Dispersion of seeds at night and day in sub-Andean forests, Cueva Los Guacharos Park, Colombia
DOI:
https://doi.org/10.15517/rev.biol.trop..v71i1.51599Keywords:
seed dispersal;, hanging seed traps;, day and night frugivores;, phenology;, Andean forestAbstract
Introduction: Much has been argued about the importance of the role that different types of frugivores play as seed dispersers in plant communities, but few studies have been actually carried out. Objective: We evaluated and compared diurnal and nocturnal seed dispersal in a primary and secondary sub-Andean forest in Southern Colombia. Methods: We estimated number and biomass (kg/ha) of seeds dispersed over one year (2017) using 60 fruit traps that were checked before sunrise and before sunset for 10 continuous days every two months. Results: We found that from 1 874 dispersed seeds, 55.8 % (10.9 kg/ha) were collected during the day and 44.2 % (6.39 kg/ha) at night. There were no significant differences between diurnal and nocturnal seed dispersal in number of seeds or biomass. We also found no difference in between seed dispersal that in the primary forest and secondary forest over time. Within diurnal organisms, primates and fruit-eating birds appear to be primarily responsible for this ecosystem service during the day; while bats, birds (e.g. oilbirds), and probably primates did so during the night. Conclusions: Diurnal and nocturnal dispersal seem to be equal in terms of number and weight of seeds, but not in the similarity of dispersed plant species. It remains a challenge to recognize the relative importance of different fruit-eating organisms as seed dispersers using fruit trap methods.
Downloads
References
Albrecht, J., Neuschulz, E. L., & Farwig, N. (2012). Impact of habitat structure and fruit abundance on avian seed dispersal and fruit predation. Basic and Applied Ecology, 13(4), 347–354. DOI: https://doi.org/10.1016/j.baae.2012.06.005
Bacles, C. F., Lowe, A. J., & Ennos, R. A. (2006). Effective seed dispersal across a fragmented landscape. Science, 311(5761), 628–628. DOI: https://doi.org/10.1126/science.1121543
Bautista-Plazas, S., Rodríguez-Bolaños, A., Castellanos, R., & Stevenson, P. R. (2017). First inventory of small non-flying mammals of the Cueva de los Guacharos National Natural Park (Huila, Colombia). Mammalogy Notes, 4(2), 18–21. DOI: https://doi.org/10.47603/manovol4n2.18-21
Bravo, S. P. (2012). The impact of seed dispersal by black and gold howler monkeys on forest regeneration. Ecological Research, 27(2), 311–321. DOI: https://doi.org/10.1007/s11284-011-0904-6
Brosset, A., Charles-Dominique, P., Cockle, A., Cosson, J. F., & Masson, D. (1996). Bat communities and deforestation in French Guiana. Canadian Journal of Zoology, 74(11), 1974–1982. DOI: https://doi.org/10.1139/z96-224
Cain, M. L., Milligan, B. G., & Strand, A. E. (2000). Long‐distance seed dispersal in plant populations. American Journal of Botany, 87(9), 1217–1227. DOI: https://doi.org/10.2307/2656714
Campbell, G., Head, J., Junker, J., & Nekaris, K. A. I. (2016). Primate abundance and distribution: background concepts and methods. In S. A. Wich & A. J. Marshall (Eds.), An introduction to primate conservation (pp. 79-104). Oxford Academic. DOI: https://doi.org/10.1093/acprof:oso/9780198703389.003.0006
Carlo, T. A., & Morales, J. M. (2016). Generalist birds promote tropical forest regeneration and increase plant diversity via rare‐biased seed dispersal. Ecology, 97(7), 1819–1831. DOI: https://doi.org/10.1890/15-2147.1
Chapman, C. A. (1995). Primate seed dispersal: coevolution and conservation implications. Evolutionary Anthropology: Issues, News, and Reviews, 4(3), 74–82. DOI: https://doi.org/10.1002/evan.1360040303
Chapman, C. A., & Dunham, A. E. (2018). Primate seed dispersal and forest restoration: an African perspective for a brighter future. International Journal of Primatology, 39(3), 427–442. DOI: https://doi.org/10.1007/s10764-018-0049-3
Chazdon, R. L. (2003). Tropical forest recovery: legacies of human impact and natural disturbances. Perspectives in Plant Ecology, Evolution and Systematics, 6(1–2), 51–71. DOI: https://doi.org/10.1078/1433-8319-00042
Chazdon, R. L., & Guariguata, M. R. (2016). Natural regeneration as a tool for large‐scale forest restoration in the tropics: prospects and challenges. Biotropica, 48(6), 716–730. DOI: https://doi.org/10.1111/btp.12381
Connell, J. H., Tracey, J. G., & Webb, L. J. (1984). Compensatory recruitment, growth, and mortality as factors maintaining rain forest tree diversity. Ecological Monographs, 54(2), 141–164. DOI: https://doi.org/10.2307/1942659
Cramer, J. M., Mesquita, R. C., & Williamson, G. B. (2007). Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation, 137(3), 415–423. DOI: https://doi.org/10.1016/j.biocon.2007.02.019
Duncan, S. R., & Chapman, C. A. (1999). Seed dispersal and potential forest succession in abandoned agriculture in tropical Africa. Ecological Applications, 9(3), 998–1008. DOI: https://doi.org/10.1890/1051-0761(1999)009[0998:SDAPFS]2.0.CO;2
Emer, C., Galetti, M., Pizo, M. A., Guimaraes-Jr, P. R., Moraes, S., Piratelli, A., & Jordano, P. (2018). Seed‐dispersal interactions in fragmented landscapes-a metanetwork approach. Ecology Letters, 21(4), 484–493. DOI: https://doi.org/10.1111/ele.12909
Fleming, T. H. (1988). The short-tailed fruit bat: a study in plant-animal interactions. University of Chicago Press.
Fleming, T. H., & Heithaus, E. R. (1981). Frugivorous bats, seed shadows, and the structure of tropical forests. Biotropica, 13(2), 45–53. DOI: https://doi.org/10.2307/2388069
Fleming, T. H., & Williams, C. F. (1990). Phenology, seed dispersal, and recruitment in Cecropia peltata (Moraceae) in Costa Rican tropical dry forest. Journal of Tropical Ecology, 6(2), 163–178. DOI: https://doi.org/10.1017/S0266467400004260
Galindo‐González, J., Guevara, S., & Sosa, V. J. (2000). Bat‐and bird‐generated seed rains at isolated trees in pastures in a tropical rainforest. Conservation Biology, 14(6), 1693–1703 DOI: https://doi.org/10.1111/j.1523-1739.2000.99072.x
Gast, F., & Stevenson, P. R. (2021). Relative abundances of medium and large mammals in the Cueva de Los Guácharos National Park (Huila, Colombia). Biota Neotropica, 20(3), e20160305. DOI: https://doi.org/10.1590/1676-0611-bn-2016-0305
Gelmi-Candusso, T. A., Bialozyt, R., Slana, D., Zarate-Gomez, R., Heymann, E. W., & Heer, K. (2019). Estimating seed dispersal distance: a comparison of methods using animal movement and plant genetic data on two primate-dispersed Neotropical plant species. Ecology and Evolution, 9(16), 8965–8977. DOI: https://doi.org/10.1002/ece3.5422
Gonzales, R. S., Ingle, N. R., Lagunzad, D. A., & Nakashizuka, T. (2009). Seed dispersal by birds and bats in lowland Philippine forest successional area. Biotropica, 41(4), 452–458. DOI: https://doi.org/10.1111/j.1744-7429.2009.00501.x
Gorchov, D. L., Cornejo, F., Ascorra, C., & Jaramillo, M. (1993). The role of seed dispersal in the natural regeneration of rain forest after strip-cutting in the Peruvian Amazon. Vegetatio, 107(1), 339–349. DOI: https://doi.org/10.1007/BF00052233
Hampe, A. (2008). Fruit tracking, frugivore satiation, and their consequences for seed dispersal. Oecologia, 156(1), 137–145. DOI: https://doi.org/10.1007/s00442-008-0979-0
Herrera, C. M., & Jordano, P. (1981). Prunus mahaleb and birds: the high‐efficiency seed dispersal system of a temperate fruiting tree. Ecological Monographs, 51(2), 203–218. DOI: https://doi.org/10.2307/2937263
Howe, H. F. (1977). Bird activity and seed dispersal of a tropical wet forest tree. Ecology, 58(3), 539–550. DOI: https://doi.org/10.2307/1939003
Howe, H. F. (1990). Seed dispersal by birds and mammals: implications for seedling demography. In K. S. Bawa & M. Hadley (Eds.), Reproductive Ecology of Tropical Forest Plants, (pp. 191–218). UNESCO.
Howe, H. F., & Smallwood, J. (1982). Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13(1), 201–228. DOI: https://doi.org/10.1146/annurev.es.13.110182.001221
Ingle, N. R. (2003). Seed dispersal by wind, birds, and bats between Philippine montane rainforest and successional vegetation. Oecologia, 134(2), 251–261. DOI: https://doi.org/10.1007/s00442-002-1081-7
Jacomassa, F. A. F., & Pizo, M. A. (2010). Birds and bats diverge in the qualitative and quantitative components of seed dispersal of a pioneer tree. Acta Oecologica, 36(5), 493–496. DOI: https://doi.org/10.1016/j.actao.2010.07.001
Jansen, P. A., Hirsch, B. T., Emsens, W. J., Zamora-Gutierrez, V., Wikelski, M., & Kays, R. (2012). Thieving rodents as substitute dispersers of megafaunal seeds. Proceedings of the National Academy of Sciences, 109(31), 12610–12615. DOI: https://doi.org/10.1073/pnas.1205184109
Janson, C. H. (1983). Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science, 219(4581), 187–189. DOI: https://doi.org/10.1126/science.219.4581.187
Janzen, D. H. (1971). Seed predation by animals. Annual Review of Ecology and Systematics, 2(1), 465–492. DOI: https://doi.org/10.1146/annurev.es.02.110171.002341
Korine, C., & Kalko, E. K. (2005). Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction. Behavioral Ecology and Sociobiology, 59(1), 12–23. DOI: https://doi.org/10.1007/s00265-005-0003-1
Kozlowski, T. T. (2002). Physiological ecology of natural regeneration of harvested and disturbed forest stands: implications for forest management. Forest ecology and management, 158(1-3), 195–221. DOI: https://doi.org/10.1016/S0378-1127(00)00712-X
Levey, D. J., Bolker, B. M., Tewksbury, J. J., Sargent, S., & Haddad, N. M. (2005). Effects of landscape corridors on seed dispersal by birds. Science, 309(5731), 146–148. DOI: https://doi.org/10.1126/science.1111479
Levey, D. J., Silva, W. R., & Galetti, M. (2002). Seed dispersal and frugivory: ecology, evolution, and conservation. CABI Publishing.
Link, A., & Di Fiore, A. (2006). Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. Journal of tropical ecology, 22(3), 235–246. DOI: https://doi.org/10.1017/S0266467405003081
McConkey, K. R., Prasad, S., Corlett, R. T., Campos-Arceiz, A., Brodie, J. F., Rogers, H., & Santamaria, L. (2012). Seed dispersal in changing landscapes. Biological Conservation, 146(1), 1–13. DOI: https://doi.org/10.1016/j.biocon.2011.09.018
Medellin, R. A., & Gaona, O. (1999). Seed dispersal by bats and birds in forest and disturbed habitats of Chiapas, Mexico. Biotropica, 31(3), 478–485. DOI: https://doi.org/10.1111/j.1744-7429.1999.tb00390.x
Mello, M. A. R., Marquitti, F. M. D., Guimaraes-Jr, P. R., Kalko, E. K. V., Jordano, P., & de Aguiar, M. A. M. (2011). The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. PLoS One, 6(2), e17395. DOI: https://doi.org/10.1371/journal.pone.0017395
Mello, M. A. R., Rodrigues, F. A., Costa, L. D. F., Kissling, W. D., Şekercioğlu, Ç. H., Marquitti, F. M. D., & Kalko, E. K. V. (2015). Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos, 124(8), 1031–1039. DOI: https://doi.org/10.1111/oik.01613
Nathan, R., & Muller-Landau, H. C. (2000). Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution, 15(7), 278–285. DOI: https://doi.org/10.1016/S0169-5347(00)01874-7
Ozinga, W. A., Römermann, C., Bekker, R. M., Prinzing, A., Tamis, W. L., Schaminée, J. H., Henneken, S. M., Thompson, K., Poschlod, P., Kleyer, M., Bakker, J. P., & van Groenendael, J. M. (2009). Dispersal failure contributes to plant losses in NW Europe. Ecology Letters, 12(1), 66–74. DOI: https://doi.org/10.1111/j.1461-0248.2008.01261.x
Parrotta, J. A., Turnbull, J. W., & Jones, N. (1997). Catalyzing native forest regeneration on degraded tropical lands. Forest Ecology and Management, 99(1-2), 1–7. DOI: https://doi.org/10.1016/S0378-1127(97)00190-4
Prada, C. M., & Stevenson, P. R. (2016). Plant composition associated with environmental gradients in tropical montane forests (Cueva de Los Guacharos National Park, Huila, Colombia). Biotropica, 48(5), 568–576. DOI: https://doi.org/10.1111/btp.12331
R Core Team. (2023). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
Ramírez, M. A., Galvis, N. F., Vargas, S. A., Léon, J. J., Cifuentes, E. F., & Stevenson, P. R. (2014). Seed dispersal by woolly monkeys in Cueva de los Guacharos National Park (Colombia): An amazonian primate dispersing montane plants. In N. B. Grow, S. Gursky-Doyen & A. Krzton (Eds.), High altitude primates (pp. 103–114). Springer. DOI: https://doi.org/10.1007/978-1-4614-8175-1_6
Saavedra, F., Hensen, I., Beck, S. G., Böhning-Gaese, K., Lippok, D., Töpfer, T., & Schleuning, M. (2014). Functional importance of avian seed dispersers changes in response to human-induced forest edges in tropical seed-dispersal networks. Oecologia, 176(2014), 837–848. DOI: https://doi.org/10.1007/s00442-014-3056-x
Stevenson, P. R. (2004). Phenological patterns of woody vegetation at Tinigua Park, Colombia: Methodological comparisons with emphasis on fruit production. Caldasia, 26(1), 125–150.
Stevenson, P. R. (2007). Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In A. J. Dennis, E. W. Schupp, R. J. Green & D. A. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 340–362). CABI Publishing. DOI: https://doi.org/10.1079/9781845931650.0340
Stevenson, P. R. (2011). The abundance of large Ateline monkeys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica, 43(4), 512–519. DOI: https://doi.org/10.1111/j.1744-7429.2010.00708.x
Stevenson, P. R., Castellanos, M. C., Pizarro, J. C., & Garavito, M. (2002). Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. International Journal of Primatology, 23(6), 1187–1204. DOI: https://doi.org/10.1023/A:1021118618936
Stevenson, P. R., Cardona, L. M., Acosta-Rojas, D. C., Henao-Diaz, F., & Cárdenas, S. (2017). Diet of oilbirds (Steatornis caripensis) in Cueva de los Guácharos National Park (Colombia): Temporal variation in fruit consumption, dispersal, and seed morphology. Ornitología Neotropical, 28(2017), 295–307. DOI: https://doi.org/10.58843/ornneo.v28i0.243
Stevenson, P. R., Cortés, C., Reyes, R., Paramero, R., Uni, J. F., Peña-Nuñez, J. L., & Henao-Díaz, L. F. (2022). Avifauna asociada a bosques primarios y secundarios del Parque Nacional Natural Cueva de Los Guácharos, Colombia. Actualidades Biológicas, 44(116), 1–18. DOI: https://doi.org/10.17533/udea.acbi.v44n116a01
Stevenson, P. R., Link, A., & Ramírez, B. H. (2005). Frugivory and seed fate in Bursera inversa (Burseraceae) at Tinigua Park, Colombia: Implications for primate conservation. Biotropica: The Journal of Biology and Conservation, 37(3), 431–438. DOI: https://doi.org/10.1111/j.1744-7429.2005.00057.x
Stevenson, P. R., & Vargas, I. N. (2008). Sample size and appropriate design of fruit and seed traps in tropical forests. Journal of Tropical Ecology, 24(1), 95–105. DOI: https://doi.org/10.1017/S0266467407004646
Stiles, E. W. (1980). Patterns of fruit presentation and seed dispersal in bird-disseminated woody plants in the eastern deciduous forest. The American Naturalist, 116(5), 670–688. DOI: https://doi.org/10.1086/283657
Thies, W., & Kalko, E. K. (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(2), 362–376. DOI: https://doi.org/10.1111/j.0030-1299.2004.12747.x
Thomas, D. W., Cloutier, D., Provencher, M., & Houle, C. (1988). The shape of bird-and batgenerated seed shadows around a tropical fruiting tree. Biotropica, 20(1988), 347–348. DOI: https://doi.org/10.2307/2388330
Uriarte, M., & Chazdon, R. L. (2016). Incorporating natural regeneration in forest landscape restoration in tropical regions: synthesis and key research gaps. Biotropica, 48(6), 915–924. DOI: https://doi.org/10.1111/btp.12411
Vargas, S. A., León, J., Ramírez, M., Galvis, N., Cifuentes, E., & Stevenson, P. R. (2014). Population density and ecological traits of highland woolly monkeys at Cueva de los Guácharos National Park, Colombia. In N. Grow, S. Gursky-Doyen & A. Krzton, (Eds.), High altitude primates (pp. 85–102). Springer. DOI: https://doi.org/10.1007/978-1-4614-8175-1_5
Vasquez-Yanes, C., & Orozco-Segovia, A. (1986). Effect of light controlled dormancy in Cecropia obtusifolia. In A. Estrada & T. H. Fleming (Eds.), Frugivores and seed dispersal (pp. 71–77). Springer Dordrecht. DOI: https://doi.org/10.1007/978-94-009-4812-9_7
Walteros-Vergara, A. (2018). Lista comentada de las especies de murciélagos presentes en el parque Nacional Natural Cueva de los Guácharos. Ubicado en el municipio de Acevedo-Huila (Degree thesis dissertation). Universidad Distrital Francisco José de Caldas, Colombia.
Wang, B. C., & Smith, T. B. (2002). Closing the seed dispersal loop. Trends in ecology & evolution, 17(8), 379–386. DOI: https://doi.org/10.1016/S0169-5347(02)02541-7
Wenny, D. G., & Levey, D. J. (1998). Directed seed dispersal by bellbirds in a tropical cloud forest. Proceedings of the National Academy of Sciences, 95(11), 6204–6207. DOI: https://doi.org/10.1073/pnas.95.11.6204
Wenny, D. G., Sekercioglu, C., Cordeiro, N. J., Rogers, H. S., & Kelly, D. (2016). Seed dispersal by fruit-eating birds. In C. H. Sekercioglu, D. G. Wenny & C. J. Whelan (Eds.), Why birds matter: avian ecological function and ecosystem services (pp. 107–145). University of Chicago Press. DOI: https://doi.org/10.7208/chicago/9780226382777.001.0001
Whittaker, R. J., & Jones, S. H. (1994). The role of frugivorous bats and birds in the rebuilding of a tropical forest ecosystem, Krakatau, Indonesia. Journal of Biogeography, 21(3), 245–258. DOI: https://doi.org/10.2307/2845528
Willson, M. F. (1993). Dispersal mode, seed shadows, and colonization patterns. In T. H. Fleming & A. Estrada (Eds.), Frugivory and seed dispersal: ecological and evolutionary aspects (pp. 261–280). Springer Dordrecht. DOI: https://doi.org/10.1007/978-94-011-1749-4_19
Willson, M. F., & Traveset, A. (2000). The ecology of seed dispersal. In M. Fenner (Ed.), Seeds: the ecology of regeneration in plant communities (pp. 85–110). CABI International. DOI: https://doi.org/10.1079/9780851994321.0085
Wright, S. J., Zeballos, H., Domínguez, I., Gallardo, M. M., Moreno, M. C., & Ibáñez, R. (2000). Poachers alter mammal abundance, seed dispersal, and seed predation in a Neotropical forest. Conservation Biology, 14(1), 227–239. DOI: https://doi.org/10.1046/j.1523-1739.2000.98333.x
Zárate, D. A., Andresen, E., & Santos-Heredia, C. (2019). Seed fate and seedling recruitment in monkey latrines in rustic cocoa plantations and rain forest in southern Mexico. Journal of Tropical Ecology, 35(1), 18–25. DOI: https://doi.org/10.1017/S026646741800041X
Published
Issue
Section
License
Copyright (c) 2023 Revista de Biología Tropical

This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Attribution 4.0 License (CC BY 4.0)
Attribution (BY) • (BY) You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work).
