SciELO - Scientific Electronic Library Online

 
vol.39 issue6Musculoskeletal ultrasonography of the elbow joint in dogs: applicability and evaluation protocolErratum author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

Share


Pesquisa Veterinária Brasileira

Print version ISSN 0100-736XOn-line version ISSN 1678-5150

Pesq. Vet. Bras. vol.39 no.6 Rio de Janeiro June 2019  Epub July 18, 2019

http://dx.doi.org/10.1590/1678-5150-pvb-5866 

ANIMAL MORPHOPHYSIOLOGY

Seasonal influence on testicular morphophysiological parameters of bat Carollia perspicillata in fragments of the Atlantic Forest, northeastern Brazil

Influência sazonal sobre os parâmetros morfofisiológicos testiculares de Carollia perspicillata (Chiroptera: Phyllostomidae) em fragmentos florestais de Mata Atlântica, Nordeste do Brasil

Maria J.G. Arandas2  * 
http://orcid.org/0000-0002-7504-6199

Álvaro A.C. Teixeira2 

Valéria W. Teixeira2 

Fabricya R. Silva2 

Ketsia S.N. Marinho2 

Nivaldo B. Lima Junior2 

Francisco C.A.A. Júnior3 

Katharine R.P. Santos3 

2 Departamento de Morfologia e Fisiologia Animal, Universidade Federal Rural de Pernambuco (UFRPE), Rua Dom Manoel de Medeiros s/n, Dois Irmãos, Recife, PE 52171-900, Brazil.

3 Núcleo de Biologia, Centro Acadêmico de Vitória (CAV), Universidade Federal de Pernambuco (UFPE), Rua Alto do Reservatório s/n, Bela Vista, Vitória de Santo Antão, PE 55608-680, Brazil.

ABSTRACT:

Bats belong to the order Chiroptera, family Phyllostomidae, and present a wide diversity of reproductive strategies. However, information on the reproductive biology of male bats is scarce, mainly in the Northeast Region of Brazil. Thus, this study evaluated the seasonal testicular histomorphometry of the bat Carollia perspicillata in fragments of the Atlantic Forest in Pernambuco state. To this end, adult males were collected, euthanized for removal of the testicles, and later submitted to a routine histological technique. Histomorphometric analysis included assessment of the areas of tubular and intertubular compartment occupation, as well as quantification of spermatocytes, rounded spermatids, elongated spermatids, and Sertoli and Leydig cells. Results indicated that this bat species presents reproductive seasonality, because significantly higher averages of the testicular parameters were observed in the rainy season, which is a period of greater availability of food resources. Such inferences indicate that there is a synchrony between peak spermatogenesis and hormonal inversion in the months of high precipitation; furthermore, a higher carrying capacity of the Sertoli cells is noted. C. perspicillata males possibly present greater sperm and androgenic activity in the rainy season, associated with increased tubular area and number of spermatogenic cells, as well as with the intertubular area and number of Leydig cells, respectively.

INDEX TERMS: Morphophysiology; Carollia perspicillata; Chiroptera; Phyllostomidae; Atlantic Forest; Brazil; bat; climatic factors; histomorphometry; testicles

RESUMO:

Os morcegos pertencem a ordem Chiroptera, família Phyllostomidae, e apresentam ampla diversidade de estratégias reprodutivas. Entretanto, as informações relacionadas à biologia reprodutiva dos machos são escassas, principalmente no Nordeste do Brasil. Dessa forma, o trabalho avaliou a histomorfometria sazonal testicular de Carollia perspicillata em fragmentos de Mata Atlântica de Pernambuco. Para tanto, os machos adultos foram coletados, eutanasiados para a remoção dos testículos, e posteriormente submetidos à técnica histológica de rotina. As análises histomorfométricas avaliaram as áreas de ocupação do compartimento tubular e intertubular, assim como a quantificação dos espermatócitos, espermátides arredondadas, espermátides alongadas, células de Sertoli e de Leydig. Os resultados indicaram que a espécie apresenta sazonalidade reprodutiva, visto que maiores médias significativas dos parâmetros testiculares foram encontradas na estação chuvosa, que é um período de maior disponibilidade de recursos alimentares. Tais inferências indicam que existe uma sincronia entre o pico de espermatogênese e investimento hormonal nos meses de alta precipitação, atrelado a isso, nota-se ainda, uma maior capacidade de suporte das células de Sertoli. Os machos de C. perspicillata possivelmente apresentam uma maior atividade espermática e androgênica na estação chuvosa, associadas ao aumento da área tubular e do número de células espermatogênicas, assim como da área intertubular e do número das células de Leydig, respectivamente.

TERMOS DE INDEXAÇÃO: Morfofisiologia; Carollia perspicillata; Chiroptera; Phyllostomidae; Mata Atlântica; Nordeste do Brasil; fatores climáticos; histomorfometria; morcego; testículo

Introduction

Bats belong to the order Chiroptera, family Phyllostomidae, present a wide diversity of species, and evolved standards and reproductive strategies that correlate to the occurrence area, climate conditions, and food availability (Neuweiler 2000, Zórtea 2003). In tropical regions, bats reproductive events are associated with periods of increased precipitation (Fleming et al. 1972, Lima Junior et al. 2014).

Despite bat diversity, there is limited information on function, physiological control, and cyclicality of spermatogenesis (Krutzsch 2000). Testicular positioning is an aspect commonly reported in studies addressing male bat reproduction, as these organs present seasonal variation between the inguinal and abdominal region (Lima Junior et al. 2014); however, sexual activity cannot be established only with the external morphological features of the gonads, reason why evaluation of the testis morphological parameters can present inferences about the dynamics of gonadal development and species reproductive capacity (Beguelini et al. 2009, 2010, 2011, 2013a, 2013b, 2013c, 2013d, 2014, 2015, 2016, Morais et al. 2013a, 2013b, 2013c, 2014a, 2014b, Lima Junior et al. 2014, Farias et al. 2015, Notini et al. 2015).

Bats of the Phyllostomidae family are present in temperate and tropical areas, with records of variable reproductive strategies, including male reproductive cyclicality during the whole year (Handley Junior et al. 1991, Zortéa 2003, Oliveira et al. 2009, Duarte & Talamoni 2010, Notini et al. 2015). The species Carollia perspicillata (Linnaeus, 1758) belongs to a family widely distributed throughout Brazil, with preferably frugivorous food habit, and thus of great importance for seed dispersion (Charles-Dominique 1991, Mello et al. 2004). Regarding the reproductive biology, studies have indicated bimodal polyestry as the predominant reproductive cycle; their spermatogenesis show ultra-structural features similar to those of other species of the Phyllostomidade family (Mello et al. 1999, Mello & Fernandez 2000, Beguelini et al. 2014).

However, there are few or no studies addressing the seasonal testicular histomorphometry of these bats. Thus, this article evaluated the testicular histomorphometry of the bat Carollia perspicillata in the dry and rainy seasons in fragments of the Atlantic Forest in Pernambuco state, Brazil.

Materials and Methods

Area of study. The study was conducted in fragments of the Atlantic Forest in the municipality of Sirinhaém (08o 35’27” S; 35o06’58” W), Pernambuco state - submontane and montane, dense ombrophilous (open and seasonal semi-deciduous) forest (Veloso et al. 1991).

Animal collection. Adult male bats (Carollia perspicillata, Chiroptera: Phyllostomidae) were captured monthly, during three consecutive nights between 5 PM and 5 AM, using mist nets, from September 2008 to October 2009.

Animals were captured using mist nets (12x3m) authorized by the Chico Mendes Institute of Biodiversity Conservation (ICMBio) and the Biodiversity Information and Authorization System (SISBIO) (no. 2800740). The study was approved by the Ethics Committee on Animal Use (CEUA) of the Federal University of Pernambuco (UFPE) under protocol no. 23076.037360/2014-92.

Meteorological data and weather stations. The dry and rainy seasons were defined by the National Institute of Meteorology (INMet 2008/2009) as per analysis of temperature, humidity and rainfall (Table 1). Two groups were considered: dry season (September to February) and rainy season (March to August).

Table 1. Monthly averages of precipitation, air temperature and humidity determined by the National Institute of Meteorology (INMET) in a fragment of the Atlantic Forest, Pernambuco state, Brazil 

Month Year Monthly averages
Precipitation (mm) Temperature (oC) Humidity (%)
September 2008 47.6 25.3 78
October 2008 53.6 26.2 75
November 2008 16.0 26.9 69
December 2008 18.3 27.2 69
January 2009 85.2 27.3 70
February* 2009 376.1 26.5 79
March 2009 142.8 27.2 76
April 2009 351.8 26.4 83
May 2009 410.1 25.8 88
June 2009 333.0 25.0 86
July 2009 386.8 24.6 86
August 2009 290.2 24.6 82

*Although rainfall was high, it was concentrated in few days, which were followed by dry days, but the temperature patterns were similar to those of the dry season (APAC 2009).

Reproductive stage. Adult males (n=60) were classified on the basis of testicular position: descending testis (located in the inguinal region) and non-descending testis (located in the abdominal region) (Gannon & Willig 1992).

Euthanasia. The animals selected for histomorphometric analysis were anesthetized with sodium pentobarbital at a concentration of 40mg kg-1 intraperitoneally, followed by a potassium chloride saturated solution at 40mg/kg-1.

Histomorphometric and statistical analyses. A total of 26 adult males, comprising at the most two bats per month, were randomly selected according to the two established groups as follows: dry season (n=13) and rainy season (n=13).

After surgical incision from the abdominal region to the inguinal region, the testes were removed and had their tissues fixed in 10% neutral buffered formalin (NBF), routinely processed for histology, and embedded in paraffin (Behmer et al. 1976, Rieder & Schmidt 1987). 5μm-thick sections were obtained, stained with hematoxylin and eosin (HE), and analyzed under optical microscopy.

Histological slides were photographed with a total of 100X and 400X magnification using the ScopePhoto software coupled to a camera positioned between the optical microscope and the computer. Thus, 10 photomicrographs were used per animal at each magnification increase.

Testicular histomorphometric analysis was performed using the ImageJ 1.44 software. The following parameters were assessed: number spermatocytes, rounded spermatids, elongated spermatids, and Leydig and Sertoli cells with 400X magnification, as well as percentage of tubular compartment and intertubular compartment occupation areas with 100X magnification.

Variables were submitted to Student’s t-test and processed using the Statistical Package for the Social Sciences 15.0 software (SPSS Inc., Chicago, IL, USA) for comparison between data for the dry and rainy seasons. Values were considered statistically significant when p<0.05.

Results

During the studied period, 60 Carollia perspicillata males were captured, 25 in the dry season, of which 80% (n=20) showed descendent testes and 20% (n=5) had non-descending testes, and 35 in the rainy season, of which 65.71% (n=23) presented descendent testes and 34.29% (n=12) showed non-descending testes (Table 2).

Table 2. Relative frequency (RF) of Carollia perspicillata males with descending and non-descending testes in the dry and rainy seasons in a fragment of the Atlantic Forest, Pernambuco state, Brazil 

Dry season Rainy season
RF (%) N RF (%) N
Descending testis 80.00 20 65.71 23
Non-descending testis 20.00 5 34.29 12
Total 100 25 100 35

N= number of individuals.

Testicular histological results indicated that Carollia perspicillata males with descending and non-descending testes observed in the dry and rainy seasons showed Sertoli cells of the spermatogenic lineage at different stages of maturation (spermatogonia, spermatocytes, rounded and elongated spermatids), as well as Leydig cells, regardless of testicular position (Fig.1).

Fig.1. (A) Testis in the dry season, (B) testis in the wet season. Note the spermatogonia (yellow arrow), spermatocytes (black arrow), rounded spermatids (arrowhead), elongated spermatids (two-headed arrows), and Leydig (asterisks) and Sertoli (blue arrow) cells. HE, obj.40x, bar=20μm. 

Testicular histomorphometric analysis showed statistically significant differences with respect to tubular compartment occupation area (p<0.001), intertubular compartment occupation area (p<0.001) and number of spermatocyte (p<0.001), rounded spermatids (p<0.001), elongated spermatids (p<0.001), and Sertoli (p<0.001) and Leydig (p<0.001) cells, with the highest averages observed in the rainy season (Table 3).

Table 3. Mean and standard deviation of the areas of tubular compartment (TCOA) intertubular compartment (ITCOA) occupation, quantification of spermatocytes (SPC), rounded spermatids (RS), elongated spermatids (ES), and Sertoli (SC) and Leydig (LC) cells of Carollia perspicillata testes in the dry and rainy seasons in a fragment of the Atlantic Forest, Pernambuco state, Brazil 

Parameter Rainy season Dry season p-value
TCOA % 64.61 ± 4.51b 58.83 ± 7.52a <0.001
ITCOA % 18.75 ± 4.15b 13.87 ± 2.77a <0.001
SPC 36.74 ± 6.29b 21.89 ± 3.68a <0.001
RS 40.38 ± 6.39b 25.86 ± 4.26a <0.001
ES 46.77 ± 15.48b 28.49 ± 7.04a <0.001
SC 14.10 ± 3.09b 11.29 ± 2.38a <0.001
LC 36.89 ± 8.74b 24.31 ± 5.61a <0.001

a, b Different letters in the same line are statistically different by the Student’s t-test (p<0.05).

Discussion

A higher proportion of male bats with descending testes was observed in both seasons; however, the external reproductive characteristics were limited, impairing verification of sexual activity. Recently, a study conducted at the same site of the present research reported that Phyllostomus discolor male bats present spermatogenic activity regardless of testis position (Lima Junior et al. 2014). Thus, studies performing testicular histomorphometric analysis become relevant to establish the reproductive dynamics of bats (Morais et al. 2013a, 2013b, 2013c, 2014a, 2014b, Farias et al. 2015, Lima Junior et al. 2014, Notini et al. 2015). Associated with this information, histology of Carollia perspicillata testis presents morphological characteristics similar to those described for other bat species (Beguelini et al. 2009, 2011, Bordignon & França 2012).

The higher testicular histomorphometric averages observed in the rainy season indicate an investment in both spermatogenesis and hormone production. These characteristics evidenced the reproductive strategy of this species in generating viable spermatozoa for mating during the months of greater precipitation; in addition, this species presents synchrony of spermatogenesis with the period of greater availability of food resources.

Thus, the larger sperm production may be synchronized with the greater sexual receptivity of females, because Carollia perspicillata bats are characterized by polygynous mating system with harem formation (Mello & Fernandez 2000), to which a greater androgenic and spermatogenic investment in the rainy season is essential. These data are associated with the reproductive characteristics of female bats in areas of the Atlantic Forest in the Southeastern Region of Brazil, because there is simultaneity of the reproductive peaks and the rainy season, which is the most favorable period of the year due to the greater availability of food resources (Mello et al. 1999, Mello & Fernandez 2000).

In addition, it is noteworthy the importance of testosterone and Sertoli cells in the maintenance of C. perspicillata spermatogenic lineage, especially evidenced by the process of spermatogenesis involving a series of complex biochemical, molecular and cellular events (Mruk & Cheng 2004), and depending on the bat species, Sertoli cells are essential for reproduction, mainly because of the support functions of germ cells, nutrition, and growth factors, as well as formation of the blood-testis barrier, thus providing greater protection to spermatozoa under development (Crichton 2000, Griswold & Skinner 2004, Fijak & Meinhardt 2006).

Conclusion

Seasonality influences the testicular morphological and physiological parameters of Carollia perspicillata male bats, as evidenced by the increased tubular and intertubular compartment occupation areas, and the increased number of spermatogenic, Leydig and Sertoli cells in the rainy season, suggesting that these bats present greater sexual activity in this period.

Acknowledgements

The authors are grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES) for the Master’s degree scholarship provided to the first author.

References

APAC 2009. Monitoramento Pluviométrico. Agência Pernambucana de Águas e Clima, Governo do Estado de Pernambuco, PE. Available at <Available at http://www.apac.pe.gov.br/meteorologia/monitoramento-pluvio.php# > Accessed on Nov. 21, 2018. [ Links ]

Beguelini M.R., Puga C.C.I., Taboga S.R. & Morielle-Versute E. 2011. Ultrastructure of spermatogenesis in the white-lined broad-nosed bat, Platyrrhinus lineatus (Chiroptera: Phyllostomidae). Micron 42(6):586-599. <http://dx.doi.org/10.1016/j.micron.2011.02.004> <PMid:21458280> [ Links ]

Beguelini M.R., Puga C.C., Morielle-Versute E. & Taboga S.R. 2016. Comparative analysis of the male reproductive accessory glands of bats Noctilioa lbiventris (Noctilionidae) and Rhynchonycterisnaso (Emballonuridae). J. Morphol. 277(11):1459-1468. <http://dx.doi.org/10.1002/jmor.20587> <PMid:27481105> [ Links ]

Beguelini M.R., Moreira P.R.L., Faria K.C., Marchesin S.R.C. & Morielle-Versute E. 2009. Morphological characterization of the testicular cells and seminiferous epithelium cycle in six species of neotropical bats. J. Morphol. 270(8):943-953. <http://dx.doi.org/10.1002/jmor.10731> <PMid:19248152> [ Links ]

Beguelini M.R., Sergio B.F.S., Leme F.L.J., Taboga S.R. & Morielle-Versute E. 2010. Morphological and morphometric characteristics of the epididymis in the Neotropical bats Eumops glaucinus and Molossus molossus (Chiroptera: Molossidae). Chirop. Neotrop. 16(2):769-779. [ Links ]

Beguelini M.R., Bueno L.M., Caun D.L., Taboga S.R. & Morielle-Versute E. 2014. Ultrastructure of spermatogenesis in the short-tailed fruit bat, Carollia perspicillata (Chiroptera: Phyllostomidae: Carollinae). J. Morphol. 275(1):111-123. <http://dx.doi.org/10.1002/jmor.20202> <PMid:24142890> [ Links ]

Beguelini M.R., Goes R.M., Rahal P., Morielle-Versute E. & Taboga S.R. 2015. Impact of the processes of total testicular regression and recrudescence on the epididymal physiology of the bat Myotis nigricans (Chiroptera: Vespertilionidae). Plos One 10(6):e0128484. <http://dx.doi.org/10.1371/journal.pone.0128484> <PMid:26057377> [ Links ]

Beguelini M.R., Puga C.C.I., Martins F.F., Betoli A.H.S., Taboga S.R. & Morielle-Versute E. 2013a. Morphological variation of primary reproductive structures in males of five families of neotropical bats. Revta Anatom. Rec. 296(1):156-167. <http://dx.doi.org/10.1002/ar.22613> <PMid:23117997> [ Links ]

Beguelini M.R., Puga C.C.I., Taboga S.R. & Morielle-Versute E. 2013b. Annual reproductive cycle of males of the flat-faced fruit-eating bat, Artibeus planirostris (Chiroptera: Phyllostomidae). General Comp. Endocrinol. 185:80-89. <http://dx.doi.org/10.1016/j.ygcen.2012.12.009> <PMid:23356978> [ Links ]

Beguelini M.R., Goes R.M., Taboga S.R. & Morielle-Versute E. 2013c. 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. Develop. 26(6):834-846. <http://dx.doi.org/10.1071/RD13109> <PMid:23830483> [ Links ]

Beguelini M.R., Taboga S.R. & Morielle-Versute E. 2013d. Ultrastructural characteristics of the spermatogenesis during the four phases of the annual reproductive cycle of the black Myotis bat, Myotis nigricans (Chiroptera: Vespertilionidae). Microsc. Res. Techniq. 76(10):1035-1049. <http://dx.doi.org/10.1002/jemt.22264> <PMid:23857678> [ Links ]

Behmer O.A., Tolosa E.M.C. & Freitas Neto A.G. 1976. Manual de Técnicas para Histologia Normal e Patológica. Edart, Universidade de São Paulo, São Paulo. 239p. [ Links ]

Bordignon M.O. & França A.O. 2012. Reproduction of the greater bulldog bat Noctilio leporinus (Chiroptera: Noctilionidae) in a mangrove area in southern Brazil. Biota Neotropica 12(4):62. <http://dx.doi.org/10.1590/S1676-06032012000400006> [ Links ]

Charles-Dominique P. 1991. Feeding strategy and activity budget of the frugivorous bat Carollia perspicillata (Chiroptera: Phyllostomidae) in French Guiana. J. Trop. Ecol. 7(2):243-256. <http://dx.doi.org/10.1017/S026646740000540X> [ Links ]

Crichton E.G. 2000. Sperm storage and fertilization, p.295-320. In: Crichton E.G. & Krutzsch F.P (Eds), Reproductive Biology of Bats. Academic Press, Boston, MA. <http://dx.doi.org/10.1016/B978-012195670-7/50008-4>. [ Links ]

Duarte A.P.G. & Talamoni S.A. 2010. Reproduction of the large fruit-eating bat Artibeus lituratus (Chiroptera: Phyllostomidae) in a Brazilian Atlantic forest area. Mammalian Biol. 75(4):320-325. <http://dx.doi.org/10.1016/j.mambio.2009.04.004> [ Links ]

Farias T.O., Notini A.A., Talamoni S.A. & Godinho H.P. 2015. Testis morphometry and stages of the seminiferous epithelium cycle in an epididymal sperm-storing neotropical vespertilionid, Myotislevis (Chiroptera). Anat. Histol. Embryol. 44(5):361-369. <http://dx.doi.org/10.1111/ahe.12148> <PMid:25258091> [ Links ]

Fijak M. & Meinhardt A. 2006. The testis in immune privilege. Immunol. Rev. 213(1):66-81. <http://dx.doi.org/10.1111/j.1600-065X.2006.00438.x> <PMid:16972897> [ Links ]

Fleming T.H., Hooper E.T. & Wilson D.E. 1972. Three central American bat communities: structure, reproductive cycles and movement patterns. Ecology 53(4):555-569. <http://dx.doi.org/10.2307/1934771> [ Links ]

Gannon M.R. & Willig M.R. 1992. Bat reproduction in the Luquillo Experimental Forest of Puerto Rico. Southwest Naturalist 37(4):414-419. <http://dx.doi.org/10.2307/3671794> [ Links ]

Griswold M.D. & Skinner M.K. 2004. Sertoli Cell Biology. Academic Press, San Diego, CA. 512p. [ Links ]

Handley Junior C.O., Wilson D.E. & Gardner A.L. 1991. Demography and natural history of the common Fruit bat, Artibeus jamaicensis on Barro Colorado Island, Panama. Smithsonian Contribution Zool. 511(511):1-173. <http://dx.doi.org/10.5479/si.00810282.511> [ Links ]

INMet 2018/2019. Instituto Nacional de Meteorologia. Ministério da Agricultura, Pecuária e Abastecimento, Brasília, DF. Available at <Available at http://www.inmet.gov.br/ > Accessed on Nov. 21, 2018. [ Links ]

Krutzsch P.H. 2000. Anatomy, physiology and cyclicity of the male reproductive tract, p.91-155. In: Crichton E.G. & Krutzsch P.H. (Eds), Reproductive Biology of Bats. Academic Press, London. <http://dx.doi.org/10.1016/B978-012195670-7/50005-9> [ Links ]

Lima Júnior N.B.D., Arandas M.J.G., Marinho K.S.D.N., Aguiar Júnior F.C.A., Pontes A.R.M. & Santos K.R.P. 2014. Histomorfometria testicular do morcego Phyllostomus discolor (Chiroptera: Phyllostomidae) em áreas de Mata Atlântica de Pernambuco. Braz. J. Vet. Res. Anim. Sci. 51(3):263-270. <http://dx.doi.org/10.11606/issn.1678-4456.v51i3p263-270> [ Links ]

Mello M.A.R. & Fernandez F.A.S. 2000. Reproduction ecology of the bat Carollia perspicillata (Chiroptera, Phyllostomidae) in a fragment of the Brazilian Atlantic coastal forest. Mammalian Biol. 65:340-349. [ Links ]

Mello M.A.R., Nascimento J.L. & Fernandez F.A.S. 1999. How often should researchers go to the field to conduct demographic studies on Carollia perspicillata? Bat Res. News 40(2):39-41. [ Links ]

Mello M.A.R., Schittini G., Selig P. & Bergallo H.G. 2004. A test of the effects of climate and fruiting of Piper species (Piperaceae) on reproductive patterns of the bat Carollia perspicillata (Phyllostomidae). Acta Chiropterologica 6(2):309-318. <http://dx.doi.org/10.3161/001.006.0209> [ Links ]

Morais D.B., Barros M.S., Freitas M.B.D., Paula T.A.R. & Matta S.L.P. 2014a. Histomorphometric characterization of the intertubular compartment in the testes of the bat Sturniralilium. Anim. Reprod. Sci. 147(3/4):180-186. <http://dx.doi.org/10.1016/j.anireprosci.2014.03.008> <PMid:24793584> [ Links ]

Morais D.B., Barros M.S., Paula T.A.R., Freitas M.B.D., Gomes M.L.M. & 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(7):e101759. <http://dx.doi.org/10.1371/journal.pone.0101759> <PMid:25003782> [ Links ]

Morais D.B., Oliveira L.C., Cupertino M.C., Freitas K.M., Freitas M.B.D., Paula T.A.R. & 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(1):94-101. <http://dx.doi.org/10.1002/jemt.22141> <PMid:23077089> [ Links ]

Morais D.B., Paula T.A.R., Barros M.S., Balarini M.K., Freitas M.B.D. & Matta S.L.P. 2013b. Stages and duration of the seminiferous epithelium cycle in the bat Sturnira lilium. J. Anat. 222(3):372-379. <http://dx.doi.org/10.1111/joa.12016> <PMid:23305159> [ Links ]

Morais D.B., Cupertino M.C., Goulart L.S., Freitas K.M., Freitas M.B.D., Paula T.A.R. & Matta S.L.P. 2013c. Histomorphometric evaluation of the Molossusmolossus (Chiroptera, Molossidae) testis: the tubular compartmentand indices of sperm production. Anim. Reprod. Sci. 140(3/4):268-278. <http://dx.doi.org/10.1016/j.anireprosci.2013.06.003> <PMid:23845822> [ Links ]

Mruk D.D. & Cheng C.Y. 2004. Sertoli-sertoli and sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocrine Rev. 25(5):747-806. <http://dx.doi.org/10.1210/er.2003-0022> <PMid:15466940> [ Links ]

Neuweiler G. 2000. The Biology of Bats. Oxford University Press, Oxford. 310p. [ Links ]

Notini A.A., Farias T.O., Talamoni S.A. & Godinho H.P. 2015. Annual male reproductive activity and stages of the seminiferous epithelium cycle of the large fruit-eating Artibeus lituratus (Chiroptera: Phyllostomidae). Zoologia 32(3):195-200. <http://dx.doi.org/10.1590/S1984-46702015000300003> [ Links ]

Oliveira R.L., Oliveira A.G., Mahecha G.A.B., Nogueira J.C. & Oliveira C.A. 2009. Distribution of estrogen receptors (Era and Erb) and androgen receptor in the testis of big fruit-eating bat Artibeus lituratus is cell-and stage-specific and increases during gonadal regression. General Comp. Endocrinol. 161(2):283-292. <http://dx.doi.org/10.1016/j.ygcen.2009.01.019> <PMid:19523379> [ Links ]

Rieder N. & Schmidt K. 1987. Morphologische Arbeitsmethoden in der Biologie. Wiley-VCH Verlagsgesellschaf, Germany. 223p. [ Links ]

Veloso H.P., Rangel-Filho A.L.R.R. & Lima J.C.A. 1991. Classificação da Vegetação Brasileira, Adaptada a um Sistema Universal. Fundação Instituto Brasileiro de Geografia e Estatística (IBGE), Rio de Janeiro. 82p. [ Links ]

Zortéa M. 2003. Reproductive patterns and feeding habits of three nectarivorous bats (Phyllostomidae: Glossophaginae) from the Brazilian Cerrado. Braz. J. Biol. 63(1):159-168. <http://dx.doi.org/10.1590/S1519-69842003000100020> <PMid:12914427> [ Links ]

Received: November 21, 2018; Accepted: January 02, 2019

*Corresponding author: julianaarandas@hotmail.com

Conflict of interest statement.- The authors declare no competing interests.

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License