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Gonad histology and vitellogenin concentrations in brown trout (Salmo trutta) from Danish streams impacted by sewage effluent

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Abstract

Brown trout (Salmo trutta) collected from a number of Danish streams impacted by sewage effluent were examined for alterations to gonadal development and induction of vitellogenin synthesis. Among fish collected in June/July 2000/2001 and November 2002 higher levels of plasma vitellogenin were found in males from six streams impacted by sewage effluent compared to males from their respective reference sites. A direct non-competitive ELISA was developed for brown trout vitellogenin in order to perform the vitellogenin measurements. Intersex in females with no apparent relation to sewage effluent exposure was observed at all sites. In one stream, male brown trout with a very high level of vitellogenin were concomitantly found to have a high degree of vacuolation of the testes and a presence of only the early spermatogenic stage, spermatogonia. The cause of these alterations to the testis structure is unclear. However, as a high level of plasma vitellogenin in these males indicated estrogenic exposure, the vacuolation might also be a result of endocrine disruption causing delayed or disrupted spermatogenesis.

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References

  • Allen Y, Scott AP, Matthiessen P, Haworth S, Thain JE, 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. Environ Toxicol Chem 18:1791–1800

    Article  CAS  Google Scholar 

  • Ashby KR (1965) The effect of steroid hormones on the development of the reproductive system of Salmo trutta L when administered at the commencement of spermatogenetic activity in the testes. Riv di Biol 58:139–169

    CAS  Google Scholar 

  • Aravindakshan J, Paquet V, Gregory M, Dufresne J, Fournier M, Marcogliese DJ, Cyr DG (2004) Consequences of xenoestrogen exposure on male reproductive function in spottail shiners (Notropis hudsonius). Toxicol Sci 78:156–165

    Article  CAS  Google Scholar 

  • Århus Amt (1998) Vandføringens median minimum 1976–95. Teknisk Rapport

  • Århus Amt (2000) Punktkilder 1999. Spildevandsudledninger i Århus Amt. Teknisk Rapport

  • Billard R (1983) A quantitative analysis of spermatogenesis in the trout, Salmo trutta fario. Cell Tissue Res 230:495–502

    Article  CAS  Google Scholar 

  • Billard R, Takashima F (1983) Resorption of spermatozoa in the sperm duct of spermatozoa during the post-spawning period. Bull Jap Soc Sci Fish 49:387–392

    Google Scholar 

  • Billard R (1987) The reproductive cycle of male and female brown trout (Salmo trutta fario): a quantitative study. Reprod Nutr Dévelop 27:29–44

    Article  Google Scholar 

  • Boekelheide K (1988) Rat testis during 2,5-hexanedione intoxication and recovery. 1. Dose response and the reversibility of germ cell loss. Toxicol Appl Pharmacol 92:18–27

    Article  CAS  Google Scholar 

  • Boekelheide K, Hall SJ (1991) 2,5-hexanedione exposure in the rat results in long-term testicular atrophy despite the presence of residual spermatogonia. J Androl 12:18–26

    CAS  Google Scholar 

  • Christiansen LB, Pedersen KL, Pedersen SN, Korsgaard B, Bjerregaard P (2000) In vivo comparison of xenoestrogens using rainbow trout vitellogenin induction as a screening system. Environ Toxicol Chem 19:1867–1874

    Article  CAS  Google Scholar 

  • Creasy DM, Foster JR, Foster PM (1983) The morphological development of di-N-pentyl phthalate induced testicular atrophy in the rat. J Pathol 139:309–321

    Article  CAS  Google Scholar 

  • Dziewulska K, Domagala J (2003) Histology of salmonid testes during maturation. Reprod Biol 3:47–61

    Google Scholar 

  • Flammarion P, Brion F, Babut M, Garric J, Migeon B, Noury AP, Thybaud E (2000) Induction of fish vitellogenin and alteration in testicular structure: preliminary results of estrogenic effects in chub (Leucicus cephalus). Ecotoxicology 9:127–135

    Article  CAS  Google Scholar 

  • Folmar LC, Denslow ND, Rao V, Chow M, Crain DA, Enblom J, Marcino J, Guillette LJ (1996) Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ Health Perspect 104:1096–1101

    Article  CAS  Google Scholar 

  • Folmar LC, Denslow ND, Kroll K, Orlando EF, Enblom J, Marcino J, Metcalfe CD, Guillette LJ (2001) Altered serum sex steroids and vitellogenin induction in walleye (Stizostedion vitreum) collected near a metropolitan sewage treatment plant. Arch Environ Contam Toxicol 40:392–398

    Article  CAS  Google Scholar 

  • Gercken J, Sordyl H (2002) Intersex in feral marine and freshwater fish from north-eastern Germany. Mar Environ Res 54:651–655

    Article  CAS  Google Scholar 

  • Gray LE Jr, Ostby J, Furr J, Price M, Veeramachaneni DNR, Parks L (2000) Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 58:350–365

    Article  CAS  Google Scholar 

  • Harries JE, Sheahan DA, Jobling S, Matthiessen P, Neall P, Sumpter JP, Tylor T, Zaman N (1997) Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout. Environ Toxicol Chem 16:534–542

    Article  CAS  Google Scholar 

  • Harries JE, Runnalls T, Hill E, Harris CA, Maddix S, Sumpter JP, Tyler CR (2000) Development of a reproductive performance test for endocrine disrupting chemicals using pair-breeding fathead minnows (Pimephales promelas). Environ Sci Technol 34:3003–3011

    Article  CAS  Google Scholar 

  • Harshbarger JC, Coffey MJ, Young MY (2000) Intersexes in Mississippi River shovelnose sturgeon sampled below Saint Louis Missouri, USA. Mar Environ Res 50:247–250

    Article  CAS  Google 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. Mar Environ Res 49:37–53

    Article  CAS  Google Scholar 

  • Hecker M, Tyler CR, Hoffmann M, Maddix S, Karbe L (2002) Plasma biomarkers in fish provide evidence for endocrine modulation in the Elbe river, Germany. Environ Sci Technol 36:2311–2321

    Article  CAS  Google Scholar 

  • Hemming JM, Waller WT, Chow MC, Denslow ND, Venables B (2001) Assessment of the estrogenicity and toxicity of a domestic wastewater effluent flowing through a constructed wetland system using biomarkers in male fathead minnow (Pimphales promelas). Environ Toxicol Chem 20:2268–2275

    Article  CAS  Google Scholar 

  • Henderson NE (1962) The annual cycle in the testis of the eastern brook trout, Salvelinus fontinalis (Mitchill). Can J Zool 40:631–645

    Article  Google Scholar 

  • Holbech H, Andersen L, Petersen GI, Korsgaard B, Pedersen KL, Bjerregaard P (2001) Development of an ELISA for vitellogenin in whole body homogenate of zebrafish (Danio danio). Comp Biochem Physiol C 130:119–131

    CAS  Google Scholar 

  • Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP (1998) Widespread sexual disruption in wild fish. Environ Sci Technol 32:2498–2506

    Article  CAS  Google Scholar 

  • Jobling S, Beresford N, Nolan M, Rodgers-Gray TP, Brighty G, Sumpter JP, Tyler CR (2002a) Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol Reprod 66:272–281

    Article  CAS  Google Scholar 

  • Jobling S, Coey S, Whitmore JG, Kime DE, Van Look KJW, McAllister BG, Beresford N, Henshaw AC, Brighty G, Tyler CR, Sumpter JP (2002b) Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol Reprod 67:515–524

    Article  CAS  Google Scholar 

  • Kime DE (1999) A strategy for assessing the effects of xenobiotics on fish reproduction. Sci Tot Environ 225:3–11

    Article  CAS  Google Scholar 

  • Larsson DGJ, Adolfsson-Erici M, Parkkonen J, Pettersson M, Berg AH, Olsson P-E, Förlin L (1999) Ethinyloestradiol – an undesired fish contraceptive? Aquat Toxicol 45:91–97

    Article  CAS  Google Scholar 

  • Lavado R, Thibaut R, Raldúa D, Martín R, Porte C (2004) First evidence of endocrine disruption in feral carp from the Ebro River. Toxicol Appl Pharmacol 196:247–257

    Article  CAS  Google Scholar 

  • Lye CM, Frid CL, Gill ME, McCormick D (1997) Abnormalities in the reproductive health of flounder, Platichthys flesus, exposed to effluent from a sewage treatment works. Mar Pollut Bull 34:34–41

    Article  CAS  Google Scholar 

  • Lye CM, Frid CL, Gill ME (1998) Seasonal reproductive health of flounder Platichthys flesus exposed to sewage effluent. Mar Ecol-Prog Ser 170:249–260

    Article  Google Scholar 

  • Maisse G, Mourot B, Breton B, Fostier A, Marcuzzi O, Le Bail PY, Bagliniére JL, Richard A (1991) Sexual maturity in sea trout, Salmo trutta L., running up the River Calonne (Normandy, France) at the ‘finnock’ stage. J Fish Biol 39:705–715

    Article  Google Scholar 

  • Maitre JL, Derrien S, Tenniswood M, Valotaire Y, Leguellec C (1985) Measurement of vitellogenin from rainbow trout by rocket immunoelectrophoresis. Application to the kinetic analysis of estrogen stimulation in the male. Can J Biochem Cell Biol 63:982–987

    Article  CAS  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. Mar Environ Res 54:645–649

    Article  CAS  Google Scholar 

  • Miles-Richardson SR, Kramer VJ, Fitzgerald SD, Render JA, Yamini B, Barbee SJ, Giesy JP (1999a) Effects of waterborne exposure of 17β-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquat Toxicol 47:129–145

    Article  CAS  Google Scholar 

  • Miles-Richardson SR, Pierens SL, Nichols KM, Kramer VJ, Snyder EM, Snyder SA, Render JA, Fitzgerald D, Giesy JP (1999b) Effects of waterborne exposure of 4-nonylphenol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Environ Res A 80:122–137

    Article  Google Scholar 

  • Minier C, Caltot G, Leboulanger F, Hill EM (2000) An investigation of the incidence of intersex fish in Seine-Maritime and Sussex regions. Analusis 28:801–806

    Article  CAS  Google Scholar 

  • Ohkubo N, Mochida K, Adachi S, Hara A, Hotta K, Nakamura Y, Matsubara T (2003) Estrogenic activity in costal areas around Japan evaluated by measuring male serum vitellogenin in Japanese common goby Acanthogobius flavimanus. Fish Sci 69:1135–1145

    Article  CAS  Google Scholar 

  • Riehl R (1980) The occurrence of spermatozoa in the ovary of nulliparous females of Heterandria formosa Agassiz, 1853 (Pisces, Poeciliidae). Cell Tissue Res 1992:289–294

    Google Scholar 

  • Russel LD, Ettlin RA, SinhaHikim AP, Clegg ED 1990 Histological and histopathological evaluation of the testis. Cache River Press, USA

    Google Scholar 

  • Russel LD, Griswold MD (1993) The sertoli cell. Cache River Press

  • Sangalang GB, Freeman HC, Crowell R (1981) Testicular abnormalities in cod (Gadus morhua) fed arochlor 1254. Arch Environ Contam Toxicol 10:617–626

    Article  CAS  Google Scholar 

  • Sengal R, Tomar V, Pandey AK (1984) Comparative effects of two heavy metallic salts on the testis of viviparous teleost, Lebistes reticulatus (Peters). J Environ Biol 5:185–192

    Google Scholar 

  • Sharpe RM, Fisher JS, Millar MM, Jobling S, Sumpter JP (1995) Gestational and lactational exposure of rats to xenoestrogens results in reduced testicular size and sperm production. Environ Health Perspect 103:1136–1143

    Article  CAS  Google Scholar 

  • Sheahan DA, Brighty GC, Daniel M, Kirby SJ, Hurst MR, Kennedy M, Morris S, Routledge EJ, Sumpter JP, Waldock MJ (2002) Estrogenic activity measured in a sewage treatment works treating industrial inputs containing high concentrations of alkylphenolic compounds – a case study. Environ Toxicol Chem 3:507–514

    Article  Google Scholar 

  • Sherry J, Gamble A, Fielden M, Hodson P, Burnison B, Solomon K (1999) An ELISA for brown trout (Salmo trutta) vitellogenin and its use in bioassays for environmental estrogens. Sci Tot Environ 225:13–31

    Article  CAS  Google Scholar 

  • Silversand C, Hyllner SJ, Haux C (1993) Isolation, immunochemical detection, and observations of the instability of vitellogenin from four teleosts. J Exp Zool 267:587–597

    Article  CAS  Google Scholar 

  • Solé M, Barceló D, Porte C (2002a) Seasonal variation of plasmatic and hepatic vitellogenin and EROD activity in carp, Cyprinus carpio, in relation to sewage treatment plants. Aquat Toxicol 60:233–248

    Article  Google Scholar 

  • Solé M, López de Alda MJ, Castillo M, Porte C, Ladegaard-Pedersen K, Barcelo D (2002b) Estrogenicity determination in sewage treatment plants and surface waters from the Catalonian area (NE Spain). Environ Sci Technol 34:5076–5083

    Article  CAS  Google Scholar 

  • Stentiford GD, Longshaw M, Lyons BP, Jones G, Green M, Feist GW (2003) Histopathological biomarkers in estuarine fish species for the assessment of biological effects of contaminants. Mar Environ Res 55:137–159

    Article  CAS  Google Scholar 

  • van Aerle R, Nolan M, Jobling S, Christiansen LB, Sumpter JP, Tyler CR (2001) Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ Toxicol Chem 20:2841–2847

    Article  Google Scholar 

  • Vethaak AD, Lahr J, Kuiper RV, Grinwins GCM, Rankouhi TR, Giesy JP, Gerritsen A (2002) Estrogenic effects in fish in The Netherlands: some preliminary results. Toxicology 181–182:147–150

    Google Scholar 

  • Wahli T, Meier W, Segner H, Burkhardt-Holm P (1998) Immunhistochemical detection of vitellogenin in male brown trout from Swiss rivers. Histochem J 30:753–758

    Article  CAS  Google Scholar 

  • Wester PW, Canton HH (1992) Histopathological effects in Poecilia reticulata (Guppy) exposed to methyl mercury chloride. Toxicol Pathol 20:80–92

    Article  Google Scholar 

  • Wine RN, Li L-H, Barnes LH, Gulati DK, Chapin RE (1997) Reproductive toxicity of di-n-butylphthalate in a continuous breeding protocol in Sprague–Dawley rats. Environ Health Perspect 105:102–107

    Article  CAS  Google Scholar 

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Acknowledgements

Technician Charlotte Nielsen is greatly appreciated for her help with development and running of the ELISA and sectioning of gonads for histology. Aarhus and Vejle County and Hørsholm Municipality are thanked for help with collection of the fish. The project was funded by the Office of Environment, Aarhus County, Denmark.

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Authors and Affiliations

  1. Institute of Biology, University of Southern Denmark, Odense University, Campusvej 55, DK-5230, Odense M, Denmark

    Lisette B. Bjerregaard, Allan H. Madsen, Bodil Korsgaard & Poul Bjerregaard

  2. Department of Environment, Aarhus County, Lyseng Allé 1, DK-8270, Højbjerg, Denmark

    Lisette B. Bjerregaard

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  1. Lisette B. Bjerregaard
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  2. Allan H. Madsen
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  3. Bodil Korsgaard
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  4. Poul Bjerregaard
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Correspondence to Lisette B. Bjerregaard.

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Bjerregaard, L.B., Madsen, A.H., Korsgaard, B. et al. Gonad histology and vitellogenin concentrations in brown trout (Salmo trutta) from Danish streams impacted by sewage effluent. Ecotoxicology 15, 315–327 (2006). https://doi.org/10.1007/s10646-006-0061-9

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