Global meta-analysis shows that relationships of leaf mass per area with species shade tolerance depend on leaf habit and ontogeny

New Phytologist

Volumn 176, Issue 4, 2007, Pages 764-774

  Lusk, Christopher H ^a   Warton, David I ^b  

^a MACQUARIE UNIVERSITY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Independent contrasts; Leaf traits; Light; Plant functional types; Sapling; Seedling; Specific leaf area

Indexed keywords

COMPARATIVE STUDY; DECIDUOUS TREE; EVERGREEN TREE; LEAF AREA; META-ANALYSIS; ONTOGENY; SAPLING; SEEDLING; SHADE TOLERANCE;

CLASSIFICATION; DARKNESS; HISTOLOGY; LIGHT; META ANALYSIS; PHYSIOLOGY; PLANT LEAF; RADIATION EXPOSURE; REVIEW;

DARKNESS; LIGHT; PLANT LEAVES;

EID: 36048932316     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2007.02264.x     Document Type: Review

References (84)

1. Abrams MD, Kubiske ME. 1990. Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin - influence of light regime and shade-tolerance rank. Forest Ecology and Management 31 : 245 253.
2. Ackerly D, Donoghue MJ. 1998. Leaf size, sapling allometry, and Corner's rules: phylogeny and correlated evolution in maples (Acer). American Naturalist 152 : 762 791.
3. Ackerly DD, Reich PB. 1999. Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. American Journal of Botany 86 : 1272 1281.
4. Alverson WS, Whitlock BA, Nyffeler R, Bayer C, Baum DA. 1999. Phylogeny of the core Malvales: evidence from ndhF sequence data. American Journal of Botany 86 : 1474 1486.
5. Baum DA, Smith SD, Yen A, Alverson WS, Nyffeler R, Whitlock BA, Oldham RL. 2004. Phylogenetic relationships of Malvatheca (Bombacoideae and Malvoideae; Malvaceae sensu lato) as inferred from plastid DNA sequences. American Journal of Botany 91 : 1863 1871.
6. Bayer C, Fay MF, De Bruijn AY, Savolainen V, Morton CM, Kubitzki K, Alverson WS, Chase MW. 1999. Support for an expanded family concept of Malvaceae within a recircumscribed order Malvales: a combined analysis of plastid atpB and rbcL DNA sequences. Botanical Journal of the Linnean Society 129 : 267 303.
7. Berendse F, Aerts R. 1987. Nitrogen use efficiency: a biologically meaningful definition? Functional Ecology 1 : 293 296.
8. Blattner FR, Weising K, Bänfer G, Maschwitz U, Fiala B. 2001. Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae). Molecular Phylogenetics and Evolution 19 : 331 344.
9. Boardman NK. 1977. Comparative photosynthetis of sun and shade plants. Annual Review of Plant Physiology 28 : 355 377.
10. Bradford JC, Barnes RW. 2001. Phylogenetics and classification of Cunoniaceae (Oxalidales) using chloroplast DNA sequences and morphology. Systematic Botany 26 : 354 385.
11. Bruneau A, Forest F, Herendeen PS, Klitgaard BB, Lewis GP. 2001. Phylogenetic relationships in the Caesalpinioideae (Leguminosae) as inferred from chloroplast trnL intron sequences. Systematic Botany 26 : 487 514.
12. Chazdon RL, Fetcher N. 1984. Photosynthetic light environments in a lowland tropical rain forest in Costa Rica. Journal of Ecology 72 : 553 564.
13. Chen Z, Manchester SR, Sun H. 1999. Phylogeny and evolution of the Betulaceae inferred from DNA sequences, morphology, and paleobotany. American Journal of Botany 86 : 1168 1181.
14. Cornelissen JHC, Diez PC, Hunt R. 1996. Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types. Journal of Ecology 84 : 755 765.
15. Datwyler SL, Weiblen GD. 2004. On the origin of the fig: phylogenetic relationships of Moraceae from ndhF sequences. American Journal of Botany 91 : 767 777.
16. Davies SJ. 1998. Photosynthetic characteristics of nine early successional Macaranga species from Borneo in relation to life-history traits. Ecology 79 : 2292 2308.
17. Ellis AR, Hubbell SP, Potvin C. 2000. In situ field measurements of photosynthetic rates of tropical tree species: a test of the functional group hypothesis. Canadian Journal of Botany 78 : 1336 1347.
18. Evans GC. 1972. The quantitative analysis of plant growth. Berkeley, CA, USA : University of California Press.
19. Felsenstein J. 1985. Phylogenies and the comparative method. American Naturalist 125 : 1 15.
20. Givnish TJ. 1988. Adaptation to sun and shade: a whole-plant perspective. Australian Journal of Plant Physiology 15 : 63 92.
21. Grafen A. 1992. The uniqueness of the phylogenetic regression. Journal of Theoretical Biology 156 : 405 423.
22. Grime JP. 1979. Plant strategies and vegetation processes. New York, NY, USA : John Wiley & Sons.
23. Grubb PJ. 1998. A reassessment of the strategies of plants which cope with shortages of resources. Perspectives in Plant Ecology, Evolution and Systematics 1 : 3 31.
24. Hammond DS, Brown VK. 1995. Seed size of woody plants in relation to disturbance, dispersal, soil type in wet neotropical forests. Ecology 76 : 2544 2561.
25. Hamzeh M, Dayanandan S. 2004. Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast TRNT-TRNF region and nuclear rDNA. American Journal of Botany 91 : 1398 1408.
26. Hanba YT, Kogami H, Terashima I. 2002. The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. Plant, Cell & Environment 25 : 1021 1030.
27. Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology. Oxford, UK : Oxford University Press.
28. Hedges LV, Olkin I. 1985. Statistical methods for meta-analysis. Orlando, FL, USA : Academic Press.
29. Hewitt N. 1998. Seed size and shade-tolerance: a comparative analysis of North American temperate trees. Oecologia 114 : 432 440.
30. Hunter JE, Schmidt FL. 2004. Methods of meta-analysis. Thousand Oaks, CA, USA : Sage Publications.
31. Indrioko S, Gailing O, Finkeldey R. 2006. Molecular phylogeny of Dipterocarpaceae in Indonesia based on chloroplast DNA. Plant Systematics and Evolution 261 : 99 115.
32. Irschick DJ, Austin CC, Petren K, Fisher RN, Losos JB, Ellers O. 1996. A comparative analysis of clinging ability among pad bearing lizards. Biological Journal of the Linnean Society 59 : 21 35.
33. Jarvinen P, Palmé ALOM, Lannenpaa M, Keinanen M, Sopanen T, Lascoux M. 2004. Phylogenetic relationships of Betula species (Betulaceae) based on nuclear ADH and chloroplast matK sequences. American Journal of Botany 91 : 1834 1845.
34. Johnson LAS, Briggs BG. 1975. On the Proteaceae - the evolution and classification of a southern family. Botanical Journal of the Linnean Society 70 : 83 182.
35. Kamiya K, Harada K, Tachida H, Ashton PS. 2005. Phylogeny of PgiC gene in Shorea and its closely related genera (Dipterocarpaceae), the dominant trees in Southeast Asian tropical rain forests. American Journal of Botany 92 : 775 788.
36. Karst A, Lechowicz MJ. 2007. Are correlations among foliar traits in ferns consistent with those in the seed plants? New Phytologist 173 : 306 312.
37. Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T. 2006. Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiology 26 : 865 873.
38. Kikuzawa K. 1995. The basis for variation in leaf longevity of plants. Vegetatio 121 : 89 100.
39. 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.
40. Koike T. 1988. Leaf structure and photosynthetic performance as related to the forest succession of deciduous broad-leaved trees. Plant Species Biology 3 : 77 87.
41. Lambers H, Chapin FS, Pons TL. 1994. Plant physiological ecology. New York, NY, USA : Springer-Verlag.
42. Lambers H, Poorter H. 1992. Inherent variation in growth rate between higher plants: a search for physiological causes and consequences. Advances in Ecological Research 23 : 187 261.
43. Light RJ, Pillemer DB. 1984. Summing up: the science of reviewing research. Cambridge, MA, USA : Harvard University Press.
44. Lorimer CG, Frelich LE, Nordheim EV. 1988. Estimating gap origin probabilities for canopy trees. Ecology 69 : 778 785.
45. Lusk CH. 2002. Leaf area accumulation helps juvenile evergreen trees tolerate shade in a temperate rainforest. Oecologia 132 : 188 196.
46. Lusk CH. 2004. Leaf area and growth of juvenile temperate evergreens in low light: species of contrasting shade tolerance change rank during ontogeny. Functional Ecology 18 : 820 828.
47. Lusk CH, Reich PB. 2000. Relationships of leaf dark respiration with light environment and tissue nitrogen content in juveniles of 11 cold-temperate tree species. Oecologia 123 : 318 329.
48. Lusk CH, Smith B. 1998. Life history differences and tree species coexistence in an old-growth New Zealand rain forest. Ecology 79 : 795 806.
49. Manos PS, Zhou Z-K, Cannon CH. 2001. Systematics of Fagaceae: phylogenetic tests of reproductive trait evolution. International Journal of Plant Sciences 162 : 1361 1379.
50. Martins EP. 2004. COMPARE, version 4.6b. Computer programs for the statistical analysis of comparative data. Bloomington, IN, USA : Department of Biology, Indiana University (distributed by the author at http://compare.bio. indiana.edu/).
51. Matsuki S, Koike T. 2006. Comparison of leaf life span, photosynthesis and defensive traits across seven species of deciduous broad-leaf tree seedlings. Annals of Botany 97 : 813 817.
52. McConnaughay KDM, Coleman JS. 1999. Biomass allocation in plants: Ontogeny or optimality? A test along three resource gradients. Ecology 80 : 2581 2593.
53. McVaugh R. 1968. The genera of American Myrtaceae - an interim report. Taxon 17 : 354 418.
54. Muellner AN, Samuel R, Johnson SA, Cheek M, Pennington TD, Chase MW. 2003. Molecular phylogenetics of Meliaceae (Sapindales) based on nuclear and plastid DNA sequences. American Journal of Botany 90 : 471 480.
55. Niinemets Ü. 1999. Components of leaf dry mass per area - thickness and density - alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 144 : 35 47.
56. Niinemets Ü. 2006. The controversy over traits conferring shade-tolerance in trees: ontogenetic changes revisited. Journal of Ecology 94 : 464 470.
57. Niinemets Ü, Portsmuth A, Tena D, Tobias M, Matesanz S, Valladares F. 2007. Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy. Annals of Botany 100 : 283 303.
58. Niinemets Ü, Valladares F. 2006. Tolerance to shade, drought, and waterlogging of temperate Northern Hemisphere trees and shrubs. Ecological Monographs 76 : 521 547.
59. Poorter L. 2007. Are species adapted to their regeneration niche, adult niche, or both? American Naturalist 169 : 433 442.
60. Poorter L, Bongers F. 2006. Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87 : 1733 1743.
61. Poorter H, Remkes C. 1990. Leaf-area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia 83 : 553 559.
62. Poorter L, Rose S. 2005. Light-dependent changes in the relationship between seed mass and seedling traits: a meta-analysis for rain forest tree species. Oecologia 142 : 378 387.
63. Popma J, Bongers F. 1988. The effect of canopy gaps on growth and morphology of seedlings of rain forest species. Oecologia 75 : 625 632.
64. Quinn GP, Keough MJ. 2002. Experimental designs and data analysis for biologists. Cambridge, UK : Cambridge University Press.
65. Reich PB, Uhl C, Walters MB, Prugh L, Ellsworth DS. 2004. Leaf demography and phenology in Amazonian rain forest: a census of 40 000 leaves of 23 tree species. Ecological Monographs 74 : 3 23.
66. Reich PB, Walters MB, Ellsworth DS. 1997. From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences, USA 94 : 13730 13734.
67. Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB. 2003. The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164 : 143 164.
68. Reich PB, Wright IJ, Lusk CH. 2007. Predicting leaf physiology from simple plant and climate attributes: a global Glopnet analysis. Ecological Applications 17 : 1982 1988.
69. Roche P, Díaz-Burlinson N, Gachet S. 2004. Congruency analysis of species ranking based on leaf traits: which traits are the more reliable? Plant Ecology 174 : 37 48.
70. Roderick ML, Berry SL, Noble IR, Farquhar GD. 1999. A theoretical approach to linking the composition and morphology with the function of leaves. Functional Ecology 13 : 683 695.
71. Sack L, Maranon T, Grubb PJ. 2002. Global allocation rules for patterns of biomass partitioning. Science 296 : 1923.
72. Shipley B, Lechoweicz MJ, Wright I, Reich PB. 2006. Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87 : 535 541.
73. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF et al. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society 133 : 381 461.
74. Tilman D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton, NJ, USA : Princeton University Press.
75. Tokuoka T, Tobe H. 2006. Phylogenetic analyses of Malpighiales using plastid and nuclear DNA sequences, with particular reference to the embryology of Euphorbiaceae sens. str. Journal of Plant Research 119 : 599 616.
76. Veenendaal EM, Swaine MD, Lecha RT, Walsh MF, Abebrese IK, Owusu-Afriyie K. 1996. Responses of West African forest tree seedlings to irradiance and soil fertility. Functional Ecology 10 : 501 511.
77. Veneklaas EJ, Poorter L. 1998. Growth and carbon partitioning of tropical tree seedlings in contrasting light environments. In : Lambers H, Poorter H, van Vuren MMI, eds. Inherent variation in plant growth. Physiological mechanisms and ecological consequences. Leiden, the Netherlands : Backhuys Publishers, 337 361.
78. Walters MB, Reich PB. 1999. Low-light carbon balance and shade tolerance in the seedlings of woody plants: do winter deciduous and broad-leaved evergreen species differ? New Phytologist 143 : 143 154.
79. 2 exchange: a component of variation in shade tolerance among cold temperate tree seedlings. Functional Ecology 14 : 155 165.
80. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33 : 125 159.
81. Williams K, Field CB, Mooney HA. 1989. Relationships among leaf construction cost, leaf longevity, and light environments in rain-forest plants of the genus Piper. The American Naturalist 133 : 199 211.
82. Wilson PJ, Thompson K, Hodgson JG. 1999. Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytologist 143 : 155 162.
83. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al. 2004. The worldwide leaf economics spectrum. Nature 428 : 821 827.
84. Wright IJ, Westoby M, Reich PB. 2002. Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span. Journal of Ecology 90 : 534 543.