Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands

Plant, Cell and Environment

Volumn 33, Issue 6, 2010, Pages 959-980

  Domingues, Tomas Ferreira ^a   Meir, Patrick ^a   Feldpausch, Ted R ^b   Saiz, Gustavo ^c   Veenendaal, Elmar M ^d   Schrodt, Franziska ^c   Bird, Michael ^b   Djagbletey, Gloria ^e   Hien, Fidele ^f   Compaore, Halidou ^f   Diallo, Adama ^g   Grace, John ^a   Lloyd, Jon ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e FORESTRY RESEARCH INSTITUTE OF GHANA   (Ghana)

^f INSTITUT DE L'ENVIRONNEMENT ET DE RECHERCHES AGRICOLES   (Burkina Faso)

^g Centre National des Semences Forestieres   (Burkina Faso)

Author keywords

A Ci curves; Dry forest; NPP; Photosynthesis; Savanna; Tropical rain forest

Indexed keywords

NITROGEN; PHOSPHORUS;

DATA SET; DRY FOREST; FOREST ECOSYSTEM; LEAF; NITROGEN; NUTRIENT LIMITATION; PHOSPHORUS; PHOTOSYNTHESIS; PRECIPITATION INTENSITY; RAINFOREST; SAVANNA; TROPICAL FOREST; VEGETATION TYPE; WOODLAND;

AFRICA; ARTICLE; BIOMASS; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; QUANTITATIVE TRAIT; REGRESSION ANALYSIS; SEASON; TREE;

AFRICA, WESTERN; BIOMASS; NITROGEN; PHOSPHORUS; PHOTOSYNTHESIS; PLANT LEAVES; QUANTITATIVE TRAIT, HERITABLE; REGRESSION ANALYSIS; SEASONS; TREES;

WEST AFRICA;

EID: 77953279866     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2010.02119.x     Document Type: Article

References (103)

1. Akaike H. A new look at the statistical model identification. IEEE Transactions on Automatic Control 1974, 19:716-723.
2. Beerling DJ, Quick WP. A new technique for estimating rates of carboxylation and electron-transport in leaves of C-3 plants for use in dynamic global vegetation models. Global Change Biology 1995, 1:289-294.
3. Bernacchi CJ, Pimentel C, Long SP. In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant, Cell & Environment 2003, 26:1419-1430.
4. Boudsocq M, Laurière C. Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. Plant Physiology 2005, 138:1185-1194.
5. Burnham KP, Anderson DR. Model Selection and Multimodel Inference: A Practical-Theoretic Approach 2002, 2nd, edn, Springer-Verlag, Fort Collins, CO, USA
6. von Caemmerer S. Biochemical Model of Leaf Photosynthesis 2000, 1-165. SCIRO Publishing, Collingwood, Victoria, Australia
7. Carswell FE, Meir P, Wandelli EV, Bonates LCM, Kruijt B, Barbosa EM, Nobre AD, Grace J, Jarvis PG. Photosynthetic capacity in a central Amazonian rain forest. Tree Physiology 2000, 20:179-186.
8. Coste S, Roggy JC, Imbert P, Born C, Bonal D, Dreyer E. Leaf photosynthetic traits of 14 tropical rain forest species in relation to leaf nitrogen concentration and shade tolerance. Tree Physiology 2005, 25:1127-1137.
9. Dietzel L, Bräutigam K, Pfannschmidt T. Photosynthetic acclimation: State transitions and adjustment of photosystem stoichiometry - functional relationships between short-term and long-term light quality acclimation in plants. FEBS Journal 2008, 275:1080-1088.
10. Domingues TF, Berry JA, Martinelli LA, Ometto JPH, Ehleringer JR. Parameterization of canopy structure and leaf-level gas exchange for an eastern Amazonian tropical rain forest (Tapajós National Forest, Pará, Brazil). Earth Interactions 2005, 9:1-23.
11. Domingues TF, Martinelli LA, Ehleringer JR. Ecophysiological traits of plant functional groups in forest and pasture ecosystems from eastern Amazônia, Brazil. Plant Ecology 2007, 193:101-112.
12. Eamus D, Myers B, Duff G, Williams D. Seasonal changes in photosynthesis of eight savanna tree species. Tree Physiology 1999, 19:665-671.
13. Evans JR. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 1989, 78:9-19.
14. Farquhar GD, von Caemmerer S, Berry JA. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 1980, 149:78-90.
15. Field CB, Mooney HA. The photosynthesis-nitrogen relationship in wild plants. On the Economy of Plant Form and Function 1986, 25-55. Givnish TJ, ed., Cambridge University Press, Cambridge
16. Franco AC. Seasonal patterns of gas exchange, water relations and growth of it Roupala montana, an evergreen savanna species. Plant Ecology 1998, 136:69-76.
17. Furley PA. Edaphic changes at the forest-savanna boundary with particular reference to the neotropics. Nature and Dynamics of Forest-Savanna Boundaries 1992, 91-117. Furley PAProctor JRatter JA. eds, Chapman & Hall, London
18. Fyllas NM, Patiño S, Baker TR. Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences Discussions 2009, 6:3707-3769.
19. Gifford RM, Evans LT. Photosynthesis, carbon partitioning, and yield. Annual Review of Plant Physiology and Plant Molecular Biology 1981, 32:485-509.
20. Green DS, Kruger EL. Light-mediated constrains on leaf function correlate with leaf structure among deciduous and evergreen tree species. Tree Physiology 2001, 21:1341-1346.
21. Güsewell S. N: P ratios in terrestrial plants: variation and functional significance. New Phytologist 2004, 164:243-266.
22. Hanan NP, Kabat P, Dolman AJ, Elbers JA. Photosynthesis and carbon balance of a Sahelian fallow savanna. Global Change Biology 1998, 4:523-538.
23. Harley PC, Thomas RB, Reynolds JF, Strain BR. Modelling photosynthesis of cotton grown in elevated CO2. Plant, Cell & Environment 1992, 15:271-282.
24. Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR. Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency. Plant, Cell & Environment 2009, 32:259-270.
25. Hayward D, Oguntoyinbo J. The Climatology of West Africa 1987, Century Hutchinson, London, 271p
26. Hedin LO. Global organization of terrestrial plant-nutrient interactions. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:10849-10850.
27. Hikosaka K, Hirose T. Photosynthetic nitrogen-use efficiency in evergreen broad-leaved woody species coexisting in a warm-temperate forest. Tree Physiology 2000, 20:1249-1254.
28. Högberg P. Soil nutrient availability, root symbioses and tree species composition in tropical Africa: A review. Journal of Tropical Ecology 1986, 2:359-372.
29. World Reference Base for Soil Resources 2006: A Framework for International Classification, Correlation and Communication. 2006, IUSS (International Union of Soil Science) Working Group WRB, World Soil Resources Report 103, FAO, Rome
30. Kattge J, Knorr W, Raddatz T, Wirth C. Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Global Change Biology 2009, 15:976-991.
31. Keay RWJ. An example of Sudan zone vegetation in Nigeria. The Journal of Ecology 1949, 37:335-364.
32. Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T. Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiology 2006, 26:865-873.
33. Kull O. Acclimation of photosynthesis in canopies: models and limitations. Oecologia 2002, 133:267-279.
34. Lambers H, Raven JA, Shaver GR, Smith SE. Plant nutrient-acquisition strategies change with soil age. Trends in Ecology and Evolution 2008, 23:95-103.
35. Lloyd J, Farquhar GD. 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 1994, 99:201-215.
36. Lloyd J, Syvertsen JP, Kriedemann PE, Farquhar GD. Low conductances for CO2 diffusion from stomata to the sites of carboxylation in leaves of woody species. Plant, Cell & Environment 1992, 15:873-899.
37. Lloyd J, Bird MI, Veenendaal EM, Kruijt B. Should phosphorus availability be constraining moist tropical forest responses to increasing CO2 concentration. Global Biochemical Cycles in the Climate System 2001, 350. Schulze E-D, Heimann M, Harrison S, Holland ELloyd JPrentice ICSchimel D. eds, p., Academic Press, London, UK
38. Lloyd J, Bird MI, Vellen L, Miranda AC, Veenendaal EM, Djagbletey G, Miranda HS, Cook G, Farquhar GD. Contributions of woody and herbaceous vegetation to tropical savanna ecosystem productivity: a quasi-global estimate. Tree Physiology 2008, 28:451.
39. Lloyd J, Goulden M, Ometto JP, Fyllas NM, Quesada CA, Patiño S. Ecophysiology of forest and savanna vegetation. Amazonia and Climate Change 2009, 463-484. Keller M, Gash J, Silva Dias P, eds, American Geophysical Union, Washington, DC, USA
40. Long SP, Bernacchi CJ. Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. Journal of Experimental Botany 2003, 54:2393-2401.
41. Mardegan SF, Nardoto GB, Higuchi N, Moreira MZ, Martinelli LA. Nitrogen availability patterns in white-sand vegetations of Central Brazilian Amazon. Trees - Structure and Function 2008, 23:479-488.
42. Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K. Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry 1999, 46:45-65.
43. Meir P, Grace J, Miranda AC. Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature. Functional Ecology 2001, 15:378-387.
44. Meir P, Kruijt B, Broadmeadow M, Barbosa E, Kull O, Carswell FE, Nobre A, Jarvis PG. Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant, Cell & Environment 2002, 25:343-357.
45. Meir P, Levy P, Grace J, Jarvis P. Photosynthetic parameters from two contrasting woody vegetation types in West Africa. Plant Ecology 2007, 192:277-287.
46. Midgley GF, Aranibar JN, Mantlana KB, Macko S. Photosynthetic and gas exchange characteristics of dominant woody plants on a moisture gradient in an African savanna. Global Change Biology 2004, 10:309-317.
47. Mooney HA, Field C, Gulmon SL, Rundel P, Kruger FJ. Photosynthetic characteristic of South-African sclerophylls. Oecologia 1983, 58:398-401.
48. New M, Hulme M, Jones P. Representing twentieth-century space-time climate variability. Part I: Development of a 1961-90 mean monthly terrestrial climatology. Journal of Climate 1999, 12:829-856.
49. Niinemets Ü. Components of leaf dry mass per area - thickness and density - alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 1999, 144:35-47.
50. Niinemets Ü, Ellsworth DS, Lukjanova A, Tobias M. Site fertility and the morphological and photosynthetic acclimation of Pinus sylvestris needles to light. Tree Physiology 2001, 21:1231-1244.
51. Nocedal J, Wright SJ. Numerical Optimization 2006, 2nd, edn, Springer, New York
52. Okin GS, Mladenov N, Wang L, Cassel D, Caylor KK, Ringrose S, Macko SA. Spatial patterns of soil nutrients in two southern African savannas. Journal of Geophysical Research 2008, 113:G02011. DOI: 10.1029/2007JG000584
53. Ollinger S, Smith M-L. Net primary production and canopy nitrogen in a temperate forest landscape: An analysis using imaging spectroscopy, modeling and field data. Ecosystems 2005, 8:760-778.
54. Paoli GD, Curran LM. Soil nutrients limit fine litter production and tree growth in mature low-land forest of Southwestern Borneo. Ecosystems 2007, 10:503-518.
55. Parkhurst DF. Diffusion of CO2 and other gases inside leaves. New Phytologist 1994, 126:449-479.
56. Poorter H, Evans JR. Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area. Oecologia 1998, 116:26-37.
57. Prado CHB, de Moraes JAPV. Photosynthetic capacity and specific leaf mass in twenty woody species of Cerrado vegetation under field conditions. Photosynthetica 1997, 33:103-112.
58. Prior LD, Eamus D, Bowman DMJ. Leaf attributes in the seasonally dry tropics: a comparison of four habitats in northern Australia. Functional Ecology 2003, 17:504-515.
59. Quesada CA, Lloyd J, Anderson LO, Fyllas NM, Schwarz M, Czimczik CI. Soils of amazonia with particular reference to the RAINFOR sites. Biogeosciences Discussions 2009a, 6:3851-3921.
60. Quesada CA, Lloyd J, Schwarz M. Chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences Discussions 2009b, 6:3923-3992.
61. Quesada CA, Lloyd J, Schwarz M. Regional and large-scale patterns in Amazon forest structure and function are mediated by variations in soil physical and chemical properties. Biogeosciences Discussions 2009c, 6:3993-4057.
62. R: A language and environment for statistical computing. 2008, http://www.R-project.org, R Development Core Team, R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL:
63. Raaimakers D, Boot RGA, Dijkstra P, Pot S, Pons T. Photosynthetic rates in relation to leaf phosphorus content in pioneer versus climax tropical forest trees. Oecologia 1995, 102:120-125.
64. Raddatz TJ, Reick CH, Knorr W, Kattge J, Roeckner E, Schnur R, Schnitzler KG, Wetzel P, Jungclaus J. Will the tropical land biosphere dominate the climate-carbon cycle feedback during the twenty-first century? Climate Dynamics 2007, 29:565-574.
65. Reich PB, Oleksyn J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:11001-11006.
66. Reich PB, Ellsworth DS, Uhl C. Leaf carbon and nutrient assimilation in species of differeing successional status in an oligotrophic Amazonian forest. Functional Ecology 1995, 9:65-76.
67. Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD. Generality of leaf trait relationships: a test across six biomes. Ecology 1999, 80:1955-1969.
68. Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JMH, Naeem S, Trost J. Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 2006, 440:922-925.
69. Reich PB, Oleksyn J, Wright I. Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 2009, 160:207-212.
70. Reich PB, Schoettle AW. Role of phosphorus and nitrogen in photosynthetic and whole plant carbon gain and nutrient use efficiency in eastern white-pine. Oecologia 1988, 77:25-33.
71. Reich PB, Walters MB, Ellsworth DS. From tropics to tundra: global convergence in plant functioning. Proceedings of the National Academy of Sciences 1997, 94:13730-13734.
72. Reich PB, Wright IJ, Lusk CH. Predicting leaf physiology from simple plant and climate attributes: a global GLOPNET analysis. Ecological Applications 2007, 17:1982-1988.
73. Rijkers T, Pons TL, Bongers F. The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Functional Ecology 2000, 14:77-86.
74. Rozendaal DMA, Hurdato VH, Poorter L. Plasticity in leaf traits of 38 tropical tree species in response to light; relationship with light demand and adult stature. Functional Ecology 2006, 20:207-216.
75. Santiago LS, Mulkey SS. A test of gas exchange measurements on excised canopy branches of ten tropical tree species. Photosynthetica 2003, 41:343-347.
76. Schulze E-D, Kelliher FM, Korner C, Lloyd J, Leuning R. Relationships among maximum stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: A global ecology scaling exercise. Annual Review of Ecology and Systematics 1994, 25:629-660.
77. Sellers PJ, Dickinson RE, Randall DA. Modeling the exchanges of energy, water, and carbon between continents and the atmosphere. Science 1997, 275:502-509.
78. Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 2007, 58:221-227.
79. Sitch S, Smith B, Prentice IC. Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Global Change Biology 2003, 9:161-185.
80. Specht RL, Specht A. Canopy structure in Eucalyptus dominated communities in Australia along climatic gradients. Acta Oecologia, Oecologia Plantarum 1989, 10:191-213.
81. Sterner RW, Elser JJ. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere 2002, Princeton University Press, 584p
82. Takashima T, Hikosaka K, Hirose T. Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell & Environment 2004, 27:1047-1054.
83. Terashima I, Araya T, Miyazawa S-I, Sone K, Yano S. Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: an eco-developmental treatise. Annals of Botany 2005, 95:507-519.
84. Tjellström H, Andersson MX, Larsson KE, Sandelius AS. Membrane phospholipids as a phosphate reserve: the dynamic nature of phospholipid-to-digalactosyl diacylglycerol exchange in higher plants. Plant, Cell & Environment 2008, 31:1388-1398.
85. Tuohy JM, Prior JAB, Stewart GR. Photosynthesis in relation to leaf nitrogen and phosphorus-content in Zimbabwean trees. Oecologia 1991, 88:378-382.
86. Turnbull MH, Doley D, Yates DJ. The dynamics of photosynthetic acclimation to changes in light quantity and quality in three Australian rainforest tree species. Oecologia 1993, 94:218-228.
87. Turner IM. The Ecology of Trees in the Tropical Rain Forest 2001, Cambridge University Press, Cambridge, 298p
88. Vitousek PM, Sanford JrRL. Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics 1986, 17:137-167.
89. Walters RG. Towards an understanding of photosynthetic acclimation. Journal of Experimental Botany 2005, 56:435-447.
90. Walters RG, Horton P. Acclimation of Arabidopsis thaliana to the light environment: Changes in composition of the photosynthetic apparatus. Planta 1994, 195:248-256.
91. Warren CR. Stand aside stomata, another actor deserves centre stage: the forgotten role of the internal conductance to CO2 transfer. Journal of Experimental Botany 2008, 59:1475-1487.
92. Warton DI, Wright IJ, Falster DS, Westoby M. Bivariate line-fitting methods for allometry. Biological Reviews 2006, 81:259-291.
93. White F. The Vegetation of Africa: A Descriptive Memoir to Accompany the UNESCO/AETFAT/UNSO Vegetation Map of Africa 1983, UNESCO, Paris, 356p
94. Woodrow IE, Berry JA. Enzymatic regulation of photosynthetic CO2, fixation in C3 plants. Annual Review of Plant Physiology and Plant Molecular Biology 1988, 39:533-594.
95. Woodward FI, Smith TM, Emanuel WR. A global land primary productivity and phytogeography model. Global Biogeochemical Cycles 1995, 9:471-490.
96. Wright IJ, Westoby M. Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Physologist 2002, 155:403-416.
97. Wright IJ, Reich PB, Westoby M. Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Functional Ecology 2001, 15:423-434.
98. Wright IJ, Reich PB, Westoby M. The worldwide leaf economics spectrum. Nature 2004, 428:821.
99. Wright IJ, Reich PB, Cornelissen JHC. Assessing the generality of global leaf trait relationships. New Phytologist 2005a, 166:485-496.
100. Wright IJ, Reich PB, Cornelissen JHC. Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography Letters 2005b, 14:411-421.
101. Wright IJ, Leishman MR, Read C, Westoby M. Gradients of light availability and leaf traits with leaf age and canopy position in 28 Australian shrubs and trees. Functional Plant Biology 2006, 33:407-419.
102. Wullschleger SD. Biochemical limitations to carbon assimilation in C3 plants. A retrospective analysis of the A/Ci curves from 109 species. Journal of Experimental Botany 1993, 44:907-920.
103. Xu C, Gertner GZ, Scheller RM. Uncertainties in the response of a forest landscape to global climatic change. Global Change Biology 2009, 15:116-131.