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This study was carried out to describe the morphophysiology of the epididymis of the adult African sideneck turtle using histological, microstereological and ultrastructural methods. The epididymal duct lies within a relatively thin sheath of connective tissue, and is lined by pseudostratified columnar epithelium. Unlike luminal diameter and stereocilial height, epithelial height, as well as the population of principal cells, decreased from the proximal to posterior segment. The clear cells of the turtle epididymis are limited to the posterior segment of the duct. Basal and apical cells as well as intra-epithelial lymphocytes are all distributed across the three segments of the epididymis while macrophage-like cells are absent throughout the length of the duct epithelium. The structure of the African sideneck turtle epididymis demonstrates, as in most mammals and few reptiles studied to date, obvious regional differentiation of the duct epithelium with evidences of secretory and endocytotic abilities as demonstrated by the contents of highly developed endoplasmic reticulum and secretory blebs in the principal and basal cells as well as clear cells, believed to be concerned with endocytosis. The outcome of the study is expected to be useful in the comparative structural and functional anatomy of turtle epididymis.
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References
- Adamali, H.I. and Hermo, L. (1996). Apical and narrow cells are distinct cell types differing in their structure, distribution, and functions in the adult rat epididymis. J.Androl., 17(3):208-222
- Aire, T.A. (2007). Anatomy of the testis and male reproductive tract. In: Jamieson BGM, Ed. Reproductive biology and phylogeny of birds. NH: Science Publishers, Enfield, pp 37-113
- Akbarsha, M.A., Tamilarasan, V. andKadalmani, B. (2007). Light and electron microscopic observations of fabrication, release, and fate of biphasic secretion granules produced by epididymal epithelial principal cells of the fan-throated lizard Sitanaponticerianacuvier. J.Morphol. 267:713–729
- Arrighi, S., Romanello, M.G. andDomeneghini, C. (1993). Ultrastructure of epidi¬dymal epithelium in Equuscaballus. Ann. Anat., 175:1-9
- Broadley, D.G. and Boycott, R.C. (2009). Pelusiossinuatus(Smith 1838) –Serrated Hinged Terrapin. Conservation Biology of Freshwater Turtles and Tortoises. Chel. Res.Monogr., 5: 036.1-036.5
- Cabral, S.R.P., Zieri, R., Franco-Belussi, L., Santos, L.R.S., Zago, C.E.S. and Taboga, S.R. (2011).Morphological changes of the epididymis and description of the excurrent ducts of Phrynopsgeoffroanus (Testudines: Chelidae) during the reproductive cycle. Anat. Rec., 294:145–155
- Cornwall, G.A. (2009). New insights into epididymal biology and function. 400, New York, EUA. Hum.Reprod. Update., 15(2):213-227
- Dacheux, J.L., Castella, S., Gatti, L.J. andDacheux, F. (2005).Epididymal cell secretory activities and the role of the proteins in boar sperm epididymis. Theriogenol., 63(2):319-341
- Djakiew, D. and Jones, R.C. (1982). Ultrastructure of the ductus epididymidis of the echidna, Tachyglossusaculeatus. J. Anat., 135:625–634
- Flesch, F.M. andGadella, B.M. (2000). Dynamics of the mammalian sperm plasm membrane in the process of fertilization. Biochimica et BiophysicaActa 1469(3):197-235
- Flickinger, C.J. (1983). Synthesis and secretion of glycoprotein by the epidi¬dymal epithelium. J.Androl., 4:157-161
- Gatti, J.L., Castella, S., Dacheux, F., Ecroyd, H., Metayer, S., Thimon, V. andDacheux, J.L. (2004). Post-testicular sperm environment and fertility. AnimReprod Sci., 82-83:321-339
- Gist, D.H., Dawes, S.M., Terry, W., Turner, T.W., Sheldon, S. and Congdon, J.D. (2001). Sperm Storage in Turtles: A Male Perspective. Expt. Zool., 292:180–186
- Goyal, H.O. and Williams, C.S. (1991). Regional differences in the morphology of the goat epididymis: a light microscopic and ultrastructural study. Am. J. Anat., 190:349-369
- Hermo, L, Chong, D.L, Moffatt, P., W.S., Waheed, A. and Smith, C.E. (2005). Region and cell – specific differences in the distribution of carbonic anhydrases II, III, XII, and XIV in the adult rat epididymis. J.Histochem.Cytochem. 53(6):699-713
- Hermo, L., Dworkin, J. and Oko, R. (1988). Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat., 183:107–124
- Hermo, L., Papp, S. andRobaire, B. (1994). Developmental expression of the Yf subunit of glutathione S-transferase P in epithelial cells of the testis, efferent ducts, and epididymis of the rat. Anat. Rec., 239:421–440
- Hermo, L. andRobaire, B. (2002). Epididymis cell types and their function. In The Epididymis: From Molecules to Clinical Practice (B. Robaire and B. T. Hinton, Eds.), Kluwer Academic/Plenum, New York, pp 81–102
- Holmes, H.J. and Gist, D.H. (2004).Excurrent duct system of the male turtle Crysemyspicta. J.Morphol., 261(3):312-322
- Kellner, A. andSchwanke, C. (2001). Repteis fosseis do Brasil: breve introducao a herpetologia. In: Brito IM. (Ed.). Geologia historica, Uberlandia: Edufu, pp 303-363
- Kirkpatrick, D.T. (1995). An Essay on Taxonomy and the Genus Pelusios. http://www.unc.edu/~dtkirkpa/stuff/pel.html. Accessed 22 February 2013.
- Massanyi, P., Jancova, A. andUhrin, V. (2003). Morphometric study of male reproductive organs in the rodent species ApodemusSylvaticus and Apodemusflavicollis. Bull. Vet. Inst.Pulway.,47:133-138
- Meeran, M.M., Daisy, P. andAkbarsha, M.A. (2001). Histological differentiation along the ductus epididymides of the lizard Calotes versicolorDaudin. J Anim.Morphol. Physiol., 48:85–96
- Oke, B.O., Aire, T.A., Adeyemo, O. and Heath, E. (1987). The structure of the epididymis of the African the giant rat (Cricetomysgambianus, Waterhouse). Histochemical and microstereological studies. J. Anat., 160:9-19
- Oke. B.O., Aire, T.A., Adeyemo, O., Heath, E. (1989). The ultrastructure of the epididymis of the African giant rat (Cricetomysgambianus, Waterhouse). J Anat., 165:75-89
- Oke, B.O. andAire, T.A. (1990). Ultrastructural evidence for secretion in different zones of the caput epididymis of the African giant rat (Cricetomysgambianus,Waterhouse). Arch. Vet. Med., 60 (4):207-212
- Olukole, S.G., Oyeyemi, M.O. andOke, B.O. (2009). Biometrical observations on the testes and epididymis of the domesticated adult African great cane rat (Thryonomysswinderianus). Eur. J. Anat., 13(2):71-75
- Olukole, S.G. andObayemi, T.E. (2010).Histomorphometry of the Testis and Epididymis in the domesticated adult African great cane rat (Thryonomysswinderianus). Int. J.Morphol.,28(4):1251-1254
- Olukole, S.G. andOke, B.O. (2014). Morphological analysis of the plastron of the African sidenck turtle (Pelusioscastaneus) Trop. Vet., 32(1&2):26-35
- Olukole,S.G.,Oyeyemi,M.O. andOke,B.O. (2014a).Biometricalandhistometrical observationsonthe testisandepididymisof the Africansideneckturtle (Pelusioscastaneus). Eur. J. Anat.,18 (2):102-108
- Olukole,S.G.,Oyeyemi,M.O. andOke,B.O. (2014b).Spermatogeniccycleofthe Africansideneckturtle,Pelusioscastaneus(Schweigger,1812)(Reptilia:Testudines), Ital.J.Zool.,81(1):25-31.
- Olukole, S.G., Madekurozwa, M-C. and Oke, B.O. (2018). Spermiogenesis in the African sideneck turtle (Pelusioscastaneus): Acrosomal vesicle formation and nuclear morphogenesis. J. King Saud Univ. - Science 30: 359-366
- Rao,R.J.andShaad, F.U. (1985). Sexual cycle of the male freshwater turtle,Trionyxgangeticus (Cuvier)Herpetologica 41(4):433-437
- Rheubert, J.L., Wilson, B.S., Wolf, K.W. andGribbins, K.M. (2010a). Ultrastructural study of spermiogenesis in the Jamaican Gray Anole, Anolislineatopus (Reptilia: Polychrotidae). Acta.Zool (Stockholm)., 91:484–494
- Rheubert, J.L., McMahan, C.D., Sever. D.M., Bundy. M.R., Siegel, D.S. andGribbins, K.M. (2010b). Ultrastructure of the reproductive system of the Black Swamp Snake (Seminatrixpygaea). VII. Spermatozoon morphology and evolutionary trends of sperm characters in snakes. J. Syst. Zool.Evol.. Res., 48:366–375
- Robaire, B. andHermo, L.(1988). Efferent ducts, epididymis and vas deferens: structure, functions and their regulation. In: The physiology of reproduction, Knobil and J. Neil, (Ed.), Raven Press, New York, pp 999-1080
- Robaire,B., Hinton, B.T. andOrgebin-Crist, M.C. (2006). The Epididymis. In: The physiology of reproduction, Knobil and J. Neil, (Ed.), Elsevier, pp 1071-1148
- Schimmimg, B.C., Pinheiro, P.F.F., Vicentini, C.A. andDomeniconi, R.F. (2012). Ultrastructure of the epithelium lining of cauda epididymidis in mongrel dogs. Pesq. Vet. Bras., 32(1):32-36
- Schimming, B.C. andVicentini, C.A. (2008). Morphological features of the apical region in the principal cells of mongrel dog epididymis. Int. J.Morphol., 26:149-153
- Setchell, B.P., Sanchez-Partida, L.G. andChairussyuhur, A. (1993).Epididymal constituents and related substances in the storage of spermatozoa: A review. Reprod.Fert.Devt. 5:601-612
- Sever, D.M. (2009). Ultrastructure of the reproductive system of the black swamp snake (Seminatrixpygaea). Vi Anterior testicular ducts and their nomenclature. J.Morphol., 241:1–12
- Sever, D.M., Rheubert, J.L., Hill, T.A. andSiegal, D.S. (2013). Observations on Variation in the Ultrastructure of the Proximal Testicular Ducts of the Ground Skink, Scincellalateralis (Reptilia: Squamata). J Morphol 274:429–446
- Sullivan, R. (2004). Male fertility markers, myth or reality. Anim.Reprod. Sci., 82-83 341- 347
- Wyneken, J. (2001). The Anatomy of Sea Turtles. U.S. Department of Commerce NOAA Technical Memorandum NMFS-SEFSC. 470, pp 1-172
- Yanagimachi, R., Kamiguchi, Y., Mikamo, K., Suzuki, F. andYanagimachi, H. (1985). Maturation of spermatozoa in the epididymis of the Chinese hamster. Amer. J. Anat., 172(4)317-330
References
Adamali, H.I. and Hermo, L. (1996). Apical and narrow cells are distinct cell types differing in their structure, distribution, and functions in the adult rat epididymis. J.Androl., 17(3):208-222
Aire, T.A. (2007). Anatomy of the testis and male reproductive tract. In: Jamieson BGM, Ed. Reproductive biology and phylogeny of birds. NH: Science Publishers, Enfield, pp 37-113
Akbarsha, M.A., Tamilarasan, V. andKadalmani, B. (2007). Light and electron microscopic observations of fabrication, release, and fate of biphasic secretion granules produced by epididymal epithelial principal cells of the fan-throated lizard Sitanaponticerianacuvier. J.Morphol. 267:713–729
Arrighi, S., Romanello, M.G. andDomeneghini, C. (1993). Ultrastructure of epidi¬dymal epithelium in Equuscaballus. Ann. Anat., 175:1-9
Broadley, D.G. and Boycott, R.C. (2009). Pelusiossinuatus(Smith 1838) –Serrated Hinged Terrapin. Conservation Biology of Freshwater Turtles and Tortoises. Chel. Res.Monogr., 5: 036.1-036.5
Cabral, S.R.P., Zieri, R., Franco-Belussi, L., Santos, L.R.S., Zago, C.E.S. and Taboga, S.R. (2011).Morphological changes of the epididymis and description of the excurrent ducts of Phrynopsgeoffroanus (Testudines: Chelidae) during the reproductive cycle. Anat. Rec., 294:145–155
Cornwall, G.A. (2009). New insights into epididymal biology and function. 400, New York, EUA. Hum.Reprod. Update., 15(2):213-227
Dacheux, J.L., Castella, S., Gatti, L.J. andDacheux, F. (2005).Epididymal cell secretory activities and the role of the proteins in boar sperm epididymis. Theriogenol., 63(2):319-341
Djakiew, D. and Jones, R.C. (1982). Ultrastructure of the ductus epididymidis of the echidna, Tachyglossusaculeatus. J. Anat., 135:625–634
Flesch, F.M. andGadella, B.M. (2000). Dynamics of the mammalian sperm plasm membrane in the process of fertilization. Biochimica et BiophysicaActa 1469(3):197-235
Flickinger, C.J. (1983). Synthesis and secretion of glycoprotein by the epidi¬dymal epithelium. J.Androl., 4:157-161
Gatti, J.L., Castella, S., Dacheux, F., Ecroyd, H., Metayer, S., Thimon, V. andDacheux, J.L. (2004). Post-testicular sperm environment and fertility. AnimReprod Sci., 82-83:321-339
Gist, D.H., Dawes, S.M., Terry, W., Turner, T.W., Sheldon, S. and Congdon, J.D. (2001). Sperm Storage in Turtles: A Male Perspective. Expt. Zool., 292:180–186
Goyal, H.O. and Williams, C.S. (1991). Regional differences in the morphology of the goat epididymis: a light microscopic and ultrastructural study. Am. J. Anat., 190:349-369
Hermo, L, Chong, D.L, Moffatt, P., W.S., Waheed, A. and Smith, C.E. (2005). Region and cell – specific differences in the distribution of carbonic anhydrases II, III, XII, and XIV in the adult rat epididymis. J.Histochem.Cytochem. 53(6):699-713
Hermo, L., Dworkin, J. and Oko, R. (1988). Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat., 183:107–124
Hermo, L., Papp, S. andRobaire, B. (1994). Developmental expression of the Yf subunit of glutathione S-transferase P in epithelial cells of the testis, efferent ducts, and epididymis of the rat. Anat. Rec., 239:421–440
Hermo, L. andRobaire, B. (2002). Epididymis cell types and their function. In The Epididymis: From Molecules to Clinical Practice (B. Robaire and B. T. Hinton, Eds.), Kluwer Academic/Plenum, New York, pp 81–102
Holmes, H.J. and Gist, D.H. (2004).Excurrent duct system of the male turtle Crysemyspicta. J.Morphol., 261(3):312-322
Kellner, A. andSchwanke, C. (2001). Repteis fosseis do Brasil: breve introducao a herpetologia. In: Brito IM. (Ed.). Geologia historica, Uberlandia: Edufu, pp 303-363
Kirkpatrick, D.T. (1995). An Essay on Taxonomy and the Genus Pelusios. http://www.unc.edu/~dtkirkpa/stuff/pel.html. Accessed 22 February 2013.
Massanyi, P., Jancova, A. andUhrin, V. (2003). Morphometric study of male reproductive organs in the rodent species ApodemusSylvaticus and Apodemusflavicollis. Bull. Vet. Inst.Pulway.,47:133-138
Meeran, M.M., Daisy, P. andAkbarsha, M.A. (2001). Histological differentiation along the ductus epididymides of the lizard Calotes versicolorDaudin. J Anim.Morphol. Physiol., 48:85–96
Oke, B.O., Aire, T.A., Adeyemo, O. and Heath, E. (1987). The structure of the epididymis of the African the giant rat (Cricetomysgambianus, Waterhouse). Histochemical and microstereological studies. J. Anat., 160:9-19
Oke. B.O., Aire, T.A., Adeyemo, O., Heath, E. (1989). The ultrastructure of the epididymis of the African giant rat (Cricetomysgambianus, Waterhouse). J Anat., 165:75-89
Oke, B.O. andAire, T.A. (1990). Ultrastructural evidence for secretion in different zones of the caput epididymis of the African giant rat (Cricetomysgambianus,Waterhouse). Arch. Vet. Med., 60 (4):207-212
Olukole, S.G., Oyeyemi, M.O. andOke, B.O. (2009). Biometrical observations on the testes and epididymis of the domesticated adult African great cane rat (Thryonomysswinderianus). Eur. J. Anat., 13(2):71-75
Olukole, S.G. andObayemi, T.E. (2010).Histomorphometry of the Testis and Epididymis in the domesticated adult African great cane rat (Thryonomysswinderianus). Int. J.Morphol.,28(4):1251-1254
Olukole, S.G. andOke, B.O. (2014). Morphological analysis of the plastron of the African sidenck turtle (Pelusioscastaneus) Trop. Vet., 32(1&2):26-35
Olukole,S.G.,Oyeyemi,M.O. andOke,B.O. (2014a).Biometricalandhistometrical observationsonthe testisandepididymisof the Africansideneckturtle (Pelusioscastaneus). Eur. J. Anat.,18 (2):102-108
Olukole,S.G.,Oyeyemi,M.O. andOke,B.O. (2014b).Spermatogeniccycleofthe Africansideneckturtle,Pelusioscastaneus(Schweigger,1812)(Reptilia:Testudines), Ital.J.Zool.,81(1):25-31.
Olukole, S.G., Madekurozwa, M-C. and Oke, B.O. (2018). Spermiogenesis in the African sideneck turtle (Pelusioscastaneus): Acrosomal vesicle formation and nuclear morphogenesis. J. King Saud Univ. - Science 30: 359-366
Rao,R.J.andShaad, F.U. (1985). Sexual cycle of the male freshwater turtle,Trionyxgangeticus (Cuvier)Herpetologica 41(4):433-437
Rheubert, J.L., Wilson, B.S., Wolf, K.W. andGribbins, K.M. (2010a). Ultrastructural study of spermiogenesis in the Jamaican Gray Anole, Anolislineatopus (Reptilia: Polychrotidae). Acta.Zool (Stockholm)., 91:484–494
Rheubert, J.L., McMahan, C.D., Sever. D.M., Bundy. M.R., Siegel, D.S. andGribbins, K.M. (2010b). Ultrastructure of the reproductive system of the Black Swamp Snake (Seminatrixpygaea). VII. Spermatozoon morphology and evolutionary trends of sperm characters in snakes. J. Syst. Zool.Evol.. Res., 48:366–375
Robaire, B. andHermo, L.(1988). Efferent ducts, epididymis and vas deferens: structure, functions and their regulation. In: The physiology of reproduction, Knobil and J. Neil, (Ed.), Raven Press, New York, pp 999-1080
Robaire,B., Hinton, B.T. andOrgebin-Crist, M.C. (2006). The Epididymis. In: The physiology of reproduction, Knobil and J. Neil, (Ed.), Elsevier, pp 1071-1148
Schimmimg, B.C., Pinheiro, P.F.F., Vicentini, C.A. andDomeniconi, R.F. (2012). Ultrastructure of the epithelium lining of cauda epididymidis in mongrel dogs. Pesq. Vet. Bras., 32(1):32-36
Schimming, B.C. andVicentini, C.A. (2008). Morphological features of the apical region in the principal cells of mongrel dog epididymis. Int. J.Morphol., 26:149-153
Setchell, B.P., Sanchez-Partida, L.G. andChairussyuhur, A. (1993).Epididymal constituents and related substances in the storage of spermatozoa: A review. Reprod.Fert.Devt. 5:601-612
Sever, D.M. (2009). Ultrastructure of the reproductive system of the black swamp snake (Seminatrixpygaea). Vi Anterior testicular ducts and their nomenclature. J.Morphol., 241:1–12
Sever, D.M., Rheubert, J.L., Hill, T.A. andSiegal, D.S. (2013). Observations on Variation in the Ultrastructure of the Proximal Testicular Ducts of the Ground Skink, Scincellalateralis (Reptilia: Squamata). J Morphol 274:429–446
Sullivan, R. (2004). Male fertility markers, myth or reality. Anim.Reprod. Sci., 82-83 341- 347
Wyneken, J. (2001). The Anatomy of Sea Turtles. U.S. Department of Commerce NOAA Technical Memorandum NMFS-SEFSC. 470, pp 1-172
Yanagimachi, R., Kamiguchi, Y., Mikamo, K., Suzuki, F. andYanagimachi, H. (1985). Maturation of spermatozoa in the epididymis of the Chinese hamster. Amer. J. Anat., 172(4)317-330