Photosynthesis–nitrogen relationships in tropical forest tree species as affected by soil phosphorus availability: a controlled environment study
Keith J. Bloomfield A B E , Graham D. Farquhar B and Jon Lloyd C DA School of Geography, University of Leeds, Leeds LS2 9JT, UK.
B Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.
C Grand Challenges in Ecosystems and the Environment Initiative, Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot SL5 7PY, Berkshire, UK.
D Centre for Tropical Environmental and Sustainability Science and School of Marine and Tropical Biology, James Cook University, Cairns, Qld 4878, Australia.
E Corresponding author. Email: keith.bloomfield@anu.edu.au
Functional Plant Biology 41(8) 820-832 https://doi.org/10.1071/FP13278
Submitted: 20 September 2013 Accepted: 17 February 2014 Published: 4 April 2014
Abstract
Tropical soils are often characterised by low phosphorus availability and tropical forest trees typically exhibit lower area-based rates of photosynthesis (Aa) for a given area-based leaf nitrogen concentration ([N]a) compared with plants growing in higher-latitude, N-limited ecosystems. Nevertheless, to date, very few studies have assessed the effects of P deprivation per se on Aa ↔ [N]a relationships in tropical trees. Our study investigated the effect of reduced soil P availability on light-saturated Aa and related leaf traits of seven Australian tropical tree species. We addressed the following questions: (1) Do contrasting species exhibit inherent differences in nutrient partitioning and morphology? (2) Does P deprivation lead to a change in the nature of the Aa ↔ [N]a relationship? (3) Does P deprivation lead to an alteration in leaf nitrogen levels or N allocation within the leaf? Applying a mixed effects model, we found that for these Australian tropical tree species, removal of P from the nutrient solution decreased area-based photosynthetic capacity (Amax,a) by 18% and reduced the slope of the Amax,a ↔ [N]a relationship and differences among species accounted for around 30% of response variation. Despite greater N allocation to chlorophyll, photosynthetic N use efficiency was significantly reduced in low-P plants. Collectively, our results support the view that low soil P availability can alter photosynthesis–nitrogen relationships in tropical trees.
Additional keywords: carboxylation capacity, leaf nutrient partitioning, leaf trait relationships, phosphorus deprivation, ribulose biphosphate regeneration.
References
Andersson MX, Stridh MH, Larsson KE, Lijenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Letters 537, 128–132.| Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol.Crossref | GoogleScholarGoogle Scholar | 12606044PubMed |
Asner GP, Martin RE, Ford AJ, Metcalfe DJ, Liddell MJ (2009) Leaf chemical and spectral diversity in Australian tropical forests. Ecological Applications 19, 236–253.
| Leaf chemical and spectral diversity in Australian tropical forests.Crossref | GoogleScholarGoogle Scholar | 19323186PubMed |
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.
| Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves.Crossref | GoogleScholarGoogle Scholar |
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.
| Photosynthetic capacity in a central Amazonian rain forest.Crossref | GoogleScholarGoogle Scholar | 12651470PubMed |
Chazdon RL (1992) Photosynthetic plasticity of two rain forest shrubs across natural gap transects. Oecologia 92, 586–595.
| Photosynthetic plasticity of two rain forest shrubs across natural gap transects.Crossref | GoogleScholarGoogle Scholar |
Conroy JP, Smillie RM, Küppers M, Bevege DI, Barlow EW (1986) Chlorophyll a fluorescence and photosynthetic and growth responses of Pinus radiata to phosphorus deficiency, drought stress and high CO2. Plant Physiology 81, 423–429.
| Chlorophyll a fluorescence and photosynthetic and growth responses of Pinus radiata to phosphorus deficiency, drought stress and high CO2.Crossref | GoogleScholarGoogle Scholar | 16664832PubMed |
Domingues TF, Meir P, Feldpausch TR, Saiz G, Veenendaal EM, Schrodt F, Bird M, Djagbletey G, Hien F, Compaore H, Diallo A, Grace J, Lloyd J (2010) Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. Plant, Cell & Environment 33, 959–980.
| Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands.Crossref | GoogleScholarGoogle Scholar |
Ellsworth DS, Reich PB (1996) Photosynthesis and leaf nitrogen in five Amazonian tree species during early secondary succession. Ecology 77, 581–594.
| Photosynthesis and leaf nitrogen in five Amazonian tree species during early secondary succession.Crossref | GoogleScholarGoogle Scholar |
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
| Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
| A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 24306196PubMed |
Field C, Mooney HA (1986) The nitrogen–photosynthesis relationship in wild plants. In ‘On the ecomomy of plant form and function’. (Ed. E Givnish.) pp. 25–55. (Cambridge University Press: Cambridge, UK)
Fyllas NM, Patino S, Baker TR, Nardoto GB, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jimenez EM, Luizao FJ, Neill DA, Silva N, Prieto A, Rudas A, Silviera M, Vieira ICG, Lopez-Gonzalez G, Malhi Y, Phillips OL, Lloyd J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6, 2677–2708.
| Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate.Crossref | GoogleScholarGoogle Scholar |
Grace J, Malhi Y, Lloyd J, McIntyre J, Miranda AC, Meir P, Miranda HS (1996) The use of eddy covariance to infer the net carbon dioxide uptake of Brazilian rain forest. Global Change Biology 2, 209–217.
| The use of eddy covariance to infer the net carbon dioxide uptake of Brazilian rain forest.Crossref | GoogleScholarGoogle Scholar |
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.
| Nitrogen in cell walls of sclerophyllous leaves accounts for little of the variation in photosynthetic nitrogen-use efficiency.Crossref | GoogleScholarGoogle Scholar |
Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and chlorophyll b in N,N-dimethylformamide and 80% acetone. Plant Physiology 77, 483–485.
| Extinction coefficients of chlorophyll a and chlorophyll b in N,N-dimethylformamide and 80% acetone.Crossref | GoogleScholarGoogle Scholar | 16664080PubMed |
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.
| Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models.Crossref | GoogleScholarGoogle Scholar |
Kiirats O, Cruz JA, Edwards GE, Kramer DM (2009) Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase. Functional Plant Biology 36, 893–901.
| Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase.Crossref | GoogleScholarGoogle Scholar |
Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible WR, Stitt M, Teste F, Turner BL (2012) Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytologist 196, 1098–1108.
| Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency.Crossref | GoogleScholarGoogle Scholar | 22937909PubMed |
Lloyd J, Farquhar GD (1996) The CO2 dependence of photosynthesis, plant growth responses to elevated atmospheric CO2 concentrations and their interaction with soil nutrient status. 1. General principles and forest ecosystems. Functional Ecology 10, 4–32.
| The CO2 dependence of photosynthesis, plant growth responses to elevated atmospheric CO2 concentrations and their interaction with soil nutrient status. 1. General principles and forest ecosystems.Crossref | GoogleScholarGoogle Scholar |
Lloyd J, Farquhar GD (2008) Effects of rising temperatures and CO2 on the physiology of tropical forest trees. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 1811–1817.
| Effects of rising temperatures and CO2 on the physiology of tropical forest trees.Crossref | GoogleScholarGoogle Scholar | 18267901PubMed |
Lloyd J, Grace J, Miranda AC, Meir P, Wong SC, Miranda BS, Wright IR, Gash JHC, McIntyre J (1995) A simple calibrated model of Amazon rain forest productivity based on leaf biochemical properties. Plant, Cell & Environment 18, 1129–1145.
| A simple calibrated model of Amazon rain forest productivity based on leaf biochemical properties.Crossref | GoogleScholarGoogle Scholar |
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.
| 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?Crossref | GoogleScholarGoogle Scholar | 23621613PubMed |
Loustau D, Ben Brahim M, Gaudillère JP, Dreyer E (1999) Photosynthetic responses to phosphorus nutrition in two-year-old maritime pine seedlings. Tree Physiology 19, 707–715.
| Photosynthetic responses to phosphorus nutrition in two-year-old maritime pine seedlings.Crossref | GoogleScholarGoogle Scholar | 12651309PubMed |
Malhi Y, Grace J (2000) Tropical forests and atmospheric carbon dioxide. Trends in Ecology & Evolution 15, 332–337.
| Tropical forests and atmospheric carbon dioxide.Crossref | GoogleScholarGoogle Scholar |
Mate CJ, Hudson GS, von Caemmerer S, Evans JR, Andrews TJ (1993) Reduction of ribulose bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphosphate carboxylase carbamylation and impairs photosynthesis. Plant Physiology 102, 1119–1128.
| Reduction of ribulose bisphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphosphate carboxylase carbamylation and impairs photosynthesis.Crossref | GoogleScholarGoogle Scholar | 8278543PubMed |
Niinemets U (1997) Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species. Functional Ecology 11, 518–531.
| Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species.Crossref | GoogleScholarGoogle Scholar |
Onoda Y, Hikosaka K, Hirose T (2004) Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency. Functional Ecology 18, 419–425.
| Allocation of nitrogen to cell walls decreases photosynthetic nitrogen-use efficiency.Crossref | GoogleScholarGoogle Scholar |
Osnas JLD, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: mass, area and the leaf economics spectrum. Science 340, 741–744.
| Global leaf trait relationships: mass, area and the leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar |
Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
| Carbon metabolite feedback regulation of leaf photosynthesis and development.Crossref | GoogleScholarGoogle Scholar | 12508065PubMed |
Phillips OL, Lewis SL, Baker TR, Chao K-J, Higuchi N (2008) The changing Amazon forest. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 1819–1827.
| The changing Amazon forest.Crossref | GoogleScholarGoogle Scholar | 18267900PubMed |
Pieters AJ, Paul MJ, Lawlor DW (2001) Low sink demand limits photosynthesis under Pi deficiency. Journal of Experimental Botany 52, 1083–1091.
| Low sink demand limits photosynthesis under Pi deficiency.Crossref | GoogleScholarGoogle Scholar | 11432924PubMed |
Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Functional Ecology 13, 396–410.
| Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Evans JR (1998) Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area. Oecologia 116, 26–37.
| Photosynthetic nitrogen-use efficiency of species that differ inherently in specific leaf area.Crossref | GoogleScholarGoogle Scholar |
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
| Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.Crossref | GoogleScholarGoogle Scholar |
Quesada CA, Lloyd J, Schwarz M, Patino S, Baker TR, Czimczik C, Fyllas NM, Martinelli L, Nardoto GB, Schmerler J, Santos AJB, Hodnett MG, Herrera R, Luizao FJ, Arneth A, Lloyd G, Dezzeo N, Hilke I, Kuhlmann I, Raessler M, Brand WA, Geilmann H, Moraes JO, Carvalho FP, Araujo RN, Chaves JE, Cruz OF, Pimentel TP, Paiva R (2010) Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7, 1515–1541.
| Variations in chemical and physical properties of Amazon forest soils in relation to their genesis.Crossref | GoogleScholarGoogle Scholar |
Quesada CA, Phillips OL, Schwarz M, Czimczik CI, Baker TR, Patino S, Fyllas NM, Hodnett MG, Herrera R, Almeida S, Davila EA, Arneth A, Arroyo L, Chao KJ, Dezzeo N, Erwin T, di Fiore A, Higuchi N, Coronado EH, Jimenez EM, Killeen T, Lezama AT, Lloyd G, Lopez-Gonzalez G, Luizao FJ, Malhi Y, Monteagudo A, Neill DA, Vargas PN, Paiva R, Peacock J, Penuela MC, Cruz AP, Pitman N, Priante N, Prieto A, Ramirez H, Rudas A, Salomao R, Santos AJB, Schmerler J, Silva N, Silveira M, Vasquez R, Vieira I, Terborgh J, Lloyd J (2012) Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate. Biogeosciences 9, 2203–2246.
| Basin-wide variations in Amazon forest structure and function are mediated by both soils and climate.Crossref | GoogleScholarGoogle Scholar |
R Development Core Team (2011) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna)
Raaimakers D, Boot RGA, Dijkstra P, Pot S, Pons T (1995) Photosynthetic rates in relation to leaf phosphorus content in pioneer versus climax tropical rainforest trees. Oecologia 102, 120–125.
Rao IM, Terry N (1989) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas-exchange and Calvin-cycle enzymes. Plant Physiology 90, 814–819.
| Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. I. Changes in growth, gas-exchange and Calvin-cycle enzymes.Crossref | GoogleScholarGoogle Scholar | 16666882PubMed |
Reich PB, Oleksyn J (2004) 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 101, 11001–11006.
| Global patterns of plant leaf N and P in relation to temperature and latitude.Crossref | GoogleScholarGoogle Scholar | 15213326PubMed |
Reich PB, Schoettle AW (1988) Role of phosphorus and nitrogen in photosynthetic and whole plant carbon gain and nutrient use efficiency in eastern white pine. Oecologia 77, 25–33.
| Role of phosphorus and nitrogen in photosynthetic and whole plant carbon gain and nutrient use efficiency in eastern white pine.Crossref | GoogleScholarGoogle Scholar |
Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160, 207–212.
| Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species.Crossref | GoogleScholarGoogle Scholar | 19212782PubMed |
Rijkers T, Pons TL, Bongers F (2000) The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Functional Ecology 14, 77–86.
| The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance.Crossref | GoogleScholarGoogle Scholar |
Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiology 91, 679–684.
| Stromal phosphate concentration is low during feedback limited photosynthesis.Crossref | GoogleScholarGoogle Scholar | 16667087PubMed |
Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
| Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar |
Sivak MN, Walker DA (1986) Photosynthesis in vivo can be limited by phosphate supply. New Phytologist 102, 499–512.
| Photosynthesis in vivo can be limited by phosphate supply.Crossref | GoogleScholarGoogle Scholar |
Smeck NE (1973) Phosphorus – indicator of pedogenetic weathering processes. Soil Science 115, 199–206.
| Phosphorus – indicator of pedogenetic weathering processes.Crossref | GoogleScholarGoogle Scholar |
Swaine MD, Whitmore TC (1988) On the definition of ecological species groups in tropical rain forests. Vegetatio 75, 81–86.
| On the definition of ecological species groups in tropical rain forests.Crossref | GoogleScholarGoogle Scholar |
Tiessen H, Stewart JWB, Cole CV (1984) Pathways of phosphorus transformations in soils of differing pedogenesis. Soil Science Society of America Journal 48, 853–858.
| Pathways of phosphorus transformations in soils of differing pedogenesis.Crossref | GoogleScholarGoogle Scholar |
Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N : P ratios in tropical rain forests. Ecology 88, 107–118.
| Controls over foliar N : P ratios in tropical rain forests.Crossref | GoogleScholarGoogle Scholar | 17489459PubMed |
Turner IM (2001) ‘The ecology of trees in the tropical rain forest.’ (Cambridge University Press: Cambridge, UK)
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.
| Responses of West African forest tree seedlings to irradiance and soil fertility.Crossref | GoogleScholarGoogle Scholar |
Vitousek PM (1984) Litterfall, nutrient cycling and nutrient limitation in tropical forests. Ecology 65, 285–298.
| Litterfall, nutrient cycling and nutrient limitation in tropical forests.Crossref | GoogleScholarGoogle Scholar |
Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annual Review of Ecology and Systematics 17, 137–167.
| Nutrient cycling in moist tropical forest.Crossref | GoogleScholarGoogle Scholar |
Warren CR, Adams MA (2002) Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster. Tree Physiology 22, 11–19.
| Phosphorus affects growth and partitioning of nitrogen to Rubisco in Pinus pinaster.Crossref | GoogleScholarGoogle Scholar | 11772551PubMed |
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biological Reviews of the Cambridge Philosophical Society 81, 259–291.
| Bivariate line-fitting methods for allometry.Crossref | GoogleScholarGoogle Scholar | 16573844PubMed |
Webb LJ (1968) Environmental relationships of the structural types of Australian rain forest vegetation. Ecology 49, 296–311.
| Environmental relationships of the structural types of Australian rain forest vegetation.Crossref | GoogleScholarGoogle Scholar |
Westoby M, Reich PB, Wright IJ (2013) Understanding ecological variation across species: area-based vs mass-based expression of leaf traits. New Phytologist 199, 322–323.
| Understanding ecological variation across species: area-based vs mass-based expression of leaf traits.Crossref | GoogleScholarGoogle Scholar | 23692294PubMed |
White PJ, Hammond JP (2008) Phosphorus nutrition of terrestrial plants. In ‘The ecophysiology of plant–phosphorus interactions’. (Eds JP Hammond, PJ White.) pp. 51–81. (Springer: Dordrecht)
Wright IJ, Reich PB, Westoby M (2001) Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats. Functional Ecology 15, 423–434.
| Strategy shifts in leaf physiology, structure and nutrient content between species of high- and low-rainfall and high- and low-nutrient habitats.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 15103368PubMed |
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) ‘Mixed effects models and extensions in ecology with R.’ (Springer Science: New York)