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

Resource allocation in Copaifera langsdorffii (Fabaceae): how a supra-annual fruiting affects plant traits and herbivory?
PT 64-2 JUN 2016

Supplementary Files

Cover letter


galling insects
mass fruiting
plant defenses
defensas de plantas
distribución de recursos (trade-off) en plantas
fructificación masiva
insectos formadores de agallas.

How to Cite

Costa, F. V. da, Queiroz, A. C. M. de, Maia, M. L. B., Júnior, R. R., & Fagundes, M. (2016). Resource allocation in Copaifera langsdorffii (Fabaceae): how a supra-annual fruiting affects plant traits and herbivory?. Revista De Biología Tropical, 64(2), 507–520.


Plants have limited resources to invest in reproduction, vegetative growth and defense against herbivorous. Trade-off in resources allocation promotes changes in plant traits that may affect higher trophic levels. In this study, we evaluated the trade-off effect between years of high and low fruiting on the investment of resources for growth and defense, and their indirect effects on herbivory in Copaifera langsdorffii. Our questions were: (i) does the resource investment on reproduction causes a depletion in vegetative growth as predicted by the Carbon/Nutrient Balance hypothesis (CNBH), resulting in more availability of resources to be allocated for defense?, (ii) does the variation in resource allocation for growth and defense between years of high and low fruiting leads to indirect changes in herbivory? Thirty-five trees located in a Cerrado area were monitored during 2008 (year of high fruiting) and 2009 (year of no fruiting) to evaluate the differential investment in vegetative traits (biomass, growth and number of ramifications), plant defense (tannin concentration and plant hypersensitivity) and herbivory (galling attack and folivory). According to our first question, we observed that in the fruiting year, woody biomass negatively affected tannin concentration, indicating that fruit production restricted the resources that could be invested both in growth as in defense. In the same way, we observed an inter-annual variation in herbivorous attack, and found that plants with higher leaf biomass and tannin concentration, experienced higher galling attack and hypersensitive reaction, regardless years. These findings suggested that plants’ resistance to herbivory is a good proxy of plant defense and an effective defense strategy for C. langsdorffii, besides the evidence of indirect responses of the third trophic, as postulated by the second question. In summary, the supra-annual fruiting pattern promoted several changes on plant development, demonstrating the importance of evaluating different plant traits when characterizing the vegetative investment. As expected by theory, the trade-off in resource allocation favored changes in defense compounds production and patterns of herbivory. The understanding of this important element of insect-plant interactions will be fundamental to decipher coevolutionary life histories and interactions between plant species reproduction and herbivory. Besides that, only through long-term studies we will be able to build models and develop more accurate forecasts about the factors that trigger the bottom-up effect on herbivory performance, as well the top-down effect of herbivores on plant trait evolution.


Abrahamson, W. G., & Caswell, H. (1982). On the comparative allocation of biomass, energy, and nutrients in plants. Ecology, 63, 982-991.

Baldwin, I. T., Gorham, D., Schmelz, E. A., Lewandowski, C. A., & Lynds, G. Y. (1998). Allocation of nitrogen to an inducible defense and seed production in Nicotiana attenuata. Oecologia, 115, 541-552.

Barbosa, M., & Fernandes, G. W. (2014). Bottom-up effects on gall distribution. En G. W. Fernandes & J. C. Santos (Eds.), Neotropical Insect Galls (pp. 99-113). New York: Springer.

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

Bryant, J. P., Chapin, F. S., & Klein, D. R. (1983). Carbon/Nutrient Balance of Boreal Plants in Relation to Vertebrate Herbivory. Oikos, 40, 357-368.

Buckley, N. E., & Sakar, G. A. (2013). Reproduction, growth, and defense trade-offs vary with gender and reproductive allocation in Ilex glabra (Aquifoliaceae). American Journal of Botany, 100, 357-364.

Coley, P. D. (1986). Costs and benefits of defense by tannins in a neotropical tree. Oecologia, 70, 238-241.

Coley, P. D., & Barone, J. A. (1996). Herbivory and plant defenses in tropical forests. Annual Review of Ecology, Evolution, and Systematics, 27, 305-335.

Costa, F. V., Fagundes, M. F., & Neves, F. S. (2010). Arquitetura da planta e diversidade de galhas associadas à Copaifera langsdorffii (Fabaceae). Ecología Austral, 20, 9-17.

Crawley, M. J. (2007). The R Book. Londres: John Wiley & Sons.

Dias, H. C. T., & Oliveira-Filho, A. T. (1996). Fenologia de quatro espécies arbóreas de uma floresta estacional semidecídua em Lavras, MG. Cerne, 2, 66-88.

Dyer, L. A., Letourneau, D. K., Dodson, C. D., Tobler, M. A., Stireman III, J. O., & Hsu, A. (2004). Ecological Causes and Consequences of Variation in Defensive Chemistry of a Neotropical Shrub. Ecology, 85, 2795-2803.

Espírito-Santo, M. M., Neves, F. S., Andrade-Neto, F. R., & Fernandes, G. W. (2007). Plant architecture and meristem dynamics as the mechanisms determining the diversity of gall-inducing insects. Oecologia, 153, 353-364.

Fagundes, M., Maia, M. L. B., Queiroz, A. C. M., Fernandes, G. W., & Costa, F. V. (2013a). Seed predation of Copaifera langsdorffii Desf. (Fabaceae: Caesalpinioideae) by Rhinochenus brevicollis Chevrolat (Coleoptera: Curculionidae) in a Cerrado fragment. Ecología Austral, 23, 218-221.

Fagundes, M., Costa, F. V., Antunes, S. F., Maia, M. L. B., Queiroz, A. C. M., Oliveira, L. Q., & Faria, M. L. (2013b). The role of historical and ecological factors on initial survival of Copaifera langsdorffii Desf. (Fabaceae). Acta Botanica Brasilica, 27, 480-487.

Faria, M., & Fernandes, G. W. (2001). Vigour of a dioecious shrub and attack by a galling herbivore. Ecological Entomology, 26, 37-45.

Feeny, P. (1976). Plant apparency and chemical defense. Recent Advances in Phytochemistry, 10, 1-40.

Fernandes, G. W. (1990). Hypersensitivity: a neglected plant resistance mechanism against insect herbivores. Environmental Entomology, 19, 1173-1182.

Fernandes, G. W., & Negreiros, D. (2001). The occurrence and effectiveness of hypersensitive reaction against galling herbivores across host taxa. Ecological Entomology, 26, 46-55.

Fernandes, G. W., & Price, P. W. (1992). The adaptative significance of insect gall distribution: survivorship of species in xeric and mesic habitat. Oecologia, 90, 14-20.

Fernandes, G. W., Santos, J. C., & Gomes, V. M. (2012). Misleading herbivory in a tropical tree. Anthropod-Plant Interactions, 6, 649-654.

Fowler, H. G., & Duarte, L. C. (1991). Herbivore pressure in a Brazilian Cerrado. Naturalia, 16, 99-102.

Freitas, C. V., & Oliveira, P. E. (2002). Biologia reprodutiva de Copaifera langsdorffii Desf. (Leguminosae, Caesalpinioideae). Brazilian Journal of Botany, 25, 311-321.

Hagerman, A. E. (1987). Radial diffusion method for determining tannin in plant extracts. Journal of Chemical Ecology, 13, 437-449.

Haring, D. A., Huber, M. J., Suter, D., Edwards, P. J., & Scher, A. L. U. (2008). Plant enemy-derived elicitors increase the foliar tannin concentration of Onobrychis viciifolia without a trade-off to growth. Annals of Botany, 102, 979-987.

Hartley, S. E. (1998). The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia, 113, 492-501.

Haslam, E. (1988). Plant polyphenols (syn. vegetable tannins) and chemical defense - a reappraisal. Journal of Chemical Ecology, 14, 1789-1806.

Herms, D. A., & Mattson, W. J. (1992). The dilemma of the plants: To grow or to defend. The Quarterly Review of Biology, 67, 283-335.

Hess, M. D., Abrahamson, W. G., & Brown, J. M. (1996). Intraspecific Competition in the Goldenrod Ball-Gallmaker (Eurosta solidaginis): Larval Mortality, Adult Fitness, Ovipositional and Host-Plant Response. The American Naturalist, 136, 121-133.

Imaji, A., & Seiwa, K. (2010). Carbon allocation to defense, storage, and growth in seedlings of two temperate broad-leaved tree species. Oecologia, 162, 273-281.

Isagi, Y., Sugimura, K., Sumida, A., & Ito, H. (1997). How does masting happen and synchronize? Journal of Theoretical Biology, 187, 231-239.

Ishihara, M. I., & Kikuzawa, K. (2009). Annual and spatial variation in shoot demography associated with masting in Betula grossa: comparison between mature trees and saplings. Annals of Botany, 104, 1195-1205.

Janzen, D. H. (1971). Seed predation by animals. Annual Review of Ecology, Evolution, and Systematics, 2, 465-492.

Jing, S. W., & Coley, P. D. (1990). Dioecy and herbivory: the effect of growth rate on plant defense in Acer negundo. Oikos, 58, 369-377.

Kelly, D. (1994). The evolutionary ecology of mast seeding. Trends in Ecology and Evolution, 9, 465-470.

Kelly, D., & Sork, V. L. (2002). Mast seeding in perennial plants: why, how, where? Annual Review of Ecology, Evolution, and Systematics, 33, 427-447.

Larcher, W. (1995). Physiological Plant Ecology. Berlin: Springer Verlag.

Leite, A. M. C., & Salomão, N. A. (1992). Estrutura populacional de regenerantes de copaíba (Copaifera langsdorffii Desf.) em mata ciliar do Distrito Federal. Acta Botanica Brasilica, 6, 123-134.

Marquis, R. J., Diniz, I. R., & Morais, H. C. (2001). Patterns and correlates of interspecific variation in foliar insect herbivory and pathogen attack in Brazilian Cerrado. Journal of Tropical Ecology, 17, 127-148.

Mole, S. (1994). Trade-Offs and Constraints in Plant-Herbivore Defense Theory: A Life-History Perspective. Oikos, 71, 3-12.

Monks, A., & Kelly, D. (2006). Testing the resource-matching hypothesis in the mast seeding tree Nothofagus truncata (Fagaceae). Austral Ecology, 31, 366-375.

Neves, F. S., Araújo, L. S., Fagundes, M., Espírito-Santo, M. M., Fernandes, G. W., Sánchez-Azofeifa, G. A., & Quesada, M. (2010). Canopy herbivory and insect herbivore diversity in a dry forest-savana transition in Brazil. Biotropica, 42, 112-118.

Newstrom, L. E., Frankie, G. W., & Baker, H. G. (1994). A New classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica, 26, 141-159.

Norton, D. A., & Kelly, D. (1988). Mast seeding over 33 years by Dacrydium cupressinum Lamb. (rimu) (Podocarpaceae) in New Zealand: the importance of economies of scale. Functional Ecology, 2, 399-408.

Obeso, J. R. (2002). The costs of reproduction in plants. New Phytologist, 155, 321-348.

Pedroni, F., Sanchez, M., & Santos, A. M. (2002). Fenologia da copaíba (Copaifera langsdorffii Desf. - Leguminosae, Caesalpinioideae) em uma floresta semidecídua no sudeste do Brasil. Revista Brasileira de Botânica, 25, 183-194.

R Development Core Team (2008). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

Rasband, W. S. (1997-2014). Image J. U. S. National Institutes of Health, Bethesda, Maryland, USA. Available at:

Ribeiro, S. P., Braga, O. A., Silva, C. H. L., & Fernandes, G. W. (1999). Leaf polyphenols in brazilian melastomataceae: sclerophylly, habitats, and insect herbivores. Ecotropica, 5, 137-146.

Rizzini, C. T. (1997). Tratado de Fitogeografia do Brasil: Aspectos Ecológicos, Sociológicos e Florísticos. Rio de Janeiro: Âmbito Cultural.

Roslin, T., & Salminen, J. P. (2008). Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos, 117, 1560-1568.

Sandvik, S. M., & Eide, W. (2009). Costs of reproduction in circumpolar Parnassia palustris in light of global warming. Plant Ecology, 205, 1-11.

Satake, A., & Iwasa Y. (2000). Pollen coupling of forest trees: forming synchronized and periodic reproduction out of chaos. Journal of Theoretical Biology, 203, 63-84.

Sebbenn, A. M., Carvalho, A. C. M., Freitas, M. L. M., Moraes, S. M. B., Gaino, A. P. S. C., da Silva, J. M., Jolivet, C., & Moraes, M. L. T. (2011). Low levels of realized seed and pollen gene flow and strong spatial genetic structure in a small, isolated and fragmented population of the tropical tree Copaifera langsdorffii Desf. Heredity, 106, 134-145.

Silva, J. O., Jesus, F. M., Fagundes, M., & Fernandes, G. W. (2009). Esclerofilia, taninos e insetos herbívoros associados a Copaifera langsdorffii Desf. (Fabaceae: Caesalpinioideae) em área de transição Cerrado - Caatinga no Brasil. Ecología Austral, 19, 197-206.

Reproductive strategy of Copaifera langsdorffii (Fabaceae): more seeds or better seeds?

Souza, M. L., Solar R. R., & Fagundes M. (2015). Revista de Biología Tropical, 63. 1161-1167.

Stamp, S. (2003). Out of the Quagmire of Plant Defense Hypotheses. The Quarterly Review of Biology, 78, 23-55.

Stone, G. N., & Schönrogge, K. (2003). The adaptive significance of insect gall morphology. Trends in Ecology and Evolution, 18, 512-522.

Weiner, J., Campbell, L. G., Pino, J., & Echarte, L. (2009). The allometry of reproduction within plant populations. Journal of Ecology, 97, 1220-1233.

Westphal, E., Bronner, R., & Le Ret, M. (1981). Changes in leaves of susceptible and resistant Solanum dulcamara infested by the gall mite Eriophyes cladophthirus (Acarina, Eriphyoidea). Canadian Journal of Botany, 59, 875-882.



Download data is not yet available.