Activity patterns of short-tailed fruit bats Carollia Gray, 1838 in a premontane forest of central Peru
DOI:
https://doi.org/10.31687/SaremNMS24.01.6Keywords:
competition, flying mammals, frugivores, nocturnal activity, temporal overlapAbstract
Time partitioning is an understudied mechanism for frugivorous bat species that coexist in competition. We describe activity patterns of Carollia perspicillata (Linnaeus, 1758), Carollia brevicauda (Schinz, 1821), and Carollia benkeithi Solari & Baker, 2006 using time of capture variation in a premontane forest of central Peru. For C. perspicillata, activity patterns of different sexes and seasons (rainy vs. dry) were also compared. We report temporal coincidence (Delta = 0.91) among the three species being more active at the beginning of the night when resources are available. Neither sex nor season changed the activity pattern of C. perspicillata. Evidence suggests that these sympatric species do not reduce competition through time partitioning.
References
Aguiar, L. M., & J. Marinho-Filho. 2004. Activity patterns of nine Phyllostomid bat species in a fragment of the Atlantic Forest in southeastern Brazil. Revista Brasileira de Zoologia 21:385–390. https://doi.org/10.1590/S0101-81752004000200037.
Alviz, A., & J. Pérez-Torres. 2020. A difference between sexes: temporal variation in the diet of Carollia perspicillata (Chiroptera, Phyllostomidae) at the Macaregua cave, Santander (Colombia). Animal Biodiversity and Conservation 43:27–35. https://doi.org/10.32800/abc.2020.43.0027.
Arriaga-Flores, J. C., I. Castro-Arellano, A. Moreno-Valdez, & A. Correa-Sandoval. 2012. Temporal niche overlap of a riparian forest bat assemblage in subtropical Mexico. Revista Mexicana de Mastozoología (Nueva Época) 2:3–17. https://doi.org/10.22201/ie.20074484e.2012.2.1.18.
Bernard, E. 2002. Diet, activity and reproduction of bat species (Mammalia, Chiroptera) in Central Amazonia, Brazil. Revista Brasileira de Zoologia 19:173–188. https://doi.org/10.1590/S0101-81752002000100016.
Blake, J. G., D. Mosquera, B. A. Loiselle, K. Swing, J. Guerra, & D. Romo. 2012. Temporal activity patterns of terrestrial mammals in lowland rainforest of eastern Ecuador. Ecotropica 137:137–146.
Bohlender, E. E., J. Pérez-Torres, N. A. Borray-Escalante, & R. D. Stevens. 2018. Dietary variation during reproduction in Seba's short-tailed fruit bat. Journal of Mammalogy 99:440–449. https://doi.org/10.1093/jmammal/gyx189.
Bonaccorso, F. J., et al. 2007. Evidence for exploitative competition: comparative foraging behavior and roosting ecology of short-tailed fruit bats (Phyllostomidae). Biotropica 39:249–256. https://doi.org/10.1111/j.1744-7429.2006.00251.x.
Borray-Escalante, N. A., J. Pérez-Torres, & M. E. Castro-Benitez. 2022. Nutritional ecology of Carollia perspicillata (Chiroptera: Phyllostomidae): relationship between the preference and the nutritional content of fruits. Acta Chiropterologica 24:177–185. https://doi.org/10.3161/15081109ACC2022.24.1.014.
Brown, J. H. 1968. Activity patterns of some Neotropical bats. Journal of Mammalogy 49:754–757. https://doi.org/10.2307/1378737.
Castillo-Figueroa, D. 2022. Does Bergmann's rule apply in bats? Evidence from two neotropical species. Neotropical Biodiversity 8:200–221. https://doi.org/10.1080/23766808.2022.2075530.
Castillo-Figueroa, D., D. Martínez-Medina, & M. E. Rodríguez-Posada. 2021. Activity patterns of medium and large mammals in two savanna ecosystems in the Colombian Llanos. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales 45:1071–1083. https://doi.org/10.18257/raccefyn.1461.
Castro-Arellano, I., S. J. Presley, M. R. Willig, J. M. Wunderle, & L. N. Saldanha. 2009. Reduced-impact logging and temporal activity of understorey bats in lowland Amazonia. Biological Conservation 142:2131–2139. https://doi.org/10.1016/j.biocon.2009.04.013.
Castro-Arellano, I., T. E. Lacher Jr., M. R. Willig, & T. F. Rangel. 2010. Assessment of assemblage-wide temporal niche segregation using null models. Methods in Ecology and Evolution 1:311–318. https://doi.org/10.1111/j.2041-210X.2010.00031.x.
Charles-Dominique, P. 1991. Feeding strategy and activity budget of the frugivorous bat Carollia perspicillata (Chiroptera: Phyllostomidae) in French Guiana. Journal of Tropical Ecology 7:243–256. https://doi.org/10.1017/S026646740000540X.
Chase, J. M., & M. A. Leibold (eds.). 2003. Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago.
Cody, M. L., & J. W. Diamond (eds.). 1975. Ecology and evolution of communities. Belknap, Harvard University Press, Massachusetts.
Davis, W. B., & J. R. Dixon. 1976. Activity of bats in a small village clearing near Iquitos, Peru. Journal of Mammalogy 57:747–749. https://doi.org/10.2307/1379444.
Dekeukeleire, D., R. Janssen, A. J. Haarsma, T. Bosch, & J. Van Schaik. 2016. Swarming behaviour, catchment area and seasonal movement patterns of the Bechstein's bats: implications for conservation. Acta Chiropterologica 18:349–358. https://doi.org/10.3161/15081109ACC2016.18.2.004.
Díaz, M. M., L. F. Aguirre, & R. M. Barquez. 2011. Clave de identificación de los murciélagos del cono sur de Sudamérica. Centro de estudios de Biología Teórica y Aplicada, Cochabamba.
Dinerstein, E. 1986. Reproductive ecology of fruit bats and the seasonality of fruit production in a Costa Rican cloud forest. Biotropica 18:307–318. https://doi.org/10.2307/2388574.
Donati, G., & S. M. Borgognini-Tarli. 2006. From darkness to daylight: cathemeral activity in primates. Journal of Anthropological Sciences 84:7–32.
Erkert , H. G.1982. Ecological aspects of bat activity rhythms. Ecology of bats (T. H. Kunz, ed.). Springer, Massachusetts.
Erkert , H. G. 2000. Bats, flying nocturnal mammals. Activity patterns in small mammals (S. Halle & N. C. Stenseth, eds.). Springer Berlin, Heidelberg.
Fleming, T. H. 1985. Coexistence of five sympatric Piper (Piperaceae) species in a tropical dry forest. Ecology 66:688–700. https://doi.org/10.2307/1940530.
Fleming, T. H. (ed.). 1988. The short-tailed fruit bat: a study in plant-animal interactions. University of Chicago Press, Chicago.
Fleming, T. H. 1991. The relationship between body size, diet, and habitat use in frugivorous bats, genus Carollia (Phyllostomidae). Journal of Mammalogy 72:493–501. https://doi.org/10.2307/1382132.
Fleming, T. H., & E. R. Heithaus. 1986. Seasonal foraging behavior of the frugivorous bat Carollia perspicillata. Journal of Mammalogy 67:660–671. https://doi.org/10.2307/1381127.
Gardner, A. L. (ed.). 2008. Mammals of South America, Volume 1: marsupials, xenarthrans, shrews, and bats. University of Chicago Press, Chicago.
Gaynor, K. M., C. E. Hojnowski, N. H. Carter, & J. S. Brashares. 2018. The influence of human disturbance on wildlife nocturnality. Science. 360:1232–1235. https://doi.org/10.1126/science.aar712.
Halle, S., & N. C. Stenseth (eds.). 2000. Activity patterns in small mammals: an ecological approach. Springer Science & Business Media, Berlin.
Heithaus, E. R., & T. H. Fleming. 1978. Foraging movements of a frugivorous bat, Carollia perspicillata (Phyllostomatidae). Ecological Monographs 48:127–143. https://doi.org/10.2307/2937296.
Heithaus, E. R., T. H. Fleming, & P. A. Opler. 1975. Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology 56:841–854. https://doi.org/10.2307/1936295.
Herbst, L. H. 1986. The role of nitrogen from fruit pulp in the nutrition of the frugivorous bat Carollia perspicillata. Biotropica 18:39–44. https://doi.org/10.2307/2388360.
Holdridge, L. R. 1967. Life zone ecology. Tropical Science Center, San José.
Kemenesi, G., et al. 2015. Genetic characterization of a novel picornavirus detected in Miniopterus schreibersii bats. Journal of General Virology 96:815–821. https://doi.org/10.1099/jgv.0.000028.
Kronfeld-Schor, N., & T. Dayan. 2003. Partitioning of time as an ecological resource. Annual Review of Ecology, Evolution, and Systematics 34:153–181. https://doi.org/10.1146/annurev.ecolsys.34.011802.132435.
Kunz, T. H., C. Wemmer, & V. Hayssen. 1996. Sex, age and reproductive condition. Measuring and monitoring biological diversity: standard methods for mammals (D. E. Wilson, F. R. Cole, J. D. Nichols, R. Rudran, & M. S. Foster, eds.). Smithsonian Institution Press, Washington D.C.
La Val, R. K. 1970. Banding returns and activity periods of some Costa Rican bats. The Southwestern Naturalist 15:1–10. https://doi.org/10.2307/3670196.
Macarthur, R., & R. Levins. 1967. The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist 101:377–385. http://dx.doi.org/10.1086/282505.
Mancina, C. A., & I. Castro-Arellano. 2013. Unusual temporal niche overlap in a phytophagous bat ensemble of western Cuba. Journal of Tropical Ecology 29:511–521. https://www.jstor.org/stable/43831681.
Marcelo-Peña, J. L., & C. Reynel. 2014. Patrones de diversidad y composición florística de parcelas de evaluación permanente en la selva central de Perú. Rodriguésia 65:35–47. https://doi.org/10.1590/S2175-78602014000100003.
Marinho-Filho, J. S., & I. Sazima. 1989. Activity patterns of six Phyllostomid bat species in southeastern Brazil. Revista Brasileira de Biologia 49:777–782.
Mello, M. A., E. K. Kalko, & W. R. Silva. 2013. Effects of moonlight on the capturability of frugivorous phyllostomid bats (Chiroptera: Phyllostomidae) at different time scales. Zoologia (Curitiba) 30:397–402. https://doi.org/10.1590/S1984-46702013000400005.
Mello, M. A., G. M. Schittini, P. Selig, & H. G. Bergallo. 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 6:309–318. https://doi.org/10.3161/001.006.0209.
Miller, R. S. 1967. Pattern and process in competition. Advances in Ecological Research 4:1–74. https://doi.org/10.1016/S0065-2504(08)60319-0.
Mistlberger, R. E., & M. C. Antle. 2011. Entrainment of circadian clocks in mammals by arousal and food. Essays in Biochemistry 49:119–136. https://doi.org/10.1042/bse0490119.
Montaño-Centellas, F., et al. 2015. Community and species–level responses of phyllostomid bats to a disturbance gradient in the tropical Andes. Acta Oecologica 62:10–17. https://doi.org/10.1016/j.actao.2014.11.002.
Moratelli, R., & A. L. Peracchi. 2007. Morcegos (Mammalia, Chiroptera) do Parque Nacional da Serra dos Órgãos. Ciência e Conservação na Serra dos Órgãos (C. Cronemberger & E. B. Viveiros de Castro, eds.). Instituto Chico Mendes para la Conservación de la Biodiversidad, Brasilia.
Ortêncio-Filho, H., N. R. Reis, & C. V. Minte-Vera. 2010. Time and seasonal patterns of activity of phyllostomid in fragments of a stational semidecidual forest from the Upper Paraná River, Southern Brazil. Brazilian Journal of Biology 70:937–945. https://doi.org/10.1590/S1519-69842010000500004.
Pacheco, V., & S. Solari. 1997. Manual de los murciélagos peruanos con énfasis en las especies hematófagas. Organización Panamericana de la Salud, Lima.
Pedro, W. A., & V. A. Taddei. 2002. Temporal distribution of five bat species (Chiroptera, Phyllostomidae) from Panga Reserve, south-eastern Brazil. Revista Brasileira de Zoologia 19:951–954. https://doi.org/10.1590/S0101-81752002000300033.
Pedrozo, A. 2014. Os morcegos frugívoros Carollia perspicillata e Sturnira lilium apresentam distribuição de atividade similar durante a noite? Uma análise local e regional. Dissertação de Mestrado, Universidade Federal Rural do Rio de Janeiro. Rio de Janeiro, Brazil.
Pellón, J. J., J. Rivero, M. Williams, & M. Flores. 2021. Trophic relationships within the genus Carollia (Chiroptera, Phyllostomidae) in a premontane forest of central Peru. Journal of Mammalogy 102:195–203. https://doi.org/10.1093/jmammal/gyaa141.
Pereira, E. M., L. F. Junior, A. C. Menezes, & D. M. C. Santos. 2018. Horário de atividades de três espécies de morcegos da RPPN Fazenda Bom Retiro, Casimiro de Abreu, RJ. Revista Ciência Atual 11:2–15.
Pianka, E. R. 1973. The structure of lizard communities. Annual Review of Ecology and Systematics 4:53–74. https://www.jstor.org/stable/2096804.
Presley, S. J., M. R. Willig, I. Castro-Arellano, & S. C. Weaver. 2009. Effects of habitat conversion on temporal activity patterns of phyllostomid bats in lowland Amazonian rain forest. Journal of Mammalogy 90:210–221. https://doi.org/10.1644/08-MAMM-A-089.1.
Racey, P. A. 2009. Reproductive assessment of bats. Ecological and behavioural methods in the study of bats (T. H. Kunz & S. Parsons, eds.). The Johns Hopkins University Press, Baltimore.
Rivera-Villanueva, A. N. 2021. Patrones de actividad de Leptonycteris yerbabuenae en relación a factores intrínsecos y extrínsecos. Tesis de Maestría. Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad Durango. Durango, México.
Rivero-Monteagudo, J. A., J. J. Pellón, & M. Williams. 2021. Environmental seasonality explains reproductive timing of short-tailed fruit bats in a premontane forest of central Peru. Acta Chiropterologica 23:59–69. https://doi.org/10.3161/15081109ACC2021.23.1.005.
Saldaña-Vázquez, R. A., & J.E. Schondube. 2013. Food intake changes in relation to food quality in the Neotropical frugivorous bat Sturnira ludovici. Acta Chiropterologica 15: 69–75. https://doi.org/10.3161/150811013X667867.
Sampedro, A. C., et al. 2007. Nuevos registros de especies de murciélagos para el departamento de Sucre y algunos datos sobre su ecología en esta región colombiana. Caldasia 29:355–362.
Servicio Nacional de Meteorología e Hidrología del Perú (SENAMHI). 2019. Estación Satipo, tipo Convencional-Meteorológica (2013–2018). Dirección de Redes de Observación y Datos. <https://www.senamhi.gob.pe/mapas/mapa-estaciones/_dat_esta_tipo.php? estaciones=000571>.
Sikes, R. S., W. L. Gannon, & The Animal Care and Use Committee of the American Society of Mammalogists. 2016. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 97:663–688. https://doi.org/10.1093/jmammal/gyw078.
Stawski, C. 2012. Capture and care of northern long-eared bats (Nyctophilus bifax) and seasonal changes in insect abundance. Australian Mammalogy 34:245–250. https://doi.org/10.1071/AM11043.
Stuhler, J. D., A. N. Kildow, & R. D. Stevens. 2019. Ecology of Platyrrhinus lineatus in the Atlantic Forest of Paraguay: reproductive patterns, activity, seasonality, and morphometric variability. From field to laboratory: a memorial volume in honor of Robert J. Baker (R. D. Bradley, H. H. Genoways, D. J. Schmidly, & L. C. Bradley, eds.). Special Publications of the Museum of Texas Tech University, Texas.
Thies, W., & E. K. Kalko. 2004. Phenology of Neotropical pepper plants (Piperaceae) and their association with their main dispersers, two short-tailed fruit bats, Carollia perspicillata and C. castanea (Phyllostomidae). Oikos 104:362–376. https://doi.org/10.1111/j.0030-1299.2004.12747.x.
Thies, W., E. K. Kalko, & H. U. Schnitzler. 2006. Influence of environment and resource availability on activity patterns of Carollia castanea (Phyllostomidae) in Panama. Journal of Mammalogy 87:331–338. https://doi.org/10.1644/05-MAMM-A-161R1.1.
Thieurmel, B., & A. Elmarharaoui. 2019. Suncalc: compute Sun position, sunlight phases, Moon position and lunar phase. R package version 0.5.0. <https://github.com/datastorm-open/suncalc>.
Thomson, B. G. 2020. Social interactions, roost usage and notes on the breeding system of the chocolate wattled bat (Chalinolobus morio) in south-east Queensland, Australia. Australian Journal of Zoology 67:290–300. https://doi.org/10.1071/ZO20049.
Vásquez-Parra, O. Y., F. J. García, & M. Machado. 2017. Actividad nocturna y uso del espacio vertical en algunas especies de murciélagos frugívoros (Chiroptera: Phyllostomidae) en Venezuela. Revista Biodiversidad Neotropical 7:258–268. https://doi.org/10.18636/bioneotropical.v7i4.689.
Verde, R. S., R. C. Silva, & A. M. Calouro. 2018. Activity patterns of frugivorous Phyllostomid bats in an urban fragment in southwest Amazonia, Brazil. Série Zoologia 108:e2018016. https://doi.org/10.1590/1678-4766e2018016.
Violle, C., D. R. Nemergut, Z. Pu, & L. Jiang. 2011. Phylogenetic limiting similarity and competitive exclusion. Ecology Letters 14:782–787. https://doi.org/10.1111/j.1461-0248.2011.01644.x.
York, H. A., & M. Papes. 2007. Limiting similarity and species assemblages in the short-tailed fruit bats. Journal of Zoology 273:249–256. https://doi.org/10.1111/j.1469-7998.2007.00321.x.
Zegarra, O. 2019. Diversidad y distribución estacional de los ensambles de quirópteros en el bosque secundario del Fundo Santa Teresa en Satipo, Perú. Tesis de Grado. Universidad Nacional Agraria La Molina. Lima, Perú.
Zeppelini, C. G., I. Jerônimo, K. M. C. Rego, M. P. A. Fracasso, & L. C. S. Lopez. 2017. Description of whole-night activity patterns for Neotropical bat species. Acta Chiropterologica 19:155–160. https://doi.org/10.3161/15081109ACC2017.19.1.012.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Jorge A. Rivero, Juan J. Pellón, Orlando J. Zegarra
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.