CSIRO Publishing blank image blank image blank image blank imageBooksblank image blank image blank image blank imageJournalsblank image blank image blank image blank imageAbout Usblank image blank image blank image blank imageShopping Cartblank image blank image blank image You are here: Journals > Reproduction, Fertility and Development   
Reproduction, Fertility and Development
Journal Banner
  Vertebrate Reproductive Science & Technology
blank image Search
blank image blank image
blank image
  Advanced Search

Journal Home
About the Journal
Editorial Board
All Issues
Special Issues
Research Fronts
Sample Issue
For Authors
General Information
Instructions to Authors
Submit Article
Open Access
For Referees
Referee Guidelines
Review an Article
Annual Referee Index
For Subscribers
Subscription Prices
Customer Service
Print Publication Dates

blue arrow e-Alerts
blank image
Subscribe to our email Early Alert or RSS feeds for the latest journal papers.

red arrow Connect with us
blank image
facebook twitter youtube

red arrow Connect with SRB
blank image
facebook TwitterIcon

Affiliated Societies

RFD is the official journal of the International Embryo Transfer Society and the Society for Reproductive Biology.


Article << Previous     |     Next >>   Contents Vol 26(6)

Two periods of total testicular regression are peculiar events of the annual reproductive cycle of the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae)

Mateus R. Beguelini A , Rejane M. Góes A , Sebastião R. Taboga A C and Eliana Morielle-Versute B

A Department of Biology, UNESP – Univ Estadual Paulista, São José do Rio Preto, São Paulo 15054-000, Brazil.
B Department of Zoology and Botany, UNESP – Univ Estadual Paulista, São José do Rio Preto, São Paulo 15054-000, Brazil.
C Corresponding author. Email: taboga@ibilce.unesp.br

Reproduction, Fertility and Development 26(6) 834-846 http://dx.doi.org/10.1071/RD13109
Submitted: 4 April 2013  Accepted: 14 May 2013   Published: 8 July 2013

PDF (1.5 MB) $25
 Export Citation

Myotis nigricans presents few and controversial reproductive data, which indicate geographical variation in reproduction. Thus, this study aimed to evaluate the seasonal modifications in testicular and epididymal morphologies in a tropical environment, submitting these organs to morphometric and immunohistochemical analysis. The observations revealed that this species presents two peaks of spermatogenic activity followed by two periods of total testicular regression (a quiescent pre-pubertal-like morphology, where only Sertoli cells and spermatogonia could be observed), in the same annual reproductive cycle, which seem to be only indirectly influenced by abiotic factors. This testicular behaviour seems to be synchronised with the caput and corpus epididymidis, but not with the cauda epididymidis, which presents aspects of sperm storage in May–June. The control of this variation seems to be directly linked to the expression of the androgen receptor, since, throughout the year, it is high in periods of testicular recrudescence and low in periods of deactivation. It is not thought to be directly linked to apoptosis, which is more pronounced in periods of recrudescence than in periods of regression.

Additional keywords: recrudescence, reproduction, seasonality, testes.


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.
CrossRef | PubMed |

Beguelini, M. R., Taboga, S. R., and Morielle-Versute, E. (2012). Ultrastructural characteristics of spermatogenesis in Pallas’s Mastiff bat, Molossus molossus (Chiroptera: Molossidae). Microsc. Res. Tech. 75, 856–868.
CrossRef | PubMed |

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

Dadhich, R. K., Real, F. M., Zurita, F., Barrionuevo, F. J., Burgos, M., and Jiménez, R. (2010). Role of apoptosis and cell proliferation in the testicular dynamics of seasonal breeding mammals: a study in the Iberian mole, Talpa occidentalis. Biol. Reprod. 83, 83–91.
CrossRef | CAS | PubMed |

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. Zoo. 57, 576–583.
CrossRef |

Dinerstein, E. (1986). Reproductive ecology of fruit bats and the seasonality of fruit production in a Costa Rican cloud forest. Biotropica 18, 307–318.
CrossRef |

Dwyer, P. D. (1970). Latitude and breeding season in a polyestrus species of Myotis. J. Mammal. 51, 405–410.
CrossRef |

Encarnação, J. A., Dietz, M., and Kierdorf, U. (2004). Reproductive condition and activity pattern of male Daubenton’s bats (Myotis daubentonii) in the summer habitat. Mamm. Biol. 69, 163–172.
CrossRef |

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.
CrossRef |

Gopalakrishna, A. (1948). Studies on the embryology of microchiroptera. Part II. Reproduction in the male vespertilionida bat Scotophilus wroughtoni (Thomas). Proceed. Indian Acad. Sci. B 27, 137–151.

Grindal, S. D., Collard, T. S., Brigham, R. M., and Barclay, R. M. R. (1992). The influence of precipitation on reproduction by Myotis bats in British Columbia. Am. Midl. Nat. 128, 339–344.
CrossRef |

Gustafson, A. W. (1979). Male reproductive patterns in hibernating bats. J. Reprod. Fertil. 56, 317–331.
CrossRef | CAS | PubMed |

Gustafson, A. W., and Damassa, D. A. (1985). Annual variations in plasma sex steroid-binding protein and testosterone concentrations in the adult little brown bat: relation to the asynchronous recrudescence of the testis and accessory reproductive organs. Biol. Reprod. 33, 1126–1137.
CrossRef | CAS | PubMed |

Gustafson, A. W., and Shemesh, M. (1976). Changes in plasma testosterone levels during the annual reproductive cycle of the hibernating bat, Myotis lucifugus lucifugus with a survey of plasma testosterone levels in adult male vertebrates. Biol. Reprod. 15, 9–24.
| CAS | PubMed |

Heideman, P. D., and Bronson, F. H. (1994). An endogenous circannual rhythm of reproduction in a tropical bat, Anoura geoffroyi, is not entrained by photoperiod. Biol. Reprod. 50, 607–614.
CrossRef | CAS | PubMed |

Heideman, P. D., Deoraj, P., and Bronson, F. H. (1992). Seasonal reproduction of a tropical bat, Anoura geoffroyi, in relation to photoperiod. J. Reprod. Fertil. 96, 765–773.
CrossRef | CAS | PubMed |

Heller, C. G., and Clermont, Y. (1963). Spermatogenesis in man: an estimate of its duration. Science 140, 184–186.
CrossRef | CAS | PubMed |

Hess, R. A., and França, L. R. (2008). Spermatogenesis and cycle of the seminiferous epithelium. In ‘Molecular Mechanisms in Spermatogenesis’. (Ed. C. Y. Cheng.) pp. 1–15. (Landes Bioscience and Springer Science + Business Media: New York, NY.)

Holdcraft, R. W., and Braun, R. E. (2004). Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development 131, 459–467.
CrossRef | CAS | PubMed |

Krishna, A., and Singh, K. (1997). The relationship between testicular activity, accessory sex glands and circulating steroid concentration during the reproductive cycle in a male Indian vespertilionid bat, Scotophilus heathi. Can. J. Zool. 75, 1042–1050.
CrossRef | CAS |

Krutzsch, P. H. (1979). Male reproductive patterns in non-hibernating bats. J. Reprod. Fertil. 56, 333–344.
CrossRef | CAS | PubMed |

Krutzsch, P. H. (2009). The reproductive biology of the cave Myotis (Myotis velifer). Acta Chiropterol. 11, 89–104.
CrossRef |

Lee, J. H., and Mori, T. (2004). Annual cycle of the seminiferous epithelium of Myotis macrodactylus. J. Facul. Agric. Kyushu Univ. 49, 355–365.
| CAS |

León-Galván, M. A., López-Wilchis, R., Hernández-Pérez, O., Arenas-Ríos, E., and Rosado, A. (2005). Male reproductive cycle of Mexican big-eared bats, Corynorhinus mexicanus (Chiroptera: Vespertilionidae). Southwest. Nat. 50, 453–460.
CrossRef |

Lewis, S. E. (1993). Effect of climatic variation on reproduction by pallid bats (Antrozous pallidus). Can. J. Zool. 71, 1429–1433.
CrossRef |

Myers, P. (1977). Patterns of reproduction of four species of vespertilionid bats in Paraguay. Univ. Calif. Publ. Zool. 107, 1–41.

O’Farrell, M. J., and Studier, E. H. (1973). Reproduction, growth and development in Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae). Ecology 54, 18–30.
CrossRef |

Onyango, D. W., Gachoka, G. E., Otianga’a-Owiti, G. E., and Hendrickx, A. G. (1995). Seasonally dependent testicular apoptosis in the tropical Long-fingered bat (Miniopterus inflatus). Z. für Säugetierkunde, Internat. J. Mammal. Biol. 60, 206–214.

Print, C. G., and Lakoski-Loveland, K. (2000). Germ-cell suicide: new insights into apoptosis during spermatogenesis. Bioessays 22, 423–430.
CrossRef | CAS | PubMed |

Racey, P. A., and Entwistle, A. C. (2000). Life-history and reproductive strategies of bats. In ‘Reproductive Biology of Bats’. (Eds E. G. Crichton and P. H. Krutzsch.) pp. 363–414. (Academic Press: London.)

Racey, P. A., Speakman, J. R., and Swift, S. M. (1987). Reproductive adaptations of heterothermic bats at the northern borders of their distribution. S. Afr. J. Sci. 83, 635–638.

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.)

Schwartzman, R. A., and Cidlowski, J. A. (1993). Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr. Rev. 14, 133–151.
| CAS | PubMed |

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.)

Sinha Hikim, A. P., and Swerdloff, R. S. (1999). Hormonal and genetic control of germ-cell apoptosis in the testis. Rev. Reprod. 4, 38–47.
CrossRef | CAS | PubMed |

Taddei, V. A. (1976). The Reproduction of Some Phyllostomidae (Chiroptera) from the Northwestern Region of the State of São Paulo. Vol. 1. Bol. Zool. Univ. São Paulo 1, 313–330.

Taddei, V. A. (1980). Biologia reprodutiva de Chiroptera: perspectivas e problemas. Inter-facies Escrit. Doc. 6, 1–18.

Tuttle, M. D., and Stevenson, D. (1982). Growth and survival of bats. In ‘Ecology of Bats’. (Ed. T. H. Kunz.) pp. 105–150. (Plenum Press: New York.)

van der Merwe, M., and Rautenbach, I. L. (1987). Reproduction in Schlieffen’s bat, Nycticeius schlieffenii, in the eastern Transvaal lowveld, South Africa. J. Reprod. Fertil. 81, 41–50.
CrossRef | CAS | PubMed |

van der Merwe, M., and Rautenbach, I. L. (1990). Reproduction in rusty bat, Pipistrellus rusticus, in the northern Transvaal bushveld, South Africa. J. Reprod. Fertil. 89, 537–542.
CrossRef | CAS | PubMed |

Wang, R. S., Yeh, S., Tzeng, C. R., and Chang, C. (2009). Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr. Rev. 30, 119–132.
CrossRef | PubMed |

Weibel, E. R., Kistler, G. S., and Scherle, W. F. (1966). Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38.
CrossRef | CAS | PubMed |

Wilson, D. E. (1971). Ecology of Myotis nigricans (Mammalia: Chiroptera) on Barro Colorado Island, Panama Canal Zone. J. Zool. 163, 1–13.
CrossRef |

Wilson, D. E., and Findley, J. S. (1970). Reproductive cycle of a Neotropical insectivorous bat, Myotis nigricans. Nature 225, 1155.
CrossRef | CAS | PubMed |

Wilson, D. E., and Findley, J. S. (1971). Spermatogenesis in some Neotropical species of Myotis. J. Mammal. 52, 420–426.
CrossRef | CAS | PubMed |

Wilson, D. E., and Laval, R. K. (1974). Myotis nigricans. Mammal. Spec. 39, 1–3.
CrossRef |

Zhang, L., Han, X. K., Qi, Y. Y., Liu, Y., and Chen, Q. S. (2008). Seasonal effects on apoptosis and proliferation of germ cells in the testes of the Chinese soft-shelled turtle, Pelodiscus sinensis. Theriogenology 69, 1148–1158.
CrossRef | CAS | PubMed |

Zortéa, M. (2003). Reproductive patterns and feeding habits of three nectarivorous bats (Phyllostomidae: Glossophaginae) from the Brazilian Cerrado. Braz. J. Biol. 63, 159–168.
CrossRef | PubMed |

Subscriber Login

Legal & Privacy | Contact Us | Help


© CSIRO 1996-2014