Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-19T03:47:07.397Z Has data issue: false hasContentIssue false
  • English
  • Français

Influence of frugivore activity on the species abundance of seedlings and saplings in a lowland tropical forest in Colombia

Published online by Cambridge University Press:  04 May 2015

Natalia Norden  and
Pablo R. Stevenson
Natalia Norden*
Affiliation:
Fundación Cedrela, Diagonal 40A # 18A-09, Bogotá, Colombia Centro Internacional de Física, Edificio Manuel Ancízar, Universidad Nacional de Colombia, Cra 30 # 45-03, Bogotá, Colombia Programa de Biología, Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Cra 24 # 63C-69, Bogotá, Colombia
Pablo R. Stevenson
Affiliation:
Departamento de Ciencias Biológicas, Universidad de los Andes, Carrera 1 # 18A-10, Bogotá, Colombia
*
1Corresponding author. Email: natnorden@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract:

Although seed dispersal plays a critical role for plant regeneration, the long-term benefits of frugivores for recruitment success have been poorly explored. We evaluated the relative importance of tree species abundance and of frugivore-related factors for successful plant recruitment on 18 tree species in a lowland Colombian rain forest. We combined census data from four 1-ha plots of trees (>10 cm dbh), saplings (1–5 cm dbh) and seedlings (<1.7 m) with a dataset describing tree–frugivore interactions. Seedling abundance was higher for large-seeded species dispersed by the spider monkey, while sapling abundance was higher for large-seeded species dispersed by birds. The identity of the dispersal agent and its interaction with seed size explained 20–30% of the total variance in seedling and sapling abundance across scales. Seed size consistently influenced the species abundance of seedlings and saplings across scales, but in opposite ways. These developmental changes suggest that what is beneficial to seedlings is not necessarily beneficial to saplings. Species identity explained 10–50% of the total variance in seedling and sapling abundance among and within 1-ha plots. Overall, our findings suggest that recruitment success is context-dependent as the relative importance of the different variables addressed may shift along spatial and temporal scales.

Keywords

Colombiaforest regenerationfrugivoryplant recruitmentsaplingseed dispersalseedlingspatial scaletropical rain forest
Type
Research Article
Information
Journal of Tropical Ecology , Volume 31 , Issue 4 , July 2015 , pp. 291 - 303
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

CLARK, C. J., POULSEN, J. R., CONNOR, E. F. & PARKER, V. T. 2004. Fruiting trees as dispersal foci in a semi-deciduous tropical forest. Oecologia 139:66–75.CrossRefGoogle Scholar
CLARK, C. J., POULSEN, J. R., BOLKER, B., CONNOR, E. F. & PARKER, V. T. 2005. Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 86:2684–2694.CrossRefGoogle Scholar
COMITA, L. S., CONDIT, R. & HUBBELL, S. P. 2007a. Developmental changes in habitat associations of tropical trees. Journal of Ecology 95:482–492.CrossRefGoogle Scholar
COMITA, L. S., AGUILAR, S., PÉREZ, R., LAO, S. & HUBBELL, S. P. 2007b. Patterns of woody plant species abundance and diversity in the seedling layer of a tropical forest. Journal of Vegetation Science 18:163–174.CrossRefGoogle Scholar
CONNELL, J. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pp. 298–312 in den Boer, P. J. & Gradwell, J. R. (eds.). Dynamics of populations. Pudoc, Wageningen.Google Scholar
DALLING, J. W., DAVIS, A. S., SCHUTTE, B. J. & ARNOLD, A. 2011. Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology 99:89–95.CrossRefGoogle Scholar
DIEZ-ROUX, A. V. 2000. Multilevel analysis in public health research. Annual Review of Public Health 21:171–192.CrossRefGoogle ScholarPubMed
ENGELBRECHT, B. M. J., COMITA, L. S., CONDIT, R., KURSAR, T. A., TYREE, M. T., TURNER, B. L. & HUBBELL, S. P. 2007. Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447:80–82.CrossRefGoogle ScholarPubMed
GELMAN, A. & HILL, J. 2006. Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge. 625 pp.CrossRefGoogle Scholar
HARMS, K. E. & DALLING, J. W. 1997. Damage and herbivory tolerance through resprouting as an advantage of large seed size in tropical trees and lianas. Journal of Tropical Ecology 13:617–621.CrossRefGoogle Scholar
HOWE, H. 1977. Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58:539–550.CrossRefGoogle Scholar
HOWE, H. & SMALLWOOD, J. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13:201–228.CrossRefGoogle Scholar
JANSEN, P. A., BONGERS, F. & HEMERIK, L. 2004. Seed mass and mast seeding enhance dispersal by a Neotropical scatter-hoarding rodent. Ecology 74:569–589.Google Scholar
JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. American Naturalist 104:501–528.CrossRefGoogle Scholar
JANZEN, D.H. 1971. Seed predation by animals. Annual Review of Ecology and Systematics 2:465–492.CrossRefGoogle Scholar
JORDANO, P., FORGET, P.-M., LAMBERT, J. E., BÖHNING-GAESE, K., TRAVESET, A. & WRIGHT, S. J. 2011. Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters 7:321–323.CrossRefGoogle ScholarPubMed
LEISHMAN, M. R., WRIGHT, I. J., MOLES, A. T., WESTOBY, M. & FENNER, M. 2000. The evolutionary ecology of seed size. Pp. 31–57 in Fenner, M. (ed.). Seeds: the ecology of regeneration in plant communities. CAB International, Wallingford.CrossRefGoogle Scholar
METZ, M. 2012. Does habitat specialization by seedlings contribute to a high diversity of a lowland rain forest? Journal of Ecology 100:969–979.CrossRefGoogle Scholar
METZ, M., SOUSA, W. & VALENCIA, R. 2010. Widespread density-dependent seedling mortality promotes species coexistence in a highly diverse Amazonian rainforest. Ecology 91:3675–3685.CrossRefGoogle Scholar
MOLES, A. & WESTOBY, M. 2004. Seedling survival and seed size: a synthesis of the literature. Ecology 92:372–383.CrossRefGoogle Scholar
MOLES, A. & WESTOBY, M. 2006. Seed size and plant strategy across the whole life cycle. Oikos 113:91–105.CrossRefGoogle Scholar
MULLER-LANDAU, H. C. & HARDESTY, B. D. 2005. Seed dispersal of woody plants in tropical forests: concepts, examples and future directions. Pp. 267–309 in Burslem, D., Pinard, A. & Hartley, S. E. (eds.). Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
MULLER-LANDAU, H. C., WRIGHT, S. J., CALDERÓN, O., CONDIT, R. & HUBBELL, S. P. 2008. Interspecific variation in primary seed dispersal in a tropical forest. Journal of Ecology 96:653–667.CrossRefGoogle Scholar
NAKAGAWA, S. & SCHIELZETH, H. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution 4:133–142.CrossRefGoogle Scholar
NATHAN, R. & MULLER-LANDAU, H. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15:278–285.CrossRefGoogle ScholarPubMed
NICOTRA, A., CHAZDON, R. & IRIARTE, S. 1999. Spatial heterogeneity of light and woody seedling regeneration in tropical wet forests. Ecology 80:1908–1926.CrossRefGoogle Scholar
NORDEN, N., CHAVE, J., CAUBERE, A., CHATELET, P., FERRONI, N., FORGET, P. & THEBAUD, C. 2007. Is temporal variation of seedling communities determined by environment or by seed arrival? A test in a neotropical forest. Journal of Ecology 95:507–516.CrossRefGoogle Scholar
NORDEN, N., DAWS, M. I., ANTOINE, C., GONZÁLEZ, M. A., GARWOOD, N. & CHAVE, J. 2009a. The relationship between seed mass and mean time to germination for 1037 tree species across five tropical forests. Functional Ecology 23:203–210.CrossRefGoogle Scholar
NORDEN, N., CHAVE, J., BELBENOIT, P., CAUBERE, A., CHATELET, P., FORGET, P., RIERA, B., VIERS, J. & THEBAUD, C. 2009b. Interspecific variation in seedling responses to seed limitation and habitat conditions for 14 Neotropical woody species. Journal of Ecology 97:186–197.CrossRefGoogle Scholar
RATIARISON, S. & FORGET, P.-M. 2013. The role of frugivores in determining seed removal and dispersal in the Neotropical nutmeg. Tropical Conservation Science 6:690–704.CrossRefGoogle Scholar
ROJAS, A.-M., CADENA, A. & STEVENSON, P. R. 2004. Preliminary study of the bat community at the CIEM, Tinigua National Park, Colombia. Field Studies of Fauna and Flora La Macarena, Colombia 14:45–56.Google Scholar
SCHUPP, E. 1995. Seed-seedling conflicts, habitat choice, and patterns of plant recruitment. American Journal of Botany 82:399–409.CrossRefGoogle Scholar
SCHUPP, E. W., JORDANO, P. & GÓMEZ, J. M. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188:333–353.CrossRefGoogle ScholarPubMed
SOKAL, R. R. & ROHLF, R. 1995. Biometry: the principle and practice of statistics in biological science, W. H. Freeman, New York. 859 pp.Google Scholar
STEVENSON, P. R. 2004a. Fruit choice by woolly monkeys in Tinigua National Park, Colombia. International Journal of Primatology 25:367–381.CrossRefGoogle Scholar
STEVENSON, P. R. 2004b. Phenological patterns of woody vegetation at Tinigua Park, Colombia: methodological comparisons with emphasis on fruit production. Caldasia 26:125–150.Google Scholar
STEVENSON, P. R. 2007. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. Pp. 340–362 in Dennis, A. J., Schupp, E. W., Green, R. J. & Westcott, D. W. (eds.). Seed dispersal: theory and its application in a changing world. CAB International, Wallingford.CrossRefGoogle Scholar
STEVENSON, P. R., QUIÑONES, M. J. & AHUMADA, J. A. 2000. Influence of fruit availability on ecological overlap among four Neotropical primates at Tinigua National Park, Colombia. Biotropica 32:533–544.CrossRefGoogle Scholar
STEVENSON, P. R., CASTELLANOS, M., PIZARRO, J. & GARAVITO, M. 2002. Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. International Journal of Primatology 23:1187–1204.CrossRefGoogle Scholar
TERBORGH, J., NUÑEZ-ITURRI, G., PITMAN, N., VALVERDE, F., ALVAREZ, P., SWAMY, V., PRINGLE, E. & PAINE, C. 2008. Tree recruitment in an empty forest. Ecology 89:1757–1768.CrossRefGoogle Scholar
TRAVESET, A. 1998. Effect of seed passage through vertebrate frugivores’ guts on germination: a review. Perspectives in Plant Ecology, Evolution and Systematics 1:151–190.CrossRefGoogle Scholar
VAN DER MEER, P. & BONGERS, F. 1996. Patterns of tree-fall and branch-fall in a tropical rain forest in French Guiana. Journal of Ecology 84:19–29.CrossRefGoogle Scholar
WANG, B. & SMITH, T. 2002. Closing the seed dispersal loop. Trends in Ecology and Evolution 17:379–385.CrossRefGoogle Scholar
WEBB, C. & PEART, D. 2000. Habitat associations of trees and seedlings in a Bornean rain forest. Journal of Ecology 88:464–478.CrossRefGoogle Scholar
WESTOBY, M., LEISHMAN, M. & LORD, J. 1996. Comparative ecology of seed size and dispersal. Philosophical Transactions of the Royal Society B: Biological Sciences 351:1309–1318.Google Scholar