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Morphological and histological changes inthe genital ducts ofthe male Atlantic stingray, Dasyatis sabina, during the seasonal reproductive cycle

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Abstract

Changes inthe morphology and histologyofthe epididymis and seminal vesicle in male Atlantic stingrays (Dasyatis sabina) were examined in relation tothe seasonal reproductive cycle. Observations onthe size and structureofthese organs were accompanied by analysisof cell proliferation in genital duct epithelia using proliferating cell nuclear antigen (PCNA) as a marker for mitotic activity. No signsof reproductive tract growth or histological alteration were apparent duringthe initial stagesof spermatogenesis. However, increased PCNA expression inthe seminal vesicle epithelium was observed during this period, suggesting that this organ begins to undergo preparatory changes at an early stage inthe reproductive cycle. During late spermatogenesis, heightened expressionof PCNA in epithelial cellsofthe epididymis and seminal vesicle was observed in conjunction with dramatic increases in size and semen contentofthese organs. Extensive changes inthe histological architectureofthe genital ducts also were evident at this time, including regressionofthe stroma and an increase in size and secretory activityofthe epithelium. Althoughthe epididymis regressed in size and structure shortly after sperm production was completed,the seminal vesicle retained its appearance and activity forthe durationofthe 7-month copulatory period. Afterwards, immune cell content increased considerably in both ducts, likely reflecting clearanceof residual spermatozoa in preparation forthe subsequent reproductive season.the present study provides a basis for future reports onthe physiological regulationof reproductive tract function in elasmobranchs, and establishes PCNA immunocytochemistry as a novel tool for such investigations.

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References

  • Betka, M. and Callard, G.V. 1998. Negative feedback controlofthe spermatogenic progression by testicular oestrogen synthesis: insights fromthe shark testis model. APMIS 106: 252–258.

    PubMed  Google Scholar 

  • Bianco, J.J., Handelsman, D.J, Pedersen, J.S. and Risbridger, G.P. 2002. Direct responseofthe murine prostate gland and seminal vesicles to estradiol. Endocrinol. 143: 4922–4933.

    Article  Google Scholar 

  • Brooks, D.E. 1983. Epididymal functions andtheir hormonal regulation. Aust. J. Biol. Sci. 36: 205–221.

    PubMed  Google Scholar 

  • Callard, I.P., Klosterman, L. and Callard, G.V. 1988. Reproductive physiology. In: Physiologyof Elasmobranch Fishes, pp. 277–317. Edited by T.J. Shuttleworth. Springer-Verlag, Berlin.

    Google Scholar 

  • Chaturapanich, G., Jones, R.C. and Clulow, J. 1992a. Protein synthesis and secretion bythe epididymisofthe tammar wallaby, Macropus eugenii(Macropodidae: Marsupialia). Reprod. Fertil. Dev. 4: 533–545.

    PubMed  Google Scholar 

  • Chaturapanich, G., Jones, R.C. and Clulow, J. 1992b. Roleof androgens in survivalof spermatozoa in epididymisof tammar wallaby (Macropus eugenii). J. Reprod. Fertil. 95: 421–429.

    PubMed  Google Scholar 

  • Chieffi, P., Franco, R., Fulgione, D. and Staibano, S. 2000. PCNA inthe testisofthe frog, Rana esculenta: a molecular markerofthe mitotic testicular epithelium proliferation. Gen. Comp. Endocrinol. 119: 11–16.

    PubMed  Google Scholar 

  • Chieffi, P., Nasti, M., Fulgione, D. and Franco, R. 2001. Expressionof PCNA inthe testisofthe lizard, Podarcis s. sicula: an endogenous molecular markerof mitotic germinal epithelium proliferation. Zygote 9: 317–322.

    PubMed  Google Scholar 

  • Chowdhury, I. and Joy, K.P. 2000. Effectsof administrationof testosterone on some biochemical correlates in seminal vesicleof Heteropneustes fossilis(Bloch) during preparatory phase: a study correlating changes in plasma testosterone level and testis activity. Indian J. Exp. Biol. 38: 713–719.

    PubMed  Google Scholar 

  • Clulow, J., Jones, R.C., Hansen, L.A. and Man, S.Y. 1998. Fluid and electrolyte reabsorption inthe ductuli efferentes testis. J. Reprod. Fertil. Suppl. 53: 1–14.

    Google Scholar 

  • Clulow, J., Jones, R.C. and Murdoch, R.N. 1992. Maturation and regulationofthe motilityof spermatozoa inthe epididymisofthe tammar wallaby (Macropus eugenii). J. Reprod. Fertil. 94: 295–303.

    PubMed  Google Scholar 

  • Cooke, P.S., Young, P., Hess, R.A. and Cunha, G.R. 1991. Estrogen receptor expression in developing epididymis, efferent ductules, and other male reproductive organs. Endocrinol. 128: 2874–2879.

    Google Scholar 

  • Eddy, E.M., Washburn, T.F., Bunch, D.O., Goulding, E.H., Gladen, B.C., Lubahn, D.B. and Korach, K.S. 1996. Targeted disruptionofthe estrogen receptor gene in male mice causes alterationof spermatogenesis and infertility. Endocrinol. 137: 4796–4805.

    Article  Google Scholar 

  • Feuchter, F.A., Tabet, A.J. and Green, M.F. 1988. Maturation antigenofthe mouse sperm flagellum. I. Analysisof its secretion, association with sperm, and function. Am. J. Anat. 181: 67–76.

    PubMed  Google Scholar 

  • Gilbert, P.W. and Wood, F.G. 1957. Methodof anesthetizing large sharks and rays safely and rapidly. Science 126: 212–213.

    PubMed  Google Scholar 

  • Gonzales, G.F. 2001. Functionof seminal vesicles andtheir role on male fertility. Asian J. Androl. 3: 251–258.

    PubMed  Google Scholar 

  • Guillette, L.J., Jr., Gross, T.S., Masson, G.R., Matter, J.M., Percival, H.F. and Woodward, A.R. 1994. Developmental abnormalitiesofthe gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 102: 680–688.

    PubMed  Google Scholar 

  • Hamlett, W.C., Hysell, M.K., Rozycki, T., Brunette, N, Tumilty, K., Henderson, A. and Dunne, J. 1999. Sperm aggregation and spermatozeugmata formation inthe male genital ducts inthe clearnose skate, Raja eglanteria.In: Proceedingsofthe 5thIndo-Pacific Fish Conference Noumea, pp. 281–291. Edited by B. Séret and J.-Y. Sire. Soc. Fr. Ichtyol., Paris.

    Google Scholar 

  • Hamlett, W.C., Reardon, M., Clark, J. and Walker, T.I. 2002. Ultrastructureof sperm storage and male genital ducts in a male holocephalan,the elephant fish, Callorhynchus milii.J. Exp. Zool. 292: 111–128.

    Article  PubMed  Google Scholar 

  • Hess, R.A., Bunick, D., Lee, K.H., Bahr, J., Taylor, J.A., Korach, K.S. and Lubahn, D.B. 1997a. A role for oestrogens inthe male reproductive system. Nature 390: 509–512.

    Article  PubMed  Google Scholar 

  • Hess, R.A., Gist, D.H., Bunick, D., Lubahn, D.B., Farrell, A., Bahr, J., Cooke, P.S. and Greene, G.L. 1997b. Estrogen receptor (alpha and beta) expression inthe excurrent ductsofthe adult male rat reproductive tract. J. Androl. 18: 602–611.

    PubMed  Google Scholar 

  • Hinton, B.T., Palladino, M.A., Rudolph, D., Lan, Z.J. and Labus, J.C. 1996.the roleofthe epididymis inthe protectionof spermatozoa. Curr. Top. Dev. Biol. 33: 61–102.

    PubMed  Google Scholar 

  • Johnson, M.R. and Snelson, F.F., Jr. 1996. Reproductive life historyofthe Atlantic stingray, Dasyatis sabina(Pisces: Dasyatidae), inthe freshwater St. Johns River, Florida. Bull. Mar. Sci. 59: 74–88.

    Google Scholar 

  • Jones, R.C. and Clulow, J. 1994. Interactionsof sperm andthe reproductive ductsofthe male tammar wallaby, Macropus eugenii(Macropodidae: Marsupialia). Reprod. Fertil. Dev. 6: 437–444.

    PubMed  Google Scholar 

  • Jones, N. and Jones, R.C. 1982.the structureofthe male genital systemofthe Port Jackson shark, Heterodontus portjacksoni, with particular reference tothe genital ducts. Aust. J. Zool. 30: 523–541.

    Google Scholar 

  • Jones, R.C., Jones, N. and Djakiew, D. 1984. Luminal composition and maturationof spermatozoa inthe male genital ductsofthe Port Jackson shark, Heterodontus portjacksoni.J. Exp. Zool. 230: 417–426.

    Google Scholar 

  • Jones, R.C. and Lin, M. 1992. Ultrastructureofthe genital duct epitheliumofthe male Port Jackson shark, Heterodontus portjacksoni.Aust. J. Zool. 40: 257–266.

    Google Scholar 

  • Jones, R.C. and Lin, M. 1993. Structure and functionofthe genital ductsofthe male Port Jackson shark, Heterodontus portjacksoni.Environ. Biol. Fish. 38: 127–138.

    Google Scholar 

  • Jones, R.C. and Murdoch, R.N. 1996. Regulationofthe motility and metabolismof spermatozoa for storage inthe epididymisof eutherian and marsupial mammals. Reprod. Fertil. Dev. 8: 553–568.

    PubMed  Google Scholar 

  • Kajiura, S.M., Sebastian, A.P. and Tricas, T.C. 2000. Dermal bite wounds as indicatorsof reproductive seasonality and behaviour inthe Atlantic stingray, Dasyatis sabina.Environ. Biol. Fish. 58: 23–31.

    Article  Google Scholar 

  • Kajiura, S. and Tricas, T. 1996. Seasonal dynamicsof dental sexual dimorphism inthe Atlantic stingray, Dasyatis sabina.J. Exp. Biol. 199: 2297–2306.

    PubMed  Google Scholar 

  • Kaunisto, K.M. and Rajaniemi, H.J. 2002. Expression and localizationofthe Na+/H+ exchanger isoform NHE3 inthe rat efferent ducts. J. Androl. 23: 237–241.

    PubMed  Google Scholar 

  • Krutzsch, P.H. and Crichton, E.G. 1990. Reproductive biologyofthe male bent-winged bat, Miniopterus schreibersii(Vespertilionidae) in southeast South Australia. Acta. Anat. (Basel) 139: 109–125.

    Google Scholar 

  • Kwon, S., Hess, R.A., Bunick, D., Kirby, J.D. and Bahr, J.M. 1997. Estrogen receptors are present inthe epididymisofthe rooster. J. Androl. 18: 378–384.

    PubMed  Google Scholar 

  • Lee, P.C. 1998. Disruptionof male reproductive tract development by administrationofthe xenoestrogen, nonylphenol, to male newborn rats. Endocrine 9: 105–111.

    Article  PubMed  Google Scholar 

  • Madsen, P. and Celis, J.E. 1995. S-Phase patternsof cyclin (PCNA) antigen staining resemble topographical patternsof DNA synthesis. FEBS Lett. 193: 5–11.

    Article  Google Scholar 

  • Maruska, K.P., Cowie, E.G. and Tricas, T.C. 1996. Periodic gonadal activity and protracted mating in elasmobranch fishes. J. Exp. Zool. 276: 219–232.

    Article  Google Scholar 

  • McIntyre, B.S., Barlow, N.J., Sar, M., Wallace, D.G. and Foster, P.M. 2002. Effectsof in utero linuron exposure on rat Wolffian duct development. Reprod. Toxicol. 16: 131–139.

    Article  PubMed  Google Scholar 

  • McLachlan, J.A., Newbold, R.R., Burow. M.E. and Li, S.F. 2001. From malformations to molecular mechanisms inthe male: three decadesof research on endocrine disrupters. APMIS 109: 263–272.

    Article  PubMed  Google Scholar 

  • Misao, R., Fujimoto, J., Niwa, K., Morishita, S., Nakanishi, Y. and Tamaya, T. 1997. Immunohistochemical expressionsof estrogen and progesterone receptors in human epididymis at different ages-a preliminary study.Int. J. Fertil. Womens Med. 42: 39–42.

    PubMed  Google Scholar 

  • Piermarini, P.M. and Evans, D.H. 1998. Osmoregulationofthe Atlantic stingray (Dasyatis sabina) fromthe freshwater Lake Jesupofthe St. Johns River, Florida. Physiol. Zool. 71: 553–560.

    PubMed  Google Scholar 

  • Piermarini, P.M. and Evans, D.H. 2000. Effectsof environmental salinity on Na(+)/K(+)-ATPase inthe gills and rectal glandof a euryhaline elasmobranch (Dasyatis sabina). J. Exp. Biol. 203: 2957–2966.

    PubMed  Google Scholar 

  • Piermarini, P.M. and Evans, D.H. 2001. Immunochemical analysisofthe vacuolar proton-ATPase B-subunit inthe gillsof a euryhaline stingray (Dasyatis sabina): effectsof salinity and relation to Na(+)/K(+)-ATPase. J. Exp. Biol. 204: 3251–3259.

    PubMed  Google Scholar 

  • Piermarini, P.M., Verlander, J.W., Royaux, I.E. and Evans, D.H. 2002. Pendrin immunoreactivity inthe gill epitheliumof a euryhaline elasmobranch. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283: R983–R992.

    PubMed  Google Scholar 

  • Reardon, M.B., Walker, T.I. and Hamlett, W.C. 2002. Microanatomyof spermatophore formation and male genital ducts inthe holocephalan, Callorhynchus milii.Mar. Freshwater Res. 53: 591–600.

    Article  Google Scholar 

  • Reyes-Moreno, C., Boilard, M., Sullivan, R. and Sirard, M.A. 2002. Characterizationof secretory proteins from cultured cauda epididymal cells that significantly sustain bovine sperm motility in vitro. Mol. Reprod. Dev. 63: 500–509.

    Article  PubMed  Google Scholar 

  • Robaire, B. and Viger, R.S. 1995. Regulationof epididymal epithelial cell functions. Biol. Reprod. 52: 226–236.

    PubMed  Google Scholar 

  • Rooney, A.A., Bermudez, D.S. and Guillette, L.J., Jr. 2003. Altered histologyofthe thymus and spleen in contaminant-exposed juvenile American alligators. J. Morphol. 256: 349–359.

    Article  PubMed  Google Scholar 

  • Singh, M.S. and Joy, K.P. 1997. Effectsof administrationof testosterone on seminal vesicle activity inthe catfish Clarias batrachusduring preparatory phase: a study correlating changes in testis and serum sex steroid levels. Acta Biol. Hung. 48: 421–430.

    PubMed  Google Scholar 

  • Sisneros, J.A. and Tricas, T.C. 2000. Androgen-induced changes inthe response dynamicsof ampullary electrosensory primary afferent neurons. J. Neurosci. 20: 8586–8595.

    PubMed  Google Scholar 

  • Snelson, F.F., Jr., Williams-Hooper, S.E. and Schmid, T.H. 1988. Reproduction and ecologyofthe Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 1988: 729–739.

  • Snelson, F.F., Jr., Rasmussen, L.E. L., Johnson, M.R. and Hess, D.L. 1997. Serum concentrationsof steroid hormones during reproduction inthe Atlantic stingray, Dasyatis sabina.Gen. Comp. Endocrinol. 108: 67–79.

    Article  PubMed  Google Scholar 

  • Stanley, H.P. 1963.the fine structureof spermatozoaof Hydrolagus collei(Chondrichthyes, Holocephali).J. Ultrastruct. Res. 83: 184–194.

    Google Scholar 

  • Stefanini, M.A., Orsi, A.M., Gregorio, E.A., Viotto, M.J. and Baraldi-Artoni, S.M. 1999. Morphologic studyofthe efferent ductulesofthe pigeon (Columba livia). J. Morphol. 242: 247–255.

    Article  PubMed  Google Scholar 

  • Sulik, M. and Guzinska-Ustymowicz, K. 2002. Expressionof Ki-67 and PCNA as proliferating markers in prostate cancer. Rocz. Akad. Med. Bialymst 47: 262–269.

    PubMed  Google Scholar 

  • Todhunter, R. and Gemmell, R.T. 1987. Seasonal changes inthe reproductive tractofthe male marsupial bandicoot, Isoodon macrourus.J. Anat. 154: 173–186.

    PubMed  Google Scholar 

  • Toft, G., Edwards, T.M., Baatrup, E. and Guillette, L.J., Jr. 2003. Disturbed Sexual Characteristics in Male Mosquitofish (Gambusia holbrooki) from a Lake Contaminated with Endocrine Disruptors. Environ. Health Perspect. 111: 695–701.

    PubMed  Google Scholar 

  • Tricas, T.C., Maruska, K.P. and Rasmussen, L.E.L. 2000. Annual cyclesof steroid hormone production, gonad development, and reproductive behavior inthe Atlantic stingray. Gen. Comp. Endocrinol. 118: 209–225.

    Article  PubMed  Google Scholar 

  • Wang, Z.P., Gu, Z.P., Cao, L., Xu, Y., You, G.D., Mao, B.Y. and Qian, S.Z. 1999. Effectsof tripchlorolide onthe epididymides and testesof rats. Asian J. Androl. 1: 121–125.

    PubMed  Google Scholar 

  • Yuasa, H., Fukabori, Y., Ono, Y., Tomita, N., Suzuki, K. and Yamanaka, H. 1999. Immunohistochemical characteristicsof estrogen receptor alpha positive cells in glandular epitheliumofthe rat seminal vesicle. Tohoku J. Exp. Med. 187: 25–35.

    PubMed  Google Scholar 

  • Zhou, Q., Clarke, L., Nie, R., Carnes, K., Lai, L.W., Lien, Y.H., Verkman, A., Lubahn, D., Fisher, J.S., Katzenellenbogen, B.S. and Hess, R.A. 2001. Estrogen action and male fertility: rolesofthe sodium/hydrogen exchanger-3 and fluid reabsorption in reproductive tract function. Proc. Natl. Acad. Sci. USA 98: 14132–14137.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Departmentof Biology, Universityof Central Florida, Orlando, FL, 32816, USA

    A. Piercy & F.F. Snelson Jr.

  2. Florida Program for Shark Research, Florida Museumof NaturalHistory, Universityof Florida, Gainesville, FL, 32611, USA

    A. Piercy & F.F. Snelson Jr.

  3. Elasmobranch Physiology and Environmental Biology Program, Center for Shark Research, Mote Marine Laboratory, Sarasota, FL, 34236, USA

    J. Gelsleichter

  4. Center for Shark Research, Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL, 34236, USA

    J. Gelsleichter

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Piercy, A., Gelsleichter, J. & Snelson, F. Morphological and histological changes inthe genital ducts ofthe male Atlantic stingray, Dasyatis sabina, during the seasonal reproductive cycle. Fish Physiology and Biochemistry 29, 23–35 (2003). https://doi.org/10.1023/B:FISH.0000035894.45256.59

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