Structure, histochemistry, ultrastructure and seasonal variations of the male prostatic complex in the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae)
Ana C. Negrin A , Mateus R. Beguelini A C , Cintia C. I. Puga A , Caroline M. Christante A , Larissa M. Bueno B , Eliana Morielle-Versute B , Patrícia S. L. Vilamaior A and Sebastião R. Taboga A
+ Author Affiliations
- Author Affiliations
A Department of Biology, UNESP–Univ. Estadual Paulista, R. Cristóvão Colombo, 2265, Jd. Nazareth, São José do Rio Preto, São Paulo 15054-000, Brazil.
B Department of Zoology and Botany, UNESP–Univ. Estadual Paulista, R. Cristóvão Colombo, 2265, Jd. Nazareth, São José do Rio Preto, São Paulo 15054-000, Brazil.
C Corresponding author. Email: mateus_sjrp@yahoo.com.br
Reproduction, Fertility and Development 26(8) 1188-1197 https://doi.org/10.1071/RD13217
Submitted: 11 July 2013 Accepted: 26 September 2013 Published: 30 October 2013
Abstract
Chiroptera are one of the most diverse orders of mammals and a unique group within Mammalia that posses a wide geographic distribution and considerable variability in reproductive strategies. The aims of the present study were to characterise the male prostatic complex of the bat Myotis nigricans (Vespertilionidae) and evaluate seasonal variations in the prostatic complex of M. nigricans specifically. Twenty-three sexually mature specimens (four sample groups: winter, spring, summer and autumn) were subjected to macroscopic, microscopic, morphometric and ultrastructural analyses. The reproductive accessory glands of M. nigricans were found to be composed of a multilobed complex associated with the urethra and a pair of inguinal bulbourethral glands. The complex was composed of three bilobed prostatic regions (ventral, dorsolateral and dorsal) with no ampullary gland and seminal vesicles. This pattern of lobulation is very similar to that described for the prostate of rodents; however, it differs from that of other mammals and even other families of bats (e.g. Phyllostomidae and Molossidae). Each prostatic region in M. nigricans has unique and distinctive characteristics, which synchronise to establish the main reproductive peak of the species in summer. The data also indicated an asynchrony in the activity of primary and secondary reproductive organs in the annual reproductive cycle of M. nigricans in São Paulo State, Brazil.
Additional keywords: asynchronous activity, prostate, reproduction.
References
Barclay, R. M. R., and Brigham, R. M. (1991). Prey detection, dietary niche breadth and body size in bats: why are aerial insectivorous bats so small. Am. Nat. 137, 693–703.Beguelini, M. R., Góes, R. M., Taboga, S. R., and Morielle-Versute, E. (2013a). Two periods of total testicular regression are peculiar events of the annual reproductive cycle of the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae). Reprod. Fertil. Dev. , .
| Two periods of total testicular regression are peculiar events of the annual reproductive cycle of the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae).Crossref | GoogleScholarGoogle Scholar | 23830483PubMed |
Beguelini, M. R., Taboga, S. R., and Morielle-Versute, E. (2013b). Ultrastructural characteristics of the spermatogenesis during the four phases of the annual reproductive cycle of the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae). Micros. Res. Tech. 76, 1035–1049.
| Ultrastructural characteristics of the spermatogenesis during the four phases of the annual reproductive cycle of the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae).Crossref | GoogleScholarGoogle Scholar |
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.)
Christante, C. M., Negrin, A. C., Puga, C. C. I., Morielle-Versute, E., Beguelini, M. R., and Taboga, S. R. (2009). Aspectos anatômico e histológico das glândulas reprodutivas acessórias de Molossus Molossus (Molossidae: Chiroptera). In ‘XXXVI Colóquio de Incentivo à Pesquisa, São José do Rio Preto’.
Crichton, E. G., and Krutzsch, P. H. (2000). ‘Reproductive biology of bats’. (Academic Press: London).
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 |
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=26bf830acd8e3757e5b68952551d278cCAS | 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 |
Gömöri, G. (1937). Silver impregnation for reticulin in paraffin sections. Am. J. Pathol. 13, 993–1002.
| 19970363PubMed |
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.
| 1:CAS:528:DyaE28XlvFSjt70%3D&md5=a694486bb85029b344dd56de3bfb7b7dCAS | 953115PubMed |
Jolly, S. E., and Blackshaw, A. W. (1989). Sex steroid levels and leydig cell ultrastructure of the male common sheath-tail bat, Taphozous georgianus. Reprod. Fertil. Dev. 1, 47–53.
| Sex steroid levels and leydig cell ultrastructure of the male common sheath-tail bat, Taphozous georgianus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1Crt7Y%3D&md5=127c9962795eb74fd49cc4587edc0439CAS | 2710959PubMed |
Justulin, L. A., Delella, F. K., and Felisbino, S. L. (2008). Doxazosin reduces cell proliferation and increases collagen fibers in rat prostatic lobes. Cell Tissue Res. 332, 171–183.
| Doxazosin reduces cell proliferation and increases collagen fibers in rat prostatic lobes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsF2msrg%3D&md5=a271113136c693a68deac734472f2f12CAS | 18188599PubMed |
Krutzsch, P. H. (1979). Male reproductive patterns in nonhibernating bats. J. Reprod. Fertil. 56, 333–344.
| Male reproductive patterns in nonhibernating bats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M3ktFOrtg%3D%3D&md5=8609a52aa559f94aae7f9ac82beca5cdCAS | 381651PubMed |
Laval, R. K., and Fitch, H. S. (1977). Structure movements and reproduction in three Costa Rican bats communities. Occas. Pap. Mus. Nat. Hist 69, 1–28.
Martins, F. F. (2012). ‘Morfofisiologia das Glândulas Acessórias do Sistema Genital de Morcegos. Estudo em Representantes das Subfamílias Carollinae, Glossophaginae e Phyllostominae (Chiroptera-Phyllostomidae).’ (Instituto de Biociências, Letras e Ciências Exatas, IBILCE/UNESP: São José do Rio Preto.)
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=54171c1d7e67f7b16488e0975029917bCAS | 1276325PubMed |
Nowak, R. M. (1999). ‘Walker’s Mammals of the World.’ (The Johns Hopkins University Press: London.)
Puga, C. C. I. (2011). ‘Morfofisiologia das Glândulas Reprodutivas Acessórias Masculinas de Morcegos: Estudos na Espécie Artibeus planirostris e Platyrrhinus lineatus (Chiroptera: Phyllostomidae).’ (Instituto de Biociências, Letras e Ciências Exatas, IBILCE/UNESP: São José do Rio Preto.)
Puga, C. C. I., Beguelini, M. R., Negrin, A. C., Christante, C. M., Morielle-Versute, E., Vilamaior, P. S. L., and Taboga, S. R. (2013). Structure, histochemistry and ultrastructure of the male reproductive accessory glands in the neotropical flat-faced fruit-eating bat Artibeus planirostris (Chiroptera: Phyllostomidae). Reprod. Fertil. Dev. 25, 558–569.
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 identy in the Mongolian gerbil prostatic complex: a new rodent model for prostate study. Anat. Rec. 290, 1233–1247.
| Lobe identy in the Mongolian gerbil prostatic complex: a new rodent model for prostate study.Crossref | GoogleScholarGoogle Scholar |
Singh, U. P., and Krishna, A. (2000). Seasonal changes in circulating testosterone and androstenedione concentration and their correlation with the anomalous reproductive pattern in the male indian sheath-tailed bat, Taphozous longimanus. J. Exp. Zool. 287, 54–61.
| Seasonal changes in circulating testosterone and androstenedione concentration and their correlation with the anomalous reproductive pattern in the male indian sheath-tailed bat, Taphozous longimanus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlKhtbo%3D&md5=5a7a4d46ab70eb6862aeb7f43bf2a007CAS | 10861550PubMed |
Swami, D. R., and Lall, S. B. (1982). Histoenzymological comparison of the prostate gland of sexually ‘quiescent’ and ‘active’ Taphozous melanopogon Temmnick (Microchiroptera: Mammalia). Acta Anat. 113, 128–134.
| Histoenzymological comparison of the prostate gland of sexually ‘quiescent’ and ‘active’ Taphozous melanopogon Temmnick (Microchiroptera: Mammalia).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xlsl2hsbw%3D&md5=061b47e603e4e1e5b489f06eef91e0aaCAS | 6214918PubMed |
Taddei, V. A., Vizotto, L. D., and Martins, M. (1976). Notas taxonômicas e biológicas sobre Molossops brachymeles cerastes (Thomas, 1901) (Chiroptera-Molossidae). Naturalia 2, 61–69.
Weibel, E. R., Kistler, G. S., and Scherle, W. F. (1966). Practical stereological methods for morphometric cytology. J. Cell Biol. 30, 23–38.
| Practical stereological methods for morphometric cytology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2s7msFersg%3D%3D&md5=0207e8eb416ca9c61ad8a07da5490db4CAS | 5338131PubMed |
Wilson, D. E., and Findley, J. S. (1971). Spermatogenesis in some neotropical species of Myotis. J. Mammal. 52, 420–426.
| Spermatogenesis in some neotropical species of Myotis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE3M3htFOntg%3D%3D&md5=b33c7f37ae053315dd2d204d3ae5204bCAS | 5581375PubMed |
Wilson, D. E., and Laval, R. K. (1974). Myotis nigricans. Mammal. Spec. 39, 1–3.
| Myotis nigricans.Crossref | GoogleScholarGoogle Scholar |
Wilson, D. E., and Reeder, D. M. (2005). ‘Mammal Species of the World: A Taxonomic and Geographic Reference.’ (The Johns Hopkins University Press: Baltimore.)
