Hostname: page-component-77c89778f8-fv566 Total loading time: 0 Render date: 2024-07-24T23:05:23.780Z Has data issue: false hasContentIssue false

Isotopic composition of leaf carbon (δ13C) and nitrogen (δ15N) of deciduous and evergreen understorey trees in two tropical Brazilian Atlantic forests

Published online by Cambridge University Press:  17 April 2018

Angela Pierre Vitória*
Universidade Estadual do Norte Fluminense Darcy Ribeiro, Laboratório de Ciências Ambientais, Av. Alberto Lamego, 2000, UENF, CBB, Parque Califórnia, 28013–602, Campos dos Goytacazes, Rio de Janeiro, Brazil
Eleinis Ávila-Lovera
Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA
Tatiane de Oliveira Vieira
Universidade Estadual do Norte Fluminense Darcy Ribeiro, Laboratório de Ciências Ambientais, Av. Alberto Lamego, 2000, UENF, CBB, Parque Califórnia, 28013–602, Campos dos Goytacazes, Rio de Janeiro, Brazil
Ana Paula Lima do Couto-Santos
Departamento de Ciências Exatas e Naturais, Universidade Estadual do Sudoeste da Bahia, BR 415, Km 3, 45700-000, Itapetinga, Bahia, Brazil
Tiago José Pereira
Department of Nematology, University of California, Riverside, CA 92521, USA
Ligia Silveira Funch
Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, BR 116, Km 3, 44031–460, Feira de Santana, Bahia, Brazil
Leandro Freitas
Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão, 915, 22460-030, Rio de Janeiro, Brazil
Lia d'Afonseca Pedreira de Miranda
Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, BR 116, Km 3, 44031–460, Feira de Santana, Bahia, Brazil
Pablo J. F. Pena Rodrigues
Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão, 915, 22460-030, Rio de Janeiro, Brazil
Carlos Eduardo Rezende
Universidade Estadual do Norte Fluminense Darcy Ribeiro, Laboratório de Ciências Ambientais, Av. Alberto Lamego, 2000, UENF, CBB, Parque Califórnia, 28013–602, Campos dos Goytacazes, Rio de Janeiro, Brazil
Louis S. Santiago
Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA Smithsonian Tropical Research Institute, Apartado 0843–03092, Balboa, Republic of Panamá
*Corresponding author. Email:


Isotopic composition of leaf carbon (δ13C) and nitrogen (δ15N) is determined by biotic and abiotic factors. In order to determine the influence of leaf habit and site on leaf δ13C and δ15N in the understorey of two Atlantic forests in Brazil that differ in annual precipitation (1200 and 1900 mm), we measured these isotopes in the shaded understorey of 38 tropical tree species (20 in the 1200-mm site and 18 in the 1900-mm site). Mean site values for δ15N were significantly lower at the 1200-mm site (−1.4‰) compared with the 1900-mm site (+3.0‰), and δ13C was significantly greater in the 1200-mm site (−30.4‰) than in the 1900-mm site (−31.6‰). Leaf C concentration was greater and leaf N concentration was lower at 1200-mm than at 1900-mm. Leaf δ15N was negatively correlated with δ13C across the two sites. Leaf δ13C and δ15N of evergreen and deciduous species were not significantly different within a site. No significant phylogenetic signal for any traits among the study species was found. Overall, site differences were the main factor distinguishing traits among species, suggesting strong functional convergence to local climate and soils within each site for individuals in the shaded understorey.

Research Article
Copyright © Cambridge University Press 2018 

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.)



AMUNDSON, R., AUSTIN, A. T., SCHUUR, E. A. G., YOO, K., MATZEK, V., KENDALL, C., UEBERSAX, A., BRENNER, D. & BAISDEN, W. T. 2003. Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochemical Cycles 17: Art. No. 1031.Google Scholar
ASNER, G. P. & MARTIN, R. E. 2012. Contrasting leaf chemical traits in tropical lianas and trees: implications for future forest composition. Ecology Letters 15:10011007.Google Scholar
AUSTIN, A. T. & VITOUSEK, P. M. 1998. Nutrient dynamics on a precipitation gradient in Hawaii. Oecologia 113:519529.Google Scholar
BAI, E., BOUTTON, T., LIU, F., WU, X., ARCHER, S. & HALLMARK, C. 2009. Spatial variation of the stable nitrogen isotope ratio of woody plants along a topoedaphic gradient in a subtropical savanna. Oecologia 159:493503.Google Scholar
BORCHERT, R. 1998. Responses of tropical trees to rainfall seasonality. Climatic Change 39:381393.Google Scholar
BRAGA, N., VITÓRIA, A. P., SOUZA, G., BARROS, C. & FREITAS, L. 2016. Weak relationships between leaf phenology and isohydric and anisohydric behavior in lowland wet tropical forest trees. Biotropica 48:453464.Google Scholar
BUSTAMANTE, M. M. C., MARTINELLI, L. A., SILVA, D. A., CAMARGO, P. B., KLINK, C. A., DOMINGUES, T. F. & SANTOS, R. V. 2004. 15N natural abundance in woody plants and soils of Central brazilian savannas (cerrado). Ecological Applications 14:200213.CrossRefGoogle Scholar
CARVALHO, F. A., NASCIMENTO, M. T. & OLIVEIRA FILHO, A. T. 2008. Composition, richness and heterogeneity of the tree flora in the São João river basin, Rio de Janeiro State, Brasil. Acta Botanica Brasilica 22:929940.Google Scholar
CHABOT, B. F. & HICKS, D. J. 1982. The ecology of leaf life spans. Annual Review of Ecology and Systematics 13:229259.Google Scholar
CLARKE, K. R. & GORLEY, R. 2006. PRIMER v6: User manual/tutorial. PRIMER-E, Plymouth.Google Scholar
CORNWELL, W. K., WRIGHT, I. J., TURNER, J., MAIRE, V., CERNUSAK, L., DAWSON, T., ELLSWORTH, D., FARQUHAR, G., GRI, H., KEITEL, C., KNOHL, A., REICH, P., WILLIAMS, D., BHASKAR, R., CORNELISSEN, J. H. C., RICHARDS, A. & SCHMIDT, S. 2018. Multivariate climate regulates photosynthetic carbon isotope discrimination worldwide within C3 plants. Global Ecology Biogeography: submitted.CrossRefGoogle Scholar
COUTO, A. P. L., FUNCH, L. S. & CONCEIÇÃO, A. A. 2011. Floristic composition and physiognomy of a submontane seasonal semi-deciduous forest on Chapada Diamantina, Bahia, Brazil. Rodriguesia 62:391405.Google Scholar
DAWSON, T. E., MAMBELLI, S., PLAMBOEK, A. H., TEMPLER, P. H. & TU, K. P. 2002. Stable isotopes in plant ecology. Annual Review of Ecology and Systematics 33:507559.Google Scholar
EAMUS, D. & PRIOR, L. 2001. Ecophysiology of trees of seasonally dry tropics: comparisons among phenologies. Advances in Ecological Research 32:113197.Google Scholar
EHLERINGER, J. R. & COOPER, T. A. 1988. Correlation between carbon isotope ratio and microhabitat. Oecologia 76:562566.Google Scholar
EVANS, R. D. 2001. Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science 6: 121126.Google Scholar
FARQUHAR, G. & RICHARDS, R. 1984. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11:539552.Google Scholar
FARQUHAR, G., O'LEARY, M. & BERRY, J. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9:121137.Google Scholar
FARQUHAR, G. D., EHLERINGER, J. R. & HUBICK, K. T. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology Plant Molecular Biology 40:503537.Google Scholar
FONSECA, C. R., OVERTON, J. M., COLLINS, B. & WESTOBY, M. 2000. Shifts in trait-combinations along rainfall and phosphorus gradients. Journal of Ecology 88:964977.Google Scholar
FRANCO, A. C., BUSTAMANTE, M., CALDAS, L. S., GOLDSTEIN, G., MEINZER, F. C., KOZOVITS, A. R., RUNDEL, P. & CORADIN, V. T. R. 2005. Leaf functional traits of Neotropical savanna trees in relation to seasonal water deficit. Trees 19:326335.Google Scholar
FRANKIE, G. W., BAKER, H. G. & OPLER, P. A. 1974. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology 62:881919.Google Scholar
FUNCH, L. S., FUNCH, R. & BARROSO, G. M. 2002. Phenology of gallery and montane forest in the Chapada Diamantina, Bahia, Brazil. Biotropica 34:4050.Google Scholar
FUNCH, L. S., RODAL, M. J. N. & FUNCH, R. R. 2008. Floristic aspects of forests of the Chapada Diamantina, Bahia, Brazil. Pp. 193220 in Thomas, W. & Britton, E. G. (eds). The coastal forests of Northeastern Brazil. Springer and NYBG Press, New York.Google Scholar
HANDLEY, L. L., AUSTIN, A. T., ROBINSON, D., SCRIMGEOUR, C. M., RAVEN, J. A., HEATON, T. H. E., SCHMIDT, S. & STEWART, G. R. 1999. The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Australian Journal of Plant Physiology 26:185199.Google Scholar
HASSELQUIST, N. J., ALLEN, M. F. & SANTIAGO, L. S. 2010a. Water relations of evergreen and drought-deciduous trees along a seasonally dry tropical forest chronosequence. Oecologia 164: 881890.Google Scholar
HASSELQUIST, N. J., SANTIAGO, L. S. & ALLEN, M. F. 2010b. Belowground nitrogen dynamics in relation to hurricane damage along a tropical dry forest chronosequence. Biogeochemistry 98:89100.CrossRefGoogle Scholar
HÖGBERG, P. 1997. 15N natural abundance in soil-plant systems. New Phytologist 137:179203.Google Scholar
IBGE. 2012. Technical manual of the Brazilian vegetation. Instituto Brasileiro de Geografia e Estatística -IBGE, Rio de Janeiro. 271 pp.Google Scholar
JOETZJER, E., DELIRE, C., DOUVILLE, H., CIAIS, P., DECHARME, B., FISHER, R., CHRISTOFFERSEN, B., CALVET, J. C., DA COSTA, A. C. L., FERREIRA, L. V. & MEIR, P. 2014. Predicting the response of the Amazon rainforest to persistent drought conditions under current and future climates: a major challenge for global land surface models. Geoscientific Model Development 7:29332950.Google Scholar
KEMBEL, S. W., ACKERLY, D. D., BLOMBERG, S. P., CORNWELL, W. K., COWAN, P. D., HELMUS, M. R., MORLON, H. & WEBB, C. O. 2010. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:14631464.Google Scholar
KIKUZAWA, K. 1991. A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern. American Naturalist 138:12501263.Google Scholar
KOTTEK, M., GRIESER, J., BECK, C., RUDOLF, B. & RUBEL, F. 2006. World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift 15:259263.CrossRefGoogle Scholar
LEFFLER, A. J. & ENQUIST, B. J. 2002. Carbon isotope composition of tree leaves from Guanacaste, Costa Rica: comparison across tropical forests and tree life history. Journal of Tropical Ecology 18: 151159.Google Scholar
LIMA, J. A. DE S., VILLELA, D. M., FILHO, B. C. & PÉREZ, D. V. 2011. Fine roots biomass in fragments of Atlantic Forest from Rio de Janeiro State. Floresta 41:2738.Google Scholar
LLOYD, J. & FARQUHAR, G. D. 1994. 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99:201215.Google Scholar
MA, J.-Y., SUN, W., LIU, X.-N. & CHEN, F.-H. 2012. Variation in the stable carbon and nitrogen isotope composition of plants and soil along a precipitation gradient in northern China. PLoS ONE 7:e51894.Google Scholar
MARSHALL, J. D. & ZHANG, J. 1994. Carbon isotope discrimination and water-use efficiency in native plants of the north-central rockies. Ecology 75:18871895.Google Scholar
MARTINELLI, L. A., PICCOLO, M. C., TOWNSEND, A. R., CUEVAS, E., ROBERTSON, G. P. & TRESEDER, K. 1999. Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:4565.Google Scholar
MARTINELLI, L. A., OMETTO, J. P. H. B., FERRAZ, E. S., VICTORIA, R. L., CAMARGO, P. B. & MOREIRA, M. Z. 2009. Nitrogen – soil and plants. Pp. 6579 in Martinelli, L. A., Ometto, J. P. H. B., Ferraz, E. S., Victoria, R. L., Camargo, P. B. & Moreira, M. Z. (eds). Uncovering environmental issues with stable isotopes. Oficina de Textos Press, Sao Paulo.Google Scholar
MEDINA, E., STERNBERG, L. & CUEVAS, E, 1991. Vertical stratification of δ13C values in closed natural and plantation forest in the Luquillo mountains, Puerto Rico. Oecologia 87:369372.Google Scholar
MORELLATO, L. P. C. & HADDAD, C. F. B. 2000. Introduction: the Brazilian Atlantic Forest. Biotropica 32:786792.Google Scholar
NARDOTO, G. B., PIERRE, J., BALBAUD, H., EHLERINGER, J. R., HIGUCHI, N., MARIA, M. & MARTINELLI, L. A. 2008. Understanding the influences of spatial patterns on N availability within the Brazilian Amazon forest. Ecosystems 11:12341246.Google Scholar
OMETTO, J. H. B., EHLERINGER, J. R., DOMINGUES, T. F., BERRY, J. A., ISHIDA, F. Y., MAZZI, E., HIGUCHI, N., FLANAGAN, L. B., NARDOTO, G. B. & MARTINELLI, L. A. 2006. The stable carbon and nitrogen isotopic composition of vegetation in tropical forests of the Amazon Basin, Brazil. Biogeochemistry 79:251274.Google Scholar
PAN, Y., BIRDSEY, R. A., FANG, J., HOUGHTON, R., KAUPPI, P. E., KURZ, W. A., PHILLIPS, O. L., SHVIDENKO, A., LEWIS, S. L., CANADELL, J. G., CIAIS, P., JACKSON, R. B., PACALA, S. W., MCGUIRE, A. D., PIAO, S., RAUTIAINEN, A., SITCH, S. & HAYES, D. 2011. A large and persistent carbon sink in the world's forests. Science 333: 988993.Google Scholar
POWERS, J. S. & TIFFIN, P. 2010. Plant functional type classifications in tropical dry forests in Costa Rica: leaf habit versus taxonomic approaches. Functional Ecology 24:927936.CrossRefGoogle Scholar
PRINGLE, E. G., ADAMS, R. I., BROADBENT, E., BUSBY, P. E., DONATTI, C. I., KURTEN, E. L., RENTON, K. & DIRZO, R. 2011. Distinct leaf-trait syndromes of evergreen and deciduous trees in a seasonally dry tropical forest. Biotropica 43:299308.Google Scholar
PUTZ, F. E., BLATE, G. M., REDFORD, K. H. & FIMBEL, R. 2001. Tropical forest management and conservation of biodiversity: an overview. Conservation Biology 15:720.Google Scholar
RICHARDS, P. W. 1998. The tropical rain forest: an ecological study. (Second edition). Cambridge University Press, Cambridge. 575 pp.Google Scholar
ROSSATTO, D. R., HOFFMANN, W. A., DE CARVALHO RAMOS SILVA, L., HARIDASAN, M., STERNBERG, L. S. L. & FRANCO, A. C. 2013. Seasonal variation in leaf traits between congeneric savanna and forest trees in Central Brazil: Implications for forest expansion into savanna. Trees – Structure and Function 27:11391150.Google Scholar
RUZICKA, K. J., PUETTMANN, K. J. & BROOKS, R. 2017. Cross-scale interactions affect tree growth and intrinsic water use efficiency and highlight the importance of spatial context in managing forests under global change. Journal of Ecology 105: 14251436.Google Scholar
SANTIAGO, L. S., KITAJIMA, K., WRIGHT, S. J. & MULKEY, S. S. 2004. Coordinated changes in photosynthesis, water relations and leaf nutritional traits of canopy trees along a precipitation gradient in lowland tropical forest. Oecologia 139:495502.Google Scholar
SANTIAGO, L. S., SILVERA, K., ANDRADE, J. L. & DAWSON, T. E. 2005. El uso de isotopos estables en biologia tropical. Interciencia 30:536542.Google Scholar
SANTIAGO, L. S., SILVEIRA, K., ANDRADE, J. L. & DAWSON, T. E. 2017. Functional strategies of tropical dry forest plants in relation to growth form and isotopic composition. Environmental Research Letters 12:115006.Google Scholar
SCHULZE, E. D., WILLIAMS, R. J., FARQUHAR, G. D., SCHULZE, W., LANGRIDGE, J., MILLER, J. M. & WALKER, B. H. 1998. Carbon and nitrogen isotope discrimination and nitrogen nutrition of trees along a rainfall gradient in northern Australia. Functional Plant Biology 25:413425.Google Scholar
SCHUUR, E. A. & MATSON, P. A. 2001. Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431442.Google Scholar
SOBRADO, M. A. & EHLERINGER, J. R. 1997. Leaf carbon isotope ratios from a tropical dry forest in Venezuela. Flora 192:112124.Google Scholar
TER STEEGE, H. & HAMMOND, D. S. 2001. Character convergence, diversity, and disturbance in tropical rain forest in Guyana. Ecology 82:31973212.Google Scholar
TER STEEGE, H., PITMAN, N. C. A., SABATIER, D., BARALOTO, C., SALOMÃO, R. P., GUEVARA, J. E., PHILLIPS, O. L., CASTILHO, C. V., MAGNUSSON, W. E., MOLINO, J.-F., MONTEAGUDO, A., NÚÑEZ VARGAS, P., MONTERO, J. C., FELDPAUSCH, T. R., CORONADO, E. N. H., KILLEEN, T. J., MOSTACEDO, B., VASQUEZ, R., ASSIS, R. L., TERBORGH, J. et al. 2013. Hyperdominance in the Amazonian tree flora. Science 342:1243092–1243092.Google Scholar
SWOFFORD, D. L. 2002. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland. 142 pp.Google Scholar
VALLADARES, F., SKILLMAN, J. B. & PEARCY, R. W. 2002. Convergence in light capture efficiencies among tropical forest understory plants with contrasting crown architectures: a case of morphological compensation. American Journal of Botany 89:12751284. Appendix 1.Google Scholar
VITORIA, A. P., VIEIRA, T. DE, O., CAMARGO, P. DE B. & SANTIAGO, L. S. 2016. Using leaf 13C and photosynthetic parameters to understand acclimation to irradiance and leaf age effects during tropical forest regeneration. Forest Ecology and Management 379: 5060.Google Scholar
XIAO, L., YANG, H., SUN, B. LI, X. & GUO, J. 2013. Stable isotope compositions of recent and fossil sun/shade leaves and implications for paleoenvironmental reconstruction. Review of Paleobotany and Palynology 190:7584.Google Scholar
ZANNE, A. E., TANK, D. C., CORNWELL, W. K., EASTMAN, J. M., SMITH, S. A, FITZJOHN, R. G., MCGLINN, D. J., O'MEARA, B. C., MOLES, A. T., REICH, P. B., ROYER, D. L., SOLTIS, D. E., STEVENS, P. F., WESTOBY, M., WRIGHT, I. J., AARSSEN, L., BERTIN, R. I., CALAMINUS, A., GOVAERTS, R., HEMMINGS, F. et al. 2014. Three keys to the radiation of angiosperms into freezing environments. Nature 506:8992.Google Scholar