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Abstract
The African sideneck turtle (Pelusios castaneus) is a freshwater turtle of West African origin used in traditional medicine with little consumption as meat. There have been documentations on the reproductive biology of the turtle with no report on the structure of the Leydig cell of the animal. We described the structure of the Leydig cell of the adult African sideneck turtle using histology, microstereology and transmission electron microscopy. The Leydig cell of the African sideneck turtle were elliptical in shape when found proximal to blood vessels and elongated at other points within the testicular interstitium. Leydig cells occurred in cords or clusters of varying sizes and numbers (3-5 cells) that appear to be random in distribution possessing round to ovoid nuclei containing small amount of peripherally disposed heterochromatin with prominent nucleoli. The seminiferous tubules of the turtle occupied about 85% of the total testicular parenchyma while the interstitium occupied 15% of it. Of this 15%, the Leydig cell occupied about 10% while the stromal elements, inclusive of blood vessels occupied the remaining 5%. The cytoplasm of the Leydig cell was about 85% of the entire cell and comprised microfilaments, lipid droplets, smooth and rough endoplasmic reticula as well as numerous mitochondria. In conclusion, the histological and ultrastructural features of the Leydig cell of the African sideneck turtle bear close similarities with those of other reptiles with little variations. These variations include interstitial location as well as in relation to blood vessels within the testicular interstitium. Information made available by this study is expected to be useful in the comparative anatomy of the Leydig cell of turtles and reptiles.
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References
- Aire, T.A. (1997). The structure of the interstitial tissue of the active and resting avian testis. Onderstepoort J. Vet. Res., 64(4):291-9.
- Ali, M.Z., Qureshi, A.S., Rehan, S., Akbar, S.Z. and Manzoor, A. (2015). Seasonal variations in histomorphology of testes and bursa, immune parameters and serum testosterone concentration in male guinea fowl (Numida meleagris). Pak. Vet. J., 35(1):88-92.
- Al-Dokhi, O.A., Al-Onazee, Y.Z. and Mubarak, M. (2004). Light and electron microscopy of the testicular tissue of the Snake Eryxjayakari (Squamata, Reptilia) with a reference to the dividing germ cells. J. Biol. Sci. 4(3): 345- 351.
- Almeida, F.F.L. (2002). Estrutura e funçãotesticularesemjavalis (Sus scrofa scrofa) sexualmentemaduros. 2002. 65 f. Dissertação (Mestrado) - Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, 2002.
- Ashanbhag, B. (2002). Reproductive Biology of Indian Reptiles. Proc. Indian Natn. Sci Acad. (PINSA) B68, 6: 497-528.
- Bacha, W.J. and Bacha, L.M. (2000). Color Atlas of Veterinary Histology. Lippincott William and Wilikins, USA, 219 pp.
- Costa, D. S., Silva J.F.S. and Silveira, L. S. (2007). Morphometry of Leydig cells in the collared peccary (Tayassu tajacu). Braz. J. Vet. Res. Anim. Sci., Sao Paulo, 44(5):384-389.
- De Kretser, D.M. and Kerr, J.B. (1994). The cytology of the testis In: Knobil, E., Neill, J.D. The physiology of reproduction. 2ed. New York: Raven Press, p.1177-1290.
- Domke, L.M. (2018). Molecular and ultrastructural characteristics of adhering junctions and cytoskeletons in cells of the seminiferous tubules and the peritubular walls of mammalian testes. PhD Thesis. Combined Faculties for the Natural Sciences and for Mathematics, University of Heidelberg, Germany
- Dubois, W., Pudney, J. and Callard, I.P. (1988). The annual testicular cycle in the turtle Chrysemys picta A histochemical and electron microscopic study. Gen. Comp. Endocrinol., 71:191-204.
- Dufaure, J.P. (1968) L’ultrastructure des cellules interstitielles du testiculeadulte chez deux Reptiles Lacertilies: le lézardvivipare (Lacerta vivipara Jacquin) et l’orvet (Anguisfragilis L.). C R Acad. Sci. Paris 267: 883–885.
- Ferreira, A. and Dolder, H. (2003). Cytochemical study of spermiogenesis and mature spermatozoa in the lizard Tropidurusitambere (Reptilia, Squamata). ActaHistochem. 105(4) 339–352.
- Franca, L.R. and Godinho, C.L. (2002). Testis morphology, seminiferous epithelium cycle length and daily sperm production in domestic cat (Feliscatus). Biol. Reprod. 68:1554–1561.
- Gribbins, K.M., Rheubert, J.L., Collier, M.H., Siegel, D.S. and Sever, D.M. (2008). Histological analysis of spermatogenesis and the germ cell development strategy within the testis of the male Western Cottonmouth Snake, Agkistrodonpiscivorusleucostoma. Ann. Anat. 190: 461—476.
- Kirkpatrick, D.T. (1995). An Essay on Taxonomy and the Genus Pelusios. Available at: http://www.unc.edu/~dtkirkpa/stuff/pel.html. Accessed 22 February 2013.
- Losinno, A.D., Morales, A., Fernandez, D., Lopez, L.A. (2012). Peritubular myoid cells from rat seminiferous tubules contain actin and myosin filaments distributed in two independent layers. Biol. Reprod. 86:150 151-158.
- Mahmoud, I.Y., Cyrus, R.V., Bennett, T.M, Woller, M.J. and Montag, D.M. (1985). Ultrastructural changes in testes of the snapping turtle Chelydru serpentina in relation to plasma testosterone, 5-3B-hydroxysteroid dehydrogenase, and cholesterol. Gen. Comp. Endocrinol., 57:454-464.
- Mcpherson, R.J. and Marion, K.R. (1981). Seasonal testicular cycle of the stinkpot turtle (Sternotherus odoratus) in central Alabama. Herpetologica 37:33-40.
- Mendis-Handagama S.M.L. and Ariyaratne, H.B.S. (2005). Leydig cells, thyroid hormones and steroidogenesis. Indian J. Exp. Biol. 43: 939-962.
- Meylan, P.A., Sculer, R. and Moler P. (2002). Spermatogenic Cycle of the Florida Softshell Turtle, Apalone ferox. Copeia(3): 779–786.
- Oke, B.O., Ugwuegbu, S.O. and Akusu, M.O. (1984). Morphometric study of the testis of the West African Dwarf goat. Bul.l Anim. Health Prod. Afri. 32:57–60.
- Olukole S.G., Okusanya, B.O., Oyeyemi, M.O. and Oke, B.O (2013): Sperm morphological characteristics and morphometry in the African sideneck turtle (Pelusios castaneus). Asian J Exp. Biol. Sci. 4(4): 607-612.
- Olukole, S.G., Oyeyemi, M.O. and Oke, B.O. (2014a): Anatomy of the male reproductive organs of the African sideneck turtle (Pelusios castaneus). Anat J. Afri. 3(3) 380-385
- Olukole, S.G., Oyeyemi, M.O. and Oke, B.O. (2014b): Spermatogenic cycle of the African sideneck turtle, Pelusios castaneus(Schweigger, 1812) (Reptilia: Testudines), Ital. J. Zool. 81(1) 25-31.
- Olukole, S.G. and Oke, B.O. (2018). Sertoli cell junctions during active spermiogenesis in the African sideneck turtle (Pelusios castaneus): Implications for the blood-testis barrier. Int J. Vet. Sci. 7 (2): 106-112.
- Olukole S.G., Onwuama, K.T., Oyeyemi, M.O. and Oke, B.O. (2018a). Gonadal and extragonadal sperm reserves in African sideneck turtle (Pelusios castaneus). Savannah Vet. J. 1(1): 10-13.
- Olukole, S.G., Madekurozwa, M-C., and Oke, B.O. (2018b): Spermiogenesis in the African sideneck turtle (Pelusios castaneus): Acrosomal vesicle formation and nuclear morphogenesis. J. King Saud Univ. - Science 30: 359-366.
- Olukole S.G. and Oke, B.O. (2020). Morphophysiology of the epididymis of the African sideneck turtle (Pelusios castaneus): Histological, microstereological and ultrastructural approach. Sahel J. Vet. Sci. 17(1): 17-25.
- Rao, R.J. and Shaad, F.U. (1985). Sexual cycle of the male freshwater turtle,Trionyx gangeticus (Cuvier) Herpetologica 41(4): 433-437.
- Russell, L.D. (1996). Mammalian Leydig cell structure. In: Payne, A.H., Hardy, M.P., Russell, L.D. The Leydig cell. Vienna, IL: Cache River Press. p.43-96.
- Sagatelli, T.M., Franca, L.R., Pinheiro, P.F.F., Alemida, C.C.D., Martinez, M. and Martinez, F.E. (2004). Spermatogenic cycle length and spermatogenic efficiency in the Gerbill (Meriones unguiculatus). J Androl. 25:210–222.
- Young, B., Lowe, J.S., Stevens, A. and Heath, J.W. (2006). Wheater’s Functional Histology: A text and colour atlas. Fifth Edition, Churchhill Livingstone, Elsevier Limited. Pg 346-358.
References
Aire, T.A. (1997). The structure of the interstitial tissue of the active and resting avian testis. Onderstepoort J. Vet. Res., 64(4):291-9.
Ali, M.Z., Qureshi, A.S., Rehan, S., Akbar, S.Z. and Manzoor, A. (2015). Seasonal variations in histomorphology of testes and bursa, immune parameters and serum testosterone concentration in male guinea fowl (Numida meleagris). Pak. Vet. J., 35(1):88-92.
Al-Dokhi, O.A., Al-Onazee, Y.Z. and Mubarak, M. (2004). Light and electron microscopy of the testicular tissue of the Snake Eryxjayakari (Squamata, Reptilia) with a reference to the dividing germ cells. J. Biol. Sci. 4(3): 345- 351.
Almeida, F.F.L. (2002). Estrutura e funçãotesticularesemjavalis (Sus scrofa scrofa) sexualmentemaduros. 2002. 65 f. Dissertação (Mestrado) - Escola de Veterinária, Universidade Federal de Minas Gerais, Belo Horizonte, 2002.
Ashanbhag, B. (2002). Reproductive Biology of Indian Reptiles. Proc. Indian Natn. Sci Acad. (PINSA) B68, 6: 497-528.
Bacha, W.J. and Bacha, L.M. (2000). Color Atlas of Veterinary Histology. Lippincott William and Wilikins, USA, 219 pp.
Costa, D. S., Silva J.F.S. and Silveira, L. S. (2007). Morphometry of Leydig cells in the collared peccary (Tayassu tajacu). Braz. J. Vet. Res. Anim. Sci., Sao Paulo, 44(5):384-389.
De Kretser, D.M. and Kerr, J.B. (1994). The cytology of the testis In: Knobil, E., Neill, J.D. The physiology of reproduction. 2ed. New York: Raven Press, p.1177-1290.
Domke, L.M. (2018). Molecular and ultrastructural characteristics of adhering junctions and cytoskeletons in cells of the seminiferous tubules and the peritubular walls of mammalian testes. PhD Thesis. Combined Faculties for the Natural Sciences and for Mathematics, University of Heidelberg, Germany
Dubois, W., Pudney, J. and Callard, I.P. (1988). The annual testicular cycle in the turtle Chrysemys picta A histochemical and electron microscopic study. Gen. Comp. Endocrinol., 71:191-204.
Dufaure, J.P. (1968) L’ultrastructure des cellules interstitielles du testiculeadulte chez deux Reptiles Lacertilies: le lézardvivipare (Lacerta vivipara Jacquin) et l’orvet (Anguisfragilis L.). C R Acad. Sci. Paris 267: 883–885.
Ferreira, A. and Dolder, H. (2003). Cytochemical study of spermiogenesis and mature spermatozoa in the lizard Tropidurusitambere (Reptilia, Squamata). ActaHistochem. 105(4) 339–352.
Franca, L.R. and Godinho, C.L. (2002). Testis morphology, seminiferous epithelium cycle length and daily sperm production in domestic cat (Feliscatus). Biol. Reprod. 68:1554–1561.
Gribbins, K.M., Rheubert, J.L., Collier, M.H., Siegel, D.S. and Sever, D.M. (2008). Histological analysis of spermatogenesis and the germ cell development strategy within the testis of the male Western Cottonmouth Snake, Agkistrodonpiscivorusleucostoma. Ann. Anat. 190: 461—476.
Kirkpatrick, D.T. (1995). An Essay on Taxonomy and the Genus Pelusios. Available at: http://www.unc.edu/~dtkirkpa/stuff/pel.html. Accessed 22 February 2013.
Losinno, A.D., Morales, A., Fernandez, D., Lopez, L.A. (2012). Peritubular myoid cells from rat seminiferous tubules contain actin and myosin filaments distributed in two independent layers. Biol. Reprod. 86:150 151-158.
Mahmoud, I.Y., Cyrus, R.V., Bennett, T.M, Woller, M.J. and Montag, D.M. (1985). Ultrastructural changes in testes of the snapping turtle Chelydru serpentina in relation to plasma testosterone, 5-3B-hydroxysteroid dehydrogenase, and cholesterol. Gen. Comp. Endocrinol., 57:454-464.
Mcpherson, R.J. and Marion, K.R. (1981). Seasonal testicular cycle of the stinkpot turtle (Sternotherus odoratus) in central Alabama. Herpetologica 37:33-40.
Mendis-Handagama S.M.L. and Ariyaratne, H.B.S. (2005). Leydig cells, thyroid hormones and steroidogenesis. Indian J. Exp. Biol. 43: 939-962.
Meylan, P.A., Sculer, R. and Moler P. (2002). Spermatogenic Cycle of the Florida Softshell Turtle, Apalone ferox. Copeia(3): 779–786.
Oke, B.O., Ugwuegbu, S.O. and Akusu, M.O. (1984). Morphometric study of the testis of the West African Dwarf goat. Bul.l Anim. Health Prod. Afri. 32:57–60.
Olukole S.G., Okusanya, B.O., Oyeyemi, M.O. and Oke, B.O (2013): Sperm morphological characteristics and morphometry in the African sideneck turtle (Pelusios castaneus). Asian J Exp. Biol. Sci. 4(4): 607-612.
Olukole, S.G., Oyeyemi, M.O. and Oke, B.O. (2014a): Anatomy of the male reproductive organs of the African sideneck turtle (Pelusios castaneus). Anat J. Afri. 3(3) 380-385
Olukole, S.G., Oyeyemi, M.O. and Oke, B.O. (2014b): Spermatogenic cycle of the African sideneck turtle, Pelusios castaneus(Schweigger, 1812) (Reptilia: Testudines), Ital. J. Zool. 81(1) 25-31.
Olukole, S.G. and Oke, B.O. (2018). Sertoli cell junctions during active spermiogenesis in the African sideneck turtle (Pelusios castaneus): Implications for the blood-testis barrier. Int J. Vet. Sci. 7 (2): 106-112.
Olukole S.G., Onwuama, K.T., Oyeyemi, M.O. and Oke, B.O. (2018a). Gonadal and extragonadal sperm reserves in African sideneck turtle (Pelusios castaneus). Savannah Vet. J. 1(1): 10-13.
Olukole, S.G., Madekurozwa, M-C., and Oke, B.O. (2018b): Spermiogenesis in the African sideneck turtle (Pelusios castaneus): Acrosomal vesicle formation and nuclear morphogenesis. J. King Saud Univ. - Science 30: 359-366.
Olukole S.G. and Oke, B.O. (2020). Morphophysiology of the epididymis of the African sideneck turtle (Pelusios castaneus): Histological, microstereological and ultrastructural approach. Sahel J. Vet. Sci. 17(1): 17-25.
Rao, R.J. and Shaad, F.U. (1985). Sexual cycle of the male freshwater turtle,Trionyx gangeticus (Cuvier) Herpetologica 41(4): 433-437.
Russell, L.D. (1996). Mammalian Leydig cell structure. In: Payne, A.H., Hardy, M.P., Russell, L.D. The Leydig cell. Vienna, IL: Cache River Press. p.43-96.
Sagatelli, T.M., Franca, L.R., Pinheiro, P.F.F., Alemida, C.C.D., Martinez, M. and Martinez, F.E. (2004). Spermatogenic cycle length and spermatogenic efficiency in the Gerbill (Meriones unguiculatus). J Androl. 25:210–222.
Young, B., Lowe, J.S., Stevens, A. and Heath, J.W. (2006). Wheater’s Functional Histology: A text and colour atlas. Fifth Edition, Churchhill Livingstone, Elsevier Limited. Pg 346-358.