Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees

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Among 13 tropical tree species on Barro Colorado Island, species with high seedling mortality rates during the first year in shade had higher reltive growth rates (RGR) from germination to 2 months in both sun (23% full sun) and shade [2%, with and without lowered red: far red (R:FR) ratio] than shade tolerant species. Species with higher RGR in sun also had higher RGR in shade. These interspecific trends could be explained by differences in morphological traits and allocation paterns among species. Within each light regime, seedlings of shade-intolerant species had lower root: shoot ratios, higher leaf mass per unit area, and higher leaf area ratios (LAR) than shade tolerant species. In contrast, leaf gas exchange characteristics, or acclimation potential in these traits, had no relationship with seedling mortality rates in shade. In both shade tolerant and intolerant species, light saturated photosynthesis rates, dark respiration, and light compensation points were higher for sungrown seedlings than for shade-grown seedlings. Differences in R:FR ratio in shade did not affect gas exchange, allocation patterns, or growth rates of any species. Survival of young tree seedlings in shade did not depend on higher net photosynthesis or biomass accumulation rates in shade. Rather, species with higher RGR died faster in shade than species with lower RGR. This trend could be explained if survival depends on morphological characteristics likely to enhance defense against herbivores and pathogens, such as dense and tough leaves, a well-established root system, and high wood density. High construction costs for these traits, and low LAR as a consequence of these traits, should result in lower rates of whole-plant carbon gain and RGR for shade tolerant species than shade-intolerant species in shade as well as in sun.

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  1. Augspurger CK (1984a) Seedling survival of tropical tree species:interactions of dispersal distance, light gaps, and pathogens. Ecology 65: 1705–1712

  2. Augspurger CK (1984b) Light requirements ofnneotropical tree seedlings: a comparative study of growth and survival. J Ecol 72:777–795

  3. Bazzaz FA (1979) Physiological ecology of plant succession. Annu Rev Ecol Syst 10:351–371

  4. Bazzaz FA, Carlson RW (1982) Photosynthetic acclimation to variability in the light environment of early and late successional plants. Oecologia 54: 313–316

  5. Bazzaz FA, Pickett STA (1980) Physiological ecology of tropical succession: a comparative review. Annu Rev Ecol Syst 11: 287–310

  6. Begon M, Mortimer M (1981) Population ecology. Sinauer Associates, Sunderland

  7. Björkman O (1981) Responses to different quantum flu densities. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology NS vol 12A. Springer Heidelberg, pp 57–107

  8. Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28: 355–377

  9. Brokaw NVL (1985) Treefalls, regrowth, and community structure in tropical forest. In: Picket STA, White PS (eds) The ecology of natural disturbance and patch dynamics. Academic Press, New York, pp 53–69

  10. Canham CD (1988) Growth and canopy architecture of shade tolerant trees: response to canopy gaps. Ecology 69: 786–795

  11. Chapin FS, Schulze ED, Mooney HA (1990). The ecology and economics of storage in plants. Annu Rev Ecol Syst 21: 432–447

  12. Chazdon RL (1992) Photosynthetic plasticity of two rain forest shrubs across natural gap transect. Oecologia 92: 586–595

  13. Chow WS, Melis A, Anderson JM (1990) Adjustments of photosystem stoichiometry in chloroplasts improve quantum efficiency of photosynthesis. Proc Natl Acad Sci USA 87: 7502–7506

  14. Coley PD (1993) Gap size and plant defenses. Trends Ecol Evol 8: 1–2.

  15. Coley PD, Bryant JP, Chapin FS III, (1985). Resource availability and plant anti-herbivore defense. Science 230: 895–899

  16. Croat TN (1978) Flora of Barro Colorado Island. Stanford University Press, Stanford

  17. Denslow JS (1987) Tropical rainforest gaps and tree species diversity. Annu Rev Ecol Syst 18: 431–451

  18. Ehleringer J (1983) Ecophysiology of Amaranthus palmeri, a Sonoran desert summer annual. Oecologia 57: 107–112

  19. Ellison AM, Denslow JS, Loiselle BA, Brenez MD (1993) Field and seedling ecology of neotropical Melastomataceae. Ecology 74: 1733–1749

  20. Fetcher N, Strain BR, Oberbauer SF (1983) Effects of light regime on the growth, leaf morphology, and water relations of two species of tropical trees. Oecologia 58: 314–319

  21. Fetcher N, Oberbauer SF, Rojas G, Strain BR (1987) Effectos delrégimen de luz sobre la fotosíntesis y el crecimiento en plántulas de árboles de un bosque lluvioso tropical de Costa Rica. Rev Biol Trop 35: 97–110

  22. Fredeen AL Field CB (1991) Leaf respiration in Piper species native to a Mexican rainforest. Physiol Plant 82: 85–95

  23. Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15: 63–92.

  24. Grime JP, Jeffrey DW (1965) Seedlings establishment in vertical gradients of sunlight. J Ecol 53: 621–642

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

  26. Hubbel SP, Foster RB (1986) Canopy gaps and the dynamics of a neotropical forest. In: Crawley MJ (ed) Plant ecology. Blackwell Scientific, Oxford, pp 77–96

  27. Hunt R (1982) Plant Growth Curves. Edward Arnold, London

  28. Kitajima K (1992a) The importance of cotyledon functional morphology and patterns of seed reserve utilization for the physiological ecology of neotropical tree seedlings. PhD Dissertation, University of Illinois, Urbana-Champaign, pp 201

  29. Kitajima K (1992b) Relationship between photosynthesis and thickness of cotyledons for tropical tree species. Funct Ecol 6: 582–589

  30. Kitajima K, Augspurger CK (1989) Seed and seedling ecology of a monocarpic tropical tree, Tachigalia versicolor. Ecology 70: 1102–1114

  31. Koike T (1988). Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant Sp Biol 3: 77–87

  32. Koyama H (1981) Photosynthetic rates in lowland rain forest trees of peninsular Malaysia. Jp J Ecol 31: 361–369

  33. Kwesiga F, Grace J (1986) The role of the red/far-red ratio in the response of tropical tree seedlings to shade. Ann Bot 57: 283–290

  34. Kwesiga FR, Grace J, Sandford AP (1986) Some photosynthetic characteristics of tropical timber trees as affected by the light regime during growth. Ann Bot 58: 23–32

  35. Langenheim JH, Osmond CB, Brooks A, Ferrar PJ (1984) Photosynthetic responses to light in seedlings of selected Amazonian and Australian rainforest tree species. Oecologia 63: 215–224

  36. Lee DW (1985) Duplicating foliage shade for research on plant development. Hort Sci 20: 116–118

  37. Lei TT, Lechowicz MJ (1990). Shade adaptation and shade tolerance in saplings of three Acer species from eastern North America. Oecologia 84: 224–228

  38. Leigh EG Jr, Rand AS, Windsor DM (1982) The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Institution Press, Washington DC

  39. Loach K (1967) Shade tolerance in tree seedlings. I. Leaf photosynthesis and respiration in plants raised under artificial shade. New Phytol 66: 607–621

  40. Loach K (1970) Shade tolerance in tree seedlings. II. Growth analysis of plants raised under artificial shade. New Phytol 69: 273–286

  41. Lugo A (1970) Photosynthetic studies on four species of rainforest seedlings. In: Odum HT (ed) A tropical rain forest. US Atomic Energy Commission, Washington DC, pp I81-I102

  42. Mooney HA (1972) The carbon balance of plants. annu Rev Ecol Syst 3: 315–346

  43. Morikawa Y, Asakawa S, Sasaki S (1976) Growth of pine and birch seedlings under lights with different spectral compositions and intensities. J Jap For Soc 58: 174–178

  44. Mulkey SS (1986) Photosynthetic acclimation and water-use efficiency of three species of understory herbaceous bamboo (Gramineae) in Panama. Oecologia 70: 514–519

  45. Oberbauer SF, Strain BR (1984) Photosynthesis and successional status of Costa Rican rain forest trees. Photosyn Res 5: 227–232

  46. Oberbauer SF, Strain BR (1986) Effects of light regime on the grwoth and physiology of Pentaclethra macroloba (Mimosaceae) J Trop Ecol 1: 303–320

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

  48. Ramos J, Grace J (1990) The effects of shade on the gas exchange of seedlings of four neotropical trees from Mexico. funct Ecol 4: 667–677

  49. Reich PB, Uhl C, Walters MB, Ellsworth DS (1991). Leaf liferspan as a determinant of leaf structure and function among 23 Amazonian tree species. Oecologia 86: 16–24.

  50. Shure DJ, Wilson LA (1993) Patch-size effects on plant phenolics in successional openings of the Southern Appalachians. Ecology 74: 55–67.

  51. Sims DA, Pearcy RW (1989) Photosynthetic characteristics of a tropical forest understory herb, Alocasia macrorrhiza, and a related crop species, Colocasia esculenta, grown in contrasting light environments. Oecologia 79: 53–59

  52. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33: 481–518

  53. Smith H (1982) Light quality, photoperception, and plant strategy. Annu Rev Plant Physiol 33: 481–518

  54. Stephens GR, Waggoner PE (1970) Carbon dioxide exchange of a tropical rain forest. Part I. BioScience 20: 1050–1053

  55. Strauss-Debenedetti S, Bazzaz FA (1991) Plasticity and acclimation to light in tropical Moraceae of different successional positions. Oecologia 87: 377–387

  56. Swaine MD, Whitmore TC (1988) On the definition of ecological species groups in tropical rain forest. Vegetatio 75: 81–86

  57. Turnbull MH (1991). The effect of light quantity and quality during development of the photosynthetic characteristics of six Australian rainforest tree species. Oecologia 87: 110–117.

  58. Turner IM (1990) Tree seedling growth and survival in a Malaysian rain forest. Biotropica 22: 146–154.

  59. Walters M, Field CB (1987) Photosynthetic light acclimation in two rainforest Piper species with different ecological amplitudes. Oecologia 72: 449–456

  60. Walters MB, Kruger EL, Reich PB (1993) Growth, biomass distribution and CO2 exchange of northern hardwood seedlings in high and low light: relationships with successional status and shade tolerance. Oecologia 94: 7–16

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Kitajima, K. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98, 419–428 (1994) doi:10.1007/BF00324232

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Key words

  • Shade tolerance
  • Leaf photosynthesis
  • Seedling morphology
  • Growth analysis
  • Light acclimation