Variation in leaf and twig CO2 flux as a function of plant size: A comparison of seedlings, saplings and trees

Tree Physiology

Volumn 33, Issue 7, 2013, Pages 713-729

  Sendall, Kerrie M ^a,b   Reich, Peter B ^a,c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b MACQUARIE UNIVERSITY   (Australia)

^c WESTERN SYDNEY UNIVERSITY   (Australia)

Author keywords

Acer rubrum; dark respiration; LMA; nitrogen; ontogeny; photosynthetic capacity; Prunus serotina; Quercus ellipsoidalis

Indexed keywords

CARBON DIOXIDE; CARBON FLUX; COMPARATIVE STUDY; DECIDUOUS TREE; ENVIRONMENTAL FACTOR; GAS EXCHANGE; HEIGHT; LEAF; LIGHT AVAILABILITY; NITROGEN; NUTRIENT AVAILABILITY; ONTOGENY; PHOTOSYNTHESIS; PHYTOMASS; PLANT ARCHITECTURE; RESPIRATION; SAPLING; SEEDLING; SIZE;

MINNESOTA; UNITED STATES;

EID: 84882803467     PISSN: 0829318X     EISSN: 17584469     Source Type: Journal    
DOI: 10.1093/treephys/tpt048     Document Type: Article

References (93)

1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with Image J. Biophotonics Int 11:36-42
2. Ambrose AR, Sillett SC, Dawson TE (2009) Effects of tree height on branch hydraulics, leaf structure and gas exchange in California red-woods. Plant Cell Environ 32:743-757
3. Baker FS (1949) A revised tolerance table. J For 47:179-181
4. Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28:355-377
5. Boege K (2005) Herbivore attack in Casearia nitida influenced by plant ontogenetic variation in foliage quality and plant architecture. Oecologia 143:117-125
6. Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5:349-353
7. Botkin DB, Janak JF, Wallis JR (1972) Rationale, limitations and assump-tions of a Northeastern forest growth simulator. IBM J Res Dev 16:101-116
8. Canham CD, Denslow JS, Platt WJ, Runkle JR, Spies TA, White PS (1990) Light regimes beneath closed canopies and tree-fall gaps in temperate and tropical forests. Can J For Res 20:620-631
9. Carswell FE, Meir P, Wandelli EV, Bonates LCM, Kruijt B, Barbosa EM, Nobre AD, Grace J, Jarvis PG (2000) Photosynthetic capacity in a central Amazonian rain forest. Tree Physiol 20:179-186
10. Cavaleri MA, Oberbauer SF, Clark DB, Clark DA, Ryan MG (2010) Height is more important than light in determining leaf morphology in a tropical forest. Ecology 91:1730-1739
11. Chabot BF, Hicks DJ (1982) The ecology of leaf lifespans. Annu Rev Ecol Syst 13:229-259
12. Chazdon RL, Field CB (1987) Determinants of photosynthetic capacity in six rainforest Piper species. Oecologia 73:222-230
13. Coopman RE, Briceno VF, Corcuera LJ, Reyes-Diaz M, Alvarez D, Saez K, Garcia-Plazaola JI, Alberdi M, Bravo LA (2011) Tree size and light availability increase photochemical instead of non-photochemical capacities of Nothofagus nitida trees growing in an evergreen tem-perate rain forest. Tree Physiol 31:1128-1141
14. Cregg BM, Halpin JE, Dougherty PM, Teskey RO (1989) Comparative physiology and morphology of seedling and mature forest trees. In: Noble RD, Martin JL, Jensen KL (eds) Air pollution effects on vegeta-tion. USDA Forest Service, Broomall, PA, p 331
15. Day ME, Greenwood MS, White AS (2001) Age-related changes in foliar morphology and physiology in red spruce and their influence on declining photosynthetic rates and productivity with tree age. Tree Physiol 21:1195-1204
16. Delagrange S, Messier C, Lechowicz MJ, Dizengremel P (2004) Physiological, morphological and allocational plasticity in understory deciduous trees: Importance of plant size and light availability. Tree Physiol 22:775-784
17. Dijkstra FA, Wrage KJ, Hobbie SE, Reich PB (2006) Tree patches show greater N losses but maintain higher soil N availability than grass-land patches in a frequently burned oak savanna. Ecosystems 9:441-452
18. Dominy NJ, Lucas PW, Wright SJ (2003) Mechanics and chemistry of rain forest leaves: Canopy and understories compared. J Exp Bot 54:2007-2014
19. Drake JE, Raetz LM, Davis SC, DeLucia EH (2010) Hydraulic limitation not declining nitrogen availability causes the age-related photosyn-thetic decline in loblolly pine (Pinus taeda L.). Plant Cell Environ 33:1756-1766
20. Ellsworth DS, Reich PB (1993) Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96:169-178
21. Falster DS, Reich PB, Ellsworth DS, Wright IJ, Westoby M, Oleksyn J, Lee T (2012) Lifetime return on investment increases with leaf lifespan among 10 Australian woodland species. New Phytol 193:409-419
22. Fredericksen TS, Steiner KC, Skelley JM, Joyce BJ, Kolb TE, Kouterick KB, Ferdinand JR (1996) Diel and seasonal patterns of leaf gas exchange and xylem water potentials of different sized Prunus sero-tina Ehrh. trees. For Sci 42:359-365
23. Gerrish G (1990) Relating carbon allocation patterns to tree senes-cence in Metrosideros forests. Ecology 71:1176-1184
24. Givnish TJ (1988) Adaptation to sun and shade: A whole-plant per-spective. Austr J Plant Physiol 15:63-92
25. Gower ST, McMurtrie RE, Murty D (1996) Aboveground net primary production decline with stand age: Potential causes. Trends Ecol Evol Res 11:378-382
26. Greenwood MS, Ward MH, Day ME, Adams SL, Bond BJ (2008) Age-related trends in red spruce foliar plasticity in relation to declining productivity. Tree Physiol 28:225-232
27. Grulke NE, Miller PR (1994) Changes in gas exchange characteristics during the life span of the giant sequoia: Implications for response to current and future concentrations of atmospheric ozone. Tree Physiol 14:658-668
28. Gulmon SL, Chu CC (1981) The effect of light and nitrogen on photo-synthesis, leaf characteristics and dry matter allocation in the Chaparral shrub Diplacus aurantiacus. Oecologia 49:207-212
29. Han Q (2011) Height-related decreases in mesophyll conductance, leaf photosynthesis and compensating adjustments associated with leaf nitrogen concentrations in Pinus densiflora. Tree Physiol 31:976-984
30. Hanba YT, Miyazawa S, Terashima I (1999) The influence of leaf thick-ness on the CO2 transfer conductance and leaf stable carbon iso-tope ratio for some evergreen tree species in Japanese warm-temperate forests. Funct Ecol 13:632-639
31. Harley P, Guenther A, Zimmerman P (1996) Effects of light, tempera-ture, and canopy position on net photosynthesis and isoprene emis-sion from sweetgum leaves. Tree Physiol 16:25-32
32. Hubbard RM, Bond BJ, Ryan MG (1999) Evidence that hydraulic con-ductance limits photosynthesis in old Pinus ponderosa trees. Tree Physiol 19:165-172
33. Iio A, Fukasawa H, Nose Y, Kakubari Y (2004) Stomatal closure induced by high vapor pressure deficit limited midday photosynthe-sis at the canopy top of Fagus crenata Blume on Naeba mountain in Japan. Trees 18:510-517
34. Iio A, Fukasawa H, Nose Y, Naramoto M, Mizunaga H, Kakubari Y (2009) Within-branch heterogeneity of the light environment and leaf temperature in a Fagus crenata crown and its significance for photosynthesis calculations. Trees 23:1053-1064
35. Ishida A, Yazaki K, Hoe AL (2005) Ontogenetic transition of leaf physi-ology and anatomy from seedlings to mature trees of a rain forest pioneer tree, Macaranga gigantea. Tree Physiol 25:513-522
36. Karlsson PS, Olsson L, Hellstrom K (1996) Trade-offs among invest-ments in different long-shoot functions - variation among mountain birch individuals. J Ecol 84:915-921
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 Physiol 26:865-873
38. King DA, Wright SJ, Connell JH (2006) The contribution of interspecific variation in maximum tree height to tropical and temperate diversity. J Trop Ecol 22:11-24
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. Kitajima K, Mulkey SS, Wright SJ (2005) Variation in crown light utiliza-tion characteristics among tropical canopy trees. Ann Bot 95:535-547
41. Kleiber M (1932) Body size and metabolism. Hilgardia 6:315-353
42. Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851-854
43. Koike T (1986) A method for measuring photosynthesis with detached parts of deciduous broad-leaved trees in Hokkaido. J Jpn For Soc 68:425-428
44. Kolb TE, Stone JE (2000) Differences in leaf gas exchange and water relations among species and tree sizes in an Arizona pine-oak for-est. Tree Physiol 20:1-12
45. Leal DA, Thomas SC (2003) Vertical gradients and tree-to-tree varia-tion in shoot morphology and foliar nitrogen in an old-growth Pinus strobus L. stand. Can J For Res 33:1304-1314
46. Lee TD, Reich PB, Bolstad PV (2005) Acclimation of leaf respiration to temperature is rapid and related to specific leaf area, soluble sugars and leaf nitrogen across three temperate deciduous tree species. Funct Ecol 19:640-647
47. Machado JL, Reich PB (1999) Evaluation of several measures of can-opy openness as predictors of photosynthetic photon flux density in deeply shaded conifer-dominated forest understory. Can J For Res - Rev Can Rech For 29:1438-1444
48. Machado JL, Reich PB (2006) Dark respiration rate increases with plant size in saplings of three temperate tree species despite decreasing tissue nitrogen and nonstructural carbohydrates. Tree Physiol 26:915-923
49. Martinez-Vilalta J, Vanderklein D, Mencuccini M (2007) Tree height and age-related decline in growth in Scots pine (Pinus sylvestris L.). Oecologia 150:529-544
50. Merilo E, Tulva I, Raim O, Kukit A, Sellin A, Kull O (2009) Changes in needle nitrogen partitioning and photosynthesis during 80 years of tree ontogeny in Picea abies. Trees 23:951-958
51. Merino J, Field C, Mooney HA (1982) Construction and maintenance costs of Mediterranean-climate evergreen and deciduous leaves. I. Growth and CO2 exchange analysis. Oecologia 53:208-213
52. Miller PR, Eddleman LE, Miller JM (1991) The response of western juniper (Juniperus occidentalis) to reductions in above- and below-ground tissue. Can J For Res 21:207-216
53. Mitchell KA, Bolstad PV, Vose JM (1999) Interspecific and environmen-tally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species. Tree Physiol 19:861-870
54. Murtaugh PA (2003) On detecting hump-shaped relationships in ecol-ogy: A bootstrap test for monotonicity. Environmetrics 14:611-616
55. Nabeshima E, Hiura H (2008) Size-dependency in hydraulic and pho-tosynthetic properties of three Acer species having different maxi-mum sizes. Ecol Res 23:281-288
56. Niinemets U (1997a) Distribution patterns of carbon and nitrogen as affected by tree dimensions and relative light conditions in the can-opy of Picea abies. Trees 11:144-154
57. Niinemets U (1997b) Energy requirements for foliage construction depends on tree size in young Picea abies trees. Trees 11:420-431
58. Niinemets U (2002) Stomatal condictance alone does not explain the decline in foliar photosynthetic rate with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiol 22:515-535
59. Niinemets U, Kull O (1995) Effects of light availability and tree size on the architecture and assimilative surface in the canopy of Picea abies: Variation in needle morphology. Tree Physiol 15:307-315
60. Niinemets U, Valladares F (2006) Tolerance to shade, drought, and waterlogging of temperate Northern Hemisphere trees and shrubs. Ecol Monogr 76:521-547
61. Niinemets U, Ellsworth DS, Lukjanova A, Tobias M (2001) Site fertility and the morphological and photosynthetic acclimation of Pinus syl-vestris needles to light. Tree Physiol 21:1231-1244
62. Niklas KJ (1991) Effects of tissue volume and location on the mechani-cal consequences of dehydration of petioles. Am J Bot 78:361-369
63. O'Brien RM (2007) A caution regarding rules of thumb for variance inflation factors. Qual Quan 41:673-690
64. Parkhurst DF (1994) Diffusion of CO2 and other gases inside leaves. New Phytol 126:449-479
65. Pastor J, Stillwell MA, Tilman D (1987) Nitrogen mineralization and nitrification in four Minnesota old fields. Oecologia 71:481-485
66. Peterson D, Reich PB (2001) Prescribed fire in oak savanna: Fire fre-quency effects on stand structure and dynamics. Ecol Appl 11:914-927
67. Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen econ-omy of 24 wild species differing in relative growth rate. Plant Physiol 94:621-627
68. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-9000051-07-0, http://www.R-project.org
69. Reich PB, Ellsworth DS, Walters MB (1991) Leaf development and sea-son influence the relationships between leaf nitrogen, leaf mass per area, and photosynthesis in maple and oak trees. Plant Cell Environ 14:251-259
70. 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
71. Reich PB, Walters MB, Ellsworth DS, Uhl C (1994) Photosynthesis-nitrogen relationships in Amazonian tree species. I. Patterns among species and communities. Oecologia 97:62-72
72. Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: Global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730-13734
73. Reich PB, Tjoelker MG, Machado JL, Oleksyn J (2006) Universal scal-ing of respiratory metabolism, size, and nitrogen in plants. Nature 435:457-461
74. Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL (2008) Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecol Lett 11:793-801
75. Rijkers T, Pons TL, Bongers F (2000) The effect of tree height and light availability on photosynthetic leaf traits of four neotropical spe-cies differing in shade tolerance. Funct Ecol 14:77-86
76. Ryan MG (1991) Effects of climate change on plant respiration. Ecol Appl 1:157-167
77. Ryan MG, Binkley D, Fownes JH (1997) Age-related declines in forest productivity: Pattern and process. Adv Ecol Res 27:213-262
78. Schmidt-Nielson K (ed) (1984) Scaling: Why is animal size so impor-tant? Cambridge University Press, Cambridge, UK
79. Schoettle AW (1994) Influence of tree size on shoot structure and physiol-ogy of Pinus contorta and Pinus aristata. Tree Physiol 14:1055-1068
80. Sipe TW, Bazzaz FA (1994) Gap partitioning among maples (Acer) in central New England - Shoot architecture and photosynthesis. Ecology 75:2318-2332
81. Thomas SC (2010) Photosynthetic capacity peaks at intermediate size in temperate deciduous trees. Tree Physiol 30:555-573
82. Thomas SC (2011) Age-related changes in tree growth and functional biology: The role of reproduction. In: Meinzer FC, Lachenbruck B, Dawson TE (eds) Size- and age-related changes in tree structure and function. Springer, New York, pp 33-64
83. Thomas SC, Bazzaz FA (1999) Asymptotic height as a predictor of photosynthetic characteristics in Malaysian rain forest trees. Ecology 80:1607-1622
84. Thomas SC, Winner WE (2002) Photosynthetic differences between saplings and adult trees: An integration of field results by meta-anal-ysis. Tree Physiol 22:117-127
85. 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
86. Waring RH, McDonald AJS, Larsson S, Ericsson T, Wiren A, Arwidsson E, Ericsson A, Lohammar T (1985) Differences in chemical composition of plants grown at constant relative growth rates with stable mineral nutrition. Oecologia 66:157-160
87. Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant eco-logical strategies: Some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125-159
88. Westoby M, Warton D, Reich PB (2000) The time value of leaf area. Am Nat 155:649-656
89. Wheelwright NT, Logan BA (2004) Previous-year reproduction reduces photosynthetic capacity and slows lifetime growth in females of a neotropical tree. Proc Natl Acad Sci USA 101: 8051-8055
90. Williams K, Field C, Mooney HA (1989) Relationships among leaf con-struction cost, leaf longevity, and light environment in rain-forst plants of the genus Piper. Am Nat 133:198-211
91. Woodruff DR, Bond BJ, Meinzer FC (2004) Does turgor limit growth in tall trees? Plant Cell Environ 27:229-236
92. Wright IJ, Reich PB, Westoby M et al. (2004) The worldwide leaf eco-nomics spectrum. Nature 428:821-827
93. Yoder BJ, Ryan MG, Waring RH, Schoettle AW, Kaufmann MR (1994) Evidence of reduced photosynthetic rates in old trees. For Sci 40:513-527