Skip to main content
Download PDF

The successional status of tropical rainforest tree species is associated with differences in leaf carbon isotope discrimination and functional traits

Le statut successionnel des espèces de la forêt tropicale humide est associé à des différences de discrimination isotopique du carbone et de traits fonctionnels foliaires

Annals of Forest Science volume 64, pages 169–176 (2007)Cite this article

Abstract

We characterised the among species variability in leaf gas exchange and morphological traits under controlled conditions of seedlings of 22 tropical rainforest canopy species to understand the origin of the variability in leaf carbon isotope discrimination (Δ) among species with different growth and dynamic characteristics (successional gradient). Our results first suggest that these species pursue a consistent strategy in terms of Δ throughout their ontogeny (juveniles grown here versus canopy adult trees from the natural forest). Second, leaf Δ was negatively correlated with WUE and N, and positively correlated with gs, but among species differences in Δ were mainly explained by differences in WUE. Finally, species belonging to different successional groups display distinct leaf functional and morphological traits. We confirmed that fast growing early successional species maximise carbon assimilation with high stomatal conductance. In contrast, fast and slow growing late successional species are both characterised by low carbon assimilation values, but by distinct stomatal conductance and leaf morphological features. Along the successional gradient, these differences result in much lower Δ for the intermediate species (i.e. fast growing late successional) as compared to the two other groups.

Résumé

Nous avons caractérisé la variabilité interspécifique des échanges gazeux et des traits morphologiques foliaires en conditions environnementales contrôlées de jeunes plants de 22 espèces d’arbres de la canopée en forêt tropicale humide afin de comprendre l’origine de la variabilité de la discrimination isotopique du carbone foliaire (Δ) observée entre ces espèces présentant des caractéristiques de croissance et de dynamique distinctes (groupes successionnels). Nous montrons premièrement que les espèces tropicales possèdent une stratégie très conservée de Δ au cours de leur ontogénie (juvéniles élevés ici versus arbres adultes de la canopée en forêt naturelle). Deuxièmement, Δ était négativement corrélée à WUE et N, et positivement à gs, mais les différences de Δ entre espèces sont principalement expliquées par des différences de WUE. Enfin, nous montrons que les espèces appartenant à des groupes successionnels distincts présentent des traits fonctionnels et morphologiques foliaires distincts. Nous confirmons que les espèces à croissance rapide qui s’installent en premier au cours de la succession écologique (FE) maximisent A avec de fortes conductances stomatiques. Les espèces climax (qui s’installent en second dans la succession écologique), à croissance rapide (FL) ou à croissance faible (SL), présentent des valeurs de A identiques, mais des valeurs de gs ainsi que des caractéristiques morphologiques foliaires distinctes. Dans la succession écologique, ces différences se traduisent par des valeurs de Δ nettement plus faibles pour les espèces intermédiaires (c’est-à-dire les espèces climax à croissance rapide) par rapport aux deux autres groupes.

References

  1. Badeck F.W., Tcherkez G., Nogue S., Piel C., Ghashghaie J., Post-photosynthetic fractionation of stable carbon isotopes between plant organs — a widespread phenomenon, Rapid. Commun. Mass Spectrom. 19 (2005) 1381–1391.

    Article  PubMed  CAS  Google Scholar 

  2. Barbour M.M., Farquhar G.D., Relative humidity- and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves, Plant Cell Environ. 23 (2000) 473–485.

    Article  CAS  Google Scholar 

  3. Bazzaz F.A., Picket S.T.A., Physiological ecology of a tropical succession: a comparative review, Annu. Rev. Ecol. Syst. 11 (1980) 287–310.

    Article  Google Scholar 

  4. Béna P., Essences forestières de Guyane, Imprimerie Nationale, 1960.

  5. Boggan J., Funk V., Kelloff C., Hoff M., Cremers G., Feuillet C., Checklist of the plants of the Guianas: Guiana, Surinam, French Guiana, Georgetown, Guyana, 1997.

  6. Bonal D., Barigah T.S., Granier A., Guehl J.-M., Late stage canopy tree species with extremely low Δ13C and high stomatal sensitivity to seasonal soil drought in the tropical rainforest of French Guiana, Plant Cell Environ. 23 (2000) 445–459.

    Article  Google Scholar 

  7. Bonal D., Sabatier D., Montpied P., Tremeaux D., Guehl J.-M., Interspecific variability of Δ13C among canopy trees in rainforests of French Guiana: Functional groups and canopy integration, Oecologia 124 (2000) 454–468.

    Article  Google Scholar 

  8. Caemmerer S. von, Farquhar G.D., Some relationships between the biochemistry of photosynthesis and the gas exchange rates of leaves, Planta 153 (1981) 376–387.

    Article  Google Scholar 

  9. Cao K.F., Water relations and gas exchange of tropical saplings during a prolonged drought in a Bornean heath forest, with reference to root architecture, J. Trop. Ecol. 16 (2000) 101–116.

    Article  Google Scholar 

  10. Coste S., Roggy J.-C, Imbert P., Born C., Bonal D., Dreyer E., Leaf photosynthetic traits of 14 tropical rain forest species in relation to leaf nitrogen concentration and shade tolerance, Tree Physiol. 25 (2005) 1127–1137.

    PubMed  CAS  Google Scholar 

  11. Covone F., Gratani L., Age-related physiological and structural traits of chestnut coppices at the Castelli Romani park (Italy), Ann. For. Sci. 63 (2006) 239–247.

    Article  Google Scholar 

  12. Cowan I.R., Economics of carbon fixation in higher plants, in: Givnish T.J. (Ed.), On the economy of plant form and function, Cambridge University Press, Cambridge, 1986, pp. 133–170.

    Google Scholar 

  13. Ehleringer J.R., Gas exchange implications of isotopic variation in arid-land plants, in: Smith J.A.C., Griffiths H. (Eds.), Water deficits, plant responses from cell to community, Environmental Plant Biology Series, Lancaster, UK, 1993, pp. 265–284.

  14. Ehleringer J.R., Hall A.E., Farquhar G.D., Stable isotopes and plant-carbon water relations, Academic Press Inc., 1993.

  15. Ellis A.R., Hubbell S.P., Potvin C., In situ field measurements of photosynthetic rates of tropical tree species: a test of the functional group hypothesis, Can. J. Bot. 78 (2000) 1336–1347.

    Google Scholar 

  16. Ellsworth D.S., Reich P.B., Photosynthesis and leaf nitrogen in five Amazonian tree species during early secondary succession, Ecology 77 (1996) 581–594.

    Article  Google Scholar 

  17. Engelbrecht B.M.J., Wright S.J., De Steven D., Survival and ecophysiology of tree seedlings during El Nino drought in a tropical moist forest in Panama, J. Trop. Ecol. 18 (2002) 569–579.

    Article  Google Scholar 

  18. Evans J.R., Sharkey T.D., Berry J.A., Farquhar G.D., Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants, Aust. J. Plant Physiol. 13 (1986) 281–292.

    Article  CAS  Google Scholar 

  19. Farquhar G.D., O’Leary M.H., Berry J.A., On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves, Aust. J. Plant Physiol. 9 (1982) 121–137.

    Article  CAS  Google Scholar 

  20. Farquhar G.D., Ehleringer J.R., Hubick K.T., Carbon isotope discrimination and photosynthesis, Annu. Rev. Plant Physiol. 40 (1989) 503–537.

    Article  CAS  Google Scholar 

  21. Farquhar G.D., Hubick K.T., Condon A.G., Richards R.A., Carbon isotope fractionation and plant water-use efficiency, in: Rundel P.W., Ehleringer J.R., Nagy K.A. (Eds.), Stable isotopes in ecological research, Springer-Verlag, New York, 1989, pp. 21–40.

    Google Scholar 

  22. Favrichon V., Classification des espèces arborées en groupes fonctionnels en vue de la réalisation d’un modèle de dynamique de peuplement en forêt Guyanaise, Rev. Ecol. (Terre Vie) 49 (1994) 379–403.

    Google Scholar 

  23. Favrichon V, Modèle matriciel déterministe en temps discret : application à l’étude de la dynamique d’un peuplement forestier tropical humide (Guyane française), Ph.D. thesis, Université Claude Bernard-Lyon I, 1995.

  24. Favrichon V., Apports d’un modèle démographique plurispécifique pour l’étude des relations diversité / dynamique en forêt tropicale guyanaise, Ann. For. Sci. 55 (1998) 655–669.

    Article  Google Scholar 

  25. Guehl J.-M., Dynamique de l’eau dans le sol en forêt tropicale humide guyanaise. Influence de la couverture pédologique, Annu. For. Sci. 41 (1984) 195–236.

    Article  Google Scholar 

  26. Guehl J.-M., Bonal D., Ferhi A., Barigah T.S., Farquhar G.D., Granier A., Community-level diversity of carbon-water relations in rainforest trees, in: Gourlet-Fleury S., Laroussini O., Guehl J.-M. (Eds.), Ecology and management of a neotropical rainforest, Paracou (French Guiana), Elsevier, Paris, 2004, pp. 65–84.

    Google Scholar 

  27. Gyenge J.E., Fernández M.E., Salda G.D., Schlichter T., Leaf and whole-plant water relations of the Patagonian conifer Austrocedrus chilensis (D. Don) Pic. Ser. et Bizzarri: implications on its drought resistance capacity, Ann. For. Sci. 62 (2005) 297–302.

    Article  Google Scholar 

  28. Hanba Y.T., Wada E., Osaki M., Nakaruma T., Growth and Δ13C responses to increasing atmospheric carbon dioxide concentrations for several crop species, Isotopes Environ. Health Stud. 32 (1996) 41–54.

    Article  CAS  Google Scholar 

  29. Hogan K.P., Smith A.P., Samaniego M., Gas exchange in six tropical semi-deciduous forest canopy tree species during the wet and dry seasons, Biotropica 27 (1995) 324–333.

    Article  Google Scholar 

  30. Hue R., Ferhi A., Guehl J.-M., Pioneer and late stage tropical rainforest tree species (French Guyana) growing under common conditions differ in leaf gas exchange regulation, carbon isotope discrimination and leaf water potential, Oecologia 99 (1994) 297–305.

    Article  Google Scholar 

  31. Jones H.G., Drought tolerance and water-use efficiency, in: Smith J.A.C., Griffiths H. (Eds.), Water deficits, plant responses from cell to community, Environmental Plant Biology Series, Lancaster, UK, 1993, pp. 193–203.

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

    Article  Google Scholar 

  33. Le Roux D., Stock W.D., Bond W.J., Maphanga D., Dry mass allocation, water use efficiency and Δ13C in clones of Eucalyptus grandis, E. grandis × camaldulensis and E. grandis × nitens grown under two irrigation regimes, Tree Physiol. 16 (1996) 497–502.

    PubMed  Google Scholar 

  34. Madhavan S., Treichel I.W, O’Leary M.H., Effects of relative humidity on carbon isotope fractionation in plants, Bot. Acta 104 (1991) 292–294.

    CAS  Google Scholar 

  35. Marino B.D., Mc Elroy M.B., Isotopic composition of atmospheric CO2 inferred from carbon in C4 plant cellulose, Nature 349 (1991) 127–131.

    Article  CAS  Google Scholar 

  36. McConnaughay K.D.M., Coleman J.S., Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients, Ecology 80 (1999) 2581–2593.

    Article  Google Scholar 

  37. Meinzer F.C., Goldstein G., Holbrook N.M., Jackson P., Cavelier J., Stomatal and environmental control of transpiration in a lowland tropical forest tree, Plant Cell Environ. 16 (1993) 429–436.

    Article  Google Scholar 

  38. Naeem S., Wright J.P., Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem, Ecol. Lett. 6 (2003) 567–579.

    Article  Google Scholar 

  39. Oldeman R.A.A., van Dijk J., Diagnosis of the temperament of tropical rain forest trees. Rain forest regeneration and management, in: Gomez-Pompa A., Whitmore T.C., Hadley M. (Eds.), Rain forest regeneration and management, Unesco, Paris, 1991, pp. 21–65.

    Google Scholar 

  40. Parkhurst D.F., Diffusion of CO2 and other gases inside leaves, New Phytol. 126 (1994) 449–479.

    Article  CAS  Google Scholar 

  41. Picon C., Guehl J.-M., Ferhi A., Leaf gas exchange and carbon isotope discrimination responses to drought in a drought-avoiding (Pinus pinaster) and a drought-tolerant (Quercus petraea) species under present and elevated atmospheric CO2 concentration, Plant Cell Environ. 19 (1996) 182–190.

    Article  Google Scholar 

  42. Poorter L., Kwant R., Hernández R., Medina E., Werger M.J.A., Leaf optical properties in Venezuelan cloud forest trees, Tree Physiol. 20 (2000) 519–526.

    PubMed  CAS  Google Scholar 

  43. Reich A., Holbrook N.M., Ewel J.J., Developmental and physiological correlates of leaf size in Hyeronima alchorneoides (Euphorbiaceae), Am. J. Bot. 91 (2004) 582–589.

    Article  PubMed  Google Scholar 

  44. Reich P.B., Walters M.B., Ellsworth D.S., Uhl C., Photosynthesis-nitrogen relations in Amazonian tree species. I: Patterns among species and communities, Oecologia 97 (1994) 62–72.

    Article  Google Scholar 

  45. Reich P.B., Walters M.B., Ellsworth D.S., From tropics to tundra: Global convergence in plant functioning, Proc. Nat. Ac. Sci. 94 (1997) 13730–13734.

    Article  CAS  Google Scholar 

  46. Reich P.B., Ellsworth D.S., Walters M.B., Vose J.M., Gresham C., Volin J.C., Bowman W.D., Generality of leaf trait relationships: a test across six biomes, Ecology 80 (1999) 1955–1969.

    Article  Google Scholar 

  47. Ricklefs R.E., Environmental heterogeneity and plant species diversity: a hypothesis, Amer.Nat. 111 (1977) 377–381.

    Google Scholar 

  48. Shipley B., Lechowicz M.J., Wright I., Reich P.B., Fundamental tradeoffs generating the worldwide leaf economics spectrum. Ecology 87 (2006) 535–541.

    Article  PubMed  Google Scholar 

  49. Strauss-Debenedetti S., Bazzaz F.A., Photosynthetic characteristics of tropical trees along successional gradients, in: Mulkey S.S., Chazdon R.L., Smith P.A. (Eds.), Tropical Forest Plant Ecophysiology, Chapman and Hall, New York, 1996, pp. 162–186.

    Google Scholar 

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

    Article  Google Scholar 

  51. Tcherkez G., Nogués S., Bleton J., Cornic G., Badeck F., Ghashghaie J., Metabolic origin of carbon isotope composition of leaf dark-respired CO2 in French bean, Plant Physiol. 131 (2003) 237–244.

    Article  PubMed  CAS  Google Scholar 

  52. Terwilliger V.J., Kitajima K., Le Roux-Swarthout D.J., Mulkey S.S., Wright S.J., Intrinsic water-use efficiency and heterotrophic investment in tropical leaf growth of two neotropical pioneer tree species as estimated from delta C-13 values, New Phytol. 152 (2001) 267–281.

    Article  Google Scholar 

  53. Thomas S.C., Bazzaz F.A., Asymptotic height as a predictor of photosynthetic characteristics in Malaysian rain forest trees, Ecology 80 (1999) 1607–1622.

    Article  Google Scholar 

  54. Tobin M.F., Lopez O.R., Kursar T.A., Responses of tropical understory plants to a severe drought: tolerance and avoidance of water stress, Biotropica 31 (1999) 570–578.

    Article  Google Scholar 

  55. Turner I., The Ecology of trees in the tropical rain forest, Cambridge Tropical Biology Series, University Press, Cambridge, 2001.

    Book  Google Scholar 

  56. Wright I.J., Reich P.B., Westoby M., Ackerly D.D., Baruch Z., Bongers F., Cavender-Bares J., Chapin T., Cornelissen J.H.C., Diemer M., Flexas J., Garnier E., Groom P.K., Gulias J., Hikosaka K., Lamont B.B., Lee T., Lee W., Lusk C., Midgley J.J., Navas M.-L., Niinemets U., Oleksyn J., Osada N., Poorter H., Poot P., Prior L., Pyankov V.I., Roumet C., Thomas S.C., Tjoelker M.G., Veneklaas E.J., Villar R., The worldwide leaf economics spectrum, Nature 428 (2004) 821–827.

    Article  PubMed  CAS  Google Scholar 

  57. Wright I.J., Reich P.B., Cornelissen J.H.C., Falster D.S., Garnier E., Hikosaka K., Lamont B.B., Lee W., Oleksyn J., Osada N., Poorter H., Villar R., Warton D.I., Westoby M., Assessing the generality of global leaf trait relationships, New Phytol. 166 (2005) 485–496.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  59. Xu Z.H., Saffigna P.G., Farquhar G.D., Simpson J.A., Haines R.J., Walker S., Osborne D.O., Guinto D., Carbon isotope discrimination and oxygen isotope composition in clones of the F1 hybrid between slash pine and Caribbean pine in relation to growth, water-use efficiency and foliar nutrient concentration, Tree Physiol. 20 (2000) 1209–1218.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. UMR Écologie des Forêts de Guyane, INRA Kourou, BP 709, 97387, Kourou Cedex, Guyane, France

    Damien Bonal, Céline Born, Eric Marcon & Jean-Christophe Roggy

  2. UMR Écologie et Écophysiologie, INRA Nancy, 54280, Champenoux, France

    Claude Brechet & Jean-Marc Guehl

Authors
  1. Damien Bonal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Céline Born
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claude Brechet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sabrina Coste
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eric Marcon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jean-Christophe Roggy
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jean-Marc Guehl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Damien Bonal.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bonal, D., Born, C., Brechet, C. et al. The successional status of tropical rainforest tree species is associated with differences in leaf carbon isotope discrimination and functional traits. Ann. For. Sci. 64, 169–176 (2007). https://doi.org/10.1051/forest:2006101

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1051/forest:2006101

  • 13C
  • functional diversity
  • leaf gas exchange
  • species grouping
  • tropical rainforest
  • 13C
  • diversité fonctionnelle
  • échanges gazeux foliaires
  • groupes successionnels
  • forêt tropicale humide

Annals of Forest Science

ISSN: 1297-966X