Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Ultrastructure of spermatogenesis and spermatozoa in agoutis during sexual development

M. A. M. Arroyo A C , F. F. S. Silva A , P. R. S. Santos A , A. R. Silva B , M. F. Oliveira B and A. C. Assis Neto A
+ Author Affiliations
- Author Affiliations

A Department of Surgery – Anatomy of Domestic and Wild Animals, Faculty of Veterinary Medicine and Animal Science, University of São Paulo, Av. Prof. Dr Orlando Marques de Paiva, 87 – Cidade Universitária, São Paulo SP, Brazil.

B Department of Animal Science, Federal Rural University of the Semi-arid Region, Br 110, Km 47, s/n – Costa e Silva, Mossoró RN, Brazil.

C Corresponding author. Email: arroyomam@usp.br

Reproduction, Fertility and Development 29(2) 383-393 https://doi.org/10.1071/RD14442
Submitted: 14 November 2014  Accepted: 21 July 2015   Published: 4 September 2015

Abstract

The aim was to study the ultrastructure of testicular parenchyma and define the morphological ultrastructure of spermatozoa of agoutis kept in captivity. Segments of testes from eight agouti males at prepubescence, prepuberty, pubescence and sexual maturity were fixed in glutaraldehyde. Laboratory procedures were performed for transmission electron microscopy. Spermatogonial cells of Type A – pale, Type A – dark, intermediate and Type B were found. Spermatocytes in the pachytene phase were abundant among primary spermatocytes. From the prepubertal phase, Sertoli cells exhibited invaginations in the nuclear membrane and lipid inclusions in the cytoplasm due to their phagocytic function. Leydig cells displayed higher metabolic activity during puberty as evidenced by the presence of lipid droplets. Spermatozoa were fully formed morphologically at prepuberty. The centriolar complex had partially degenerated and featured a centriolar space as in rodents. Sperm heads were tapered, without prominence of the acrosome or evidence of the perforatorium, differing from cavies, rats and mice. This is the first study to describe the ultrastructure of agouti spermatozoa. This research may assist as a basis for future work related to fertility and other biotechnologies applied to reproductive biology in agoutis.

Additional keywords: acrosome, germ cell, Leydig cell, meiosis, puberty, Sertoli cell, spermatocyte, testis.


References

Alvarenga, F. C. L. (1992). Diferenças ultraestruturais entre as células de Leydig de cavalo, jumento e seu hibrido. Braz. J. Vet. Res. Anim. Sci. 29, 173–180.

Assis-Neto, A. C., Melo, M. I. V., Carvalho, M. A. M., Miglino, M. A., Oliveira, M. F., and Menezes, D. J. A. (2003a). Análise qualitativa do estabelecimento da espermatogênese em cutias (Dasyprocta agouti) criadas em cativeiros. Braz. J. Vet. Res. Anim. Sci. 40, 180–184.
Análise qualitativa do estabelecimento da espermatogênese em cutias (Dasyprocta agouti) criadas em cativeiros.Crossref | GoogleScholarGoogle Scholar |

Assis-Neto, A. C., Carvalho, M. A. M., Melo, M. I. V., Miglino, M. A., Oliveira, M. F., and Mariana, A. N. B. (2003b). Fases do desenvolvimento e diferenciação testicular em cutias (Dasyprocta agouti) criadas em cativeiros. Braz. J. Vet. Res. Anim. Sci. 40, 71–79.

Assis-Neto, A. C., Melo, M. I. V., Carvalho, M. A. M., Miglino, M. A., Oliveira, M. F., Ambrósio, C. E., Silva, S. M. M. S., Blasquez, F. X. H., Papa, P. C., and Kfoury Jr, J. R. (2003c). Quantificação de células dos túbulos seminíferos e rendimento da espermatogênese em cutias (Dasyprocta agouti) criadas em cativeiro. Braz. J. Vet. Res. Anim. Sci. 40, 175–179.
Quantificação de células dos túbulos seminíferos e rendimento da espermatogênese em cutias (Dasyprocta agouti) criadas em cativeiro.Crossref | GoogleScholarGoogle Scholar |

Baker, M. A., Naumovski, N., Hetherington, L., Weinberg, A., Velkov, T., and Aitken, J. (2013). Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics 13, 61–74.
Head and flagella subcompartmental proteomic analysis of human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvVShtA%3D%3D&md5=19976b407b657e86d7a8f87d7d2edcf5CAS | 23161668PubMed |

Beguelini, M. R., Puga, C. C. I., Taboga, S. R., and Morielle-Versute, E. (2011). Ultrastructure of spermatogenesis in the white-lined broad-nosed bat, Platyrrhinus lineatus (Chiroptera: Phyllostomidae). Micron 42, 586–599.
Ultrastructure of spermatogenesis in the white-lined broad-nosed bat, Platyrrhinus lineatus (Chiroptera: Phyllostomidae).Crossref | GoogleScholarGoogle Scholar | 21458280PubMed |

Byers, S., Pelletier, R. M., and Suárez-Quian, C. (1993). Sertoli cell junctions and the seminiferous epithelium barrier. In ‘The Sertoli Cell’. (Eds L. Russell and M. Griswold.) pp. 431–446. (Casher River Press: Clearwater.)

Costa, D. S., Henry, M., and Paula, T. A. R. (2004). Espermatogênese de catetos (Tayassu tajacu). Arq. Bras. Med. Vet. Zoot. 56, 46–51.
Espermatogênese de catetos (Tayassu tajacu).Crossref | GoogleScholarGoogle Scholar |

Ferreira, A. C. S., Guimarães, D. A., Luz-Ramos, R. S., Souza, P. C., Batista, C. R., and Ohashi, O. M. (2004). Reproductive developmental phases of male agouti (Dasyprocta sp.) raised in captivity determined by quantitative analysis of spermatogenic cells. Rev. Bras. Reprod. Anim 28, 196–201.

Godoy Pieri, N. C., Silva Santos, P. R., Roballo, K. C. S., Flamini, M. A., Barbeito, C. G., Ambrósio, C. E., Miglino, M. A., and Martins, D. S. (2014). Seasonal variations cause morphological changes and altered spermatogenesis in the testes of viscacha (Lagostomus maximus). Anim. Reprod. Sci. 149, 316–324.
Seasonal variations cause morphological changes and altered spermatogenesis in the testes of viscacha (Lagostomus maximus).Crossref | GoogleScholarGoogle Scholar | 25069754PubMed |

Guraya, S. S. (1987). ‘Biology of Spermatogenesis and Spermatozoa in Mammals’. (Springer-Verlag: London.)

Hess, R. A., and Franca, L. R. (2008). Spermatogenesis and cycle of the seminiferous epithelium. Adv. Exp. Med. Biol. 636, 1–15.
Spermatogenesis and cycle of the seminiferous epithelium.Crossref | GoogleScholarGoogle Scholar | 19856159PubMed |

Jan, S. Z., Hamer, G., Repping, S., Rooij, D. G., Pelt, A. M. M., and Vormer, T. L. (2012). Molecular control of rodent spermatogenesis. Biochim. Biophys. Acta 1822, 1838–1850.
Molecular control of rodent spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvVerurk%3D&md5=d8bf8eb626e29f828731aee0231f5872CAS | 22366765PubMed |

Johnson, M. (2012). Laboratory mice and rats. Mater. Methods. 2, 113.
Laboratory mice and rats.Crossref | GoogleScholarGoogle Scholar |

Kerr, J. B. (2000). Male reproduction system. In ‘Atlas of Functional Histology’. (Ed. J. B. Kerr.) pp. 339–358. (Mosby International Limited: New York.)

Manandhar, G., and Sutovsky, P. (2007) Comparative histology and subcellular structure of mammalian spermatogenesis and spermatozoa. In ‘Comparative Reproductive Biology’. (Eds H. Schattenand G. M. Constantinescu.) pp. 81–95. (Blackwell Publishing Professional: Carlton, Ames.)

Manandhar, G., Sutovskya, P., Joshib, H. C., Stearnsc, T., and Schattena, G. (1998). Centrosome reduction during mouse spermiogenesis. Dev. Biol. 203, 424–434.
Centrosome reduction during mouse spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnslyqt7w%3D&md5=b32050ddca7869693cc9872dbaae93efCAS | 9808791PubMed |

Manandhar, G., Simerly, C., Salisbury, J. L., and Schatten, G. (1999). Centriole and centrin degeneration during mouse spermiogenesis. Cell Motil. Cytoskeleton 43, 137–144.
| 1:STN:280:DyaK1Mzgs1GjtA%3D%3D&md5=d18f879e999b982299cfd507fcc23dafCAS | 10379838PubMed |

Menezes, D. J. A., Carvalho, M. A. M., Assis Neto, A. C., Oliveira, M. F., Farias, E. C., Miglino, M. A., and Medeiros, G. X. (2003). Morphology of the external male genital organs of agouti (Dasyprocta agouti. Linnaeus, 1766). Braz. J. Vet. Res. Anim. Sci. 40, 148–153.
Morphology of the external male genital organs of agouti (Dasyprocta agouti. Linnaeus, 1766).Crossref | GoogleScholarGoogle Scholar |

Mollineau, W. M., Adogwa, A. O., and Garcia, G. W. (2008). Spermatozoal morphologies and fructose and citric acid concentrations in agouti (Dasyprocta leporina) semen. Anim. Reprod. Sci. 105, 378–383.
Spermatozoal morphologies and fructose and citric acid concentrations in agouti (Dasyprocta leporina) semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtVWhsr8%3D&md5=7b68d83fdf942f7c8aab56f412e5bdd8CAS | 17919856PubMed |

Nogueira Filho, S. L. G., and Nogueira, S. S. C. (2000). Criação comercial de animais silvestres: produção e comercialização da carne e de subprodutos na região sudeste do Brasil. Rev. Econ. Nordeste 31, 188–195.

Norman, A. W., and Litwack, G. (1997). ‘Hormones’. (Academic Press: London.)

Phillips, B. T., Gassei, K., and Orwig, K. E. (2010). Spermatogonial stem cell regulation and spermatogenesis. Philos. Trans. R Soc. Lond. B Biol. Sci. 365, 1663–1678.
Spermatogonial stem cell regulation and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaisrrK&md5=e3e479d17f390016486b054a1e11b021CAS | 20403877PubMed |

Pudney, J. (1986). Fine structural changes in Sertoli and Leydig cells during the reproductive cycle of ground squirrel, Citellus lateralis. J. Reprod. Fertil. 77, 37–49.
Fine structural changes in Sertoli and Leydig cells during the reproductive cycle of ground squirrel, Citellus lateralis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL283lsVSltA%3D%3D&md5=3754942d9f45745d10028414e6a4be15CAS | 3723476PubMed |

Russell, L. D., França, L. R., and Brinster, R. L. (1996). Ultrastructural observations of spermatogenesis in mice resulting from transplantation of mouse spermatogonia. J. Androl. 17, 603–614.
| 1:STN:280:DyaK2s7mvVOqtQ%3D%3D&md5=5b327066d36bfd0ebe3be221ed83de92CAS | 9016390PubMed |

Santos, P. R. S., Oliveira, M. F., Arroyo, M. A. M., Silva, A. R., and Assis Neto, A. C. (2014). Ultrastructure of spermatogenesis in Spix’s yellow-toothed cavy (Galea spixii). Reproduction 147, 13–19.
Ultrastructure of spermatogenesis in Spix’s yellow-toothed cavy (Galea spixii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtV2ksb0%3D&md5=54630462c632a803cd21909b4fb1c0bcCAS |

Sousa, P. C., Santos, E. A. A., Bezerra, J. A. B., Lima, G. L., Castelo, T. S., Fontenele-Neto, J. D., and Silva, A. R. (2013). Morphology, morphometry and ultrastructure of captive six-banded armadillo (Euphractus sexcinctus) spermatozoa. Anim. Reprod. Sci. 140, 279–285.
Morphology, morphometry and ultrastructure of captive six-banded armadillo (Euphractus sexcinctus) spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVOjsbzO&md5=08d4fc6049f4fa064f3f7027e953a6abCAS | 23820069PubMed |

Weir, B. J. (1967). The care and management of laboratory histrycomorph rodents. Lab. Anim. 1, 95–104.
The care and management of laboratory histrycomorph rodents.Crossref | GoogleScholarGoogle Scholar |