Leaf-level photosynthetic capacity in lowland Amazonian and high-elevation Andean tropical moist forests of Peru

New Phytologist

Volumn 214, Issue 3, 2017, Pages 1002-1018

  Bahar, Nur H A ^a   Ishida, F Yoko ^b   Weerasinghe, Lasantha K ^a,c   Guerrieri, Rossella ^d,e   O'Sullivan, Odhran S ^a   Bloomfield, Keith J ^a   Asner, Gregory P ^f   Martin, Roberta E ^f   Lloyd, Jon ^b,g   Malhi, Yadvinder ^h   Phillips, Oliver L ⁱ   Meir, Patrick ^a,e   Salinas, Norma ^h,j   Cosio, Eric G ^j   Domingues, Tomas F ^k   Quesada, Carlos A ^l   Sinca, Felipe ^f   Escudero Vega, Alberto ^j   Zuloaga Ccorimanya, Paola P ^m   del Aguila Pasquel, Jhon ^n,o   Quispe Huaypar, Katherine ^m   Cuba Torres, Israel ^m   Butrón Loayza, Rosalbina ^p   Pelaez Tapia, Yulina ^m   Huaman Ovalle, Judit ^m   Long, Benedict M ^a,q   Evans, John R ^a,q   Atkin, Owen K ^a   more..

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

^c UNIVERSITY OF PERADENIYA   (Sri Lanka)

^d UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f GEOPHYSICAL LABORATORY   (United States)

^g IMPERIAL COLLEGE LONDON   (United Kingdom)

^h UNIVERSITY OF OXFORD   (United Kingdom)

ⁱ UNIVERSITY OF LEEDS   (United Kingdom)

^j PONTIFICIA UNIVERSIDAD CATÓLICA DEL PERÚ   (Peru)

^k UNIVERSITY OF SÃO PAULO   (Brazil)

^l INSTITUTO NACIONAL DE PESQUISAS DA AMAZÔNIA   (Brazil)

^m UNIVERSIDAD NACIONAL DE SAN ANTONIO ABAD DEL CUSCO   (Peru)

ⁿ INSTITUTO DE INVESTIGACIONES DE LA AMAZONÍA PERUANA   (Peru)

^o MICHIGAN TECHNOLOGICAL UNIVERSITY   (United States)

^p Museo de Historia Natural de la Universidad Nacional de San Antonio Abad del Cusco   (Peru)

^q AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

more..

Author keywords

carboxylation capacity; elevation; leaf traits; nitrogen (N); phosphorus (P); ribulose bisphosphate regeneration; temperature; tropical forests

Indexed keywords

ABUNDANCE; CARBON DIOXIDE; CARBOXYLIC ACID; ELEVATION; ENZYME ACTIVITY; FOREST ECOSYSTEM; LEAF AREA; MOISTURE CONTENT; NITROGEN; PHOSPHORUS; PHOTOSYNTHESIS; TEMPERATURE EFFECT; TROPICAL FOREST;

AMAZONAS [BRAZIL]; ANDES; BRAZIL; PERU;

CARBON DIOXIDE; NITROGEN; RIBULOSEBISPHOSPHATE CARBOXYLASE;

ALTITUDE; ANATOMY AND HISTOLOGY; BIOLOGICAL MODEL; CHEMISTRY; ENZYME ASSAY; FOREST; HUMIDITY; KINETICS; METABOLISM; PERU; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; SPECIES DIFFERENCE; TEMPERATURE; TROPIC CLIMATE;

ALTITUDE; CARBON DIOXIDE; ENZYME ASSAYS; FORESTS; HUMIDITY; KINETICS; MODELS, BIOLOGICAL; NITROGEN; PERU; PHOTOSYNTHESIS; PLANT LEAVES; RIBULOSE-BISPHOSPHATE CARBOXYLASE; SPECIES SPECIFICITY; TEMPERATURE; TROPICAL CLIMATE;

EID: 84978194561     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14079     Document Type: Article

References (91)

1. Aerts R, Chapin FSI. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30: 1–67.
2. Almeida JP, Montúfar R, Anthelme F. 2012. Patterns and origin of intraspecific functional variability in a tropical alpine species along an altitudinal gradient. Plant Ecology & Diversity 6: 423–433.
3. Asner GP, Anderson CB, Martin RE, Knapp DE, Tupayachi R, Sinca F, Malhi Y. 2014a. Landscape-scale changes in forest structure and functional traits along an Andes-to-Amazon elevation gradient. Biogeosciences 11: 843–856.
4. Asner GP, Martin RE. 2011. Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest. New Phytologist 189: 999–1012.
5. Asner GP, Martin RE, Tupayachi R, Anderson CB, Sinca F, Carranza-Jiménez L, Martinez P. 2014b. Amazonian functional diversity from forest canopy chemical assembly. Proceedings of the National Academy of Sciences, USA 111: 5604–5609.
6. 2 and growth temperature. New Phytologist 190: 1003–1018.
7. Beer C, Reichstein M, Tomelleri E, Ciais P, Jung M, Carvalhais N, Rödenbeck C, Arain MA, Baldocchi D, Bonan GB et al. 2010. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329: 834–838.
8. Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP. 2002. Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology 130: 1992–1998.
9. Bloomfield KJ, Domingues TF, Saiz G, Bird MI, Crayn DM, Ford A, Metcalfe D, Farquhar GD, Lloyd J. 2014a. Contrasting photosynthetic characteristics of forest vs. savanna species (far North Queensland, Australia). Biogeosciences 11: 7331–7347.
10. Bloomfield KJ, Farquhar GD, Lloyd J. 2014b. Photosynthesis–nitrogen relationships in tropical forest tree species as affected by soil phosphorus availability: a controlled environment study. Functional Plant Biology 41: 820–832.
11. Brooks A. 1986. Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves. Australian Journal of Plant Physiology 13: 221–237.
12. 2 concentration on leaf respiration vary with temperature? Responses in two species of Plantago that differ in relative growth rate. Physiologia Plantarum 114: 57–64.
13. Bruijnzeel LA, Scatena FN, Hamilton LS. 2011. Tropical montane cloud forests: science for conservation and management. New York, USA: Cambridge University Press.
14. Bruijnzeel LA, Veneklaas EJ. 1998. Climatic conditions and tropical montane forest productivity: the fog has not lifted yet. Ecology 79: 3–9.
15. von Caemmerer S, Evans JR, Hudson GS, Andrews TJ. 1994. The kinetics of ribulose-1, 5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195: 88–97.
16. 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 Physiology 20: 179–186.
17. 13C along an altitudinal gradient. Functional Ecology 13: 811–818.
18. Coste S, Roggy J-C, Imbert P, Born C, Bonal D, Dreyer E. 2005. Leaf photosynthetic traits of 14 tropical rain forest species in relation to leaf nitrogen concentration and shade tolerance. Tree Physiology 25: 1127–1137.
19. Domingues TF, Berry JA, Martinelli LA, Ometto JPHB, Ehleringer JR. 2005. Parameterization of canopy structure and leaf-level gas exchange for an eastern Amazonian tropical rain forest (Tapajós National Forest, Pará, Brazil). Earth Interactions 9: 1–23.
20. Domingues TF, Ishida FY, Feldpausch T, Grace J, Meir P, Saiz G, Sene O, Schrodt F, Sonké B, Taedoumg H et al. 2015. Biome-specific effects of nitrogen and phosphorus on the photosynthetic characteristics of trees at a forest-savanna boundary in Cameroon. Oecologia 178: 659–672.
21. Domingues TF, Martinelli LA, Ehleringer JR. 2007. Ecophysiological traits of plant functional groups in forest and pasture ecosystems from eastern Amazônia, Brazil. Plant Ecology 193: 101–112.
22. Domingues TF, Meir P, Feldpausch TR, Saiz G, Veenendaal EM, Schrodt F, Bird M, Djagbletey G, Hien F, Compaore H et al. 2010. Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. Plant, Cell & Environment 33: 959–980.
23. Dusenge M, Wallin G, Gårdesten J, Niyonzima F, Adolfsson L, Nsabimana D, Uddling J. 2015. Photosynthetic capacity of tropical montane tree species in relation to leaf nutrients, successional strategy and growth temperature. Oecologia 177: 1183–1194.
24. 3 plants. Oecologia 78: 9–19.
25. Evans JR, Seemann JR. 1989. The allocation of protein nitrogen in the photosynthetic apparatus: costs, consequences, and control. New York, USA: Alan R. Liss.
26. Falster DS, Warton DI, Wright IJ. 2006. SMATR: Standardised major axis tests and routines, version 2.0. [WWW document] URL https://github.com/dfalster/smatr/ [accessed 4 April 2015].
27. 3 species. Planta 149: 78–90.
28. 2: current knowledge and future prospects. Plant, Cell & Environment 31: 602–621.
29. Fredeen AL, Rao IM, Terry N. 1989. Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiology 89: 225–230.
30. Fyllas NM, Patiño S, Baker TR, Bielefeld Nardoto G, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM et al. 2009. Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6: 2677–2708.
31. Gaspar MM, Ferreira RB, Chaves MM, Teixeira AR. 1997. Improved method for the extraction of proteins from Eucalyptus leaves. Application in leaf response to temperature. Phytochemical Analysis 8: 279–285.
32. Gentry AH. 1988. Changes in plant community diversity and floristic composition on environmental and geographical gradients. Annals of the Missouri Botanical Garden 75: 1–34.
33. Girardin CAJ, Espejob JES, Doughty CE, Huasco WH, Metcalfe DB, Durand-Baca L, Marthews TR, Aragao LE, Farfán-Rios W, García-Cabrera K. 2014a. Productivity and carbon allocation in a tropical montane cloud forest in the Peruvian Andes. Plant Ecology & Diversity 7: 107–123.
34. Girardin CAJ, Farfan-Rios W, Garcia K, Feeley KJ, Jørgensen PM, Murakami AA, Cayola Pérez L, Seidel R, Paniagua N, Fuentes Claros AF et al. 2014b. Spatial patterns of above-ground structure, biomass and composition in a network of six Andean elevation transects. Plant Ecology & Diversity 7: 161–171.
35. Girardin CAJ, Malhi Y, Aragao LE, Mamani M, Huaraca Huasco W, Durand L, Feeley KJ, Rapp J, Silva-Espejo JE, Silman M et al. 2010. Net primary productivity allocation and cycling of carbon along a tropical forest elevational transect in the Peruvian Andes. Global Change Biology 16: 3176–3192.
36. Grubb PJ. 1977. Control of forest growth and distribution on wet tropical mountains: with special reference to mineral nutrition. Annual Review of Ecology and Systematics 8: 83–107.
37. Güsewell S. 2004. N: P ratios in terrestrial plants: variation and functional significance. New Phytologist 164: 243–266.
38. Harrison MT, Edwards EJ, Farquhar GD, Nicotra AB, Evans JR. 2009. Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency. Plant, Cell & Environment 32: 259–270.
39. Hikosaka K. 2004. Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. Journal of Plant Research 117: 481–494.
40. Hikosaka K, Ishikawa K, Borjigidai A, Muller O, Onoda Y. 2006. Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. Journal of Experimental Botany 57: 291–302.
41. Hikosaka K, Nagamatsu D, Ishii HS, Hirose T. 2002. Photosynthesis–nitrogen relationships in species at different altitudes on Mount Kinabalu, Malaysia. Ecological Research 17: 305–313.
42. Hikosaka K, Shigeno A. 2009. The role of Rubisco and cell walls in the interspecific variation in photosynthetic capacity. Oecologia 160: 443–451.
43. Jacob J, Lawlor DW. 1992. Dependence of photosynthesis of sunflower and maize leaves on phosphate supply, ribulose-1,5-bisphosphate carboxylase oxygenase activity, and ribulose-1,5-bisphosphate pool size. Plant Physiology 98: 801–807.
44. 2 specificity factor of Ribulose 1,5-Bisphosphate Carboxylase-Oxygenase in intact leaves of sunflower. Journal of Experimental Botany 44: 1635–1641.
45. Kattge J, Knorr W, Raddatz T, Wirth C. 2009. Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Global Change Biology 15: 976–991.
46. Kraft NJB, Valencia R, Ackerly DD. 2008. Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322: 580–582.
47. 2 exchange over a Bornean tropical rain forest using measured vertical and horizontal variations in leaf-level physiological parameters and leaf area densities. Journal of Geophysical Research: Atmospheres 111: D10107.
48. Lauer MJ, Pallardy SG, Blevins DG, Randall DD. 1989. Whole leaf carbon exchange characteristics of phosphate deficient soybeans (Glycine max L.). Plant Physiology 91: 848–854.
49. Letts MG, Mulligan M. 2005. The impact of light quality and leaf wetness on photosynthesis in north-west Andean tropical montane cloud forest. Journal of Tropical Ecology 21: 549–557.
50. Lloyd J, Bloomfield K, Domingues TF, Farquhar GD. 2013. Photosynthetically relevant foliar traits correlating better on a mass vs an area basis: of ecophysiological relevance or just a case of mathematical imperatives and statistical quicksand? New Phytologist 199: 311–321.
51. Loustau D, Brahim MB, Gaudillère J-P, Dreyer E. 1999. Photosynthetic responses to phosphorus nutrition in two-year-old maritime pine seedlings. Tree Physiology 19: 707–715.
52. Malhi Y. 2010. The carbon balance of tropical forest regions, 1990–2005. Current Opinion in Environmental Sustainability 2: 237–244.
53. Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A et al. 2002. Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25: 1167–1179.
54. Meir P, Kruijt B, Broadmeadow M, Barbosa E, Kull O, Carswell F, Nobre A, Jarvis PG. 2002. Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area. Plant, Cell & Environment 25: 343–357.
55. Meir P, Levy P, Grace J, Jarvis P. 2007. Photosynthetic parameters from two contrasting woody vegetation types in West Africa. Plant Ecology 192: 277–287.
56. Mercado LM, Patiño S, Domingues TF, Fyllas NM, Weedon GP, Sitch S, Quesada CA, Phillips OL, Aragao LE, Malhi Y et al. 2011. Variations in Amazon forest productivity correlated with foliar nutrients and modelled rates of photosynthetic carbon supply. Philosophical Transactions of the Royal Society B: Biological Sciences 366: 3316–3329.
57. Niinemets Ü, Tenhunen JD. 1997. A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell & Environment 20: 845–866.
58. Pinheiro J, Bates D. 2000. Mixed-effects models in S and S-PLUS. New York, USA: Springer.
59. Pons TL, van der Werf A, Lambers H. 1994. Photosynthetic nitrogen use efficiency of inherently low- and fast-growing species: possible explanations for observed differences. The Hague, the Netherlands: SPB Academic Publishing.
60. Poorter H, Evans JR. 1998. Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area. Oecologia 116: 26–37.
61. Quesada CA, Lloyd J, Schwarz M, Patiño S, Baker TR, Czimczik C, Fyllas NM, Martinelli L, Nardoto GB, Schmerler J et al. 2010. Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7: 1515–1541.
62. Quesada CA, Phillips OL, Schwarz M, Czimczik CI, Baker TR, Patiño S, Fyllas NM, Hodnett MG, Herrera R, Almeida S et al. 2012. Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9: 2203–2246.
63. Quilici A, Medina E. 1998. Photosynthesis-nitrogen relationships in pioneer plants of disturbed tropical montane forest sites. Photosynthetica 35: 525–534.
64. R Development Core Team 2011. R: a language and environment for statistical computing. [WWW document] URL http://www.R-project.org/. Vienna, Austria: The R Foundation for Statistical Computing.
65. Raaimakers D, Boot RGA, Dijkstra P, Pot S. 1995. Photosynthetic rates in relation to leaf phosphorus content in pioneer versus climax tropical rainforest trees. Oecologia 102: 120–125.
66. Rada F, García-Núñez C, Ataroff M. 2009. Leaf gas exchange in canopy species of a Venezuelan cloud forest. Biotropica 41: 659–664.
67. Reich P, Oleksyn J, Wright I. 2009. Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160: 207–212.
68. Reich PB, Walters MB. 1994. Photosynthesis-nitrogen relations in Amazonian tree species. Oecologia 97: 73–81.
69. 4 photosynthesis. Plant, Cell & Environment 30: 1086–1106.
70. Santiago LS, Mulkey SS. 2003. A test of gas exchange measurements on excised canopy branches of ten tropical tree species. Photosynthetica 41: 343–347.
71. Silman MR. 2014. Functional megadiversity. Proceedings of the National Academy of Sciences, USA 111: 5763–5764.
72. Stitt M, Schulze D. 1994. Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant, Cell & Environment 17: 465–487.
73. Takashima T, Hikosaka K, Hirose T. 2004. Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell & Environment 27: 1047–1054.
74. Tanner E, Vitousek PM, Cuevas E. 1998. Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79: 10–22.
75. 2 pressure? Ecology 76: 2663–2668.
76. Townsend AR, Cleveland CC, Asner GP, Bustamante MMC. 2007. Controls over foliar N: P ratios in tropical rain forests. Ecology 88: 107–118.
77. Vårhammar A, Wallin G, McLean CM, Dusenge ME, Medlyn BE, Hasper TB, Nsabimana D, Uddling J. 2015. Photosynthetic temperature responses of tree species in Rwanda: evidence of pronounced negative effects of high temperature in montane rainforest climax species. New Phytologist 206: 1000–1012.
78. Vitousek PM. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65: 285–298.
79. max - to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecology and Evolution 4: 3218–3235.
80. Warren CR, Adams MA. 2001. Distribution of N, Rubisco and photosynthesis in Pinus pinaster and acclimation to light. Plant, Cell & Environment 24: 597–609.
81. Warren CR, Adams MA. 2002. Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster. Tree Physiology 22: 11–19.
82. Warren CR, Adams MA, Chen Z. 2000. Is photosynthesis related to concentrations of nitrogen and Rubisco in leaves of Australian native plants? Functional Plant Biology 27: 407–416.
83. Warton DI, Wright IJ, Falster DS, Westoby M. 2006. Bivariate line-fitting methods for allometry. Biological Reviews 81: 259–291.
84. van de Weg M, Meir P, Grace J, Atkin OK. 2009. Altitudinal variation in leaf mass per unit area, leaf tissue density and foliar nitrogen and phosphorus content along an Amazon-Andes gradient in Peru. Plant Ecology & Diversity 2: 243–254.
85. van de Weg M, Meir P, Grace J, Ramos G. 2012. Photosynthetic parameters, dark respiration and leaf traits in the canopy of a Peruvian tropical montane cloud forest. Oecologia 168: 23–34.
86. van de Weg M, Meir P, Williams M, Girardin C, Malhi Y, Silva-Espejo J, Grace J. 2014. Gross primary productivity of a high elevation tropical montane cloud forest. Ecosystems 17: 751–764.
87. Westbeek MHM, Pons TL, Cambridge ML, Atkin OK. 1999. Analysis of differences in photosynthetic nitrogen use efficiency of alpine and lowland Poa species. Oecologia 120: 19–26.
88. Wittich B, Horna V, Homeier J, Leuschner C. 2012. Altitudinal change in the photosynthetic capacity of tropical trees: a case study from Ecuador and a pantropical literature analysis. Ecosystems 15: 958–973.
89. 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.
90. i curves from 109 species. Journal of Experimental Botany 44: 907–920.
91. Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM. 2009. Mixed effects models and extensions in ecology with R. Berlin and Heidelberg, Germany: Springer.