Advertisement

Fish Physiology and Biochemistry

, Volume 26, Issue 1, pp 85–101 | Cite as

Histopathological assessment of gonadal tissue in wild fishes

  • V.S. Blazer
Article

Abstract

Histology offers a powerful tool in the study of reproductive health of fishes. It is routinely used for sex verification, identifying stage of development, documenting presence of intersex, tumors, parasites and other abnormalities and quantifying atresia. It can also be used for more subtle changes such as thickness of the vitelline envelope at various stages, yolk appearance, necrosis of sperm, and Sertoli cell proliferation. Gonadal histology, in conjunction with hormone and vitellogenin measurements, morphological and fecundity studies, can provide insights into the effects of various environmental stressors on reproductive health. However, much research, both field and laboratory, is needed to understand cause and effect for observed changes and to understand the meaning of many of the histological observations made in field studies, in terms of reproductive success of fish populations.

fish gonads histology ovary pathology testes 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ahsan, S.N. 1966. Cyclical changes in the testicular activity of lake chub, Couesius plumbeus. Can. J. Zool. 44: 149–159.Google Scholar
  2. Arukwe, A., Knudsen, F.R. and Goksøyr, A. 1997. Fish zona radiata (eggshell) protein: a sensitive biomarker for environmental estrogens. Environ. Health Perspect. 105: 418.PubMedGoogle Scholar
  3. Atz, J.W. 1964. Intersexuality in fishes. In: Intersexuality in Vertebrates Including Man, pp. 145–232. Edited by C.N. Armstrong and A.J. Marshall. Academic Press, NY.Google Scholar
  4. Balon, E.K. 1975. Reproductive guilds of fishes: a proposal and definitions. J. Fish. Res. Bd. Can. 32: 821–864.Google Scholar
  5. Balon, E.K. 1981. Additions and amendments to the classification of reproductive styles in fishes. Env. Biol. Fish. 6: 377–389.CrossRefGoogle Scholar
  6. Bandyopadhyay, M.P. and Aditya, A.K. 1998. Chemical induced changes in percentage and sizes of diameter in the ovarian oocytes of Anabas testudineus (Bloch). J. Freshwat. Biol. 10: 75–82.Google Scholar
  7. Barry, C.E., Wainscott, M.R., Foott, S.J. and Patiño, R. 2001. Gonadal macrophage aggregates: novel biomarker of contaminant exposure and effect in male fishes? Proceedings of the Society of Environmental Toxicology and Chemistry 2001 Annual meeting, Nov. 11–15, Baltimore, MD, 222 pp.Google Scholar
  8. Berlinsky, D.L., Jackson, L.F., Smith, T.I.J. and Sullivan, C.V. 1995. The annual reproductive cycle of the white bass Morone chrysops. J. World Aqua. Soc. 26: 252–260.Google Scholar
  9. Besseau, L. and Faliex, E. 1994. Resorption of unemitted gametes in Lithognathus mormyrus (Sparidae, Teleostei): a possible synergic action of somatic and immune cells. Cell. Tissue Res. 276: 123–132.PubMedCrossRefGoogle Scholar
  10. Bhatti, M.N. and Al-Daham, N.K. 1978. Annual cyclical changes in the testicular activity of a freshwater teleost, Barbus luteus (Heckel) from Shatt-Al-Arab, Iraq. J. Fish Biol. 13: 321–326.CrossRefGoogle Scholar
  11. Blazer, V.S., Facey, D.E., Fournie, J.W., Courtney, L.A. and Summers, J.K. 1994. Macrophage aggregates as indicators of environmental stress. In: Modulators of Fish Immune Responses, Vol. 1, pp. 169–185. Edited by J.S. Stolen J.S. and T.C. Fletcher. SOS Publications, Fair Haven, NJ.Google Scholar
  12. Blazer, V.S., Fournie, J.W. and Weeks-Perkins, B.A. 1997. Macrophage aggregates: Biomarker for immune function in fish? In: Environmental Toxicology and Risk Assessment: Modeling and Risk Assessment (Sixth Volume), pp. 360–375. F.J. Dwyer, T.R. Doane and M.L. Hinman. American Society for Testing and Materials, Philadelphia, PA.Google Scholar
  13. Borg, B. and Van Veen, T.H. 1982. Seasonal effects of photoperiod and temperature on the ovary of the three-spined stickleback, Gasterosteus aculeatus L. Can. J. Zool. 60: 3387–3393.Google Scholar
  14. Bortone, S.A. and Cody, R.F. 1999. Morphological masculinization in poeciliid females from a paper mill effluent receiving tributary of the St. Johns River, Florida, USA. Bull. Environ. Contam. Toxicol. 63: 150–156.PubMedCrossRefGoogle Scholar
  15. Braekevelt, C.R. and McMillan, D.B. 1967. Cyclic changes in the ovary of the brook stickelback, Eucalia inconstans (Kirtland). J. Morphol. 123: 373–396.PubMedCrossRefGoogle Scholar
  16. Breder, C.M., Jr., and Rosen, D.E. 1966. Modes of reproduction in fishes. Natural History Press, Garden City, NJ. 941 pp.Google Scholar
  17. Burke, M.G. and Leatherland, J.F. 1984. Seasonal changes in testicular histology of brown bullheads, Ictalurus nebulosus Lesueur. Can. J. Zool. 62: 1185–1194.CrossRefGoogle Scholar
  18. Budd, J., Schroder, J.D., and Dukes, K.D. 1975. Tumors of yellow perch. In: The Pathology of Fishes, pp. 895–906. Edited by W.E. Ribeln and G. Migaki. University of Wisconsin Press, Madison, WIGoogle Scholar
  19. Chan, S.T.H., Wright, A. and Phillips, J.G. 1967. The atretic structures in the gonads of the rice-field eel (Monopterus albus) during natural sex-reversal. J. Zool. London 151: 129–141.CrossRefGoogle Scholar
  20. Cheek, A.O., Brouwer, T.H., Carroll, S., Manning, S., McLachlan, J.A. and Brouwer, M. 2001. Experimental evaluation of vitellogenin as a predictive biomarker for reproductive disruption. Environ. Health Perspect. 109: 681–690.PubMedGoogle Scholar
  21. Chitwood, M. and Lichtenfels, J.R. 1972. Identification of parasitic metazoa in tissue sections. Exp. Parasitol. 32: 407–519.PubMedCrossRefGoogle Scholar
  22. Cross, J.N. and Hose, J.E. 1988. Evidence for impaired reproduction in white croaker Genyonemus lineatus from contaminated areas off southern California. Mar. Environ. Res. 24: 185–188.CrossRefGoogle Scholar
  23. DeVlaming, V. 1983. Oocyte development patterns and hormonal involvements among teleosts. In: Control Processes in Fish Physiology, pp. 176–210. Edited by J.C. Rankin, T.J. Pitcher and R.T. Duggan. John Wiley & Sons, NY.Google Scholar
  24. DeVlaming, V., Grossman, G. and Chapman, F. 1982. On the use of the gonadosomatic index. Comp. Biochem. Physiol. 73A: 1–39.Google Scholar
  25. Denslow, N.D., Chow, M.C., Kroll, K.J. and Green, L. 1999. Vitellogenin as a biomarker of exposure for estrogen or estrogen mimics. Ecotoxicol. 8: 385–398.CrossRefGoogle Scholar
  26. Down, N.E. and Leatherland, J.F. 1989. Histopathology of gonadal neoplasms in cyprinid fish from the lower Great Lakes of North America. J. Fish Dis. 12: 415–437.CrossRefGoogle Scholar
  27. Ellis, A.E. 1980. Antigen-trapping in the spleen and kidney of plaice Pleuronectes platessa L. J. Fish Dis. 3: 413–426.CrossRefGoogle Scholar
  28. Ellis, A.E., Munroe, A.L.S. and Roberts, R.J. 1976. Defense mechanisms in fish. 1. A study of the phagocytic system and the fate of intraperitoneally injected material in the plaice (Pleuronectes platessa). J. Fish Biol. 8: 67–78.CrossRefGoogle Scholar
  29. Flammarion, P., Brion, F., Babut, M., Garric, J., Migeon, B., Noury, P., Thybaud, E., Tyler, C.R. and Palazzi, X. 2000. Induction of fish vitellogenin and alterations in testicular structue: Preliminary results of estrogenic effects in chub (Leuciscus cephaus). Ecotoxicol. 9: 127–135.CrossRefGoogle Scholar
  30. Fournie, J.W., Summers, J.K., Courtney, L.A., Engle, V.D. and Blazer, V.S. 2001. Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. J. Aquat. Anim. Health 13: 105–116.CrossRefGoogle Scholar
  31. Gardiner, C.H., Fayer, R. and Dubey, J.P. 1998. An Atlas of Protozoan Parasites in Animal Tissues. Registry of Veterinary Pathology, Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DC, 84 pp.Google Scholar
  32. Gardiner, C.H. and Poynton, S.L. 1999. An Atlas of Metazoan Parasites in Animal Tissues. Registry of Veterinary Pathology, Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DC, 63 pp.Google Scholar
  33. Goodbred, S.L., Gilliom, R.J., Gross, T.S., Denslow, N.P., Bryant, W.L. and Schoeb, T.R. 1997. Reconnaissance of 17β-estradiol, 11–ketotestosterone, vitellogenin, and gonadal histopathology in common carp of United States streams: Potential for contaminant-induced endocine disruption. U.S. Geological Survey Open-File Report 96–627, Sacramento, California, 47 pp.Google Scholar
  34. Grier, H. 1981. Cellular organization of the testis and spermatogenesis in fishes. Amer. Zool. 21: 345–357.Google Scholar
  35. Grier, H. 2000. Ovarian germinal epithelium and folliculogenesis in the common snook, Centropomus undecimalis (Teleostei: Centropomidae). J. Morphol. 243: 265–281.PubMedCrossRefGoogle Scholar
  36. Grier, H.J. and Taylor, R.G. 1998. Testicular maturation and regression in common snook. J. Fish Biol. 53: 521–542.CrossRefGoogle Scholar
  37. Guraya, S.S. 1986. The Cell and Molecular Biology of Fish Oogenesis. In: Monographs in Developmental Biology Vol. 18, 223 pp. Edited by H.W. Sauer. Karger, Basel.Google Scholar
  38. Hawkins, W.E., Fournie, J.W., Ishikawa, T. and Walker, W.W. 1996. Germ cell neoplasms in Japanese medaka. J. Aquat. Anim. Health 8: 120–129.CrossRefGoogle Scholar
  39. Hemming, J.M., Waller, W.T. and Ammann, L.P. 2001. Assessment of wastewater effluent estrogenicity in North Central Texas using the vitellogenin biomarker in male fathead minnows (Pimephales promelas Rafinesque). Texas J. Sci. 53: 335–344.Google Scholar
  40. Henderson, N.E. 1962. The annual cycle in the testis of the eastern brook trout, Salvelinus fontinalis (Mitchell). Can. J. Zool. 40: 631–641.Google Scholar
  41. Hinton, D.E., Baumann, P.C., Gardner, G.R., Hawkins, W.E., Hendricks, J.D., Murchelano, R.A. and Okihiro, M.S. 1992. Histopathologic biomarkers. In: Biomarkers Biochemical, Physiological and Histological Markers of Anthropogenic Stress, pp. 155–210. Edited by R.J. Huggett, R.A. Kimerle, P.M. Mehrle, Jr., and H.L. Bergman. Lewis Publishers, Chelsea, MI.Google Scholar
  42. Hinton, D.E. and Laurén, D.J. 1990. Integrative histopathological approaches to detecting effects of environmental stressors in fishes. Am. Fish. Soc. Symp. 8: 51–66.Google Scholar
  43. Htun-Han, M. 1978. The reproductive biology of the dab Limanda limanda (L.) in the North Sea: Seasonal changes in the ovary. J. Fish Biol. 13: 351–359.CrossRefGoogle Scholar
  44. Jackson, L.F. and Sullivan, C.V. 1995. Reproduction of white perch: Annual gametogenic cycle. Trans. Amer. Fish. Soc. 124: 563–577.CrossRefGoogle Scholar
  45. Jobling, S., Nolan, M., Tyler, C.B., Brighty, G. and Sumpter, J.P. 1998. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 32: 2498–2506.CrossRefGoogle Scholar
  46. Johnson, L.L., Casillas, E., Collier, T.K., McCain, B.B. and Varanasi, U. 1988. Contaminant effects on ovarian development in English sole (Parophrys vetulus) from Puget Sound, Washington. Can. J. Fish. Aquat. Sci. 45: 2133–2146.CrossRefGoogle Scholar
  47. Johnson, L.L., Sol, S.Y., Lomax, D.P., Nelson, G.M., Sloan, C.A., and Casillas, E. 1997. Fecundity and egg weight in English sole, Pleuronectes vetulus, from Puget Sound, Washington: influences of nutritional status and chemical contaminants. Fish. Bull. 95: 231–249.Google Scholar
  48. Kendall, R.J., Dickerson, R.I., Giesy, J.P., and Suk, W.A. 1998. Principles and Processes for Evaluating Endocrine Disruption in Wildlife. Society for Environmental Toxicology and Chemistry Press, Pensacola, FL. 515 pp.Google Scholar
  49. Kime, D.E. 1998. Endocrine Disruption in Fish. Kluwer Academic Publishers, Norwell.Google Scholar
  50. Leatherland, J.F., Down, N.E., Falkmer, S. and Sonstegard, R.A. In Press. Endocrine glands and reproductive system. In: Pathobiology of Spontaneous and Induced Neoplasms in Fishes: Comparative Characterization, Nomenclature and Literature. Edited by C.J. Dawe, J.C. Harshbarger, S.R. Wellings and J.D. Standberg. Academic Press, NY.Google Scholar
  51. Lucano-Ramirez, G., Cruz, M. V.-S., Ruiz-Ramirez, S. and López-Murilla, T. 2001. Histology of the oocytes of Lutjanus peru (Nichols and Murphy, 1922) (Pisces: Lutjanidae). Ciencias Marinus 27: 335–349.Google Scholar
  52. Luna, L.G. 1992. Histopathological methods and color atlas of special stains and artifacts. American HistoLabs, Gaithersburg, MD.Google Scholar
  53. Lye, C.M., Frid, C.L.J. and Gill, M.E. 1998. Seasonal reproductive health of flounder Platichthys flesus exposed to sewage effluent. Mar. Ecol. Prog. Ser. 170: 249–260.Google Scholar
  54. Mackay, N.J. 1973. Reproductive cycle of the fire-tail gudgeon, Hypseleotris galii. 2. Seasonal histological changes in the testis. Austr. J. Zool. 21: 53–66.CrossRefGoogle Scholar
  55. McCormick, J.H., Stokes, G.N. and Hermanutz, R.O. 1989. Oocyte atresia and reproductive success in fathead minnows (Pimephales promelas) exposed to acidified hardwater environments. Arch. Environ. Contam. Toxicol. 18: 207–214.PubMedCrossRefGoogle Scholar
  56. McMaster, M.E., Van Der Kraak, G.J. and Munkittrick, K.R. 1996. An epidemiological evaluation of the biochemical basis for steroid hormone depressions in fish exposed to industrial wastes. J. Great Lakes Res. 22: 153–171.CrossRefGoogle Scholar
  57. Mikaelian, I., de Lafontaine, Y., Harshbarger, J.C., Lee, L.L.J. and Martineau, D. 2002. Health of lake whitefish (Coregonus clupeaformis) with elevated tissue levels of environmental contaminants. Environ. Toxicol. Chem. 21: 532–541.PubMedCrossRefGoogle Scholar
  58. Miles-Richardson, S.R., Kramer, V.J., Fitzgerald, S.D., Render, J.A., Yamini, B., Barbee, S.J. and Giesey, J.P. 1999. Effects of waterborne exposure of 17 β-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquat. Toxicol. 47: 129–145.CrossRefGoogle Scholar
  59. Miranda, A.C.L., Bazzoli, N., Rizzo, E. and Sato, Y. 1999. Ovarian follicular atresia in two teleost species: a histological and ultrastructural study. Tis. Cell. 31: 480–488.CrossRefGoogle Scholar
  60. Monosson, E., Hogson, R.G., Fleming, W.J. and Sullivan, C.V. 1996. Blood plasma levels of sex steroid hormones and vitellogenin in striped bass (Morone saxatilis) exposed to 3,3′,4,4′-tetrachlorobiphenyl (TCB). Bull. Environ. Contam. Toxicol. 56: 782–787.PubMedCrossRefGoogle Scholar
  61. Munro, A.D., Scott, A.P. and Lam, T.J. (eds.). 1990. Reproductive Seasonality in Teleosts: Environmental Influences. CRC Press, Inc., Baton Raton, FL. 254 pp.Google Scholar
  62. Mytilineou, C.H. 2000. Histological study of atresia in Pagellus acarne (Pisces: Sparidae). In: Proceedings of the 6th Hellenic Symposium on Oceanography and Fisheries, Vol. 2, pp. 28–33. NCMR Association of Employees, Athens, Greece.Google Scholar
  63. Nagahama, Y. 1983. The functional morphology of teleost gonads. In: Fish Physiology, Vol. IXA, pp. 223–264. Edited by W.S. Hoar, D.J. Randall and E.M. Donaldson. Academic Press, Orlando, FL.Google Scholar
  64. Niimi, A.J. 1983. Biological and toxicological effects of environmental contaminants in fish and their eggs. Can. J. Fish. Aquat. Sci. 40: 306–312.Google Scholar
  65. Nolan, M., Jobling, S., Brighty, G., Sumpter, J.P. and Tyler, C.R. 2001. A histological description of intersexuality in the roach. J. Fish Biol. 58: 160–176.CrossRefGoogle Scholar
  66. Okumura, H., Saeki, F., Matsubara, H., Adachi, S. and Tamauchi, K. 2001. Changes in serum vitellogenin levels and immunohistochemical localization of vitellogenin in hepatic cells during ovarian development in the Japanese eel. Fish. Sci. 67: 880–887.CrossRefGoogle Scholar
  67. Palmer, E.E., Sorensen, P.W. and Adelman, I.R. 1995. A histological study of seasonal ovarian development in freshwater drum in the Red Lakes, Minnesota. J. Fish Biol. 47: 199–210.CrossRefGoogle Scholar
  68. Parrott, J.L., Jardine, J.J., Blunt, B.R., McCarthy, L.H., McMaster, M.E., Wood, C.S., Roberts, J. and Carey, J.H. 1999. Comparing biological responses to mill process changes: A study of steroid concentrations in goldfish exposed to effluent and waste streams from a Canadian bleached sulphite mill. Wat. Sci. Tech. 40: 115–121.CrossRefGoogle Scholar
  69. Patiño, R., and Sullivan, C.V. 2002. Ovarian follicle growth, maturation, and ovulation in teleost fishes. Fish Physiol. Biochem. 26: 57–70.CrossRefGoogle Scholar
  70. Potts, G.W. and Wootton, R.J. (eds). 1984. Fish Reproduction: Strategies and Tactics. Academic Press, New York. 410 pp.Google Scholar
  71. Purdom, C.E., Hardiman, P.A., Bye, V.J., Eno, N.C., Tyler, C.R. and Sumpter, J.P. 1994. Estrogenic effects of effluents from sewage treatment works. Chem. Ecol. 8: 275–285.Google Scholar
  72. Ravaglia, M.A. and Maggese, M.C. 1995. Melano-macrophage centers in the gonads of the swamp eel, Synbranchus marmoratus Bloch, (Pisces, Synbranchidae): histological and histochemical characterization. J. Fish Dis. 18: 117–125.CrossRefGoogle Scholar
  73. Rideout, R.M., Maddock, D.M. and Burton, M.P.M. 1999. Oogenesis and the spawning pattern in Greenland halibut from the North-west Atlantic. J. Fish Biol. 54: 196–207.CrossRefGoogle Scholar
  74. Rodriguez, J.N., Oteme, Z.J. and Hem, S. 1995. Comparative study of vitellogenesis of two African catfish species Chrysichthys nigrodigitatus (Claroteidae) and Heterobranchus longifilis (Clariidae). Aquat. Living Res. 8: 291–296.Google Scholar
  75. Rolland, R.M. 2000. Ecoepidemiology of the effects of pollution on reproduction and survival of early life stages in teleosts. Fish Fish. 1: 41–72.Google Scholar
  76. Rolland, R.M., Gilbertson, M. and Petersen, R.E. (eds.). 1997. Chemically induced alterations in functional development and reproduction of fishes. Proceedings from a session at the Wingspread Conference Center, July 1995, Racine, WI. Society of Environmental Toxicology and Chemistry Press, Pensacola, FL. 224 pp.Google Scholar
  77. Saidapur, S.K. 1978. Follicular atresia in the ovaries of nonmammalian vertebrates. Int. Rev. Cytol. 54: 225–244.PubMedCrossRefGoogle Scholar
  78. Sangalang, G.B., Freeman, H.C. and Crowell, R. 1981. Testicular abnormalities in cod (Gadus morhua) fed aroclor 1254. Arch. Environ. Contam. Toxicol. 10: 617–626.PubMedCrossRefGoogle Scholar
  79. Santos, J.E., Bazzoli, N., Rizzo, E. and Santos, G.B. 2001. Morphofunctional organization of the male reproductive system, of the catfish Iheringichthys labrosus (Lütken, 1874) (Siluriformes: Pimelodidae). Tis. Cell 33: 533–540.CrossRefGoogle Scholar
  80. Schmitt, C.J., Blazer, V.S., Dethloff, G.M., Tillitt, D.E., Gross, T.S., Bryant, W.L. Jr., DeWeese, L.R., Smith, S.B., Goede, R.W., Bartish, T.M. and Kubiak, T.J. 1999. Biomonitoring of Environmental Status and Trends (BEST) Program: Field procedures for assessing the exposure of fish to environmental contaminants. U.S. Geological Survey, Biological Resources Division, Columbia, (MO). Information and Technology Report USGS/BRD-1999–0007, 70 pp.Google Scholar
  81. Schmitt, C.J. and Dethloff, G.M. (eds). 2000. Biomonitoring of Environmental Status and Trends (BEST) Program: Selected methods for monitoring chemical contaminants and their effects in aquatic ecosystems. U.S. Geological Survey, Biological Resources Division, Columbia (MO): Information and Technology Report USGS/BRD-2000–0005, 81 pp.Google Scholar
  82. Schulz, R.W. and Miura, T. 2002. Spermatogenesis and its endocrine regulation. Fish Physiol. Biochem. 26: 43–56.CrossRefGoogle Scholar
  83. Selman, K. and Wallace, R.A. 1989. Cellular aspects of oocyte growth in teleosts. Zool. Sci. 6: 211–231.Google Scholar
  84. Selman, K., Wallace, R.A., Sarka, A. and Xiaoping, Q. 1993. Stages of oocyte development in the zebrafish, Brachydanio rerio. J. Morphol. 218: 203–224.CrossRefGoogle Scholar
  85. Spies, R.B., Stegeman, J.J., Hinton, D.E. Woodin, B., Smolowitz, R., Okihiro, M. and Shea, D. 1996. Biomarkers of hydrocarbon exposure and sublethal effects in embiotocid fishes from a natural petroleum seep in the Santa Barbara Channel. Aquat. Toxicol. 34: 195–219.CrossRefGoogle Scholar
  86. Spitsbergen, J.M., Tsai, H.-W., Reddy, A., Miller, T., Arbogast, D., Hendricks, J.D. and Bailey, G.S. 2000. Neoplasia in zebrafish (Danio rerio) treated with N-methyl-N′-nitro-N-nitrosoguanidine by three exposure routes at different developmental stages. Toxicol. Pathol. 28: 716–725.PubMedGoogle Scholar
  87. Stott, G.G., McArthur, N.H., Tarpley, R., Jacobs, V. and Sis, R.F. 1981. Histopathologic survey of ovaries of fish from petroleum production and control sites in the Gulf of Mexico. J. Fish Biol. 18: 261–269.CrossRefGoogle Scholar
  88. Stott, G.G., Haensly, W., Neff, J. and Sharp, J. 1983. Histopathologic survey of ovaries of plaice, Pleuronectes platessa L., from AberWrac'h and Aber Benoit, Brittany, France oil spills. J. Fish. Dis. 6: 429–437.CrossRefGoogle Scholar
  89. Strüssmann, C.A. and Nakamura, M. 2002. Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiol. Biochem. 26: 13–29.CrossRefGoogle Scholar
  90. Sulistyo, I., Fontaine, P., Rinchard, J., Gardeur, J.-N., Migaud, H., Capeville, B. and Kestemont, P. 2000. Reproductive cycle and plasma levels of steroids in male Eurasian perch Perca fluviatilis. Aquat. Living Res. 13: 99–106.CrossRefGoogle Scholar
  91. Sumpter, J.P. 1995. Feminized responses in fish to environmental estrogens. Toxicol. Lett. 82/83: 737–742.PubMedCrossRefGoogle Scholar
  92. Teh, S.J., Adams, S.M. and Hinton, D.E. 1997. Histopathological biomarkers in feral freshwater fish populations exposed to different types of contaminant stress. Aquat. Toxicol. 37: 51–70.CrossRefGoogle Scholar
  93. Treasurer, J.W. and Holliday, F.G.T. 1981. Some aspects of the reproductive biology of perch Perca fluviatilis L. A histological description of the reproductive cycle. J. Fish Biol. 18: 359–376.CrossRefGoogle Scholar
  94. Tyler, C.R. and Sumpter, J.P. 1996. Oocyte growth and development in teleosts. Rev. Fish Biol. Fish. 6: 287–318.CrossRefGoogle Scholar
  95. Tyler, C.R., Sumpter, J.P. and Witthames, P.R. 1990. The dynamics of oocyte growth during vitellogenesis in the rainbow trout (Oncorhychus mykiss). Biol. Reprod. 43: 202–209.PubMedCrossRefGoogle Scholar
  96. Van Den Belt, K., Wester, P.W., Van Der Ven, L.T.M., Verheyen, R. and Witters, H. 2002. Effects of ethynylestradiol on the reproductive physiology in zebrafish (Danio rerio): time dependency and reversibility. Environ. Toxicol. Chem. 21: 767–775.PubMedCrossRefGoogle Scholar
  97. Wallace, R.A. and Selman, K. 1981. Cellular and dynamic aspects of oocyte growth in teleosts. Amer. Zool. 21: 325–343.Google Scholar
  98. Wester, P.W. 1991. Histopathological effects of environmental pollutants β-HCH and methyl mercury on reproductive organs in freshwater fish. Comp. Biochem Physiol. 100C: 237–239.Google Scholar
  99. Wolke, R.E. 1992. Piscine macrophage aggregates: A review. Ann. Rev. Fish Dis. 2: 91–108.CrossRefGoogle Scholar
  100. Wood, A.W. and Van Der Kraak, G. 2001. Apoptosis and ovarian function: Novel perspectives from the teleosts. Biol. Reprod. 64: 264–271.PubMedCrossRefGoogle Scholar
  101. Yamamoto, K. and Yamazaki, F. 1961. Rhythm of development in the oocyte of the gold-fish, Carassius auratus. Bull. Fac. Fish. Hokkaido Univ. 12: 93–114.Google Scholar
  102. Yin, D. 1996. Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Rad. Biol. Med. 21: 871–888.PubMedCrossRefGoogle Scholar
  103. Ziegenfuss, M.C. and Wolke, R.E. 1991. The use of fluorescent microspheres in the study of piscine macrophage aggregate kinetics. Dev. Comp. Immunol. 15: 165–171.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • V.S. Blazer
    • 1
  1. 1.National Fish Health Research Laboratory, U.S. Geological SurveyLeetown Science CenterKearneysvilleUSA (Fax

Personalised recommendations