Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Structure, histochemistry and ultrastructure of the male reproductive accessory glands in the neotropical flat-faced fruit-eating bat Artibeus planirostris (Chiroptera: Phyllostomidae)

Cíntia C. I. Puga A , Mateus R. Beguelini A , Ana C. Negrin A , Caroline M. Christante A , Eliana Morielle-Versute B , Patricia S. L. Vilamaior A and Sebastião R. Taboga A C
+ Author Affiliations
- Author Affiliations

A Univ. Estadual Paulista, UNESP; Instituto de Biociências, Letras e Ciências Exatas, IBILCE; Departamento de Biologia. Rua Cristóvão Colombo no 2265, Jardim Nazareth, 15054-000, São José do Rio Preto, São Paulo, Brazil.

B Univ. Estadual Paulista, UNESP; Instituto de Biociências, Letras e Ciências Exatas, IBILCE; Departamento de Zoologia e Botânica. Rua Cristóvão Colombo no 2265, Jardim Nazareth, 15054-000, São José do Rio Preto, São Paulo, Brazil.

C Corresponding author. Email: taboga@ibilce.unesp.br

Reproduction, Fertility and Development 25(3) 558-569 https://doi.org/10.1071/RD12029
Submitted: 8 October 2011  Accepted: 19 April 2012   Published: 17 September 2012

Abstract

Chiroptera, the second largest mammalian order, presents different reproductive strategies and unique reproductive features. However, there are few reports regarding male reproductive accessory glands (RAGs) in Chiroptera. Thus, the aim of the present study was to characterise the RAGs of the exclusively neotropical bat Artibeus planirostris (Chiroptera: Phyllostomidae) macroscopically, microscopically and ultrastructurally. The RAGs were composed of a prostatic complex with two regions (ventral and dorsal) and paraurethral and bulbourethral glands, but no seminal vesicles. The ventral region had an undefined epithelium, with secretory and basal cells, and its secretions were periodic acid-Schiff (PAS) positive. The dorsal region received both deferens ducts, had a columnar pseudostratified epithelium with secretory and basal cells. There were two types of secretions from the dorsal region: one that was basophilic and another that was mixed PAS positive and PAS negative. The paraurethral glands were dispersed in the connective tissue of the urethra, whereas the bulbourethral glands were located in the penile root. Histological and ultrastructural data confirmed the prostatic nature of the ventral and dorsal regions and the holocrine nature of the ventral region, with the latter finding never having been described previously for the prostate gland. Our findings demonstrate the wide discrepancy of RAGs between A. planirostris and other mammals in terms of their composition, structure and morphology.

Additional keywords: bulbourethral, paraurethral gland, prostate.


References

Ali, H. A., Tingari, M. D., and Moniem, K. A. (1978). On the morphology of the accessory male glands and histochemistry of the ampulla ductus deferentis of the camel (Camelus dromedarius). J. Anat. 125, 277–292.
| 1:STN:280:DyaE1c7gvFahuw%3D%3D&md5=015f43005bbe5da0d5b8d18e05dae42eCAS | 624677PubMed |

Aumüller, G., and Seitz, J. (1990). Protein secretion and secretory process in male accessory sex glands. Int. Rev. Cytol. 121, 127–231.
Protein secretion and secretory process in male accessory sex glands.Crossref | GoogleScholarGoogle Scholar | 2190945PubMed |

Beguelini, M. R., Moreira, P. R. L., Faria, K. C., Marchesin, S. R. C., and Morielle-Versute, E. (2009). Morphological characterization of the testicular cells and seminiferous epithelium cycle in six species of neotropical bats. J. Morphol. 270, 943–953.
Morphological characterization of the testicular cells and seminiferous epithelium cycle in six species of neotropical bats.Crossref | GoogleScholarGoogle Scholar | 19248152PubMed |

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 |

Behmer, O. A., Tolosa, E. M. C., and Freitas-Neto, A. G. (1976). ‘Manual de Técnicas para Histologia Normal e Patológica.’ (Editora da Universidade de São Paulo: São Paulo.)

Cerri, L. M. O., Ajzen, S., Arap, S., and Cerri, G. G. (1999). ‘Ultra-sonografia da Próstata.’ (Sarvier, São Paulo.)

Cotta-Pereira, G., Rodrigo, F. G., and David-Ferreira, J. F. (1976). The use of tannic acid–glutaraldehyde in the study of elastic related fibers. Stain. Technol. 51, 7–11.
| 1:STN:280:DyaE283isFeltg%3D%3D&md5=5c131a5b7d33684df4be4baa5eb3f98cCAS |

Crichton, E. G., and Krutzsch, P. H. (2000). ‘Reproductive Biology of Bats.’ (Academic Press: London.)

Custódio, A. M. G., Góes, R. M., and Taboga, S. R. (2004). Acid phosphatase activity in gerbil prostate: comparative study in male and female during postnatal development. Cell Biol. Int. 28, 335–344.
Acid phosphatase activity in gerbil prostate: comparative study in male and female during postnatal development.Crossref | GoogleScholarGoogle Scholar |

De Knegt, L. V., Silva, J. A., Moreira, E. C., and Sales, G. L. (2005). Bats found in the city of Belo Horizonte, MG, 1999–2003. Arq. Bras. Med. Vet. Zootec. 57, 576–583.
Bats found in the city of Belo Horizonte, MG, 1999–2003.Crossref | GoogleScholarGoogle Scholar |

Dyce, K. M., and Sack, W. O. (2002). ‘Textbook of Veterinary Anatomy.’ (WB Saunders: Philadelphia.)

Eckstein, P., and Zuckerman, S. (1956). Morphology of the reproductive tract. In ‘Marshall’s Physiology of Reproduction. Vol. 1, Part 1.’ (Ed. A. S. Parkes.). pp. 43–155. (Longmans, Green & Co.: London.)

Fiala, J. C. (2005). Reconstruct: a free editor for serial section microscopy. J. Microsc. 218, 52–61.
Reconstruct: a free editor for serial section microscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M7osV2msQ%3D%3D&md5=2ec22603032c18f4e1497264bc702f8aCAS | 15817063PubMed |

Fleming, T. H., Hooper, E. T., and Wilson, D. E. (1972). Three central American bat communities: structure, reproductive cycles and movement patterns. Ecology 53, 555–569.
Three central American bat communities: structure, reproductive cycles and movement patterns.Crossref | GoogleScholarGoogle Scholar |

Frandson, R., and Spurgeon, T. (1995). ‘Anatomía y Fisiología de los Animales Domésticos.’ (Interamericana, Mcgraw-Hill: Mexico.)

Gömöri, G. (1937). Silver impregnation for reticulin in paraffin sections. Am. J. Pathol. 13, 993–1002.
| 19970363PubMed |

Hamilton, D. W. (1990). Anatomy of mammalian male accessory reproductive organs. In ‘Marshall’s Physiology of Reproduction. Vol. 2.’ (Ed. G. E. Lamming.). pp. 691–746. (Churchill Livingstone: Edinburgh.)

Jesik, C. J., Holland, J. M., and Lee, C. (1982). An anatomic and histologic study of the rat prostate. Prostate 3, 81–97.
An anatomic and histologic study of the rat prostate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL387pslensQ%3D%3D&md5=e1b5f9bab01732f01a8c2de758bad092CAS | 7079198PubMed |

Junqueira, L. M., and Carneiro, J. (2008). ‘Histologia Básica.’ (Guanabara Koogan: Rio de Janeiro.)

Krutzsch, P. H., and Nellis, D. W. (2006). Reproductive anatomy and cyclicity of the male Brachyphylla cavernarum (Chiroptera: Phyllostomidae). Acta Chirop. 8, 497–507.
Reproductive anatomy and cyclicity of the male Brachyphylla cavernarum (Chiroptera: Phyllostomidae).Crossref | GoogleScholarGoogle Scholar |

Krutzsch, P. H., Watson, R. H., and Lox, C. D. (1976). Reproductive biology of the male leaf-nosed bat, Macrotus waterhousii in southwestern United States. Anat. Rec. 184, 611–635.
Reproductive biology of the male leaf-nosed bat, Macrotus waterhousii in southwestern United States.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XhslOmtbo%3D&md5=253d33b620b010dea6494eb826462251CAS | 943969PubMed |

Mann, T., and Lutwak-Mann, C. (1981). ‘Male Reproductive Function and Semen.’ (Springer-Verlag, Berlin.)

Marchesin, S. R. C., Beguelini, M. R., Faria, K. C., Moreira, P. R. L., and Morielle-Versute, E. (2008). Assessing genetic variability in bat species of Emballonuridae, Phyllostomidae, Vespertilionidae and Molossidae families (Chiroptera) by RFLP-PCR. Genet. Mol. Res. 7, 1164–1178.
Assessing genetic variability in bat species of Emballonuridae, Phyllostomidae, Vespertilionidae and Molossidae families (Chiroptera) by RFLP-PCR.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKhu7rE&md5=de66cab2000e97fc161e8ad0813b8669CAS |

Mello, M. L. S., and Vidal, B. C. (1980). ‘Práticas de Biologia Celular.’ (Edgard Blücher-Funcamp: Campinas.)

Mokkapati, S., and Dominic, C. J. (1976). Sites of production of fructose and citric acid in the accessory reproductive glands of three species of male chiropterans. Biol. Reprod. 14, 627–629.
Sites of production of fructose and citric acid in the accessory reproductive glands of three species of male chiropterans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XkslGnur0%3D&md5=3a4f7a86072171f1d78c59d311b3e96dCAS | 1276325PubMed |

Moore, K. L., and Persaud, T. V. N. (2000). Sistema Urogenital. In ‘Embriologia Clínica.’ (Eds K. L. Moore and T. V. N. Persaud.) pp. 219–255. (Guanabara Koogan: Rio de Janeiro.)

Peracchi, A. L., Lima, I. P., Reis, N. R., Nogueira, M. R., and Hortêncio-Filho, H. (2006). Ordem Chiroptera. In ‘Mamíferos do Brasil.’ (Eds N. R. Reis, A. L Peracchi, W. A. Pedro and I. P. Lima.) pp. 153–230. (Nélio R. dos Reis: Londrina.)

Pinheiro, P. F., Almeida, C. C., Segatelli, T. M., Martinez, M., Padovani, C. B., and Martinez, F. E. (2003). Structure of the pelvic and penile urethra: relationship with the ducts of the sex accessory glands of the Mongolian gerbil (Meriones unguiculatus). J. Anat. 202, 431–444.
Structure of the pelvic and penile urethra: relationship with the ducts of the sex accessory glands of the Mongolian gerbil (Meriones unguiculatus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3hvVaitQ%3D%3D&md5=5e4066ffd351787a14628522ad578de6CAS | 12739620PubMed |

Price, D. (1963). Comparative aspects of development and structure in the prostate. Natl Cancer Inst. Monogr. 12, 1–27.
| 1:STN:280:DyaF2c%2FjtVKhtw%3D%3D&md5=2fdc7127d129c5ad75b5a921d3875b14CAS | 14072991PubMed |

Racey, P. A. (1974). The reproductive cycle in male noctule bats, Nyctalus noctula. J. Reprod. Fertil. 41, 169–182.
The reproductive cycle in male noctule bats, Nyctalus noctula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXivVOruw%3D%3D&md5=d4f1e88389a8b7cf246adae4963dee39CAS | 4431008PubMed |

Racey, P. A. (1978). Seasonal changes in testosterone levels and androgen-dependent organs in male moles (Talpa europaea). J. Reprod. Fertil. 52, 195–200.
Seasonal changes in testosterone levels and androgen-dependent organs in male moles (Talpa europaea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhvVOhsro%3D&md5=695cea3cb4f1c7803fa3e8751f2a18d9CAS | 633203PubMed |

Racey, P. A., and Tam, W. H. (1974). Reproduction in male Pipistrellus pipistrellus (Mammalia: Chiroptera). J. Zool. 172, 101–122.
Reproduction in male Pipistrellus pipistrellus (Mammalia: Chiroptera).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE28%2Fms1Oiuw%3D%3D&md5=f4ae97e6ad88d63a87bcd9c1ef6f37a5CAS | 4468890PubMed |

Reis, N. R., Peracchi, A. L., Pedro, W. A. and Lima, I. P. (2007). ‘Morcegos do Brasil.’ (Universidade Estadual de Londrina: Londrina.)

Ribeiro, M. G., and Lima, S. R. (2000). ‘Iniciação às técnicas de preparação de material para o estudo e pesquisa em morfologia.’ (SEGRAC–Editora e Gráfica Limitada: Belo Horizonte.)

Rochel, S. S., Bruni-Cardoso, A., Taboga, S. R., Vilamaior, P. S. L., and Góes, R. M. (2007). Lobe identity in the Mongolian gerbil prostatic complex: a new rodent model for prostate study. Anat. Rec. 290, 1233–1247.
Lobe identity in the Mongolian gerbil prostatic complex: a new rodent model for prostate study.Crossref | GoogleScholarGoogle Scholar |

Setchell, B. P., and Breed, W. G. (2006). Anatomy, vasculature, and innervation of the male reproductive tract In ‘Knobil and Neill’s Physiology of Reproduction’. 3rd edn. (Ed. J. D. Neill.) pp. 771–808. (Elsevier: New York.)

Short, R. V., and Mann, T. (1966). The sexual cycle of a seasonally breeding mammal, the roebuck (Capreolus capreolus). J. Reprod. Fertil. 12, 337–351.
The sexual cycle of a seasonally breeding mammal, the roebuck (Capreolus capreolus).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2s%2FksF2nsA%3D%3D&md5=8fd735c20fa5d1470a385a25b58a03f3CAS | 5951122PubMed |

Simmons, N. B. (2005). Order Chiroptera. In ‘Mammal Species of the World: A Taxonomic and Geographic Reference’. (Eds D. E. Wilson and D. M. Reeder.) pp. 312–529. (Johns Hopkins University Press: Baltimore.)

Spix, J. D. (1823). ‘Simiarum et vespertilionum brasiliensium species novae, ou histoire naturelle des espèces nouvelles de singes et de chauves-souris observées et recueillies pendant le voyage dans l’intérieur du Brésil execute par ordre de S. M. le Roi de Bavière dans les années 1817, 1818, 1819, 1820.’ (Francisci Seraphici Hubschmanni: Munich).

Thomson, A. A., and Cunha, G. R. (1999). Prostatic growth and development are regulated by FGF10. Development 126, 3693–3701.
| 1:CAS:528:DyaK1MXlvFSjsr8%3D&md5=591af60dd9399d4bd9ffc635f14d4476CAS | 10409514PubMed |

Venable, J. H., and Coggeshall, R. A. (1965). A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408.
A simplified lead citrate stain for use in electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2M%2FptFOltQ%3D%3D&md5=cd8dc6a88828244584aba649bc71d9caCAS | 14287192PubMed |

Voss, R. S., and Linzey, A. V. (1981). Comparative gross morphology of male accessory glands among neotropical Muridae (Mammalia: Rodentia) with comments on systematic implications. Miscellaneous Publications of the Museum of Zoology, University of Michigan 159, 1–41.

Watson, M. L. (1958). Staining tissue section of electron microscopy with heavy metals. J. Biophys. Biochem. Cytol. 4, 475–478.
Staining tissue section of electron microscopy with heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG1c7gs1Klsg%3D%3D&md5=057cc85a5a25964a1a091fedf611aa1eCAS | 13563554PubMed |

Williams, W. M. (1974). ‘The anatomy of the Mongolian gerbil (Meriones unguiculatus)’. (Tumblebrook Farm: West Brookfield, MA.)