Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

Shade tolerance within the context of the successional process in tropical rain forests


environmental filtering; functional traits; gap phase; leaf-economics spectrum; niche differentiation; ontogenetic niche shifts; plant-economics spectrum; secondary succession; shade tolerance; regeneration niche.
filtrado ambiental; cambios de nicho ontogenéticos; caracteres funcionales; diferenciación de nicho; espectro económico foliar; espectro de economía de plantas; nicho de regeneración; sucesión secundaria; tolerancia a la sombra

How to Cite

Avalos, G. (2019). Shade tolerance within the context of the successional process in tropical rain forests. Revista De Biología Tropical, 67(S2), S53–S77.


Shade tolerance (the capacity to survive and grow over long periods under shade) is a key component of plant fitness and the foundation of current theories of forest succession in tropical rain forests. It serves as a paradigm to understand the optimal allocation of limited resources under dynamic light regimes. I analyze how tropical rain forest succession influences the expression of ecophysiological mechanisms leading to shade tolerance, and identify future areas that will increase our understanding of the ecological and evolutionary consequences of this phenomenon. Shade tolerance is a multivariate, continuous functional trait reflecting the growth-mortality trade-off of investing resources under limited light vs. exploiting high light conditions. I propose the life cycle successional trajectory model of Gómez-Pompa & Vázquez-Yanes as an integrative tool to understand tropical rain forest succession. This model shows how species distribute along the successional environmental gradient based on their degree of shade tolerance and represents a more integrative paradigm to understand the interface between different aspects of species diversity (ontogenetic variation and functional diversity) throughout succession. It proposes that different trait combinations determining shade tolerance are expressed at different stages of the life cycle, which affects how and when plants enter the successional trajectory. Models explaining the expression of shade tolerance (resource availability, carbon gain, CSR, resource competition) are based on whole-plant economics and are not mutually exclusive. The analysis of shade tolerance is biased towards tree seedlings in the understory of mature forests. Other life stages (juvenile and adult trees), life forms, and microhabitats throughout the forest profile are almost always excluded from these analyses. More integrative explanations based on the distribution of functional traits among species, ontogenetic stages, and the nature of the environmental gradient are being developed based on long-term data and chronosequence comparisons. In summary, shade-tolerance is a complex phenomenon, is determined by multiple characters that change ontogenetically over space and time and entails considerable plasticity. Current methods do not account for this plasticity. Understanding the nature of shade tolerance and its functional basis is critical to comprehending plant performance and improving the management, restoration and conservation of tropical rain forests given the combined threats of global warming and habitat loss


Acevedo, M. F., Urban, D. L., & Shugart H. H. (1996). Models of forest dynamics based on roles of tree species. Ecological Modeling, 87(1-3), 267-284.

Ackerly, D. D. (2003). Community assembly, niche conservatism, and adaptive evolution in changing environments. International Journal of Plant Sciences, K(S3), S165-S184.

Ackerly, D. D., & Cornwell, W.K. (2007). A trait-based approach to community assembly: partitioning of species trait values into within-and among-community components. Ecology Letters, 10(2), 135-145.

Álvarez-Clare, S., & Avalos, G. (2007). Light interception efficiency of the understory palm Calyptrogyne ghiesbreghtiana under deep shade conditions. Ecotropica, 13, 1-8.

Álvarez-Clare, S., & Kitajima, K. (2009). Susceptibility of tree seedlings to biotic and abiotic hazards in the understory of a moist tropical forest in Panama. Biotropica, 41(1), 47-56.

Arnold, S. J. (1983). Morphology, performance and fitness. American Zoologist, 23(2), 347-361.

Arroyo-Rodríguez, V., Melo, F. P., Martínez-Ramos, M., Bongers, F., Chazdon, R. L., Meave, J. A., ... & Tabarelli, M. (2017). Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biological Reviews, 92(1), 326-340.

Augspurger, C. K. (1984). Light requirements of neotropical tree seedlings: a comparative study of growth and survival. Journal of Ecology, 72(3), 777-795.

Avalos, G. (2016). Growth of the neotropical palm Euterpe precatoria Mart. in an agroforestry system in Costa Rica. Brenesia, 85-86, 1-8.

Avalos, G., Fernández, M., & Engeln, J. T. (2013). Successional stage, fragmentation and exposure to extraction influence the population structure of Euterpe precatoria (Arecaeae). Revista de Biología Tropical, 61(3), 1415-1424.

Avalos, G., & Mulkey, S. S. (2014). Photosynthetic and morphological acclimation of seedlings of tropical lianas to changes in the light environment. American Journal of Botany, 101(12), 2088-2096.

Avalos, G., Mulkey, S. S., & Kitajima, K. (1999). Leaf optical properties of trees and lianas in the outer canopy of a tropical dry forest. Biotropica, 31(3), 517-520.

Avalos, G., Mulkey, S. S., Kitajima, K, & Wright, S.J. (2007). Colonization strategies of two liana species in a tropical dry forest canopy. Biotropica, 39(3), 393-399.

Baltzer, J. L., & Thomas, S. C. (2007). Determinants of whole-plant light requirements in Bornean rain forest tree saplings. Journal of Ecology, 95(6), 1208-1221.

Bazzaz, F. A., Chiariello, N. R., Coley, P. D., & Pitelka, L. F. (1987). Allocating resources to reproduction and defense. BioScience, 37(1), 58-67.

Benzing, D. H. (2008). Vascular epiphytes: general biology and related biota. Cambridge: Cambridge University Press.

Boege, K., & Marquis, R. J. (2005). Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution, 20(8), 441-448.

Boukili, V. K., & Chazdon, R. L. (2017). Environmental filtering, local site factors and landscape context drive changes in functional trait composition during tropical forest succession. Perspectives in Plant Ecology, Evolution and Systematics, 24, 37-47.

Bradshaw, C. J., Sodhi, N. S., & Brook, B. W. (2009). Tropical turmoil: a biodiversity tragedy in progress. Frontiers in Ecology and the Environment, 7(2), 79-87.

Brandani, A., Hartshorn, G. S., & Orians, G. H. (1988). Internal heterogeneity of gaps and species richness in Costa Rican tropical wet forest. Journal of Tropical Ecology, 4(2), 99-119.

Budowski, G. (1965). Distribution of tropical American rain forest species in the light of successional processes. Turrialba, 15(1), 40-42.

Cambronero, M., Avalos, G., & Alvarez-Vergnani, C. (2018). Carbon accumulation in seven neotropical palm species from different forest strata. Palms, 62(1), 25-34.

Campo, J., & Vázquez-Yanes, C. (2004). Effects of nutrient limitation on aboveground carbon dynamics during tropical dry forest regeneration in Yucatán, Mexico. Ecosystems, 7(3), 311-319.

Cardelús, C. L., & Chazdon, R. L. (2005). Inner-crown Microenvironments of Two Emergent Tree Species in a Lowland Wet Forest. Biotropica, 37(2), 238-244.

Chave, J., Coomes, D., Jansen, S., Lewis, S. L., Swenson, N. G., & Zanne, A. E. (2009). Towards a worldwide wood economics spectrum. Ecology Letters, 12(4), 351-366.

Chazdon, R. L. (1985). Leaf display, canopy structure, and light interception of two understory palm species. American Journal of Botany, 72(10), 1493-1502.

Chazdon, R. L. (1986). The costs of leaf support in understory palms: economy versus safety. The American Naturalist, 127(1), 9-30.

Chazdon, R. L. (2008). Chance and determinism in tropical forest succession. In W. Carson, & S. Schnitzer (Eds.), Tropical forest community ecology (pp. 384-409). Oxford: Wiley-Blackwell.

Chazdon, R. L. (2014). Second growth: the promise of tropical forest regeneration in an age of deforestation. Chicago: University of Chicago Press.

Chazdon, R. L., Chao, A., Colwell, R. K., Lin, S. Y., Norden, N., Letcher, S. G., ... & Arroyo, J. P. (2011). A novel statistical method for classifying habitat generalists and specialists. Ecology, 92(6), 1332-1343.

Chazdon, R. L., & Fetcher, N. (1984). Photosynthetic light environments in a lowland tropical rain forest in Costa Rica. The Journal of Ecology, 72(2), 553-564.

Chazdon, R. L., & Pearcy, R. W. (1991). The importance of sunflecks for forest understory plants. BioScience, 41(11), 760-766.

Chazdon, R. L., Pearcy, R. W., Lee, D. W., & Fetcher, N. (1996). Photosynthetic responses of tropical forest plants to contrasting light environments. In S. S. Mulkey, R. L. Chazdon, & A. P. Smith (Eds.), Tropical forest plant ecophysiology (pp. 5-55). Boston, MA: Springer.

Clark, D. B., & Clark, D. A. (1991). Herbivores, herbivory, and plant phenology: patterns and consequences in a tropical rain-forest cycad. In P. W. Price, T. M. Lewinsohn, G. W. Fernandes, & W. W. Benson (Eds.), Plant-animal interactions: evolutionary ecology in tropical and temperate regions (pp. 209-225). New York: John Wiley & Sons.

Clark, D. A., & Clark, D. B. (1992). Life history diversity of canopy and emergent trees in a neotropical rain forest. Ecological monographs, 62(3), 315-344.

Clark, D. B., Clark, D. A., & Oberbauer, S. F. (2010). Annual wood production in a tropical rain forest in NE Costa Rica linked to climatic variation but not to increasing CO2. Global Change Biology, 16(2), 747-759.

Clements, F. E. (1936). Nature and structure of the climax. Journal of Ecology, 24(1), 252-284.

Coley, P. D., Bryant, J. P., & Chapin, F. S. (1985). Resource availability and plant antiherbivore defense. Science, 230(4728), 895-899.

Condit, R., Hubbell, S. P., & Foster, R. B. (1996). Changes in tree species abundance in a neotropical forest: impact of climate change. Journal of tropical ecology, 12(2), 231-256.

Craine, J. M. (2005). Reconciling plant strategy theories of Grime and Tilman. Journal of Ecology, 93(6), 1041-1052.

Craine, J. M. (2007). Plant strategy theories: replies to Grime and Tilman. Journal of Ecology, 95(2), 235-240.

Craven, D., Hall, J. S., Berlyn, G. P., Ashton, M. S., & van Breugel, M. (2015). Changing gears during succession: shifting functional strategies in young tropical secondary forests. Oecologia, 179(1), 293-305.

Crayn, D. M., Winter, K., & Smith, J. A. C. (2004). Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences of the United States of America, 101(10), 3703-3708.

Diaz, S., Hodgson, J. G., Thompson, K., Cabido, M., Cornelissen, J. H. C., Jalili, A., ... & Band, S. R. (2004). The plant traits that drive ecosystems: evidence from three continents. Journal of Vegetation Science, 15(3), 295-304.

Dalling, J. W., Winter, K., Nason, J. D., Hubbell, S. P., Murawski, D. A., & Hamrick, J. L. (2001). The unusual life history of Alseis blackiana: a shade-persistent pioneer tree?. Ecology, 82(4), 933-945.

Denslow, J. S. (1987). Tropical rain forest gaps and tree species diversity. Annual Review of Ecology and Systematics, 18(1), 431-451.

Donoghue, M. J. (2008). A phylogenetic perspective on the distribution of plant diversity. Proceedings of the National Academy of Sciences, 105(Suppl. 1), 11549-11555.

Gilbert, B., Wright, S. J., Muller-Landau, H. C., Kitajima, K., & Hernandéz, A. (2006). Life history trade-offs in tropical trees and lianas. Ecology, 87(5), 1281-1288.

Givnish, T. J. (1988). Adaptation to sun and shade: a whole-plant perspective. Functional Plant Biology, 15(2), 63-92.

Givnish, T. J. (1999). On the causes of gradients in tropical tree diversity. Journal of Ecology, 87(2), 193-210.

Gleason, H. A. (1926). The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club, 53(1), 7-26.

Gómez-Pompa, A., & Vázquez-Yanes, C. (1981). Successional studies of a rain forest in Mexico. In D. C. West, H. H. Shugart, & D. B. Botkin (Eds.), Forest Succession (pp. 246-266). New York: Springer.

Gommers, C. M., Visser, E. J., St Onge, K. R., Voesenek, L. A., & Pierik, R. (2013). Shade tolerance: when growing tall is not an option. Trends in Plant Science, 18(2), 65-71.

Gravel, D., Canham, C. D., Beaudet, M., & Messier, C. (2010). Shade tolerance, canopy gaps and mechanisms of coexistence of forest trees. Oikos, 119(3), 475-484.

Greig, N. (1993). Regeneration mode in neotropical Piper: habitat and species comparisons. Ecology, 74(7), 2125-2135.

Grime, J. P. (1977). Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist, 111(982), 1169-1194.

Grime, J. P. (1989). Whole-plant responses to stress in natural and agricultural systems. In H. G. Jones, T. J. Flowers, & M. B. Jones (Eds.), Plants under stress: biochemistry, physiology and ecology and their application to plant improvement (pp. 31-46). Cambridge: Cambridge University Press.

Grime, J. P. (2007). Plant strategy theories: a comment on Craine (2005). Journal of Ecology, 95(2), 227-230.

Guariguata, M. R., & Ostertag, R. (2001). Neotropical secondary forest succession: changes in structural and functional characteristics. Forest Ecology and Management, 148(1-3), 185-206.

Hillebrand, H. (2004). On the generality of the latitudinal diversity gradient. The American Naturalist, 163(2), 192-211.

Hubbell, S. P. (1997). A unified theory of biogeography and relative species abundance and its application to tropical rain forests and coral reefs. Coral Reefs, 16(1), S9-S21.

Hubbell, S. P., Foster, R. B., O’Brien, S. T., Harms, K. E., Condit, R., Wechsler, B., ... & De Lao, S. L. (1999). Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science, 283(5401), 554-557.

Hubbell, S. P. (2001). The unified neutral theory of biodiversity and biogeography. Princeton & Oxford: Princeton University Press.

Huston, M. A. (1999). Local processes and regional patterns: appropriate scales for understanding variation in the diversity of plants and animals. Oikos, 86(3), 393-401.

Jansson, R., Rodríguez-Castañeda, G., & Harding, L. E. (2013). What can multiple phylogenies say about the latitudinal diversity gradient? A new look at the tropical conservatism, out of the tropics, and diversification rate hypotheses. Evolution, 67(6), 1741-1755.

Janzen, D. H. (1970). Herbivores and the number of tree species in tropical forests. The American Naturalist, 104(940), 501-528.

Kitajima, K. (1994). Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia, 98(3-4), 419-428.

Kitajima, K. (2002). Do shade-tolerant tropical tree seedlings depend longer on seed reserves? Functional growth analysis of three Bignoniaceae species. Functional Ecology, 16(4), 433-444.

Kitajima, K., Mulkey, S. S., & Wright, S. J. (2004). Variation in crown light utilization characteristics among tropical canopy trees. Annals of Botany, 95(3), 535-547.

Kitajima, K., & Poorter, L. (2008). Functional basis for resource niche partitioning by tropical trees. In W. P. Carson, & S. A. Schnitzer (Eds.), Tropical Forest Community Ecology (pp. 172-188). Oxford: Blackwell.

Kitajima, K., & Poorter, L. (2010). Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytologist, 186(3), 708-721.

Kobe, R. K., & Coates, K. D. (1997). Models of sapling mortality as a function of growth to characterize interspecific variation in shade tolerance of eight tree species of northwestern British Columbia. Canadian Journal of Forest Research, 27(2), 227-236.

Kozlowski, T. T., & Pallardy, S. G. (2002). Acclimation and adaptive responses of woody plants to environmental stresses. The Botanical Review, 68(2), 270-334.

Kraft, N. J., Adler, P. B., Godoy, O., James, E. C., Fuller, S., & Levine, J. M. (2015). Community assembly, coexistence and the environmental filtering metaphor. Functional Ecology, 29(5), 592-599.

Kraft, N. J., Valencia, R., & Ackerly, D. D. (2008). Functional traits and niche-based tree community assembly in an Amazonian forest. Science, 322(5901), 580-582.

Kursar, T. A., & Coley, P. D. (1992). Delayed greening in tropical leaves: an antiherbivore defense?. Biotropica, 24(2), 256-262.

Lebrija-Trejos, E., Pérez-García, E. A., Meave, J. A., Bongers, F., & Poorter, L. (2010). Functional traits and environmental filtering drive community assembly in a species-rich tropical system. Ecology, 91(2), 386-398.

Lebrija-Trejos, E., Pérez-García, E. A., Meave, J. A., Poorter, L., & Bongers, F. (2011). Environmental changes during secondary succession in a tropical dry forest in Mexico. Journal of Tropical Ecology, 27(5), 477-489.

Lee, D. W., Baskaran, K., Mansor, M., Mohamad, H., & Yap, S. K. (1996). Irradiance and spectral quality affect Asian tropical rain forest tree seedling development. Ecology, 77(2), 568-580.

Letcher, S. G. (2010). Phylogenetic structure of angiosperm communities during tropical forest succession. Proceedings of the Royal Society of London B: Biological Sciences, 277(1678), 97-104.

Letcher, S. G., Chazdon, R. L., Andrade, A. C., Bongers, F., van Breugel, M., Finegan, B., ... & Williamson, G. B. (2012). Phylogenetic community structure during succession: evidence from three Neotropical forest sites. Perspectives in Plant Ecology, Evolution and Systematics, 14(2), 79-87.

Letcher, S. G., Lasky, J. R., Chazdon, R. L., Norden, N., Wright, S. J., Meave, J. A., ... & Andrade, J. L. (2015). Environmental gradients and the evolution of successional habitat specialization: a test case with 14 Neotropical forest sites. Journal of Ecology, 103(5), 1276-1290.

Lohbeck, M., Lebrija-Trejos, E., Martínez-Ramos, M., Meave, J. A., Poorter, L., & Bongers, F. (2015). Functional trait strategies of trees in dry and wet tropical forests are similar but differ in their consequences for succession. PloS One, 10(4), e0123741.

MacArthur, R., & Levins, R. (1964). Competition, habitat selection, and character displacement in a patchy environment. Proceedings of the National Academy of Sciences, 51(6), 1207-1210.

Markesteijn, L., Poorter, L., Bongers, F., Paz, H., & Sack, L. (2011). Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance. New Phytologist, 191(2), 480-495.

Martínez-Ramos, M., Alvarez-Buylla, E., & Sarukhan, J. (1989). Tree demography and gap dynamics in a tropical rain forest. Ecology, 70(3), 555-558.

Martínez-Ramos, M., & Soto-Castro, A. (1993). Seed rain and advanced regeneration in a tropical rain forest. Vegetatio, 107(1), 299-318.

McCarthy, M. C., & Enquist, B. J. (2007). Consistency between an allometric approach and optimal partitioning theory in global patterns of plant biomass allocation. Functional Ecology, 21(4), 713-720.

McGill, B. J., Enquist, B. J., Weiher, E., & Westoby, M. (2006). Rebuilding community ecology from functional traits. Trends in Ecology & Evolution, 21(4), 178-185.

Meiners, S. J., Cadotte, M. W., Fridley, J. D., Pickett, S. T., & Walker, L. R. (2015). Is successional research nearing its climax? New approaches for understanding dynamic communities. Functional Ecology, 29(2), 154-164.

Melo, F. P., Arroyo-Rodríguez, V., Fahrig, L., Martínez-Ramos, M., & Tabarelli, M. (2013). On the hope for biodiversity-friendly tropical landscapes. Trends in Ecology & Evolution, 28(8), 462-468.

Mesquita, R. D. C. G., Massoca, P. E. D. S., Jakovac, C. C., Bentos, T. V., & Williamson, G. B. (2015). Amazon rain forest succession: stochasticity or land-use legacy? BioScience, 65(9), 849-861.

Mittelbach, G. G., Schemske, D. W., Cornell, H. V., Allen, A. P., Brown, J. M., Bush, M. B., ... & McCain, C. M. (2007). Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters, 10(4), 315-331.

Montgomery, R., & Chazdon, R. J. (2002). Light gradient partitioning by tropical tree seedlings in the absence of canopy gaps. Oecologia, 131(2), 165-174.

Muscarella, R., Uriarte, M., Aide, T. M., Erickson, D. L., Forero-Montaña, J., Kress, W. J., ... & Zimmerman, J. K. (2016). Functional convergence and phylogenetic divergence during secondary succession of subtropical wet forests in Puerto Rico. Journal of Vegetation Science, 27(2), 283-294.

Niinemets, Ü. (2006). The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited. Journal of Ecology, 94(2), 464-470.

Niinemets, Ü. (2010a). A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecological Research, 25(4), 693-714.

Niinemets, Ü. (2010b). Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. Forest Ecology and Management, 260(10), 1623-1639.

Norden, N., Angarita, H. A., Bongers, F., Martínez-Ramos, M., Granzow-de la Cerda, I., Van Breugel, M., ... & Finegan, B. (2015). Successional dynamics in Neotropical forests are as uncertain as they are predictable. Proceedings of the National Academy of Sciences, 112(26), 8013-8018.

Norden, N., Boukili, V., Chao, A., Ma, K. H., Letcher, S. G., & Chazdon, R. L. (2017). Opposing mechanisms affect taxonomic convergence between tree assemblages during tropical forest succession. Ecology Letters, 20(11), 1448-1458L.

Novotny, V., Drozd, P., Miller, S. E., Kulfan, M., Janda, M., Basset, Y., & Weiblen, G. D. (2006). Why are there so many species of herbivorous insects in tropical rain forests? Science, 313(5790), 1115-1118.

Oliver, C. D., & Larson, B. C. (1996). Forest stand dynamics: updated edition. New Jersey: John Wiley.

Pacala, S. W., & Rees, M. (1998). Models suggesting field experiments to test two hypotheses explaining successional diversity. The American Naturalist, 152(5), 729-737.

Peña-Claros, M., & Zuidema, P. (2000). Demographic limitations for the sustainable extraction of palm heart from Euterpe precatoria in two forest types in Bolivia. Ecología en Bolivia, 34, 7-25.

Peterson, C. J., & Carson, W. P. (2008). Processes constraining woody species succession on abandoned pastures in the tropics: on the relevance of temperate models of succession. In W. Carson, & S. Schnitzer (Eds.), Tropical forest community ecology (pp. 367-383). Oxford: Wiley-Blackwell.

Plourde, B. T., Boukili, V. K., & Chazdon, R. L. (2015). Radial changes in wood specific gravity of tropical trees: inter-and intraspecific variation during secondary succession. Functional Ecology, 29(1), 111-120.

Poorter, L. (2007). Are species adapted to their regeneration niche, adult niche, or both? The American Naturalist, 169(4), 433-442.

Poorter, L. (2009). Leaf traits show different relationships with shade tolerance in moist versus dry tropical forests. New Phytologist, 181(4), 890-900.

Poorter, L., & Arets, E. J. (2003). Light environment and tree strategies in a Bolivian tropical moist forest: an evaluation of the light partitioning hypothesis. Plant Ecology, 166(2), 295-306.

Poorter, L., Bongers, F., Sterck, F. J., & Wöll, H. (2005). Beyond the regeneration phase: differentiation of height-light trajectories among tropical tree species. Journal of Ecology, 93(2), 256-267.

Poorter, L., & Rose, S. A. (2005). Light-dependent changes in the relationship between seed mass and seedling traits: a meta-analysis for rain forest tree species. Oecologia, 142(3), 378-387.

Poorter, L., Wright, S. J., Paz, H., Ackerly, D. D., Condit, R., Ibarra-Manríquez, G., ... & Muller-Landau, H. C. (2008). Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology, 89(7), 1908-1920.

Prado, A., Sierra, A., Windsor, D., & Bede, J. C. (2014). Leaf traits and herbivory levels in a tropical gymnosperm, Zamia stevensonii (Zamiaceae). American Journal of Botany, 101(3), 437-447.

Prescott, C. E. (2002). The influence of the forest canopy on nutrient cycling. Tree physiology, 22(15-16), 1193-1200.

Putz, F. E. (1984). The natural history of lianas on Barro Colorado Island, Panama. Ecology, 65(6), 1713-1724.

Rees, M., Condit, R., Crawley, M., Pacala, S., & Tilman, D. (2001). Long-term studies of vegetation dynamics. Science, 293(5530), 650-655.

Reich, P. B. (2014). The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. Journal of Ecology, 102(2), 275-301.

Reich, P. B., Wright, I. J., Cavender-Bares, J., Craine, J. M., Oleksyn, J., Westoby, M., & Walters, M. B. (2003). The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences, 164(S3), S143-S164.

Richards, P.W. (1952). The tropical rain forest: an ecological study. Cambridge: Cambridge University Press.

Rosindell, J., Hubbell, S. P., & Etienne, R. S. (2011). The unified neutral theory of biodiversity and biogeography at age ten. Trends in Ecology &Evolution, 26(7), 340-348.

Santiago, L. S., & Wright, S. J. (2007). Leaf functional traits of tropical forest plants in relation to growth form. Functional Ecology, 21(1), 19-27.

Sapijanskas, J., Paquette, A., Potvin, C., Kunert, N., & Loreau, M. (2014). Tropical tree diversity enhances light capture through crown plasticity and spatial and temporal niche differences. Ecology, 95(9), 2479-2492.

Schaetzl, R. J., Burns, S. F., Johnson, D. L., & Small, T. W. (1988). Tree uprooting: review of impacts on forest ecology. Vegetatio, 79(3), 165-176.

Schaller, A. (2008). Induced plant resistance to herbivory. Berlin: Springer.

Schlichting, C. D., & Pigliucci, M. (1998). Phenotypic evolution: a reaction norm perspective. Sunderland: Sinauer.

Schnitzer, S. A., Mascaro, J., & Carson, W. P. (2008). Treefall gaps and the maintenance of plant species diversity in tropical forests. In W. P. Carson, & S. A. Schnitzer (Eds.), Tropical Forest Community Ecology (pp. 196-209). Oxford: Blackwell.

Schupp, E. W., Howe, H. F., Augspurger, C. K., & Levey, D. J. (1989). Arrival and survival in tropical treefall gaps. Ecology, 70(3), 562-564.

Schwalm, C. R., Anderegg, W. R., Michalak, A. M., Fisher, J. B., Biondi, F., Koch, G., ... & Huntzinger, D. N. (2017). Global patterns of drought recovery. Nature, 548(7666), 202.

Spasojevic, M. J., Yablon, E. A., Oberle, B., & Myers, J. A. (2014). Ontogenetic trait variation influences tree community assembly across environmental gradients. Ecosphere, 5(10), 1-20.

Sterck, F., Markesteijn, L., Schieving, F., & Poorter, L. (2011). Functional traits determine trade-offs and niches in a tropical forest community. Proceedings of the National Academy of Sciences, 108(51), 20627-20632.

Strauss-Deberiedetti, S., & Bazzaz, F. A. (1996). Photosynthetic characteristics of tropical trees along successional gradients. In S. S. Mulkey, R. L. Chazdon, & A. P. Smith (Eds.), Tropical forest plant ecophysiology (pp. 162-186). Boston: Springer.

Swaine, M. D., & Whitmore, T. C. (1988). On the definition of ecological species groups in tropical rain forests. Vegetatio, 75(1-2), 81-86.

Swenson, N. G., Stegen, J. C., Davies, S. J., Erickson, D. L., Forero-Montaña, J., Hurlbert, A. H., ... & Zimmerman, J. K. (2012). Temporal turnover in the composition of tropical tree communities: functional determinism and phylogenetic stochasticity. Ecology, 93(3), 490-499.

Svenning, J. C. (1999). Microhabitat specialization in a species-rich palm community in Amazonian Ecuador. Journal of Ecology, 87(1), 55-65.

Sylvester, O., & Avalos, G. (2013). Influence of light conditions on the allometry and growth of the understory palm Geonoma undata subsp. edulis (Arecaceae) of neotropical cloud forests. American Journal of Botany, 100(12), 2357-2363.

Tilman, D. (1977). Resource competition between plankton algae: an experimental and theoretical approach. Ecology, 58(2), 338-348.

Tilman, D. (1990). Constraints and tradeoffs: toward a predictive theory of competition and succession. Oikos, 58(1), 3-15.

Tilman, D. (1994). Competition and biodiversity in spatially structured habitats. Ecology, 75(1), 2-16.

Tomlinson, P. B. (2006). The uniqueness of palms. Botanical Journal of the Linnean Society, 151(1), 5-14.

Urban, M. C., Leibold, M. A., Amarasekare, P., De Meester, L., Gomulkiewicz, R., Hochberg, M. E., ... & Pantel, J. H. (2008). The evolutionary ecology of metacommunities. Trends in Ecology & Evolution, 23(6), 311-317.

Valladares, F., & Niinemets, Ü. (2008). Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology, Evolution, and Systematics, 39, 237-257.

Valladares, F., Laanisto, L., Niinemets, Ü., & Zavala, M. A. (2016). Shedding light on shade: ecological perspectives of understorey plant life. Plant Ecology & Diversity, 9(3), 237-251.

Valladares, F., Sánchez-Gómez, D., & Zavala, M. A. (2006). Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. Journal of Ecology, 94(6), 1103-1116.

Vellend, M. (2010). Conceptual synthesis in community ecology. The Quarterly Review of Biology, 85(2), 183-206.

Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., & Garnier, E. (2007). Let the concept of trait be functional! Oikos, 116(5), 882-892.

Way, D. A., & Pearcy, R. W. (2012). Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiology, 32(9), 1066-1081.

Webb, C. O. (2000). Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. The American Naturalist, 156(2), 145-155.

Webb, C. O., Ackerly, D. D., McPeek, M. A., & Donoghue, M. J. (2002). Phylogenies and community ecology. Annual Review of Ecology and Systematics, 33(1), 475-505.

Webb, C. O., Cannon, C. H., & Davies, S. J. (2008). Ecological organization, biogeography, and the phylogenetic structure of tropical forest tree communities. In W. P. Carson, & S. A. Schnitzer (Eds.), Tropical Forest Community Ecology (pp. 79-97). New Jersey: Wiley-Blackwell.

Weiher, E., Freund, D., Bunton, T., Stefanski, A., Lee, T., & S. Bentivenga. (2013). Advances, challenges and developing synthesis of ecological community assembly theory. Philosophical Transactions of the Royal Society B, 366, 2403-2413.

Weiner, J. (2004). Allocation, plasticity and allometry in plants. Perspectives in Plant Ecology, Evolution and Systematics, 6(4), 207-215.

West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.

Wright, J. S. (2002). Plant diversity in tropical forests: a review of mechanisms of species coexistence. Oecologia, 130(1), 1-14.

Wright, S. J., Kitajima, K., Kraft, N. J., Reich, P. B., Wright, I. J., Bunker, D. E., ... & Engelbrecht, B. M. (2010). Functional traits and the growth-mortality trade-off in tropical trees. Ecology, 91(12), 3664-3674.

Wright, S. J., Muller-Landau, H. C., Condit, R., & Hubbell, S. P. (2003). Gap-dependent recruitment, realized vital rates, and size distributions of tropical trees. Ecology, 84(12), 3174-3185.

Wright, I. J., Reich, P. B., Westoby, M., Ackerly, D. D., Baruch, Z., Bongers, F., ... & Flexas, J. (2004). The worldwide leaf economics spectrum. Nature, 428(6985), 821.

Zimmerman, J. K., Thompson, J., & Brokaw, N. (2008). Large tropical forest dynamics plots: testing explanations for the maintenance of species diversity. In W. Carson, & S. Schnitzer (Eds.), Tropical forest community ecology (pp. 98-117). Oxford: Wiley-Blackwell.

Zotz, G., & Hietz, P. (2001). The physiological ecology of vascular epiphytes: current knowledge, open questions. Journal of Experimental Botany, 52(364), 2067-2078.


Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Copyright (c) 2019 Revista de Biología Tropical


Download data is not yet available.