Keywords
reproductive pattern
rainfall
monoestrus.
murciélago
patrón reproductivo
monoestro
Artibeus amplus
Venezuela.
How to Cite
Abstract
Bimodal polyestry is the most common reproductive pattern in tropical bats, and it consists in producing one offspring per female twice a year. Reproductive patterns are closely related to rainfall regimes, frequently occurring twice a year in tropical regions. The goal of our study was to determine the reproductive pattern of the large fruit-eating bat, Artibeus amplus Handley, 1987 in a cave in the Venezuelan Andes inhabited by a large, stable colony. Thus, in this study we describe for the first time this important biological aspect of this unknown Neotropical bat species through the examination of external reproductive characteristics of males (inguinal or scrotal testes) and females (pregnant, lactating, post-lactating), based on 211 individuals (120 males and 91 females) captured between September 2008 and August 2009, in Cueva del Parque Las Escaleras, Estado Táchira, Venezuela. During this period of monthly sampling for a full year, most males displayed large scrotal testes, averaging 10 mm maximum length. The examination of females indicated that although pregnancy was first observed in November 2008, it reached a maximum during January and February 2009. Although adult males with scrotal testes throughout the year could imply that females have more than one pregnancy, our results suggested a seasonally monoestrous reproductive pattern for A. amplus. This study represents the first report of reproductive pattern for this poorly-known Neotropical frugivorous species. The observed monoestrous reproductive pattern supports the existence of synchronization between precipitation and reproduction. This synchronization has been frequently observed in most species of fruit bats. In this study, Artibeus amplus presumably adjust the parturition to anticipate the rainy season, as a strategy that allows maintenance of offspring during high availability of fruits.
References
Baumgarten, J. E., & Vieira, E. M. (1994). Reproductive seasonality and development of Anoura geoffroyi (Chiroptera: Phyllostomidae) in central Brazil. Mammalia, 58, 415-422. DOI: 10.1515/mamm.1994.58.3.415
Bronson, F. H. (1985). Mammalian reproduction: an ecological perspective. Biology of Reproduction, 32, 1-26. DOI: 10.1095/biolreprod32.1.1
Brown, T. (1999). Steroid hormones, overview. In E. Knobil, & D. J. Neill (Eds.), Encyclopedia of Reproduction (Vol. 4, pp. 634-644). San Diego: Academic Press.
Brunet-Rossinni, A. K., & Wilkinson, G. S. (2009). Methods for age estimation and the study of senescence in bats. In T. H. Kunz, & S. Parsons (Eds.), Ecological and behavioral methods for the study of bats (2nd ed, pp. 315-325), Baltimore: The Johns Hopkins University Press.
Dinerstein, E. (1986). Reproductive ecology of fruit bats and the seasonality of fruit production in a Costa Rican cloud forest. Biotropica, 18, 307-318. DOI: 10.2307/2388574
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 Biology, 75, 320-325. DOI: 10.1016/j.mambio.2009.04.004
Estrada, A., & Coates-Estrada, R. (2001). Species composition and reproductive phenology of bats in a tropical landscape at Los Tuxtlas. Journal of Tropical Ecology, 17, 627-646. DOI: 10.1017/S026646740100147X
Fleming, T. H. (1971). Artibeus jamaicensis: delayed embryonic development in a Neotropical bat. Science, 171, 402-404. DOI: 10.1126/science.171.3969.402
Fleming, T. H., Hooper, E. T., & Wilson, D. E. (1972). Three Central American bat communities: structure, reproductive cycles, and movement patterns. Ecology, 53, 555-569.
Fleming, T. H. (1988). The short-tailed fruit bat. A study in plant-animal interactions. Wildlife Behavior and Ecology Series. Chicago: The University of Chicago Press.
Handley, C. O. Jr. (1987). New species of mammals from Northern South America: fruit-eating bats, Genus Artibeus Leach. In B. D. Patterson, & R. M. Timm (Eds.), Studies in Neotropical Mammalogy: essays in honor of Philip Hershkovitz (pp. 163-172). Fieldiana: Field Museum of Natural History.
Hastenrath, S. (1984). Interannual variability and annual cycle: mechanisms of circulation and climate in the tropical Atlantic sector. Monthly Weather Review, 112, 1097-1106. DOI: 10.1175/1520-0493(1984)112%3C1097:IVAACM%3E2.0.CO;2
Heideman, P. D. (2000). Environmental regulation of reproduction. In E. G. Crichton, & P. H. Krutzsch (Eds.), Reproductive biology of bats (pp. 469-499). Cambridge: Academic Press. DOI: 10.1016/B978-012195670-7/50012-6
Krutzsch, H. P. (2000). Anatomy, physiology and cyclicity of the male reproductive tract. In E. G. Crichton, & P. H. Krutzsch (Eds.), Reproductive biology of bats (pp. 92-155). Cambridge: Academic Press. DOI: 10.1016/B978-012195670-7/50005-9
Kunz, T. H., Hodgkison, R., & Weise, C. (2009). Methods of capturing and handling bats. In T. H. Kunz, & S. Parsons (Eds.), Ecological and behavioral methods for the study of bats (2nd ed., pp. 3-35). Baltimore: Johns Hopkins University Press.
Kunz, T. H., & Weise, C. (2009). Methods and devices for marking bats. In T. H. Kunz, & S. Parsons (Eds.), Ecological and behavioral methods for the study of bats (2nd ed., pp. 36-56). Baltimore: The Johns Hopkins University Press.
Lim, B. K., Genoways, H. H., & Engstrom, M. D. (2003). Results of the Alcoa Foundation-Suriname Expeditions. XII. First record of the giant fruit-eating bat, Artibeus amplus, (Mammalia: Chiroptera) from Suriname with a review of the species. Annals of Carnegie Museum, 72, 99-107.
Linares, O. J. (1998). Mamíferos de Venezuela. Caracas, Venezuela: Sociedad Conservacionista Audubon de Venezuela & British Petroleum.
Loecher, M., & Ropkins, K. (2015). RgoogleMaps and loa: Unleashing R Graphics Power on Map Tiles. Journal of Statistical Software, 63(4), 1-18. Retrieved from http://www.jstatsoft.org/v63/i04/
Martin, L., & Bernard, T. F. (2000). Endocrine regulation of reproduction in bats: The role of circulating gonadal hormones. In E. G. Crichton, & P. H. Krutzsch (Eds.), Reproductive biology of bats (pp. 27-64). Cambridge: Academic Press. DOI: 10.1016/B978-012195670-7/50003-5
McCracken, G. F., & Wilkinson, G. S. (Eds.). (2000). Bat mating systems. Reproductive biology of bats (pp. 321-362). New York, Academic Press. DOI: 10.1016/B978-012195670-7/50009-6
Medellin, R., & Shipper, J. (2009). IUCN Red List Threatened Species (2009): Artibeus amplus. (Electronic-based document). United Kingdom. Retrieved from http://www.iucnredlist.org/apps/redlist/details/2121/0.
Mello, M. A. R., & Fernández, F. A. (2000). Reproductive ecology of the bat Carollia perspicillata (Chiroptera, Phyllostomidae) in a fragment of the Brazilian Atlantic coastal forest. Mammalian Biology, 65, 340-349.
Molina-Chacón, A. J. (1983). Ecología regional de la cuenca alta del río Uribante: contribución a un método para el estudio integral del medio andino venezolano. Tesis de Maestría, Facultad de Ciencias Forestales y Ambientales. Universidad de Los Andes, Mérida.
Molinari, J., & Soriano, P. (2014). Breeding and age-structure seasonality in Carollia brevicauda and other frugivorous bats (Phyllostomidae) in cloud forests in the Venezuelan Andes. Therya, 5, 81-109. DOI: 10.12933/therya-14-179
Monasterio, M., & Reyes, S. (1980). Diversidad ambiental y variación de la vegetación en los páramos de los Andes Venezolanos. M. Monasterio (Ed.), Estudios Ecológicos en los Páramos Andinos (pp. 47-91). Mérida: Editorial de la Universidad de Los Andes.
Opler, P. A., Frankie, G. W., & Baker, H. G. (1980). Comparative phenological studies of treelet and shrub species in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology, 68, 167-188. DOI: 10.2307/2259250
Ortega, J., & Castro-Arellano, I. (2001). Artibeus jamaicensis. Mammalian Species, 662, 1-9. DOI: 10.1644/1545-1410(2001)662%3C0001:AJ%3E2.0.CO;2
R Core Team. (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Retrieved from https://www.R-project.org/
Racey, P. A. (1982). Ecology of bat reproduction. In T. H. Kunz (Ed.), Ecology of bats (pp. 57-104). New York: Plenum Press. DOI: 10.1007/978-1-4613-3421-7_2
Racey, P. A. (2009). Reproductive assessment of bats. In T.H. Kunz, & S. Parsons (Eds.), Ecological and behavioral methods for the study of bats (2nd ed., pp. 249-264). Maryland: The Johns Hopkins University Press.
Racey, P. A., & Entwistle, A. C. (2000). Life-history and reproductive strategies of bats. In E. G. Crichton, & P. H. Krutzsch (Eds.), Reproductive biology of bats (pp. 364-414). New York: Academic Press. DOI: 10.1016/B978-012195670-7/50010-2
Ramoni-Perazzi, P., Muñoz-Romo, M., Chaves, L. F., & Kunz, T. H. (2012). Range prediction for the Giant Fruit-Eating Bat, Artibeus amplus (Phyllostomidae: Stenodermatinae) in South America. Studies on Neotropical Fauna and Environment, 47, 87-103.
Ramoni-Perazzi, P., Ruiz-Ramoni, D., Muñoz-Romo, M., Thielen Engelbertz, D., & Soto Werschitz, I.A. (2014). Some considerations on the conservation status of the giant fruit-eating bat, Artibeus amplus (Phyllostomidae: Stenodermatinae). Interciencia, 39, 354-356.
Ruiz-Ramoni, D. (2010). Patrón reproductivo y dieta del murciélago frugívoro, Artibeus amplus (Chiroptera: Phyllostomidae), en una cueva cercana a Pregonero, Edo. Táchira-Venezuela. (Trabajo Especial de Grado para optar el título de Licenciado en Biología). Departamento de Biología, Facultad de Ciencias, Universidad de Los Andes, Mérida.
Ruiz-Ramoni, D., Muñoz-Romo, M., Ramoni-Perazzi, P., Aranguren, Y., & Fermin, G. (2011). Folivory in the giant fruit-eating bat Artibeus amplus (Phyllostomidae): a non-seasonal phenomenon. Acta Chiropterologica, 13, 195-199.
Sikes, R.S., Gannon, W.L. & the Animal Care and Use Committee of the American Society of Mammalogists. (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92, 235-253. DOI: 10.1644/10-MAMM-F-355.1
Sobral, G. L., & Machado, I. C. (2001). Fruiting phenology and seed dispersal syndromes in caatinga, a tropical dry forest in the northeast of Brazil. Journal of Tropical Ecology, 17, 303-321.
Sosa, M. (1991). Relaciones ecológicas entre el murciélago Glossophaga longirostris y las cactáceas columnares en el bolsón árido de Lagunillas, Mérida, Venezuela (Tesis para optar el título de Licenciado en Biología, Departamento de Biología). Facultad de Ciencias, Universidad de Los Andes, Mérida.
Sosa, M., & Ramoni-Perazzi, P. (1995). Patrón reproductivo de Artibeus jamaicensis Leach, 1821 y A. lituratus (Olfers,1818) (Chiroptera: Phyllostomidae) en una zona árida de Los Andes venezolanos. Revista Brasileira de Biología, 55, 705-713.
Sosa, M., & Soriano, P. (1996). Resource availability, diet and reproduction in Glossophaga longirostris (Mammalia: Chiroptera) in an arid zone of the Venezuelan Andes. Journal of Tropical Ecology, 12, 805-818. DOI: 10.1017/S0266467400010063
Speakman, J. R. 2008. The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 375-398. DOI: 10.1098/rstb.2007.2145
Taylor, M. A., & Alfaro, E. J. (2005). Central America and the Caribbean, Climate of. In J. E. Oliver (Ed.), Encyclopedia of World Climatology. Encyclopedia of Earth Sciences Series (pp. 183-1988). Holanda: Springer Dordrecht.
Vela-Vargas, I. M. (2013). Variaciones en la fenología reproductiva de las especies de murciélagos en dos sistemas ganaderos: efecto de la disponibilidad de recurso (Tesis de Maestría en Ciencias Biológicas). Facultad de Ciencias, Pontificia Universidad Javeriana, Bogotá.
Willig, M. R. (1985). Reproductive patterns of bats from Caatingas and Cerrado Biomes in Northeast Brazil. Journal of Mammalogy, 66, 668-681. DOI: 10.2307/1380793
Wilson, D. E. (1979). Reproductive patterns. In R. J. Baker, J. K. Jones, Jr., & D. C. Carter (Eds.), Biology of Bats of the New World Family Phyllostomatidae, Part III. Special Publications of The Museum, Texas Tech University, 16, 317-378.
Wilson, D. E., Handley, C. O., Jr., & Gardner, A. L. (1991). Reproduction on Barro Colorado Island. In C. O. Jr. Handley, D. E., Wilson, & A. L., Gardner (Eds.), Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panama (pp. 43-52). Washington, D. C.:Smithsonian Contributions to Zoology 511, Smithsonian Institution Press.
Zortéa, M. (2003). Reproductive patterns and feeding habits of three nectarivorous bats (Phyllostomidae: Glossophaginae) from the Brazilian Cerrado. Brazilian Journal of Biology, 63, 159-168. DOI: 10.1590/S1519-69842003000100020
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