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Endocrine disruption, parasites and pollutants in wild freshwater fish

Published online by Cambridge University Press:  10 November 2003

S. JOBLING  and
C. R. TYLER
S. JOBLING
Affiliation:
Department of Biological Sciences, Brunel University, Uxbridge, Middlesex, UK
C. R. TYLER
Affiliation:
School of Biological Sciences, Hatherly Laboratory, Exeter University, Exeter, Devon EX4 4PS, UK
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Abstract

Disruption of the endocrine system has been shown to occur in wild freshwater fish populations across the globe. Effects range from subtle changes in the physiology and sexual behaviour of fish to permanently altered sexual differentiation, impairment of gonad development and/or altered fertility. A wide variety of adverse environmental conditions may induce endocrine disruption, including sub-optimal temperatures, restricted food supply, low pH, environmental pollutants, and/or parasites. Furthermore, it is conceivable that any/all of these factors could act simultaneously to cause a range of disparate or inter-related effects. Some of the strongest evidence for a link between an adverse health effect, as a consequence of endocrine disruption, and a causative agent(s) is between the condition of intersex in wild roach (Rutlius rutilus) in UK rivers and exposure to effluents from sewage treatment works. The evidence to indicate that intersex in roach (and other cyprinid fish living in these rivers) is caused by chemicals that mimic and/or disrupt hormone function/balance in treated sewage effluent is substantial. There are a few parasites that affect the endocrine system directly in fish, including the tape worm Ligula intestinalis and a few parasites from the micropsora phylum. L. intestinalis acts at the level of the hypothalamus restricting GnRH secretion (resulting in poorly developed gonads) and is one of the very few examples where an endocrine disrupting event has been shown to result in a population-level effect (reducing it). It is well established that many parasites affect the immune system and thus the most common effect of parasites on the endocrine system in fish is likely to be an indirect one.

Keywords

parasitepollutantendocrinefishdisruptionintersex
Type
Research Article
Information
Parasitology , Volume 126 , Issue 7 , March 2003 , pp. S103 - S107
Copyright
© 2003 Cambridge University Press

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References

REFERENCES

ALLEN, Y., MATTHIESSEN, P., HAWORTH, S., THAIN, J. E. & FEIST, S. (1999). Survey of estrogenic activity in United Kingdom estuarine and coastal waters and its effects on gonadal development of the flounder Platichthys flesus. Environmental Toxicology and Chemistry 18, 1791–1800.CrossRefGoogle Scholar
ARME, C. (1997). Ligula intestinalis: Interactions with the pituitary-gonadal axis of its fish host. Journal of Helminthology 71, 83–84.CrossRefGoogle Scholar
BATTY, J. & LIM, R. (1999). Morphological and reproductive characteristics of male mosquitofish (Gambusia affinis holbrooki) inhabiting sewage-contaminated waters in New South Wales, Australia. Archives of Environmental Contamination and Toxicology 36, 301–307.CrossRefGoogle Scholar
BECKAGE, N. E. (1993). Endocrine and neuro-endocrine host–parasite relationships. Receptor 3, 233–245.Google Scholar
BESSELINK, H. T., FLIPSEN, E. M. T. E., EGGENS, M. L., VETHAAK, A. D., KOEMAN, J. H. & BROUWER, A. (1998). Alterations in plasma and hepatic retinoid levels in flounder (Platichthys flesus) after chronic exposure to contaminated harbour sludge in a mesocosm study. Aquatic Toxicology 42, 271–285.CrossRefGoogle Scholar
BORTONE, S. A. & CODY, R. (1999). Morphological masculinization in poeciliid females from a paper mill effluent receiving tributary of the St. Johns River, Florida, USA. Bulletin of Environmental Contamination and Toxicology 63, 150–156.CrossRefGoogle Scholar
CARLETTA, M. A., WEIS, P. & WEIS, J. S. (2002). Development of thyroid abnormalities in mummichogs, Fundulus heteroclitus, from a polluted site. Marine Environmental Research 54, 201–604.CrossRefGoogle Scholar
DESBROW, C., ROUTLEDGE, E. J., BRIGHTY, G. C., SUMPTER, J. P. & WALDOCK, M. (1998). Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environmental Science and Technology 32, 1549–1558.Google Scholar
FATIMA, M., AHMAD, I., SIDDIQUI, R. & RAISUDDIN, S. (2001). Paper and pulp mill effluent-induced immunotoxicity in freshwater fish Channa punctatus (Bloch). Archives of Environmental Contamination and Toxicology 40, 271–276.CrossRefGoogle Scholar
FLAMMARION, P., BRION, F., BABUT, M., BARRIC, J., MIGEON, B., NOURY, P., THYBAUD, E., TYLER, C. R. & PALAZZI, X. (2000). Induction of fish vitellogenin and alterations in testicular structure: Preliminary results of estrogenic effects in chub (Leuciscus cephalus). Ecotoxicology 9, 127–135.CrossRefGoogle Scholar
FOLMAR, L. C., DENSLOW, N. D., KROLL, K., ORLANDO, E. F., ENBLOM, J., MARCINO, J., METCALF, C. & GUILETTE, L. J. (2001). Altered serum sex steroids and vitellogenin induction in walleye (Stizostedion vitreum) collected near a metropolitan sewage treatment plant. Archives of Environmental Contamination and Toxicology 40, 392–398.Google Scholar
FOLMAR, L. C., DENSLOW, N. D., RAO, V., CHOW, M., CRAIN, D. A., ENBLOM, J., MARCINO, J. & GUILLETTE, L. J. (1996). Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environmental Health Perspectives 104, 1096–1101.CrossRefGoogle Scholar
GBANKOTO, A., PAMPOULIE, C., MARQUES, A. & SAKITI, G. N. (2001). Myxobolus dahomeyensis infection in ovaries of Tilapia species from Benin (West Africa). Journal of Fish Biology 58, 883–886.CrossRefGoogle Scholar
GERCKEN, J. & SORDYL, H. ( 2002). Intersex in feral marine and freshwater fish from northeastern Germany. Marine Environmental Research 54, 651–655.CrossRefGoogle Scholar
GRAY, M. A., TEATHER, K. L. & METCALFE, C. D. (1999). Reproductive success and behavior of Japanese medaka (Oryzias latipes) exposed to 4-tert-octylphenol. Environmental Toxicology and Chemistry 18, 2587–2594.Google Scholar
HARSHBARGER, J. C., COFFEY, M. J. & YOUNG, M. Y. ( 2000). Intersexes in Mississippi River shovelnose sturgeon sampled below Saint Louis, Missouri, USA. Marine Environmental Research 50, 247–250.CrossRefGoogle Scholar
HASHIMOTO, S., BESSHO, H., HARA, A., NAKAMURA, M., IGUCHI, T. & FUJITA, K. ( 2000). Elevated serum vitellogenin levels and gonadal abnormalities in wild male flounder (Pleuronectes yokohamae) from Tokyo Bay, Japan. Marine Environmental Research 49, 37–53.CrossRefGoogle Scholar
HECKER, M., TYLER, C. R., HOFFMANN, M., MADDIX, S. & KARBE, L. ( 2002). Plasma biomarkers in fish provide evidence for endocrine modulation in the Elbe River, Germany. Environmental Science and Technology 36, 2311–2321.CrossRefGoogle Scholar
HIRSCH, K. S., WEAVER, D. E., BLACK, L. J., FALCONE, J. F. & MACLUSKY, N. J. ( 1987). Inhibition of central nervous system aromatase activity – a mechanism for fenarimol-induced infertility in the male rat. Toxicology and Applied Pharmacology 91, 235–245.CrossRefGoogle Scholar
HOWELL, W. M., BLACK, D. A. & BORTONE, S. A. (1980). Abnormal expression of secondary sex characters in a population of mosquitofish, Gambusia affinis holbrooki – evidence for environmentally-induced masculinization. Copeia 980, 676–681.CrossRefGoogle Scholar
JOBLING, S., BERESFORD, N., NOLAN, M., RODGERS-GRAY, T., BRIGHTY, G. C., SUMPTER, J. P. & TYLER, C. R. (2002 a). Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biology of Reproduction 66, 272–281.Google Scholar
JOBLING, S., COEY, S., WHITMORE, J. G., KIME, D. E., VAN LOOK, K. J. W., McALLISTER, B. G., BERESFORD, N., HENSHAW, A. C., BRIGHTY, G., TYLER, C. R. & SUMPTER, J. P. (2002 b). Wild intersex roach (Rutilus rutilus) have reduced fertility. Biology of Reproduction 67, 515–524.Google Scholar
JOBLING, S., NOLAN, M., TYLER, C. R., BRIGHTY, G. & SUMPTER, J. P. ( 1998). Widespread sexual disruption in wild fish. Environmental Science and Technology 32, 2498–2506.CrossRefGoogle Scholar
JOBLING, S., SHEAHAN, D., OSBORNE, J. A., MATTHIESSEN, P. & SUMPTER, J. P. (1996). Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environmental Toxicology and Chemistry 15, 194–202.CrossRefGoogle Scholar
KIME, D. E. (1998). Endocrine Disruption in Fish. Boston Kluwer Academic Publishers, pp. 396.CrossRef
KIRK, L. A., TYLER, C. R., LYE, C. M. & SUMPTER, J. P. (2002). Changes in estrogenic and androgenic activities at different stages of treatment in wastewater treatment works. Environmental Toxicology and Chemistry 21, 972–979.CrossRefGoogle Scholar
KOLLNER, B., WASSERRAB, B., KOTTERBA, G. & FISCHER, U. (2002). Evaluation of immune functions of rainbow trout (Oncorhynchus mykiss) – how can environmental influences be detected? Toxicology Letters 131, 83–95.Google Scholar
LACROIX, A., FOURNIER, M., LEBEUF, M., NAGLER, J. J. & CYR, D. G. (2001). Phagocytic response of macrophages from the pronephros of American plaice (Hipoglossoides platessoides) exposed to contaminated sediments from Baie des Anglais, Quebec. Chemosphere 45, 599–607.CrossRefGoogle Scholar
LEATHERLAND, J. F. (1993). Field observations on reproductive and developmental dysfunction in introduced and native salmonids from the Great Lakes. Journal of Great Lakes Research 19, 737–751.CrossRefGoogle Scholar
LEATHERLAND, J. F., LIN, L., DOWN, N. E. & DONALDSON, E. M. (1989). Thyroid hormone content of eggs and early developmental stages of 3 stocks of goitered coho salmon (Oncorhynchus kisutch) from the Great-Lakes of North-America, and a comparison with a stock from British Columbia. Canadian Journal of Fisheries and Aquatic Science 46, 2146–2152.CrossRefGoogle Scholar
LEATHERLAND, J. F. & SONSTEGARD, R. A. (1982). Bioaccumulation of organochlorines by yearling coho salmon (Oncorhynchus kisutch walbaum) fed diets containing great-lakes coho salmon, and the pathophysiological responses of the recipients. Comparative Biochemistry and Physiology 72C, 91–100.CrossRefGoogle Scholar
LOOT, G., POULIN, R., LEK, S. & GUEGAN, J. F. (2002). The differential effects of Ligula intestinalis (L.) plerocercoids on host growth in three natural populations of roach, Rutilus rutilus (L.). Ecology of Freshwater Fish 11, 168–177.Google Scholar
MARCOGLIESE, D. J. & CONE, D. K. (2001). Myxozoan communities parasitizing Notropis hudsonius (Cyprinidae) at selected localities on the St. Lawrence River, Quebec: Possible effects of urban effluents. Journal of Parasitology 87, 951–956.Google Scholar
MATTHIESSEN, P., ALLEN, Y., BAMBER, S., CRAFT, J., HURST, M., HUTCHINSON, T., FEIST, S., KATSIADAKI, I., KIRBY, M., ROBINSON, C., SCOTT, S., THAIN, J. & THOMAS, K. (2002). The impact of oestrogenic and androgenic contamination on marine organisms in the United Kingdom – summary of the EDMAR programme. Marine Environmental Research 54, 645–649.CrossRefGoogle Scholar
MUNKITTRICK, K. R., McMASTER, M. E., McCARTHY, L., SERVOS, M. & VAN DER KRAAK, G. (1998). An overview of recent studies on the potential of pulp-mill effluents to alter reproductive parameters in fish. Journal of Toxicology and Environmental Health B 1, 347–371.CrossRefGoogle Scholar
MUNKITTRICK, K. R., PORTT, C. B., VAN DER KRAAK, G. J., SMITH, I. R. & ROKOSH, D. A. (1991). Impact of bleached kraft mill effluent on population characteristics, liver mfo activity, and serum steroid-levels of a Lake Superior white sucker (Catostomus commersoni) population. Canadian Journal of Fisheries and Aquatic Science 48, 1371–1380.CrossRefGoogle Scholar
McMASTER, M. E., VAN DER KRAAK, G. J., PORTT, C. B., MUNKITTRICK, K. R., SIBLEY, P. K., SMITH, I. R. & DIXON, D. G. (1991). Changes in hepatic mixed-function oxygenase (mfo) activity, plasma steroid-levels and age at maturity of a white sucker (Catostomus commersoni) population exposed to bleached kraft pulp-mill effluent. Aquatic Toxicology 21, 199–218.CrossRefGoogle Scholar
PEKKARINEN, M. (1995). Pleistophora mirandellae Vaney & Conte, 1901 (Protozoa: Microspora) infection in the ovary of the roach, Rutilus rutilus. Memoranda of the Society of Fauna Flora Fennica 71, 19–32.Google Scholar
ROUTLEDGE, E. J., SHEAHAN, D., DESBROW, C., BRIGHTY, G. C., WALDOCK, M. & SUMPTER, J. P. ( 1998). Identification of estrogenic chemicals in STW effluent. 2. In vivo responses in trout and roach. Environmental Science and Technology 32, 1559–1565.Google Scholar
SANDERSON, J. T., LETCHER, R. J., HENEWEER, M., GIESY, J. P. & VAN DEN BERG, M. (2001). Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environmental Health Perspectives 109, 1027–1031.CrossRefGoogle Scholar
SHEAHAN, D. A., BUCKE, D., MATTHIESSEN, P., SUMPTER, J. P., KIRBY, M. F., NEALL, P. & WALDOCK, M. (1994). Chapter 9. In Sublethal and Chronic Effects of Pollutants on Freshwater Fish (ed. Muller, R. & Lloyd, R.), pp. 99–112. Cambridge, FAO, Fishing News Books, Blackwell Scientific.
VAN AERLE, R., NOLAN, M., JOBLING, S., CHRISTIENSEN, L. B., SUMPTER, J. P. & TYLER, C. R. (2001). Sexual disruption in a second species of wild cyprinid fish (the Gudgeon, Gobio Gobio) in United Kingdom freshwaters. Environmental Toxicology and Chemistry 20, 2841–2847.CrossRefGoogle Scholar
VAN AERLE, R., POUNDS, N., HUTCHINSON, T. H., MADDIX, S. & TYLER, C. R. ( 2002). Window of sensitivity for the estrogenic effects of ethinylestradiol in early life-stages of fathead minnow, Pimephales promelas. Ecotoxicology 11, 423–434.CrossRefGoogle Scholar
VAN DER KRAAK, G. J., MUNKITTRICK, K. R., McMASTER, M. E., PORTT, C. B. & CHANG, J. P. (1992). Exposure to bleached kraft pulp-mill effluent disrupts the pituitary-gonadal axis of white sucker at multiple sites. Toxicology and Applied Pharmacology 115, 224–233.CrossRefGoogle Scholar
VIGANO, L., ARILLO, A., BOTTERO, S., MASSARI, A. & MANDICH, A. (2001). First observation of intersex cyprinids in the Po River (Italy). Science of the Total Environment 269, 189–194.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
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
WILLIAMS, M. A., PENLINGTON, M. C., KING, J. A., HOOLE, D. & ARME, C. ( 1998). Ligula intestinalis (Cestoda) infections of roach (Rutilus rutilus) (Cyprinidae): immunocytochemical investigations into the salmon- and chicken-II type gonadotrophin-releasing hormone (GnRH) systems in host brains. Acta Parasitologica 43, 232–235.Google Scholar
YADA, T. & NAKANISHI, T. ( 2002). Interaction between endocrine and immune systems in fish. International Reviews in Cytology 220, 35–92.CrossRefGoogle Scholar
YOKOTA, H., SEKI, M., MAEDA, M., OSHIMA, Y., TADOKORO, H., HONJO, T. & KOBAYASHI, K. (2001). Life-cycle toxicity of 4-nonylphenol to medaka (Oryzias latipes). Environmental Toxicology and Chemistry 20, 2552–2560.CrossRefGoogle Scholar