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Gap effects on leaf traits of tropical rainforest trees differing in juvenile light requirement

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Abstract

The relationships of 16 leaf traits and their plasticity with the dependence of tree species on gaps for regeneration (gap association index; GAI) were examined in a Neotropical rainforest. Young saplings of 24 species with varying GAI were grown under a closed canopy, in a medium-sized and in a large gap, thus capturing the full range of plasticity with respect to canopy openness. Structural, biomechanical, chemical and photosynthetic traits were measured. At the chloroplast level, the chlorophyll a/b ratio and plasticity in this variable were not related to the GAI. However, plasticity in total carotenoids per unit chlorophyll was larger in shade-tolerant species. At the leaf level, leaf mass per unit area (LMA) decreased with the GAI under the closed canopy and in the medium gap, but did not significantly decrease with the GAI in the large gap. This was a reflection of the larger plasticity in LMA and leaf thickness of gap-dependent species. The well-known opposite trends in LMA for adaptation and acclimation to high irradiance in evergreen tropical trees were thus not invariably found. Although leaf strength was dependent on LMA and thickness, plasticity in this trait was not related to the GAI. Photosynthetic capacity expressed on each basis increased with the GAI, but the large plasticity in these traits was not clearly related to the GAI. Although gap-dependent species tended to have a greater plasticity overall, as evident from a principle component analysis, leaf traits of gap-dependent species are thus not invariably more phenotypically plastic.

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References

  • Alvarez-Clare S, Kitajima K (2007) Physical defense traits enhance seedling survival of Neotropical tree species. Funct Ecol 21:1044–1054

    Article  Google Scholar 

  • Anderson JM, Chow WS, Park YI (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139

    Article  CAS  PubMed  Google Scholar 

  • Bongers F, Popma J (1990) Leaf dynamics of seedlings of rain forest species in relation to canopy gaps. Oecologia 82:122–127

    Article  Google Scholar 

  • Bungard RA, Press MC, Scholes JD (2000) The influence of nitrogen on rain forest dipterocarp seedlings exposed to a large increase in irradiance. Plant Cell Environ 23:1183–1194

    Article  Google Scholar 

  • Chazdon RL, Pearcy RW, Lee DW, Fetcher N (1996) Photosynthetic responses of tropical forest plants to contrasting light environments. In: Mulkey SS, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Chapman and Hall, New York, pp 5–55

    Chapter  Google Scholar 

  • Choong MF, Lucas P, Ong JSY, Pereira B, Tan HTW, Turner IM (1992) Leaf fracture toughness and sclerophylly: their correations and ecological implications. New Phytol 121:597–610

    Article  Google Scholar 

  • Coley PD, Barone JA (1996) Herbivory and plant defenses in tropical forests. Annu Rev Ecol Syst 27:305–335

    Article  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS III (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Coste S, Roggy JC, Sonnier G, Dreyer E (2010) Similar irradiance-elicited plasticity of leaf traits in saplings of 12 tropical rainforest tree species with highly different leaf mass to area ratio. Funct Plant Biol 37:342–355

    Article  Google Scholar 

  • Coste S, Roggy JC, Schimann H, Epron D, Dreyer E (2011) A cost-benefit analysis of acclimation to low irradiance in tropical rainforest tree seedlings: leaf life span and payback time for leaf deployment. J Exp Bot 62:3941–3955

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ellsworth DS, Reich PB (1996) Photosynthesis and leaf nitrogen in five Amazonian tree species during early secondary succession. Ecology 77:581–594

    Article  Google Scholar 

  • Evans JR (1989) Partitioning of nitrogen between and within leaves grown under different irradiances. Aust J Plant Physiol 16:533–548

    Article  Google Scholar 

  • Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ 24:755–767

    Article  CAS  Google Scholar 

  • Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:565–581

    Article  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605–618

    Article  CAS  Google Scholar 

  • Hikosaka K, Terashima I (1996) Nitrogen partitioning among photosynthetic components and its consequence in sun and shade plants. Funct Ecol 10:335–343

    Article  Google Scholar 

  • Hikosaka K, Hanba YT, Hirose T, Terashima I (1998) Photosynthetic nitrogen use efficiency in leaves of woody and herbaceous species. Funct Ecol 12:896–905

    Article  Google Scholar 

  • Houter NC, Pons TL (2005) Gap size effects on photoinhibition in understorey saplings in tropical rainforest. Plant Ecol 179:43–51

    Article  Google Scholar 

  • Houter NC, Pons TL (2012) Ontogenetic changes in leaf traits of tropical rainforest trees differing in juvenile light requirement. Oecologia 169:33–45

    Article  PubMed Central  PubMed  Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-Dimethylformamide and 80 % acetone. Plant Physiol 77:483–485

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857–865

    Article  PubMed  Google Scholar 

  • Kitajima K, Llorens AM, Stefanescu C, Timchenko MV, Lucas PW, Wright SJ (2012) How cellulose-based leaf toughness and lamina density contribute to long leaf lifespans of shade-tolerant species. New Phytol 195:640-652

    Article  PubMed  Google Scholar 

  • Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ 24:1345–1352

    Article  CAS  Google Scholar 

  • Krause GH, Grube E, Koroleva OY, Barth C, Winter K (2004) Do mature shade leaves of tropical tree seedlings acclimate to high sunlight and UV radiation? Funct Plant Biol 31:743–756

    Article  Google Scholar 

  • Krause GH, Winter K, Matsubara S, Krause B, Jahns P, Virgo A, Aranda J, Garcia M (2012) Photosynthesis, photoprotection, and growth of shade-tolerant tropical tree seedlings under full sunlight. Photosynth Res 113:273–285

    Article  CAS  PubMed  Google Scholar 

  • Kull O, Niinemets U (1998) Distribution of leaf photosynthetic properties in tree canopies: comparison of species with different shade tolerance. Funct Ecol 12:472–479

    Article  Google Scholar 

  • Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Laurans M, Martin O, Nicolini E, Vincent G (2012) Functional traits and their plasticity predict tropical trees regeneration niche even among species with intermediate light requirements. J Ecol 100:1440–1452

    Article  Google Scholar 

  • Lovelock CE, Jebb M, Osmond CB (1994) Photoinhibition and recovery in tropical plant species: response to disturbance. Oecologia 97:297–307

    Google Scholar 

  • Lusk CH, Warton DI (2007) Global meta-analysis shows that relationships of leaf mass per area with species shade tolerance depend on leaf habit and ontogeny. New Phytol 176:178–189

    Article  Google Scholar 

  • Lusk CH, Reich PB, Montgomery RA, Ackerly DD, Cavender-Bares J (2008) Why are evergreen leaves so contrary about shade? Trends Ecol Evol 23:299–303

    Article  PubMed  Google Scholar 

  • Lusk CH, Onoda Y, Kooyman R, Gutierrez-Giron A (2010) Reconciling species-level vs plastic responses of evergreen leaf structure to light gradients: shade leaves punch above their weight. New Phytol 186:429–438

    Article  PubMed  Google Scholar 

  • Matsubara S, Krause GH, Aranda J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of Neotropical forest plants. Funct Plant Biol 36:20–36

    Article  CAS  Google Scholar 

  • Mooney HA, Gulmon SL (1982) Constraints on leaf structure and function in reference to herbivory. Bioscience 32:189–206

    Google Scholar 

  • Mostacedo CB, Fredericksen TS (1999) Regeneration status of important tropical forest tree species in Bolivia: assessment and recommendations. For Ecol Manage 124:263–273

    Article  Google Scholar 

  • Mulkey SS, Pearcy RW (1992) Interactions between acclimation and photoinhibition of photosynthesis of a tropical forest understorey herb, Alocasia macrorrhiza, during simulated canopy gap formation. Funct Ecol 6:719–729

    Article  Google Scholar 

  • Niinemets U (1997) 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 U, Wright IJ, Evans JR (2009) Leaf mesophyll diffusion conductance in 35 Australian sclerophylls covering a broad range of foliage structural and physiological variation. J Exp Bot 60:2433–2449

    Article  CAS  PubMed  Google Scholar 

  • Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Funct Ecol 18:419–425

    Article  Google Scholar 

  • Onoda Y, Schieving F, Anten NPR (2008) Effects of light and nutrient availability on leaf mechanical properties of Plantago major: a conceptual approach. Ann Bot 101:727–736

    Article  PubMed Central  PubMed  Google Scholar 

  • Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC, Diaz S, Dominy NJ, Elgart A, Enrico L, Fine PVA, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Perez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE, Van Bael SA, Warton DI, Wright IJ, Wright SJ, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312

    Article  PubMed  Google Scholar 

  • Osunkoya OO, Ash JE, Hopkins MS, Graham AW (1994) Influence of seed size and seedling ecological attributes on shade-tolerance of rain-forest tree species in northern Queensland. J Ecol 82:149–163

    Article  Google Scholar 

  • Pons TL, Anten NPR (2004) Is plasticity in partitioning of photosynthetic resources between and within leaves important for whole-plant carbon gain in canopies? Funct Ecol 18:802–811

    Article  Google Scholar 

  • Pons TL, Helle G (2011) Identification of anatomically non-distinct annual rings in tropical trees using stable isotopes. Trees Struct Funct 25:83–93

    Article  Google Scholar 

  • Pons TL, Westbeek MHM (2004) Analysis of differences in photosynthetic nitrogen-use efficiency between four contrasting species. Physiol Plant 122:68–78

    Article  CAS  Google Scholar 

  • Poorter H, Evans JR (1998) Photosynthetic nitrogen use efficiency of species that differ inherently in specific leaf area. Oecologia 116:26–37

    Article  Google Scholar 

  • Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588

    Article  PubMed  Google Scholar 

  • Poorter H, Buhler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Funct Plant Biol 39:839–850

    Article  Google Scholar 

  • Poorter L (2007) Are species adapted to their regeneration niche, adult niche, or both? Am Nat 169:433–442

    Article  PubMed  Google Scholar 

  • Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 forest species. Ecology 87:1733–1743

    Article  PubMed  Google Scholar 

  • Poorter L, van de Plassche M, Willems S, Boot RGA (2004) Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biol 6:746–754

    Article  CAS  PubMed  Google Scholar 

  • Popma J, Bongers F (1988) The effect of canopy gaps on growth and morphology of rainforest species. Oecologia 75:625–632

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Raaimakers D, Boot RGA, Dijkstra P, Pot S, Pons T (1995) Photosynthetic rates in relation to leaf phosphorus content in pioneer versus climax tropical rainforest trees. Oecologia 102:120–125

    Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392

    Article  Google Scholar 

  • Renton M, Poorter H (2011) Using log-log scaling slope analysis for determining the contributions to variability in biological variables such as leaf mass per area: why it works, when it works and how it can be extended. New Phytol 190:5–8

    Article  PubMed  Google Scholar 

  • Rozendaal DMA, Hurtado VH, 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 

  • Strauss-Debenedetti S, Bazzaz FA (1996) Photosynthetic characteristics of tropical trees along a successional gradient. In: Mulkey S, Chazdon RL, Smith AP (eds) Tropical forest plant ecophysiology. Chapman and Hall, New York, pp 162–186

    Chapter  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182

    Article  CAS  PubMed  Google Scholar 

  • ter Steege H (2013) Hyperdominance in the Amazonian Tree Flora. Science 342:1243092

    Google Scholar 

  • Terashima I, Hanba YT, Tazoe Y, Vyas P, Yano S (2006) Irradiance and phenotype: comparative eco-development of sun and shade leaves in relation to photosynthetic CO2 diffusion. J Exp Bot 57:343–354

    Article  CAS  PubMed  Google Scholar 

  • Thomas SC, Bazzaz FA (1999) Asymptotic height as a predictor of photosynthetic characteristics in Malaysian rain forest trees. Ecology 80:1607–1622

    Article  Google Scholar 

  • Valladares F, Niinemets U (2008) Shade tolerance, a key plant feature of complex nature and consequences. Ann Rev Ecol Evol Syst 39:237–257

    Article  Google Scholar 

  • Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116

    Article  Google Scholar 

  • Valladares F, Wright SJ, Lasso E, Kitajima K, Pearcy RW (2000) Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81:1925–1936

    Article  Google Scholar 

  • van Arendonk JJCM, Poorter H (1994) The chemical composition and anatomical structure of leaves of grass species differing in relative growth rate. Plant Cell Environ 17:963–970

    Article  CAS  Google Scholar 

  • van Dam O (2001) Forest filled with gaps. Effects of gap size on water and nutrient cycling in tropical rain forest. A study in Guyana. Tropenbos-Guyana series 10, Georgetown, Guyana

  • van Kekem AJ, Pulles JHM, Khan Z (1996) Soils of the rainforest in central Guyana. Tropenbos-Guyana series 2, Georgetown, Guyana

  • Veneklaas EJ, Poorter L (1998) Growth and carbon partitioning of tropical tree seedlings in contrasting light environments. In: Lambers H, Poorter H, van Vuuren MMI (eds) Inherent variation in plant growth; physiological mechanisms and ecological consequences. Backhuys, Leiden, pp 337–361

    Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435-447

    Article  CAS  PubMed  Google Scholar 

  • Westbrook JW, Kitajima K, Burleigh J, Kress W, Erickson DL, Wright SJ (2011) What makes a leaf tough? Patterns of correlated evolution between leaf toughness traits and demographic rates among 197 shade-tolerant woody species in a Neotropical Forest. Am Nat 177:800–811

    Article  PubMed  Google Scholar 

  • Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159

    Article  Google Scholar 

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Acknowledgments

The Guyana programme of Tropenbos International is thanked for providing financial and logistic support. Julian Pilay, Benedict Harry and Julian Williams are thanked for assistance with tree identification and sampling in the field. Yvonne de Jong–van Berkel did the nitrogen analyses. Lourens Poorter and Niels Anten are acknowledged for valuable comments on earlier drafts of the manuscript.

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  1. Department Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3508 CH, Utrecht, The Netherlands

    Nico C. Houter & Thijs L. Pons

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  1. Nico C. Houter
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Correspondence to Thijs L. Pons.

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Communicated by Fernando Valladares.

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Houter, N.C., Pons, T.L. Gap effects on leaf traits of tropical rainforest trees differing in juvenile light requirement. Oecologia 175, 37–50 (2014). https://doi.org/10.1007/s00442-014-2887-9

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