Abstract
Comparisons among European, Japanese and North-American temperate deciduous woody floras revealed that there is no difference in shade-tolerance or in successional position between the compound- and simple-leaved species. Given that the compound-leaved species usually have greater biomass investments in non-productive throwaway supporting structures, it remained unclear how they could be as shade-tolerant as the simple-leaved analogues. To find out the role of the variability in leaf structure and composition in shade-tolerance of these species, foliar morphology and chemistry were analysed in 15 Estonian temperate compound-leaved deciduous woody taxa.
Both foliar morphological and chemical parameters influenced the fractional investment of foliar biomass in petioles. The proportion of leaf biomass in petioles was independent of leaf size, but it increased with increasing leaflet number per leaf, suggesting that spacing rather than support requirements determined the biomass investment in petioles. The leaves with greater nitrogen concentrations also had larger foliar biomass investments in petioles. The latter effect possibly resulted from a greater water demand of functionally more active protein-rich leaves. Though the proportion of leaf biomass invested in petioles was high (for the whole material on average 15.9±0.4%), petioles were considerably cheaper to construct in terms of mineral nutrients than leaflets. e.g., petioles contained on average only 5.55±0.14% of total leaf nitrogen. Since in many cases the availability of mineral nutrients such as nitrogen rather than organic carbon sets limits to total leaf biomass on the plant, I suggested, contrary to previous claims, that the costs for foliage formation should not necessarily be different between compound- and simple-leaved species. Compound-leaved species also fit the basic relationships previously observed in simple-leaved analogues. Leaf size increased and leaf dry mass per area (LMA) decreased with increasing shade-tolerance. Thus, more shade-tolerant species construct a more effective foliar display for light interception at low irradiance with similar biomass investment in leaves. Species shade-tolerance was independent of biomass investment in petioles. However, due to the genotypic plasticity in LMA, more shade-tolerant species supported more foliar area at a constant leaf biomass investment in petioles.
Similar content being viewed by others
References
Abrams, M. D. 1994. Genotypic and phenotypic variation as stress adaptations in temperate tree species: a review of several case studies. Tree Physiol. 14: 833–842.
Baker, F. S. 1949. A revised tolerance table. J. Forestry 47: 179–181.
Bazzaz, F. A. 1979. The physiological ecology of plant succession. Annu. Rev. Ecol. Syst. 10: 351–371.
Bazzaz, F. A. & Wayne, P. M. 1994. Coping with environmental heterogeneity: the physiological ecology of tree seedling regeneration across the gap – understory continuum. Pp. 349–390. In: Caldwell M. M. & Pearcy R. W. (eds), Physiological ecology. A series of monographs, texts, and treatises. Exploitation of Environmental Heterogeneity by Plants. Ecophysiological Processes Above-and Belowground. Academic Press, San Diego.
Bonser, S. P. & Aarssen, L.W. 1994. Plastic allometry in young sugar maple (Acer saccharum): adaptive responses to light availability. Amer. J. Bot. 81: 400–406.
Castellanos, A. E., Mooney, H. A., Bullock, S. H., Jones, C. & Robichaux, R. 1989. Leaf, stem, and metamer characteristics of vines in a tropical deciduous forest in Jalisco, Mexico. Biotropica 21: 41–49.
Chapin, F. S., III. 1989. The cost of tundra plant structures: evaluation of concepts and currencies. Am. Nat. 133: 1–19.
Chiariello, N. 1984. Leaf energy balance in the wet lowland tropics. Pp. 85–98. In: Medina E., Mooney H. A. & Vasquez-Yanes C. (eds), Tasks for vegetation science 12. Physiological Ecology of Plants of the Wet Tropics. Proceedings of an International Symposium Held in Oxatepec and Los Tuxtlas, Mexico, June 29 to July 6, 1983. Dr. W. Junk Publishers, The Hague.
Chung, H.-H. & Barnes, R. L. 1977. Photosynthate allocation in Pinus taeda. I. Substrate requirements for synthesis of shoot biomass. Can. J. For. Res. 7: 106–111.
Curtis, J. T. & McIntosh, R. P. 1951. An upland forest continuum in the prairie-forest border region of Wisconsin. Ecology 32: 476–496.
Ducrey, M. 1992. Variation in leaf morphology and branching pattern of some tropical rain forest species from Guadeloupe (French West Indies) under semi-controlled light conditions. Ann. Sci. For. 49: 553–570.
Ellenberg, H. 1982. Vegetation Mitteleuropas mit den Alpen in Okologischer Sicht. Ed. 3. Verlag Eugen Ulmer, Stuttgart.
Ellenberg, H. 1991. Zeigerwerte der Gefäßpflanzen (ohne Rubus). Pp. 9–166. In: Ellenberg H., Düll R., Wirth V., Werner W. & Paulißen D. (eds), Scripta Geobotanica 18. Zeigerwerte von Pflanzen in Mitteleuropa. Erich Goltze KG, Göttingen.
Flora of the Estonian SSR. 1960–1984. Ed. 2. Vols. I-XII. Eesti Riiklik Kirjastus, Tallinn (in Estonian).
Fowells, H.A. 1965. Agriculture handbook No. 271. Silvics of Forest Trees of the United States. U.S. Department of Agriculture Forest Service, Washington, DC.
Gates, D. M. 1980. Biophysical Ecology. Springer-Verlag, New York.
Gayer, K. 1898. Der Waldbau. vierte, verbesserte Auflage. Verlagsbuchhandlung Paul Parey, Berlin.
Gholz, H. L., Fitz, F. K. & Waring, R. H. 1976. Leaf area differences associated with old-growth forest communities in the western Oregon Cascades. Can. J. For. Res. 6: 49–57.
Givnish, T. J. 1978. On the adaptive significance of compound leaves, with special reference to tropical trees. Pp. 351–380. In: Tomlinson P. B. & Zimmermann M. H. (eds), Tropical Trees as Living Systems. The Proceedings of the Fourth Cabot Symposium Held at Harvard Forest, Petersham, Massachusetts on April 26–30, 1976. Cambridge University Press, Cambridge.
Givnish, T. J. 1984. Leaf and canopy adaptations in tropical forests. Pp. 51–84. In: Medina E., Mooney H. A. & Vásquez-Yánes C. (eds), Tasks for vegetation science 12. Physiological Ecology of Plants of the Wet Tropics. Proceedings of an International Symposium Held in Oxatepec and Los Tuxtlas, Mexico, June 29 to July 6, 1983. Dr. W. Junk Publishers, The Hague.
Givnish, T. J. 1986. Biomechanical constraints on crown geometry in forest herbs. Pp. 525–583. In: Givnish T. J. (ed), On the Economy of Plant Formand Function. Proceedings of the Sixth Maria Moors Cabot Symposium, 'Evolutionary Constraints on Primary Productivity: Adaptive Patterns of Energy Capture in Plants', Harvard Forest, August 1983. Cambridge University Press, Cambridge.
Givnish, T. J. & Vermeij, G. J. 1976. Sizes and shapes of liana leaves. Am. Nat. 110: 743–776.
Greis, I. & Kellomäki, S. 1981. Crown structure and stem growth of Norway spruce undergrowth under varying shading. Silva Fenn. 40: 86–93.
Gulmon, S. L. & Chu, C. C. 1981. The effects of light and nitrogen on photosynthesis, leaf characteristics, and dry matter allocation in the chaparral shrub, Diplacus aurantiacus. Oecologia 65: 214–222.
Horn, H. S. 1971. The Adaptive Geometry of Trees. Princeton University Press, Princeton, New Jersey.
Howland, H. C. 1962. Structural, hydraulic, and 'economic' aspects of leaf venation and shape. Pp. 183–191. In: Bernard E. E. & Kare M. R. (eds), Biological Prototypes and Synthetic Systems. Proceedings of the Second Annual Symposium Sponsored by Cornell University and the General Electric Company, Advanced Electronics Center, Held at Cornell University, August 30–September 1, 1961. Vol. I. Plenum Press, New York.
Jahn, G. 1991. Temperate deciduous forests of Europe. Pp. 377–502. In: Röhrig E. & Ulrich B. (eds), Ecosystems of the world 7. Temperate Deciduous Forests. Elsevier, Amsterdam.
Kikuzawa, K. 1984. Leaf survival of woody plants in deciduous broad-leaved forests. 2. Small trees and shrubs. Can. J. Bot. 62: 2551–2556.
Kohyama, T. 1987. Significance of architecture and allometry in saplings. Funct. Ecol. 1: 399–404.
Koike, T. 1987. Photosynthesis and expansion in leaves of early, mid, and late successional tree species, birch, ash, and maple. Photosynthetica 21: 503–508.
Koike, T. 1988. Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Pl. Sp. Biol. 3: 77–87.
Küppers, M. 1989. Ecological significance of aboveground architectural patterns in woody plants: a question of cost-benefit relationships. TREE 4: 375–379.
Küppers, M. 1994. Canopy gaps: competitive light interception and economic space filling – a matter of whole-plant allocation. Pp. 111–144. In: Caldwell M. M. & Pearcy R.W. (eds), Physiological ecology. A series of monographs, texts, and treatises. Exploitation of Environmental Heterogeneity by Plants. Ecophysiological Processes Above-and Belowground. Academic Press, San Diego.
Kukk, T. & Ploompuu, T. 1992. Pôhja-kukemari. (Empetrum hermaphroditum in Estonia). Eesti Loodus 35: 250–251 (in Estonian).
Kuusk, V., Tabaka, L. & Jankevičhienè, R. (eds) 1996. Flora of the Baltic Countries. Compendium of Vascular Plants. Vol. II. Eesti Loodusfoto AS, Tartu.
Leuning, R., Kelliher, F. M., de Pury, D. G. G. & Schulze, E.-D. 1995. Leaf nitrogen, photosynthesis, conductance and transpiration: scaling from leaves to canopies. Plant Cell Environ. 18: 1183–1200.
Lieffers, V. J. & Stadt, K. J. 1994. Growth of understory Picea glauca, Calamagrostis canadensis, and Epilobium angustifolium in relation to overstory light transmission. Can. J. For. Res. 24: 1193–1198.
Maruyama, K. 1978. Ecological studies on natural beech forest. 32. Shoot elongation characteristics and phenological behavior of forest trees in natural beech forest. Bull. Niigata Univ. For. 11: 1–30.
Niinemets, Ü. 1995. Distribution of foliar carbon and nitrogen across the canopy of Fagus sylvatica: adaptation to a vertical light gradient. Acta Oecol. 16: 525–541.
Niinemets, Ü. 1996a. Dissertationes Biologicae Universitatis Tartuensis 19. Importance of Structural Features of Leaves and Canopy in Determining Species Shade-Tolerance in Temperate Deciduous Woody Taxa. Tartu University Press, Tartu.
Niinemets, Ü. 1996b. Plant growth-form alters the relationship between foliar morphology and species shade-tolerance ranking in temperate woody taxa. Vegetatio 124: 145–153.
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.
Niinemets, Ü. 1997b. Energy requirement for foliage construction depends on tree size in young Picea abies trees. Trees 11: 420–431.
Niinemets, Ü. 1997c. Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species. Funct. Ecol. 11: 518–531.
Niinemets, Ü. & Kull, K. 1994. Leaf weight per area and leaf size of 85 Estonian woody species in relation to shade tolerance and light availability. For. Ecol. Manage. 70: 1–10.
Niklas, K. J. 1991a. Biomechanical responses of Chamaedorea and Spathiphyllum petioles to tissue dehydration. Ann. Bot. 67: 67–76.
Niklas, K. J. 1991b. Effects of tissue volume and location on the mechanical consequences of dehydration of petioles. Amer. J. Bot. 78: 361–369.
Niklas, K. J. 1991c. Flexural stiffness allometries of angiosperm and fern petioles and rachises: evidence for biomechanical convergence. Evolution 45: 734–750.
Niklas, K. J. 1992. Petiole mechanics, light interception by lamina, and 'Economy in Design'. Oecologia 90: 518–526.
Niklas, K. J. 1994. Plant Allometry: The Scaling of Form and Process. The University of Chicago Press, Chicago.
Oberbauer, S. F., Strain, B. R. & Riechers, G. H. 1987. Field water relations of a wet-tropical forest tree species, Pentaclethra macroloba (Mimosaceae). Oecologia 71: 369–374.
Pearcy, R. W. & Sims, D. A. 1994. Photosynthetic acclimation to changing light environments: scaling from the leaf to the whole plant. Pp. 145–174. In: Caldwell M. M. & Pearcy R. W. (eds), Physiological ecology. A series of monographs, texts, and treatises. Exploitation of Environmental Heterogeneity by Plants. Ecophysiological Processes Above-and Belowground. Academic Press, San Diego.
Ploompuu, T. & Sander, H. 1995. Mitut liiki tuhkpuid kasvab Eesti metsades? (How many Cotoneaster species does growin Estonian forests?). Eesti Loodus 46: 232–233 (in Estonian).
Poorter, H. 1994. Construction costs and payback time of biomass: a whole plant perspective. Pp. 111–127. In: Roy J. & Garnier E. (eds), A Whole Plant Perspective on Carbon-Nitrogen Interactions. SPB Academic Publishing BV, The Hague.
Poorter, L., Oberbauer, S. F. & Clark, D. B. 1995. Leaf optical properties along a vertical gradient in a tropical rain forest canopy in Costa Rica. Amer. J. Bot. 82: 1257–1263.
Popma, J., Bongers, F. & Werger, M. J. A. 1992. Gap-dependence and leaf characteristics of trees in a tropical lowland rain forest in Mexico. Oikos 63: 207–214.
SAS Institute Inc. 1990. SAS/STAT User's Guide, Version 6. Ed. 4. Vol. 1–2. SAS Institute, Inc., Cary, NC.
Sims, D. A. & Pearcy, R. W. 1994. Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance – I. Carbon balance and allocation at different daily photon flux densities. Plant Cell Environ. 17: 881–887.
Sims, D. A., Gebauer, R. L. E. & Pearcy, R. W. 1994. Scaling sun and shade photosynthetic acclimation of Alocasia macrorrhiza to whole-plant performance – II. Simulation of carbon balance and growth at different photon flux densities. Plant Cell Environ. 17: 889–900.
Stowe, L. G. & Brown, J. L. 1981. A geographic perspective on the ecology of compound leaves. Evolution 35: 818–821.
Talbert, C. M. & Holch, A. E. 1957. A study of the lobing of sun and shade leaves. Ecology 38: 655–658.
Taylor, S. E. 1975. Optimal leaf form. Pp. 73–86. In: Gates D. M. & Schmerl R. B. (eds), Perspectives in Biophysical Ecology. Springer Verlag, Berlin.
ter Braak, C. J. F. & Gremmen, N. J. M. 1987. Ecological amplitudes of plant species and the internal consistency of Ellenberg's indicator values for moisture. Vegetatio 69: 79–87.
Turner, I. M., Gong, W. K., Ong, J. E., Bujang, J. S. & Kohyama, T. 1995. The architecture and allometry of mangrove saplings. Funct. Ecol. 9: 205–212.
Tyree, M. T., Cochard, H., Cruiziat, P., Sinclair, B. & Ameglio, T. 1993. Drought-induced leaf shedding in walnut: evidence for vulnerability segmentation. Plant Cell Environ. 16: 879–882.
Van Soest, P. J. 1963. Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. J. Assoc. Offic. Agric. Chem. 46: 829–835.
Vertregt, N. & Penning de Vries, F. W. T. 1987. A rapid method for determining the efficiency of biosynthesis of plant biomass. J. Theor. Biol. 128: 109–119.
Vogel, S. 1968. 'sun leaves' and 'shade leaves': differences in convective heat dissipation. Ecology 49: 1203–1204.
Weber, H. E. 1991. Zeigerwerte der Rubus-Arten. Pp. 167–174. In: Ellenberg H., Düll R., Wirth V., Werner W. & Paulißen D. (eds), Scripta Geobotanica 18. Zeigerwerte von Pflanzen in Mitteleuropa. Erich Goltze KG, Göttingen.
White, P. S. 1983. Corner's rules in eastern deciduous trees: allometry and its implications for the adaptive architecture of trees. Bull. Torrey Bot. Club 110: 203–212.
Woodwell, G. M., Whittaker, R. H. & Houghton, R. A. 1975. Nutrient concentrations in plants in the Brookhaven oak-pine forest. Ecology 56: 318–332.
Zon, R. & Graves, H. S. 1911. U.S. Department of Agriculture, Forest Service – Bulletin 92. Light in Relation to Tree Growth. Government Printing Office, Washington.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Niinemets, Ü. Are compound-leaved woody species inherently shade-intolerant? An analysis of species ecological requirements and foliar support costs. Plant Ecology 134, 1–11 (1998). https://doi.org/10.1023/A:1009773704558
Issue Date:
DOI: https://doi.org/10.1023/A:1009773704558