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Does ontogeny modulate irradiance-elicited plasticity of leaf traits in saplings of rain-forest tree species? A test with Dicorynia guianensis and Tachigali melinonii (Fabaceae, Caesalpinioideae)

L’ontogenèse module-t-elle la plasticité des traits foliaires induite par la lumière dans des semis d’arbres de forêt tropicale humide? Un test avec Dicorynia guianensis et Tachigali melinonii (Fabaceae, Caesalpinioideae)

Annals of Forest Science volume 66, page 709 (2009)Cite this article

Abstract

  • • Irradiance elicits a large plasticity in leaf traits, but little is known about the modulation of this plasticity by ontogeny. Interactive effects of relative irradiance and ontogeny were assessed on leaf traits for two tropical rainforest tree species: Dicorynia guianensis Amshoff and Tachigali melinonii (Harms) Barneby (Fabaceae, Caesalpinioideae).

  • • Eleven morphological and physiological leaf traits, relative to photosynthetic performance, were measured on saplings at three different architectural development stages (ASD 1, 2 and 3) and used to derive composite traits like photosynthetic N-use efficiency. Measurements were made along a natural irradiance gradient.

  • • The effect of ASD was very visible and differed between the two species. For Dicorynia guianensis, only leaf mass-per-area (LMA) significantly increased with ASDs whereas for Tachigali melinonii, almost all traits were affected by ASD: LMA, leaf N content and photosynthetic capacity increased from ASD 1 to ASD 3. Photosynthetic N-use-efficiency was not affected by ASD in any species.

  • • Leaf traits were severely modulated by irradiance, whereas the degree of plasticity was very similar among ASDs. Only few interactions were detected between irradiance and ASD, for leaf thickness, carbon content, and the ratio Chl/N in T. melinonii and for photosynthetic capacity in D. guianensis.

  • • We conclude that ontogenic development and irradiance-elicited plasticity modulated leaf traits, with almost no interaction, i.e., the degree of irradiance-elicited plasticity was stable across development stages and independent of ontogeny in these two species, at least in the early stages of development assessed here.

Résumé

  • • Les traits foliaires varient fortement avec l’éclairement mais également avec l’ontogenèse. Cependant, l’impact de l’ontogenèse sur la plasticité induite par l’éclairement reste mal connu. Les interactions entre ontogenèse et éclairement relatif ont ainsi été étudiées pour des traits fonctionnels foliaires de deux espèces de forêt tropicale humide de Guyane française : Dicorynia guianensis Amshoff et Tachigali melinonii (Harms) Barneby (Fabaceae, Caesalpinioideae).

  • • Onze traits morphologiques et physiologiques foliaires, relatifs aux capacités photosynthétiques, ont été mesurés sur de jeunes arbres ayant atteint trois stades architecturaux de développement successifs (ASD 1, 2 et 3) et utilisés pour en déduire des traits composites. Les mesures ont été réalisées le long d’un gradient naturel d’évlairement en forêt.

  • • L’impact de stades successifs de développement différait entre espèces. Pour D. guianensis, seule la masse surfacique (LMA) a augmenté significativement avec les stades de développement tandis que pour T. melinonii, presque tous les traits foliaires étaient modulés. Pour cette espèce, LMA, teneur en N et capacité photosynthétique ont augmenté de ASD 1 à ASD 3. Par contre, l’efficience d’utilisation de N par la photosynthèse est restée stable entre ASDs.

  • • Les traits foliaires ont été fortement modifiés par l’éclairement mais le degré de plasticité était similaire entre les ASDs. Des interactions entre ASD et éclairement n’ont été observées que pour l’épaisseur, la teneur en C et le rapport Chl/N de T. melinonii ainsi que pour la capacité photosynthétique de D. guianensis.

  • • En dépit de l’effet significatif de l’ontogénèse sur les traits foliaires, seules de très faibles interactions ont pu être détectées avec l’éclairement pour les deux espèces. On peut en conclure que les stades successifs de développement ne modifient pas le degré de plasticité foliaire en réponse à l’éclairement tout au moins dans le cas des stades jeunes pris en compte ici

References

  • Baraloto C., Morneau F., Bonal D., Blanc L., and Ferry B., 2007. Seasonal water stress tolerance and habitat associations within four neotropical tree genera. Ecology 88: 478–489.

    Article  PubMed  Google Scholar 

  • Barthelemy D. and Caraglio Y., 2007. Plant architecture: A dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann. Bot. 99: 375–407.

    Article  PubMed  Google Scholar 

  • Bonal D., Sabatier D., Montpied P., Tremeaux D., and Guehl J.M., 2000. Interspecific variability of δ13C among trees in rainforests of French Guiana: functional groups and canopy integration. Oecologia 124: 454–468.

    Article  Google Scholar 

  • Bradshaw A.D., 1965. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 13: 115–155.

    Article  Google Scholar 

  • Cavender-Bares J. and Bazzaz F.A., 2000. Changes in drought response strategies with ontogeny in Quercus rubra: implications for scaling from seedlings to mature trees. Oecologia 124: 8–18.

    Article  Google Scholar 

  • Coleman J.C., McConnaughay K.D.M., and Ackerly D.D., 1994. Interpreting phenotypic variation in plants. Trends Ecol. Evol. 9: 187–191.

    Article  PubMed  CAS  Google Scholar 

  • Cornelissen J.H.C., Cerabolini B., Castro-Díez P., Villar-Salvador P., Montserrat-Martí G., Puyravaud J.P., Maestro M., Werger M.J.A., and Aerts R., 2003. Functional traits of woody plants: correspondence of species rankings between field adults and laboratory-grown seedlings? J. Veg. Sci. 14: 311–322.

    Article  Google Scholar 

  • Coste S., 2008. Diversité et plasticité des traits foliaires en forêt tropicale humide. Une analyse coût/bénéfice de l’acquisition de carbone, Ph.D. thesis, Nancy, AgroParisTech-Engref.

    Google Scholar 

  • Dreyer E., Le Roux X., Montpied P., Daudet F.A., and Masson F., 2001. Temperature response of leaf photosynthetic capacity in seedlings from seven temperate tree species. Tree Physiol. 21: 223–232.

    PubMed  CAS  Google Scholar 

  • Ellsworth D.S. and Reich P.B., 1993. Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96: 169–178.

    Article  Google Scholar 

  • Ethier G.J. and Livingston N., 2004. On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ. 27: 137–153.

    Article  CAS  Google Scholar 

  • Farquhar G.D., von Caemmerer S., and Berry J.A., 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78–90.

    Article  CAS  Google Scholar 

  • Favrichon V., 1994. 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 et vie) 49: 379–403.

    Google Scholar 

  • Givnish T.J., 1988. Adaptation to sun and shade: A whole plant perspective. Aust. J. Plant. Physiol. 15: 63–92.

    Article  Google Scholar 

  • Harley P.C., Thomas R.B., Reynolds J.F., and Strain B.R., 1992. Modelling photosynthesis of cotton grown in elevated CO2. Plant Cell Environ. 15: 271–282.

    Article  CAS  Google Scholar 

  • Hoflacher H. and Bauer H., 1982. Light acclimation in leaves of the juvenile and adult life phases of ivy (Hedera helix). Physiol. Plant. 56: 177–182.

    Article  Google Scholar 

  • Holscher D., 2004. Leaf traits and photosynthetic parameters of saplings and adult trees of co-existing species in a temperate broad-leaved forest. Bas. App. Ecol. 5: 163–172.

    Article  Google Scholar 

  • Kenzo T., Ichie T., Watanabe Y., Yoneda R., Ninomiya I., and Koike T., 2006. Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiol. 26: 865–873.

    PubMed  CAS  Google Scholar 

  • Le Roux X., Grand S., Dreyer E., and Daudet F.A., 1999. Parameterization and testing of a biochemically based photosynthesis model for walnut trees (Juglans regia) and seedlings. Tree Physiol. 19: 481–492.

    PubMed  Google Scholar 

  • Lusk C.H. and Warton D.I., 2007. Global meta-analysis shows that relationships of leaf mass per area with species shade tolerance depend on leaf habit and ontogeny. New Phytol. 176: 764–774.

    Article  PubMed  Google Scholar 

  • Lusk C.H., Falster D.S., Jara-Vergara C.K., Jimenez-Castillo M., and Saldana-Mendoza A., 2008. Ontogenetic variation in light requirements of juvenile rainforest evergreens. Funct. Ecol. 22: 454–459.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Mediavilla S. and Escudero A., 2003. Mature trees versus seedlings: Differences in leaf traits and gas exchange patterns in three co-occurring Mediterranean oaks. Ann. For. Sci. 60: 455–460.

    Article  Google Scholar 

  • Molino J.-F. and Sabatier D., 2001. Tree diversity in tropical rain forests: A validation of the intermediate disturbance hypothesis. Science 294: 1702–1704.

    Article  PubMed  CAS  Google Scholar 

  • Nicolini E., 1998. Architecture et gradients morphogénétiques chez de jeunes hêtres (Fagus sylvatica L. Fagaceae) en milieu forestier. Can. J. Bot. 76: 1232–1244.

    Google Scholar 

  • Nicolini E., Barthélémy D., and Heuret P., 2000. Influence de la densité du couvert forestier sur le développement architectural de jeunes chênes sessiles, Quercus petraea (Matt.) Liebl. (Fagaceae), en régénération forestière. Can. J. Bot. 78: 1531–1344.

    Google Scholar 

  • Niinemets Ü., 1997a. Distribution patterns of foliar carbon and nitrogen as affected by tree dimensions and relative light conditions in the canopy of Picea abies. Trees 11: 144–154.

    Google Scholar 

  • Niinemets Ü., 1997b. Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species. Funct. Ecol. 11: 518–531.

    Article  Google Scholar 

  • Niinemets Ü., 1999a. Components of leaf dry mass per area — thickness and density — alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol. 144: 35–47.

    Article  Google Scholar 

  • Niinemets Ü., 1999b. Energy requirement for foliage formation is not constant along canopy light gradients in temperate deciduous trees. New Phytol. 141: 459–470.

    Article  Google Scholar 

  • Niinemets Ü., 2002. Stomatal conductance alone does not explain the decline in foliar photosynthetic rates with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiol. 22: 515–535.

    PubMed  Google Scholar 

  • Niinemets Ü., 2006. The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited. J. Ecol. 94: 464–470.

    Article  Google Scholar 

  • Niinemets Ü. and Kull O., 1998. Stoichiometry of foliar carbon constituents varies along light gradients in temperate woody canopies: implications for foliage morphological plasticity. Tree Physiol. 18: 467–479.

    PubMed  Google Scholar 

  • Poorter L., 1999. Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Funct. Ecol. 13: 396–410.

    Article  Google Scholar 

  • Poorter L., Oberbauer S.F., and Clark D.B., 1995. Leaf optical properties along a vertical gradient in a tropical rain forest canopy in Costa Rica. Am. J. Bot. 82: 1257–1263.

    Article  Google Scholar 

  • Poorter L., Bongers L., and Bongers F., 2006. Architecture of 54 moist-forest tree species: Traits, trade-offs, and functional groups. Ecology 87: 1289–1301.

    Article  PubMed  Google Scholar 

  • Popma J., Bongers F., and Werger M.J.A., 1992. Gap-dependence and leaf characteristics of trees in a tropical lowland rain forest in Mexico. Oikos 63: 207–214.

    Article  Google Scholar 

  • Rijkers T., Pons T.L., and Bongers F., 2000. The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Funct. Ecol. 14: 77–86.

    Article  Google Scholar 

  • Roggy J.-C., Nicolini E., Imbert P., Caraglio Y., Bosc A., and Heuret P., 2005. Links between tree structure and functional leaf traits in the tropical forest tree Dicorynia guianensis Amshoff (Caesalpiniaceae). Ann. For. Sci. 62: 553–564.

    Article  Google Scholar 

  • Rozendaal D.M.A., Hurtado V.H., and Poorter L., 2006. Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature. Funct. Ecol. 20: 207–216.

    Article  Google Scholar 

  • Sterck F.J. and Bongers F., 1998. Ontogenetic changes in size, allometry, and mechanical design of tropical rain forest trees. Am. J. Bot. 85: 266–272.

    Article  PubMed  CAS  Google Scholar 

  • Thomas S.C. and Winner W.E., 2002. Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis. Tree Physiol. 22: 117–127.

    PubMed  Google Scholar 

  • Valladares F. and Niinemets U., 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annu. Rev. Ecol. Evol. Syst. 39: 237–57.

    Article  Google Scholar 

  • Valladares F., Wright S.J., Lasso E., Kitajima K., and Pearcy R.W., 2000. Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81: 1925–1936.

    Article  Google Scholar 

  • Veneklaas E.J. and Poorter L., 1988. Growth and carbon partitioning of tropical tree seedlings in contrasting light environments. In: H. Lambers, H. Poorter and M. Van Vuuren (Eds.), Inherent variation in plant growth: physiological mechanisms and ecological consequences, Backhuys publishers, Leiden, The Netherlands, pp. 337–355.

    Google Scholar 

  • Warren C.R., 2006. Estimating the internal conductance to CO2 movement. Funct. Plant Biol. 33: 431–442.

    Article  CAS  Google Scholar 

  • Wright S.D. and McConnaughay K.D.M., 2002. Interpreting pheno-typic plasticity: the importance of ontogeny. Plant Species Biol. 17: 119–131.

    Article  Google Scholar 

Download references

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Authors and Affiliations

  1. Écologie des Forêts de Guyane, AgroParisTech-ENGREF, INRA, UMR CIRAD-ENGREF-INRA-CNRS, Campus Agronomique de Kourou, 97387, Kourou, Guyane, France

    Sabrina Coste, Jean-Christophe Roggy & Laurianne Garraud

  2. Botanique et Bioinformatique de l’Architecture des Plantes, INRA, UMR AMAP, TA A51/PS2, 34398, Montpellier Cedex 5, France

    Patrick Heuret

  3. Botanique et Bioinformatique des plantes, CIRAD, UMR AMAP, F97310, Kourou, Guyane, France

    Eric Nicolini

  4. 1137 “Écologie et Écophysiologie Forestières”, INRA, UMR, 54280, Champenoux, France

    Erwin Dreyer

  5. UMR 1137 “ Écologie et Écophysiologie Forestières”, Nancy-Université, 54500, Vandœuvre, France

    Erwin Dreyer

Authors
  1. Sabrina Coste
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  2. Jean-Christophe Roggy
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  3. Laurianne Garraud
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  4. Patrick Heuret
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  5. Eric Nicolini
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  6. Erwin Dreyer
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Correspondence to Erwin Dreyer.

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Coste, S., Roggy, JC., Garraud, L. et al. Does ontogeny modulate irradiance-elicited plasticity of leaf traits in saplings of rain-forest tree species? A test with Dicorynia guianensis and Tachigali melinonii (Fabaceae, Caesalpinioideae). Ann. For. Sci. 66, 709 (2009). https://doi.org/10.1051/forest/2009062

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  • DOI: https://doi.org/10.1051/forest/2009062

Keywords

  • plant architecture
  • phenotypic plasticity
  • photosynthetic capacity
  • leaf structure
  • tropical rain forest

Mots-clés

  • architecture des arbres
  • plasticité phénotypique
  • capacité photosynthétique
  • structure des feuilles
  • forêt tropicale humide

Annals of Forest Science

ISSN: 1297-966X