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Dispersal patterns of large-seeded plants and the foraging behaviour of a frugivorous bat

Published online by Cambridge University Press:  31 March 2020

David Villalobos-Chaves*
Affiliation:
Department of Biology, University of Washington, Seattle, WA98195, USA
Felipe P. L. Melo
Affiliation:
Laboratório de Ecologia Aplicada, Universidade Federal de Pernambuco, Recife, Pernambuco, Brasil Avenida Prof. Moraes Rêgo S/N, Cidade Universitária, Recife-PE, Brasil
Bernal Rodríguez-Herrera
Affiliation:
Escuela de Biología, Universidad de Costa Rica, San José11501, Costa Rica
*
Author for correspondence: *David Villalobos-Chaves, Email: [email protected]

Abstract

Mutualistic interactions are biologically important, diverse and poorly understood. Comprehending these interactions and the effectiveness of the mutualistic partners has been the central focus of ecological and evolutionary studies, as this task requires disentangling the pieces of mutualism under study. Here, we tested the hypothesis that feeding activity of Artibeus phaeotis influences density, diversity and distance effects of the seed rain of large-seeded plant species in a Neotropical dry forest of Costa Rica. We predicted that bats’ activity increases density and diversity metrics on dispersing sites and that bats behave as short-distance dispersers. Our data revealed that, by dispersing hundreds of seeds within their small foraging areas and mostly close to fruiting trees, the feeding activity of A. phaeotis increases the density and richness of seeds underneath night feeding roosts. The functional role of A. phaeotis as disperser may vary among plant species, as we also detected that some seeds are more dispersed than others. Further inquiries to elucidate mutualistic interactions between frugivorous bats and large-seeded plant species should focus on understanding demographic and fitness outcomes, as strong selective pressures may be shaping morphological and behavioural traits of both plants and animals, ultimately influencing the survival of each partner.

Type
Research Article
Copyright
© The Author(s) 2020. Published by Cambridge University Press

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References

Literature cited

Audet, D (1990) Foraging behavior and habitat use by a gleaning bat Myotis myotis (Chiroptera: Vespertilionidae). Journal of Mammalogy 71, 420427.CrossRefGoogle Scholar
Bello, C, Galetti, M, Pizo, MA, Magnano, LFS, Rocha, MF, Lima, RAF, Peres, CA, Ovaskainen, O and Jordano, P (2015) Defaunation affects carbon storage in tropical forests. Scientific Advances 1, e1501105.Google ScholarPubMed
Bonaccorso, FJ, Todd, CM, Miles, AC and Gorresen, PM (2015) Foraging movements of the endangered Hawaiian hoary bat, Lasiurus cinereus semotus (Chiroptera: Vespertilionidae). Journal of Mammalogy 96, 6471.CrossRefGoogle Scholar
Calenge, C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecological Modelling 197, 516519.CrossRefGoogle Scholar
Chavarría, U, González, J and Zamora, N (2001) Common trees of Palo Verde National Park. Heredia: Editorial InBio, 212 pp.Google Scholar
Côrtes, MC and Uriarte, M (2013) Integrating frugivory and animal movement: a review of the evidence and implications for scaling seed dispersal. Biological Reviews 88, 255272.CrossRefGoogle ScholarPubMed
Corlett, RT (1998) Frugivory and seed dispersal by vertebrates in the Oriental (Indomalayan) region. Biological Reviews of the Cambridge Philosophical Society 73, 413448.CrossRefGoogle ScholarPubMed
De Solla, SR, Bonduriansky, B and Brooks, RJ (1999) Eliminating autocorrelation reduces biological relevance of home range estimates. Journal of Animal Ecology 68, 221234.CrossRefGoogle Scholar
Docters van Leeuwen, WM (1935) The dispersal of plants by fruit-eating bats. Gardens Bulletin, S.S. 9, 5863.Google Scholar
Emmons, LH and Feer, F (1997) Neotropical Rainforest Mammals: A Field Guide. Chicago, IL: University of Chicago Press, 396 pp.Google Scholar
Farwing, N, Schabo, DG and Albrecht, J (2017) Trait-associated loss of frugivores in fragmented forest does not affect seed removal rates. Journal of Ecology 105, 2028.CrossRefGoogle Scholar
Fournier, LA (1974) Un método cuantitativo para la medición de características fenológicas en árboles. Turrialba 24, 422423.Google Scholar
Getz, WM, Fortmann-Roe, S, Cross, PC, Lyons, AJ, Ryan, SJ and Wilmers, CC (2007) LoCoH: nonparametric kernel methods for constructing home ranges and utilization distributions. PLoS ONE 2, 111.CrossRefGoogle ScholarPubMed
Hodgkison, R, Ayasse, M, Häberlein, C, Schulz, S, Zubaid, A, Mustapha, WAW, Kunz, TH and Kalko, EKV (2013) Fruit bats and bat fruits: the evolution of fruit scent in relation to the foraging behaviour of bats in the New and Old World tropics. Functional Ecology 27, 10751084.CrossRefGoogle Scholar
Holdridge, LR (1967) Life Zone Ecology. San José: Tropical Science Center, 206 pp.Google Scholar
Howe, HF (1989) Scatter-and clump-dispersal and seedling demography: hypothesis and implications. Oecologia 79, 417426.CrossRefGoogle ScholarPubMed
Howe, HF and Smallwood, J (1982) Ecology of seed dispersal. Annual Review of Ecology, Evolution and Systematics 13, 201228.CrossRefGoogle Scholar
Janzen, DH (1970) Herbivores and the number of tree species in tropical forests. American Naturalist 104, 501528.CrossRefGoogle Scholar
Janzen, DH (1983) Seed and pollen dispersal by animals: convergence in the ecology of contamination and sloppy harvest. Biological Journal of the Linnean Society 20, 103113.CrossRefGoogle Scholar
Janzen, DH (1985) Spondias mombin is culturally deprived in megafauna-free forest. Journal of Tropical Ecology 1, 131155.CrossRefGoogle Scholar
Janzen, DH, Miller, GA, Hackforth-Jones, J, Pond, CM, Hooper, K and Janos, DP (1976) Two Costa Rican bat-generated seed shadow of Andira inermis (Leguminosae). Ecology 57, 10681075.CrossRefGoogle Scholar
Jordano, P (2001) Fruits and frugivory. In Fenner, M (ed.), Seeds: The Ecology of Regeneration in Plant Communities. Wallingford: CABI Publishing, pp. 125166.Google Scholar
Jost, L (2006) Entropy and diversity. Oikos 113, 363375.CrossRefGoogle Scholar
Loayza, AP and Rios, RS (2014) Seed-swallowing toucans are less effective dispersers of Guettarda viburnoides (Rubiaceae) than pulp feeding jays. Biotropica 46, 6977.CrossRefGoogle Scholar
Lobova, TA, Mori, SA, Blanchard, E, Peckham, H and Charles-Dominique, P (2003) Cecropia as food resource for bats in French Guiana and the significance of fruit structure in seed dispersal and longevity. American Journal of Botany 90, 388403.CrossRefGoogle ScholarPubMed
Marcon, E and Herault, B (2015) Entropart: an R Package to measure and partition diversity. Journal of Statistical Software 67, 126.CrossRefGoogle Scholar
Melo, FPL, Rodríguez-Herrera, B, Chazdon, RL, Medellin, RA and Ceballos, GC (2009) Small tent-roosting bats promote dispersal of large-seeded plants in a neotropical forest. Biotropica 41, 737743.CrossRefGoogle Scholar
Mitchell, MS and Powell, RA (2004) A mechanistic home range model for optimal use of spatially distributed resources. Ecological Modelling 177, 209232.CrossRefGoogle Scholar
Mitchell, MS and Powell, RA (2012) Foraging optimally for home ranges. Journal of Mammalogy 93, 917928.CrossRefGoogle Scholar
Muscarella, R and Fleming, TH (2007) The role of frugivorous bats in tropical forest succession. Biological Reviews 82, 573590.CrossRefGoogle ScholarPubMed
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O’Hara, RB, Simpson, GL, Solymos, P, Henry, M, Stevens, H, Szoecs, E and Wagner, H (2017) vegan: Community Ecology Package. R package version 2.4-3.Google Scholar
QGIS Development Team (2018) QGIS geographic information system. Open Source Geospatial Foundation Project, Oregon. http://www.qgis.org/.Google Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/.Google Scholar
Raymond Heithaus, E, Fleming, TH and Opler, PA (1975) Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology 56, 841854.CrossRefGoogle Scholar
Rodríguez-Herrera, B, Medellin, RA and Timm, RM (2007) Murciélagos Neotropicales que acampan en hojas: Neotropical tent-roosting bats. Heredia: INBio.Google Scholar
Romo, M, Tuomisto, H and Loiselle, BA (2004) On the density-dependence of seed predation in Dipteryx micrantha, a bat-dispersed rain forest tree. Oecologia 140, 7685.Google ScholarPubMed
Rothenwöhrer, C, Becker, NI and Tschapka, M (2010) Resource landscape and spatio-temporal activity patterns of a plant-visiting bat in a Costa Rican lowland rainforest. Journal of Zoology 283, 108116.CrossRefGoogle Scholar
Russo, SE and Augspurger, CK (2004) Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecology Letters 7, 10581067.CrossRefGoogle Scholar
Russo, SE, Portnoy, S and Augspurger, CK (2006) Incorporating animal behavior into seed dispersal models: implications for seed shadows. Ecology 87, 31603174.CrossRefGoogle ScholarPubMed
Schupp, EW, Jordano, P and Gómez, JM (2017) A general framework for effectiveness concepts in mutualism. Ecology Letters 20, 577590.CrossRefGoogle Scholar
Stoner, KE and Timm, RM (2004) Tropical dry-forest mammals of Palo Verde. In Frankie, GW, Mata, A and Vinson, SB (eds), Biodiversity Conservation in Costa Rica. Berkeley, CA: University of California Press, pp. 4866.Google Scholar
Stoner, K, Riba-Hérnandez, P, Vulenic, K and Lambert, JE (2007) The role of mammals in creating and modifying seed shadows in tropical forests and some possible consequences of their elimination. Biotropica 39, 316327.CrossRefGoogle Scholar
Slud, P (1980) The birds of Hacienda Palo Verde, Guanacaste, Costa Rica. Smithsonian Contributions to Zoology 292, 1104.CrossRefGoogle Scholar
Sugiyama, A, Comita, LS, Masaki, T, Condit, R and Hubbell, SP (2018) Resolving the paradox of clumped seed dispersal: positive density and distance dependence in a bat-dispersed species. Ecology 99, 25832591.CrossRefGoogle Scholar
Thomas, DW (1984) Fruit intake and energy budgets of frugivorous bats. Physiological and Biochemical Zoology 57, 457467.Google Scholar
Timm, RM (1985) Artibeus phaeotis. Mammalian Species 235, 16.CrossRefGoogle Scholar
Villalobos-Chaves, D (2016) Uso del hábitat y dispersión de semillas grandes por los murciélagos frugívoros Dermanura phaeotis y Uroderma bilobatum (Chiroptera: Phyllostomidae) en el bosque seco y seco-transicional a húmedo de Costa Rica. MSc Dissertation. Universidad de Costa Rica, Costa Rica.Google Scholar
Villalobos-Chaves, D, Padilla-Alvárez, S and Rodríguez-Herrera, B (2016 a) Seed predation by the wrinkle-faced bat Centurio senex: a new case of this unusual feeding strategy in Chiroptera. Journal of Mammalogy 97, 726733.CrossRefGoogle Scholar
Villalobos-Chaves, D, Bonaccorso, FJ, Rodríguez-Herrera, B, Cordero-Schmidt, E, Arias-Aguilar, A and Todd, CM (2016 b) The influence of sex and reproductive status on foraging behavior and seed dispersal by Uroderma convexum (Chiroptera: Phyllostomidae). In Ortega, J (ed.), Sociality in Bats. Berlin: Springer-Verlag, pp. 281301.CrossRefGoogle Scholar
Wendeln, MC, Runkle, JR and Kalko, EKV (2000) Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32, 489501.CrossRefGoogle Scholar