Implications of body condition and seasonality on morphological and functional parameters of testes of Myotis nigricans (Chiroptera: Vespertilionidae)
Marcelo Ferreira A C , Aline Soldati A , Sirlene S. S. Rodrigues B and Laércio dos Anjos Benjamin A
+ Author Affiliations
- Author Affiliations
A Department of Veterinary, Center of Biological and Health Sciences, Federal University of Viçosa, Viçosa, MG 36570-900, Brazil.
B Department of Animal Biology, Center of Biological and Health Sciences, Federal University of Viçosa, Viçosa, MG 36570-900, Brazil.
C Corresponding author. Email: ferreira.bats@gmail.com
Reproduction, Fertility and Development 30(7) 1029-1037 https://doi.org/10.1071/RD17316
Submitted: 30 September 2016 Accepted: 20 November 2017 Published: 12 January 2018
Abstract
The insectivorous bat Myotis nigricans is widely distributed throughout the Neotropics, including Brazil, and has a reproductive biology that is affected by climate and food availability. To evaluate the reproductive capacity of this species, morphofunctional parameters of the testes were correlated with environmental variables and the body condition of individuals captured. After bats had been killed, their testes were removed, fixed in Karnovsky’s fluid for 24 h and embedded in resin for evaluation by light microscopy. The mean annual tubulosomatic index (0.58%) and the percentage of seminiferous tubules in the testes (88.96%) were the highest ever recorded for the Order Chiroptera. The percentage of Leydig cells and volume of the cytoplasm of Leydig cells were higher in the rainy than dry season (80.62 ± 3.19% and 573.57 ± 166.95 μm, respectively; mean ± s.d.). Conversely, the percentage of nuclei of the Leydig cells in the dry season (26.17 ± 3.70%; mean ± s.d.) and the total number of Leydig cells (6.38 ± 1.84 × 109; mean ± s.d.) were higher in the dry season. The results of the present study could help in future conservation of these bats because they provide a better understanding of the bats’ reproductive strategies and how the species can adapt to changes.
Additional keywords: behaviour, ecology, Leydig cell, Mammalia, reproduction.
References
Alencar, J. B. R., Andrade, L. R., Silva, A. S., Lima, A. M. R., Montenegro, I. F., Melo, F. C. O., Albuquerque, R. R. S., and Brito, C. H. (2012). Abundância e sazonalidade de insetos em brejo de altitude no nordeste do Brasil. In ‘Anais do XXIV Congresso Brasileiro de Entomologia’. (Ed. Sociedade Brasileira de Entomologia.) (Sociedade Brasileira de Entomologia: Curitiba, Brasil.)Andrade, L. R., Alencar, J. B. R., Silva, A. S., Lima, A. M. R., Montenegro, I. F., Melo, F. C. O., Albuquerque, R. R. S., and Brito, C. H. (2012). Abundância e sazonalidade de artrópodes em brejo de altitude no nordeste do Brasil. In ‘Anais do XXIV Congresso Brasileiro de Entomologia’. (Ed. Sociedade Brasileira de Entomologia.) (Sociedade Brasileira de Entomologia: Curitiba, Brasil.)
Anthony, E. L. P. (1988). Age determination in bats. In ‘Ecological and Behavioral Methods for the Study of Bats’. (Eds T. H. Kunz.) pp. 47–58. (Smithsonian Institution Press: Washington, DC)
Azevedo, M. H. F. (2004). Análise morfofuncional do testículo de onça pintada (Panthera onca) adulta. Ph.D. Thesis, Universidade Federal de Viçosa.
Balarini, M. K. (2008). Avaliação morfofuncional do processo espermatogênico do gato-do-mato-pequeno (Leopardus tigrinus Schreber, 1775). MSc Thesis, Universidade Federal de Viçosa.
Balarini, M. K. (2013). Avaliação morfofuncional do testículo e do processo espermatogênico dos roedores silvestres Akodon cursor e Oligoryzomys nigripes (Rodentia: Cricetidae). Ph.D. Thesis, Universidade Federal de Viçosa.
Bancroft, J. D., and Stevens, A. (1996). ‘Theory and Practice of Histological Techniques.’ (Churchill Livingstone: New York.)
Beguelini, M. R., Góes, R. M., Taboga, S. R., and Morielle-Versute, E. (2014). Two periods of total testicular regression are peculiar events of the anual reproductive cycle of the black Myotis nigricans (Chiropera, Vespertilionidae). Reprod. Fertil. Dev. 26, 834–846.
| Two periods of total testicular regression are peculiar events of the anual reproductive cycle of the black Myotis nigricans (Chiropera, Vespertilionidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFynsbjN&md5=56d4037e7d9f627c4ea33ecc9a87db7aCAS |
Brito, J. L. M. (2014). Caracterização histomorfométrica de testículos de quatro espécies de morcegos frequentes na região de cerrado do Distrito Federal nas estações seca e chuvosa. MSc Thesis, Universidade de Brasília.
Bueno, L. M., Comelis, M. T., Begueline, M. R., Taboga, S. R., and Morielle-Versute, E. (2013). Características morfológicas das espemátides durante a espermiogênese de Eptesicus furinalis. In ‘Anais do VII Encontro Brasileiro para o Estudo de Quirópteros’. (Ed. Sociedade Brasileira para o Estudo de Quirópteros.) pp. 60–62. (Sociedade Brasileira para o Estudo de Quirópteros: Brasília.)
Carvalho, F. A. R. (2007). ‘Morfologia e morfometria testicular do roedor silvestre Akodon cursor (Winge, 1887) (Rodentia: Muridae).’ (Universidade Federal de Viçosa: Viçosa.)
Castro, P. S. (1980). Influência da cobertura florestal na qualidade da água em duas bacias hidrográficas da região de Viçosa, MG. MSc Thesis, Escola Superior de Agricultura de Luiz de Queiroz, Piracicaba.
Costa, D. S., Paula, T. A. R., and Matta, S. L. P. (2006). The intertubular compartment morphometry in capybaras (Hydrochoerus hydrochaeris) testis. Anim. Reprod. Sci. 91, 173–179.
| The intertubular compartment morphometry in capybaras (Hydrochoerus hydrochaeris) testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MnivVOgtA%3D%3D&md5=3260941e4c74f6162cbe8761052c5893CAS |
Costa, G. M. J., Chiarini-Garcia, H., Morato, R. G., Alvarenga, R. L. L. S., and França, L. R. (2008). Duration of spermatogenesis and daily sperm production in the jaguar (Panthera onca). Theriogenology 70, 1136–1146.
| Duration of spermatogenesis and daily sperm production in the jaguar (Panthera onca).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cngtVyksA%3D%3D&md5=9004e5f70d05d575d1b3816836069b6cCAS |
Costa, G. M. J., Leal, M. C., Silva, J. V., Ferreira, A. C. S., Guimarães, D. A., and França, A. L. (2010). Spermatogenic cycle length and sperm production in a feral pig species (collared peccary, Tayassu tajacu). J. Androl. 31, 221–230.
| Spermatogenic cycle length and sperm production in a feral pig species (collared peccary, Tayassu tajacu).Crossref | GoogleScholarGoogle Scholar |
Drummond, G. M., Martins, C. S., Machado, A. B. M., Sebaio, F. A., and Antonini, Y. (2005). ‘Biodiversidade em Minas Gerais: um atlas para sua conservação’. (Fundação Biodiversitas: Belo Horizonte.)
Dwyer, P. D. (1970). Latitude and breeding season in a polyestrus species of Myotis. J. Mammal. 51, 405–410.
| Latitude and breeding season in a polyestrus species of Myotis.Crossref | GoogleScholarGoogle Scholar |
Fawcett, D. W., Neaves, W. B., and Flores, M. N. (1973). Comparative observations on intertubular lymphatics and the organization of the intersticial tissue of the mammalian testis. Biol. Reprod. 9, 500–532.
| Comparative observations on intertubular lymphatics and the organization of the intersticial tissue of the mammalian testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c%2Fms1entw%3D%3D&md5=ef9b157d405b6479fd3fdae5a6fc013dCAS |
Feijó, J. A., and Nunes, H. L. (2010). Primeiro registro de Myotis nigricans para o estado do Rio Grande do Norte, nordeste do Brasil. Chiropt. Neotrop 16, 524–531.
Ferreira, M. J. D., Soldati, A. M. M., Lopes, D. S., Anjos, L. R., and Benjamin, L. A. (2015). Análise comparative do compartimento tubular do testículo em machos adultos de três espécies de morcegos. In ‘Anais do VIII Encontro Brasileiro para o estudo de Quirópteros’. (Ed. Sociedade Brasileira para o Estudo de Quirópteros.) pp. 150–151. [Abstract] (Sociedade Brasileira para o Estudo de Quirópteros: Ouro Preto.)
Filho, H. O., Reis, N. R., Pinto, D., and Vieira, D. C. (2007). Aspectos reprodutivos de Artibeus lituratus em fragmentos florestais na região de Porto Rico, Paraná, Brasil. Chiropt. Neotrop 13, 313–318.
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 |
França, L. R. (1987). Desenvolvimento testicular de suínos da raça Piau, do nascimento aos 12 meses de idade. MSc Thesis, Universidade Federal de Minas Gerais, Belo Horizonte.
França, L. R. (1991). Análise morfofuncional da espermatogênese de suínos adultos da raça Piau. Ph.D. Thesis, Universidade Federal de Minas Gerais, Belo Horizonte.
França, L. R., and Godinho, C. L. (2003). Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus). Biol. Reprod. 68, 1554–1561.
| Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus).Crossref | GoogleScholarGoogle Scholar |
França, L. R., and Russell, L. D. (1998). The testis of domestic mammals. In ‘Male Reproduction: A Multidisciplinary Overview’. (Eds J. Regadera and F. Martinez-Garcia.) pp. 197–219. (Churchill Livingstone: Madrid.)
Griffin, D. R., Webster, F. A., and Michael, C. R. (1960). The echolocation of flying insects by bats. Anim. Behav. 8, 141–154.
| The echolocation of flying insects by bats.Crossref | GoogleScholarGoogle Scholar |
Gustafson, A. W. (1979). Male reproductive patterns in hibernating bats. J. Reprod. Fertil. 56, 317–331.
| Male reproductive patterns in hibernating bats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXksFeitbk%3D&md5=9d57fbd94ded59207e49bffdb9c65155CAS |
Hammer, O., Harper, D. A. T., and Ryan, P. D. (2001). Past: paleontological statistic software package analysis. Pal. Electron. 4, 1–9.
Hutson, A. M., and Racey, P. A. (2004) Examining bats. In ‘Bat Worker’s Manual’. Vol. 3. (Eds J. A. Mitchell-Jones and A. P. Mcleish.) pp. 48–57. (Histologia básica: Rio de Janeiro.)
Junqueira, L. C., and Carneiro, J. (2008). ‘Histologia básica: Livros texto/Atlas.’ Vol. 11. (Guanabara Koogan: Rio de Janeiro.)
Leal Filho, N. (1992). Caracterização do banco de sementes de três estádios de uma sucessão vegetal na Zona da Mata de Minas Gerais. MSc Thesis, Universidade Federal de Viçosa.
Lima-Júnior, N. B., Arandas, M. J. G., Marinho, K. S. N., Aguiar-Júnior, F. C. A., Pontes, A. R. M., and Santos, K. R. P. (2014). Histomorfometria testicular do morcego Phyllostomus discolor (Chiroptera, Phyllostomidae) em áreas de Mata Atlântica de Pernambuco. Brazil. J. Veter. Res. An. Sc. 51, 263–270.
Lučan, R. K., Weiser, M., and Hanák, V. (2013). Contrasting effects of climate change on the timing of reproduction and reproductive success of a temperate insectivorous bat. J. Zool. (Lond.) 290, 151–159.
| Contrasting effects of climate change on the timing of reproduction and reproductive success of a temperate insectivorous bat.Crossref | GoogleScholarGoogle Scholar |
Mascarenhas, R. M., Paula, T. A. R., Matta, S. L. P., Lana, L. L., Fonseca, C. C., and Neves, M. T. D. (2006). Morfometria macro e microscópica e índices somáticos dos componentes testiculares de cães sem raça definida, da puberdade à senilidade. Rev. Cer. 53, 113–119.
Meyer, C. F. J., Struebeg, M. J., and Willig, M. R. (2016). Responses of tropical bats to habitat fragmentation, logging and deforestation. In ‘Bats in the Anthropocene: Conservation of Bats in a Changing World’. (Eds C. C. Voigt and T. Kingston.) pp. 63–103. (Springer Open Press.)
Morais, D. B. (2008). Morfologia e morfometria testicular em morcego insetívoro (Molossus molossus Pallas, 1776) (Chiroptera: Molossidae). MSc Thesis, Universidade Federal de Viçosa.
Morais, D. B., Barbosa, L. P., Melo, B. E. S., Matta, S. L. P., Neves, M. M., Balarini, M. K., and Rodrigues, M. V. (2012). Microscopia e morfometria de componentes tubulares de testículos de coelhos suplementados com geleia real. Arq. Bras. Med. Vet. Zootec. 64, 810–816.
| Microscopia e morfometria de componentes tubulares de testículos de coelhos suplementados com geleia real.Crossref | GoogleScholarGoogle Scholar |
Morais, D. B., Oliveira, L. C., Cupertino, M. C., Freitas, K. M., Freitas, M. B. D., Paula, T. A. R., and Matta, S. L. P. (2013a). Organization and seasonal quantification of the intertubular compartment in the bat Molossus molossus (Pallas, 1776) testis. Microsc. Res. Tech. 76, 94–101.
| Organization and seasonal quantification of the intertubular compartment in the bat Molossus molossus (Pallas, 1776) testis.Crossref | GoogleScholarGoogle Scholar |
Morais, D. B., Cupertino, M. C., Goulart, L. S., Freitas, K. M., Freitas, M. B. D., Paula, T. A. R., and Matta, S. L. P. (2013b). Histomorphometric evaluation of the Molossus molossus (Chiroptera, Molossidae) testis: the tubular compartment and indices of sperm production. Anim. Reprod. Sci. 140, 268–278.
| Histomorphometric evaluation of the Molossus molossus (Chiroptera, Molossidae) testis: the tubular compartment and indices of sperm production.Crossref | GoogleScholarGoogle Scholar |
Morais, D. B., Barros, M. S., Freitas, M. B. D., Paula, T. A. R., and Matta, S. L. P. (2014a). Histomorphometric characterization of the intertubular compartment in the teste of the bat Sturnira lilium. Anim. Reprod. Sci. 147, 180–186.
| Histomorphometric characterization of the intertubular compartment in the teste of the bat Sturnira lilium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXns1Wns74%3D&md5=331f2117489ab679bb8792f76713b029CAS |
Morais, D. B., Barros, M. S., Paula, T. A. R., Freitas, M. B. D., Gomes, M. L. M., and Matta, S. L. P. (2014b). Evaluation of the cell population of the seminiferous epithelium and spermatic indexes of the bat Sturnira lilium (Chiroptera: Phyllostomidae). PLoS One 9, e101759.
| Evaluation of the cell population of the seminiferous epithelium and spermatic indexes of the bat Sturnira lilium (Chiroptera: Phyllostomidae).Crossref | GoogleScholarGoogle Scholar |
Morais, A. C. T., Balarin, I. M. K., Lopes, E. O., Menezes, T. P., Quintela, M. K., Morais, D. B., Gomes, M. L. M., and Matta, S. L. P. (2014c). The tubular compartment and the spermatogenic dynamics of the wild rodent Oxymycterus nasutus (Rodentia: Cricetidae). Anim. Reprod. Sci. 149, 249–258.
| The tubular compartment and the spermatogenic dynamics of the wild rodent Oxymycterus nasutus (Rodentia: Cricetidae).Crossref | GoogleScholarGoogle Scholar |
Moratelli, R., Peracchi, A. L., Dias, D., and Oliveira, J. A. (2011). Geographic variation in South American populations of Myotis nigricans (Schinz, 1821) (Chiroptera, Vespertilionidae), with the description of two new species. Mamm. Biol. 76, 592–607.
| Geographic variation in South American populations of Myotis nigricans (Schinz, 1821) (Chiroptera, Vespertilionidae), with the description of two new species.Crossref | GoogleScholarGoogle Scholar |
Ortega, J., and Maldonado, J. E. (2006). Female interactions in harem groups of the Jamaican fruit-eating bat, Artibeus jamaicensis (Chiroptera: Phyllostomidae). Acta Chiropt. 8, 485–495.
| Female interactions in harem groups of the Jamaican fruit-eating bat, Artibeus jamaicensis (Chiroptera: Phyllostomidae).Crossref | GoogleScholarGoogle Scholar |
Paula, T. A. R., Costa, D. S., and Matta, S. L. P. (2002). Avaliação histológica quantitativa do testículo de capivaras (Hydrochoerus hydrochaeris) adultas. Biosci. J. 18, 121–136.
Peracchi, A. L., and Nogueira, M. R. (2010). Métodos de captura de quirópteros em áreas silvestres. In ‘Técnicas de estudos aplicadas aos mamíferos silvestres brasileiros’. (Eds N. R. Reis, A. L. Peracchi, B. K. Rossaneis, and M. N. Fregonezi.) pp. 42–58. (Technical Books Editora: Rio de Janeiro.)
Racey, P. A. (1979). The prolonged storage and survival of spermatozoa in Chiroptera. J. Reprod. Fertil. 56, 391–402.
| The prolonged storage and survival of spermatozoa in Chiroptera.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE1M3ktFOqsg%3D%3D&md5=45d860e579431d212965a2cd3e5b892cCAS |
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.)
Rodriguês, I. M. C., and Garcia, F. C. P. (2008). Papilionoideae (Leguminosae) na Mata do Paraiso, Viçosa, Minas Gerais, Brasil: ervas, subarbustos e trepadeiras. Hoehnea 35, 519–536.
| Papilionoideae (Leguminosae) na Mata do Paraiso, Viçosa, Minas Gerais, Brasil: ervas, subarbustos e trepadeiras.Crossref | GoogleScholarGoogle Scholar |
Russell, L. D., Ettlin, R. A., Sinha-Hikim, A. P., and Clegg, E. D. (1990). ‘Histological and Histopathological Evaluation of the Testis.’ (Cache River Press: Clearwater, FL.)
Santos, M. O. (2012). Efeitos do inseticida Endossulfan sobre a morfologia e a morfometria testicular em morcegos frugívoros Artibeus lituratus (Olfers, 1818). MSc Thesis, Universidade Federal de Viçosa.
Schulte-Hostedde, A. I., Millar, J. S., and Hickling, G. J. (2001). Evaluating body condition in small mammals. Can. J. Zool. 79, 1021–1029.
| Evaluating body condition in small mammals.Crossref | GoogleScholarGoogle Scholar |
Schulte-Hostedde, A. I., Millar, J. S., and Hickling, G. J. (2005). Condition dependence of testis size in small mammals. Evol. Ecol. Res. 7, 143–149.
Silva, J. O. (2014a). Variação na diversidade de insetos e herbívora entre grupos fenológicos de uma floresta tropical seca. Ph.D. Thesis, Universidade de Brasília.
Silva, V. H. D. (2014b). Avaliação do processo espermatogênico de gatos-mouriscos (Puma yagouarundi, Lacépède, 1809) adultos. MSc Thesis, Universidade Federal de Viçosa.
Soldati, A. M. M., Ferreira, M. J. D., Lopes, D. S., Anjos, L. R., and Benjamin, L. A. (2014). Feeding patterns of bats captured in two different environments. In ‘Anais do II International Symposium of Ecology and Evolution’. pp. 19–19. (Viçosa.)
Speakman, J. R., and Racey, P. A. (1986). The influence of body condition on sexual development of male brown long-eared bats (Plecotus auritus) in the wild. J. Zool. 210, 515–525.
| The influence of body condition on sexual development of male brown long-eared bats (Plecotus auritus) in the wild.Crossref | GoogleScholarGoogle Scholar |
Tabosa, L. O., Pedrozo, A. R., Costa, L. M., Vilela, E. L., and Esberard, C. E. L. (2013). Efeito da sazonalidade sobre a condição corpórea de Anoura geoffroyi Gray, 1838 no estado do Rio de Janeiro. In ‘Anais do MastoSerra’. pp. 34–34. (Rio de Janeiro.)
Van Der Pijl, L. (1957). The dispersal of plants by bats (Chiropterochory). Acta Bot. Neerland. 6, 291–315.
| The dispersal of plants by bats (Chiropterochory).Crossref | GoogleScholarGoogle Scholar |
Vasconcelos, P. F., Falcão, L. A. D., Cabadilha, K. S., and Santo, M. M. E. (2013). Efeito da sazonalidade na condição corporal de Artibeus panirostris Spix, 1858 e Carollia perspicillata (Linnaeus, 1758). In ‘Anais do Encontro Brasileiro para o Estudo de Quiropteros’. (Ed. Sociedade Brasileira para o Estudo de Quirópteros.) pp. 215–217. (Sociedade Brasileira para o Estudo de Quirópteros: Brasília.)
Veloso, H. P., Rangel Filho, A. L. R., and Lima, J. C. A. (1991). ‘Classificação da vegetação brasileira, adaptada a um sistema universal.’ Vol. 1. (Instituto Brasileiro de Geografia e Estatistica: Rio de Janeiro.)
Wilson, D. E. (1971). Ecology of Myotis nigricans (Mammalia: Chiroptera) on Barro Colorado Island, Panama Canal Zone. J. Zool. 163, 1–13.
| Ecology of Myotis nigricans (Mammalia: Chiroptera) on Barro Colorado Island, Panama Canal Zone.Crossref | GoogleScholarGoogle Scholar |
Wilson, D. E., and Findley, J. S. (1970). Reproductive cycle of a Neotropical insectivorous bat, Myotis nigricans. Nature 225, 11–55.
| Reproductive cycle of a Neotropical insectivorous bat, Myotis nigricans.Crossref | GoogleScholarGoogle Scholar |
Zortéa, M. (2003). Reproductive patterns and feeding habits of three nectarivorous bats (Phyllostomidae: Glossophaginae) from the Brazilian Cerrado. Braz. J. Biol. 63, 159–168.
| Reproductive patterns and feeding habits of three nectarivorous bats (Phyllostomidae: Glossophaginae) from the Brazilian Cerrado.Crossref | GoogleScholarGoogle Scholar |
