine system, which itself is closely related to the immune system in fish. Laboratory studies on eels experimentally infected with the swimbladder nematode Anguillicola crassus reveal that toxic chemicals such as polychlorinated biphenyls produce immunosuppressive effects which facilitate parasite infection. Similarly, an increase in serum cortisol concentration in eels due to chemical exposure and infection is correlated with decreasing levels of anti-A. crassus antibodies. Furthermore, parasites are able to elicit physiological changes which are attributed to chemicals with endocrine disrupting activity, e.g. the cestode Ligula intestinalis is known to suppress gonad development in roach. The most thoroughly documented examples of endocrine disruption in wild fish are in roach, and it is conceivable that this disruption is not only due to chemical activity but also to parasites such as L. intestinalis or species of the phylum Microspora.

Type
Research Article
Information
Journal of Helminthology , Volume 80 , Issue 2 , June 2006 , pp. 151 - 157
Copyright
Copyright © Cambridge University Press 2006

References

Arkoosh, M.R., Casillas, E., Clemons, E., Kagley, A.N., Olson, R., Reno, P. & Stein, J.E. (1998a) Effect of pollution on fish diseases: potential impacts on salmonid populations. Journal of Aquatic Animal Health 10, 182–190.2.0.CO;2>CrossRefGoogle Scholar
Arkoosh, M.R., Casillas, E., Huffman, P., Clemons, E., Evered, J., Stein, J.E. & Varanasi, U. (1998b) Increased susceptibility of juvenile chinook salmon from a contaminated estuary to Vibrio anguillarum . Transactions of the American Fisheries Society 127, 360–374.2.0.CO;2>CrossRefGoogle Scholar
Arme, C. (1997) Ligula intestinalis: interaction with the pituitary-gonadal axis of its fish host. Journal of Helminthology 71, 83–84.CrossRefGoogle Scholar
Barrett, J., Cain, G.D. & Fairbairn, D. (1970) Sterols in Ascaris lumbricoides (Nematoda), Macracanthorhynchus hirudinaceus and Moniliformis dubius (Acanthocephala), and Echinostoma revolutum (Trematoda). Journal of Parasitology 56, 1004–1008.CrossRefGoogle ScholarPubMed
Benveniste, P. (2002) Sterol metabolism. pp. 1–3 in Somerville, C. & Meyerowitz, E. (Eds) The Arabidopsis book. http://www.aspb.org/publications/arabidopsis/ CrossRefGoogle Scholar
Bloch, K.E. (1983) Sterol structure and membrane function. Critical Reviews in Biochemistry 14, 47–91.CrossRefGoogle ScholarPubMed
Demel, R.A. & De Kruyff, B. (1976) The function of sterols in membranes. Biochimica et Biophysica Acta 457, 109–132.CrossRefGoogle ScholarPubMed
Hahn, M.E. & Stegemann, J.J. (1994) Regulation of cytochrome P4501A1 in teleosts: sustained induction of CYP1A1 mRNA, protein, and catalytic activity by 2,3,7,8-tetrachlorodibenzo-p-dioxin in the marine fish Stenotomous chrysops . Toxicology and Applied Pharmacology 127, 187–198.CrossRefGoogle Scholar
Hecker, M. & Karbe, L. (2005) Parasitism in fish–an endocrine modulator of ecological relevance? Aquatic Toxicology 72, 195–207.CrossRefGoogle ScholarPubMed
Jobling, S. & Tyler, C.R. (2003) Endocrine disruption, parasites and pollutants in wild freshwater fish. Parasitology 126, S103–S108.CrossRefGoogle ScholarPubMed
Kafafi, S.A., Afeefy, H.Y., Ali, A.H., Said, H.K. & Kafafi, G. (1993) Binding of polychlorinated biphenyls to the aryl hydrocarbon receptor. Environmental Health Perspectives 101, 422–428.CrossRefGoogle ScholarPubMed
Kennedy, C.R., Broughton, P.F. & Hine, P.M. (1978) The status of brown trout, Salmo trutta and Salmo gairdneri as hosts of the acanthocephalan, Pomphorhynchus laevis . Journal of Fish Biology 13, 265–275.CrossRefGoogle Scholar
Kime, D.E. (1998) Endocrine disruption in fish. 396 pp. Boston, Kluwer Academic Publishers.CrossRefGoogle Scholar
Knopf, K., Naser, K., van der Heijden, M.H.T. & Taraschewski, H. (2000) Development of the humoral immune-response in European eel (Anguilla anguilla) experimentally infected with Anguillicola crassus . Diseases of Aquatic Organisms 42, 61–69.CrossRefGoogle Scholar
Lafferty, K.D. (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.CrossRefGoogle ScholarPubMed
Nickol, B.B. (1985) Epizootiology. pp. 307–346 in Crompton, D.W.T. & Nickol, B.B. (Eds) Biology of the Acanthocephala, Cambridge, Cambridge University Press.Google Scholar
Overstreet, R.M. (1997) Parasitological data as monitors of environmental health. Parassitologia 39, 169–175.Google ScholarPubMed
Pietrock, M. & Marcogliese, D.J. (2003) Free-living endohelminth stages: at the mercy of environmental conditions. Trends in Parasitology 19, 293–299.CrossRefGoogle ScholarPubMed
Regala, R.P., Rice, C.D., Schwedler, T.E. & Dorociak, I.R. (2001) The effects of tributyltin (TBT) and 3,3′4,4′5-pentachlorobiphenyl (PCB-126) mixtures on antibody responses and phagocyte oxidative burst activity in channel catfish, Ictalurus punctatus . Archives of Environmental Contamination and Toxicology 40, 386–391.CrossRefGoogle ScholarPubMed
Rodgers-Gray, T.P., Smith, J.E., Ashcroft, A.E., Isaac, R.E. & Dunn, A.M. (2004) Mechanisms of parasite-induced sex reversal in Gammarus duebeni . International Journal for Parasitology 34, 747–753.CrossRefGoogle ScholarPubMed
Safe, S. (1994) Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs) and related compounds. Environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs) . Critical Reviews in Toxicology 21, 51–88.CrossRefGoogle Scholar
Schabuss, M., Gemeiner, M., Gleiß, A., Lewis, J.W., Miller, I., Möstl, E., Schober, U., Tschulenk, W., Walter, I. & Grillitsch, B. (2005) Ligula intestinalis infection as a potential source of bias in the bioindication of endocrine disruption in the European chub Leuciscus cephalus . Journal of Helminthology 79, 91–94.CrossRefGoogle ScholarPubMed
Starling, J.A. (1985) Feeding, nutrition and metabolism, pp. 125–212 in Crompton, D.W.T. & Nickol, B.B. (Eds) Biology of the Acanthocephala. Cambridge, Cambridge University Press.Google Scholar
Sures, B. (2002) Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis). International Journal for Parasitology 32, 1117–1122.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. (2005) Effects of pollution on parasites, and use of parasites in pollution monitoring. pp. 421–425 in Rohe, K. (Ed.) Marine parasitology. Collingwood, CSIRO Publishing.Google Scholar
Sures, B. & Knopf, K. (2004a) Individual and combined effects of Cd and 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) on the humoral immune response in European eel (Anguilla anguilla) experimentally infected with larvae of Anguillicola crassus (Nematoda). Parasitology 128, 445–454.CrossRefGoogle ScholarPubMed
Sures, B. & Knopf, K. (2004b) Parasites as a threat to freshwater eels? Science 304, 208–209.CrossRefGoogle ScholarPubMed
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 26, 680–686.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 ScholarPubMed
Sures, B. & Siddall, R. (2003) Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) as an indicator of metal pollution. International Journal for Parasitology 33, 65–70.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., Taraschewski, H. & Jackwerth, E. (1994) Lead accumulation in Pomphorhynchus laevis and its host. Journal of Parasitology 80, 355–357.CrossRefGoogle ScholarPubMed
Sures, B., Steiner, W., Rydlo, M. & Taraschewski, H. (1999) 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 subalpine lake Mondsee (Austria). Environmental Toxicology and Chemistry 18, 2574–2579.CrossRefGoogle Scholar
Sures, B., Knopf, K. & Kloas, W. (2001) Induction of stress by the swimbladder nematode Anguillicola crassus in European eels, Anguilla anguilla, after repeated experimental infection. Parasitology 123, 179–184.CrossRefGoogle ScholarPubMed
Sures, B., Dezfuli, B. & Krug, H. (2003) The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (210 Pb) in its fish host chub (Leuciscus cephalus). International Journal for Parasitology 33, 1617–1622.CrossRefGoogle ScholarPubMed
Sures, B., Lutz, I. & Kloas, W. (2006) Effects of infection with Anguillicola crassus and simultaneous exposure with Cd and 3,3′,4,4′,5-pentachlorobiphenyl (PCB 126) on the levels of cortisol and glucose in European eel (Anguilla anguilla. Parasitology 132, 281–288.CrossRefGoogle ScholarPubMed
Thuvander, A. (1989) Cadmium exposure of rainbow trout, Salmo gairdneri Richardson: effects on immune functions. Journal of Fish Biology 35, 521–529.CrossRefGoogle Scholar
Vos, G., Dybing, E., Greim, H.A., Ladefoged, O., Lambre, C., Tarazona, J.V., Brandt, I. & Vethaak, A.D. (2000) Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Critical Reviews in Toxicology 30, 71–133.CrossRefGoogle Scholar
Wendelaar Bonga, S.E. (1997) The stress response in fish. Physiological Reviews 77, 591–625.CrossRefGoogle ScholarPubMed
Weyts, F.A.A., Cohen, N., Flik, G. & Verburg-van Kemenade, B.M.L. (1999) Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish and Shellfish Immunology 9, 1–20.CrossRefGoogle Scholar
Wiklund, T., Lounasheimo, L., Lom, J. & Bylund, G. (1996) Gonadal impairment in roach Rutilus rutilus from Finnish coastal areas of the northern Baltic Sea. Diseases of Aquatic Organisms 26, 163–171.CrossRefGoogle Scholar
Zelikoff, J.T. (1998) Biomarkers of immunotoxicity in fish and other non-mammalian sentinel species: predictive value for mammals? Toxicology 129, 63–71.CrossRefGoogle ScholarPubMed