Separating species and environmental determinants of leaf functional traits in temperate rainforest plants along a soil-development chronosequence
Matthew H. Turnbull A H , Kevin L. Griffin B , Nikolaos M. Fyllas C , Jon Lloyd D E , Patrick Meir F G and Owen K. Atkin FA Centre for Integrative Ecology, School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand.
B Department of Earth and Environmental Sciences, Lamont-Doherty Earth Observatory, Columbia University, Palisades, NY 10964-8000, USA.
C Department of Ecology and Systematics, Faculty of Biology, National and Kapodistrian University of Athens, Athens 15784, Greece.
D Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK.
E School of Marine and Tropical Biology, James Cook University, Cairns, Qld 4870, Australia.
F Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
G School of Geosciences, University of Edinburgh, Edinburgh EH8 9XP, UK.
H Corresponding author. Email: matthew.turnbull@canterbury.ac.nz
Functional Plant Biology 43(8) 751-765 https://doi.org/10.1071/FP16035
Submitted: 25 January 2016 Accepted: 11 April 2016 Published: 17 May 2016
Abstract
We measured a diverse range of foliar characteristics in shrub and tree species in temperate rainforest communities along a soil chronosequence (six sites from 8 to 120 000 years) and used multilevel model analysis to attribute the proportion of variance for each trait into genetic (G, here meaning species-level), environmental (E) and residual error components. We hypothesised that differences in leaf traits would be driven primarily by changes in soil nutrient availability during ecosystem progression and retrogression. Several leaf structural, chemical and gas-exchange traits were more strongly driven by G than E effects. For leaf mass per unit area (MA), foliar [N], net CO2 assimilation and dark respiration rates and foliar carbohydrate concentration, the G component accounted for 60–87% of the total variance, with the variability associated with plot, the E effect, much less important. Other traits, such as foliar [P] and N : P, displayed strong E and residual effects. Analyses revealed significant reductions in the slopes of G-only bivariate relationships when compared with raw relationships, indicating that a large proportion of trait–trait relationships is species based, and not a response to environment per se. This should be accounted for when assessing the mechanistic basis for using such relationships in order to make predictions of responses of plants to short-term environmental change.
Additional keywords: carbohydrates, dark respiration, genotypic, nitrogen, phenotypic, phosphorus, photosynthesis, soil nutrient availability, temperate rainforest.
References
Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. International Journal of Plant Sciences 164, S165–S184.| Community assembly, niche conservatism, and adaptive evolution in changing environments.Crossref | GoogleScholarGoogle Scholar |
Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1–67.
| The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns.Crossref | GoogleScholarGoogle Scholar |
Albert CH, Grassein F, Schurr FM, Vieilledent G, Violle C (2011) When and how should intraspecific variability be considered in trait-based plant ecology? Perspectives in Plant Ecology, Evolution and Systematics 13, 217–225.
| When and how should intraspecific variability be considered in trait-based plant ecology?Crossref | GoogleScholarGoogle Scholar |
Asner GP, Martin RE (2011) Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest. New Phytologist 189, 999–1012.
| Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest.Crossref | GoogleScholarGoogle Scholar | 21118261PubMed |
Asner GP, Martin RE, Tupayachi R, Anderson CB, Sinca F, Carranza-Jiménez L, Martinez P (2014) Amazonian functional diversity from forest canopy chemical assembly. Proceedings of the National Academy of Sciences of the United States of America 111, 5604–5609.
| Amazonian functional diversity from forest canopy chemical assembly.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtlyhs7w%3D&md5=caae9824c4a3229f96a015a41c71f2f0CAS | 24591585PubMed |
Atkin OK, Turnbull MH, Zaragoza-Castell J, Fyllas NM, Lloyd J, Meir P, Griffin KL (2013) Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: an analysis using the Kok method. Plant and Soil 367, 163–182.
| Light inhibition of leaf respiration as soil fertility declines along a post-glacial chronosequence in New Zealand: an analysis using the Kok method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsVKitrs%3D&md5=a6716c38892d2bb2d4ca506bc232aa7bCAS |
Atkin OK, Bloomfield KJ, Reich PB, Tjoelker MG, Asner GP, Bonal D, Bönisch G, Bradford MG, Cernusak LA, Cosio EG, Creek D, Crous KY, Domingues TF, Dukes JS, Egerton JJG, Evans JR, Farquhar GD, Fyllas NM, Gauthier PPG, Gloor E, Gimeno TE, Griffin KL, Guerrieri R, Heskel MA, Huntingford C, Ishida FY, Kattge J, Lambers H, Liddell MJ, Lloyd J, Lusk CH, Martin RE, Maksimov AP, Maximov TC, Malhi Y, Medlyn BE, Meir P, Mercado LM, Mirotchnick N, Ng D, Niinemets Ü, O’Sullivan OS, Phillips OL, Poorter L, Poot P, Prentice IC, Salinas N, Rowland LM, Ryan MG, Sitch S, Slot M, Smith NG, Turnbull MH, VanderWel MC, Valladares F, Veneklaas EJ, Weerasinghe LK, Wirth C, Wright IJ, Wythers KR, Xiang J, Xiang S, Zaragoza-Castells J (2015) Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytologist 206, 614–636.
| Global variability in leaf respiration in relation to climate, plant functional types and leaf traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvFCksb8%3D&md5=7190bb8158d4dc1caa512b97bc07caa8CAS | 25581061PubMed |
Auger S, Shipley B (2013) Inter-specific and intra-specific trait variation along short environmental gradients in an old-growth temperate forest. Journal of Vegetation Science 24, 419–428.
| Inter-specific and intra-specific trait variation along short environmental gradients in an old-growth temperate forest.Crossref | GoogleScholarGoogle Scholar |
Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytologist 190, 1003–1018.
| Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature.Crossref | GoogleScholarGoogle Scholar | 21434926PubMed |
Bates D, Sarkar D (2007) ‘lme4: linear mixed-effects models using S4 classes. R package version 0.9975-12. Available at http://CRAN.R-project.org/
Bolnick DI, Amarasekare P, Araujo M, Bürger R, Jiang Y, Levine J, Novak M, Rudolf V, Schreiber S, Urban M, Vasseur D (2011) Why intraspecific trait variation matters in ecology. Trends in Ecology & Evolution 26, 183–192.
| Why intraspecific trait variation matters in ecology.Crossref | GoogleScholarGoogle Scholar |
Crews TE, Kitayama K, Fownes JH, Riley RH, Herbert DA, Muellerdombois D, Vitousek PM (1995) Changes in soil-phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76, 1407–1424.
| Changes in soil-phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii.Crossref | GoogleScholarGoogle Scholar |
Dahlin KM, Asner GP, Field C (2013) Environmental and community controls on plant canopy chemistry in a Mediterranean-type ecosystem. Proceedings of the National Academy of Sciences of the United States of America 110, 6895–6900.
| Environmental and community controls on plant canopy chemistry in a Mediterranean-type ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXot1GhtrY%3D&md5=0c153176c539912c1e92b147000c38a8CAS | 23569241PubMed |
de Groot CC, Marcelis LFM, Van den Boogaard R, Kaiser WM, Lambers H (2003) Interaction of nitrogen and phosphorus nutrition in determining growth. Plant and Soil 248, 257–268.
| Interaction of nitrogen and phosphorus nutrition in determining growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtFCqsrw%3D&md5=617652a843d100bc3d8b6ae8883dd86fCAS |
DeWitt TJ, Scheiner SM (2004) ‘Phenotypic plasticity – functional and conceptual approaches.’ (Oxford University Press: Oxford)
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 | 1:CAS:528:DC%2BC3cXnvVagsbw%3D&md5=28084e4c0d334141e5be351f5c7d1705CAS |
Donovan LA, Mason CM, Bowsher AW, Goolsby EW, Ishibashi CDA (2014) Ecological and evolutionary lability of plant traits affecting carbon and nutrient cycling. Journal of Ecology 102, 302–314.
| Ecological and evolutionary lability of plant traits affecting carbon and nutrient cycling.Crossref | GoogleScholarGoogle Scholar |
Escudero A, del Arco JM, Sanz IC, Ayala J (1992) Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia 90, 80–87.
| Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species.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 |
Field C, Mooney HA (1986) The photosynthesis nitrogen relationship in wild plants. In ‘On the economy of plant form and function’. (Ed. TJ Givnish) pp. 25–55. (Cambridge University Press: Cambridge)
Fonseca CR, Overton JM, Collins B, Westoby M (2000) Shifts in trait-combinations along rainfall and phosphorus gradients. Journal of Ecology 88, 964–977.
| Shifts in trait-combinations along rainfall and phosphorus gradients.Crossref | GoogleScholarGoogle Scholar |
Fyllas NM, Patino S, Baker TR, Bielefeld Nardoto G, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jiménez EM, Luizão FJ, Neill A, 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 |
Galwey NW (2006) ‘Introduction to mixed modelling: beyond regression and analysis of variance.’ (Wiley: Chichester, UK)
Gelman A, Hill J (2006) ‘Data analysis using regression and multi-level/hierarchical models.’ (Cambridge University Press: Cambridge, UK)
Gleason SM, Read J, Ares A, Metcalfe DA (2009) Phosphorus economics of tropical rainforest species and stands across soil contrasts in Queensland, Australia: understanding the effects of soil specialization and trait plasticity. Functional Ecology 23, 1157–1166.
| Phosphorus economics of tropical rainforest species and stands across soil contrasts in Queensland, Australia: understanding the effects of soil specialization and trait plasticity.Crossref | GoogleScholarGoogle Scholar |
Gonzalez-Meler MA, Giles L, Thomas RB, Siedow JN (2001) Metabolic regulation of leaf respiration and alternative pathway activity in response to phosphate supply. Plant, Cell & Environment 24, 205–215.
| Metabolic regulation of leaf respiration and alternative pathway activity in response to phosphate supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsFGrt70%3D&md5=1e58406d362d47e8a4481511ab108e7bCAS |
Hawkins BJ, Xue JM, Bown HE, Clinton PW (2010) Relating nutritional and physiological characteristics to growth of Pinus radiata clones planted on a range of sites in New Zealand. Tree Physiology 30, 1174–1191.
| Relating nutritional and physiological characteristics to growth of Pinus radiata clones planted on a range of sites in New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKhtLfJ&md5=dce1131bda088f7a9ef84af5d8b6847eCAS | 20660492PubMed |
Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. Journal of Ecology 102, 396–410.
| Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjt1Shsro%3D&md5=26f94e9caa5fb848b6375a09400c9523CAS |
He J, Wang L, Flynn DFB, Wang X, Ma W, Fang J (2008) Leaf nitrogen : phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155, 301–310.
| Leaf nitrogen : phosphorus stoichiometry across Chinese grassland biomes.Crossref | GoogleScholarGoogle Scholar | 18278518PubMed |
Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. Journal of Ecology 97, 984–991.
| Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOktL%2FF&md5=47abacd04cf722d84b905b4ef7ddc2d1CAS |
Hikosaka K, Hirose T (2000) Photosynthetic nitrogen-use efficiency in evergreen broad-leaved woody species coexisting in a warm-temperate forest. Tree Physiology 20, 1249–1254.
| Photosynthetic nitrogen-use efficiency in evergreen broad-leaved woody species coexisting in a warm-temperate forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXovVGgs7g%3D&md5=7594ca71a1417e8803df28d7fcaef9d1CAS | 12651488PubMed |
Holdaway RJ, Richardson SJ, Dickie IA, Peltzer DA, Coomes DA (2011) Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest. Journal of Ecology 99, 954–963.
| Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest.Crossref | GoogleScholarGoogle Scholar |
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 |
Kattge J, Diaz S, Lavorel S, Prentice IC, Leadley P, Bonisch G, Garnier E, Westoby M, Reich PB, Wright IJ, et al (2011) TRY – a global database of plant traits. Global Change Biology 17, 2905–2935.
| TRY – a global database of plant traits.Crossref | GoogleScholarGoogle Scholar |
Lambers H, Chapin FS, III, Pons TL (1998) ‘Plant physiological ecology.’ (Springer-Verlag: New York)
Loveys BR, Atkinson LJ, Sherlock DJ, Roberts RL, Fitter AH, Atkin OK (2003) Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species. Global Change Biology 9, 895–910.
| Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species.Crossref | GoogleScholarGoogle Scholar |
Lusk CH, Kaneko T, Grierson E, Clearwater M (2013) Correlates of tree species sorting along a temperature gradient in New Zealand rain forests: seedling functional traits, growth and shade tolerance. Journal of Ecology 101, 1531–1541.
| Correlates of tree species sorting along a temperature gradient in New Zealand rain forests: seedling functional traits, growth and shade tolerance.Crossref | GoogleScholarGoogle Scholar |
McMahon SM, Diez JM (2007) Scales of association: hierarchical linear models and the measurement of ecological systems. Ecology Letters 10, 437–452.
| Scales of association: hierarchical linear models and the measurement of ecological systems.Crossref | GoogleScholarGoogle Scholar | 17498143PubMed |
Meir P, Grace J, Miranda AC (2001) Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature. Functional Ecology 15, 378–387.
| Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature.Crossref | GoogleScholarGoogle Scholar |
Messier J, McGill BJ, Lechowicz MJ (2010) How do traits vary across ecological scales? A case for trait-based ecology. Ecology Letters 13, 838–848.
| How do traits vary across ecological scales? A case for trait-based ecology.Crossref | GoogleScholarGoogle Scholar | 20482582PubMed |
Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends in Ecology & Evolution 20, 685–692.
| Ecological consequences of phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar |
Mitchell KA, Bolstad PV, Vose JM (1999) Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species. Tree Physiology 19, 861–870.
| Interspecific and environmentally induced variation in foliar dark respiration among eighteen southeastern deciduous tree species.Crossref | GoogleScholarGoogle Scholar | 10562403PubMed |
Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15, 684–692.
| Plant phenotypic plasticity in a changing climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVyht73K&md5=6ed4bd22d67b2f44155e3e9a6e2ac7c4CAS | 20970368PubMed |
Niklas KJ (2006) Plant allometry, leaf nitrogen and phosphorus stoichiometry, and interspecific trends in annual growth rates. Annals of Botany 97, 155–163.
| Plant allometry, leaf nitrogen and phosphorus stoichiometry, and interspecific trends in annual growth rates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVWht7Y%3D&md5=6da70b63a56e384f78ac91e34f20027fCAS | 16287903PubMed |
Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecology Letters 8, 636–642.
| Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth.Crossref | GoogleScholarGoogle Scholar |
Paul MJ, Stitt M (1993) Effects of nitrogen and phosphorus deficiencies an levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose. Plant, Cell & Environment 16, 1047–1057.
| Effects of nitrogen and phosphorus deficiencies an levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXisVSiu7c%3D&md5=5f733dac9d5b6f77ac1e62755075a341CAS |
Plaxton WC, Podesta FE (2006) The functional organization and control of plant respiration Critical Reviews in Plant Sciences 25, 159–198.
| The functional organization and control of plant respirationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVKqtrs%3D&md5=bf4a563db091f8b53704d6f589f18341CAS |
Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytologist 182, 565–588.
| Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis.Crossref | GoogleScholarGoogle Scholar | 19434804PubMed |
Poorter H, Lambers H, Evans JR (2013) Trait correlation networks: a whole-plant perspective on the recently criticized leaf economic spectrum. New Phytologist
| Trait correlation networks: a whole-plant perspective on the recently criticized leaf economic spectrum.Crossref | GoogleScholarGoogle Scholar | 24117716PubMed |
Reich PB, Walters MB, Ellsworth DS, Vose JM, Volin JC, Gresham C, Bowman WD (1998) Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups. Oecologia 114, 471–482.
| Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: a test across biomes and functional groups.Crossref | GoogleScholarGoogle Scholar |
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. Ecology Letters 11, 793–801.
| Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants.Crossref | GoogleScholarGoogle Scholar | 18445031PubMed |
Reich PB, Oleksyn J, Wright IJ, Niklas KJ, Hedin L, Elser JJ (2010) Evidence of a general 2/3-power law of scaling leaf nitrogen to phosphorus among major plant groups and biomes. Proceedings. Biological Sciences 277, 877–883.
| Evidence of a general 2/3-power law of scaling leaf nitrogen to phosphorus among major plant groups and biomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFyqtbs%3D&md5=eba6555829c08c775ee6d2d99733f007CAS |
Richardson SJ, Peltzer D, Allen RB, McGlone M, Parfitt RL (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139, 267–276.
| Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence.Crossref | GoogleScholarGoogle Scholar | 14758535PubMed |
Richardson SJ, Peltzer DA, Allen RB, McGlone MS (2005) Resorption proficiency along a chronosequence: response among communities and within species. Ecology 86, 20–25.
| Resorption proficiency along a chronosequence: response among communities and within species.Crossref | GoogleScholarGoogle Scholar |
Ryan MG (1995) Foliar maintenance respiration of subalpine and boreal trees and shrubs in relation to nitrogen content. Plant, Cell & Environment 18, 765–772.
| Foliar maintenance respiration of subalpine and boreal trees and shrubs in relation to nitrogen content.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnsFKmurg%3D&md5=bbd1f542b4b39513660a68314b17aa06CAS |
Stevens PR (1968) A chronosequence of soils near Franz Josef Glacier. PhD thesis, Department of Forestry, University of Canterbury.
Strand JA, Weisner SEB (2004) Phenotypic plasticity – contrasting species-specific traits induced by identical environmental constraints. New Phytologist 163, 449–451.
| Phenotypic plasticity – contrasting species-specific traits induced by identical environmental constraints.Crossref | GoogleScholarGoogle Scholar |
Theodorou ME, Elrifi IR, Turpin DH, Plaxton WC (1991) Effects of phosphorus limitation on respiratory metabolism in the green alga Selenastrum minutum. Plant Physiology 95, 1089–1095.
| Effects of phosphorus limitation on respiratory metabolism in the green alga Selenastrum minutum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXisVCjt7w%3D&md5=d2fb50c77c581bec412211200b80229bCAS | 16668095PubMed |
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 |
Turnbull MH, Whitehead D, Tissue DT, Schuster WSF, Brown KJ, Griffin KL (2003) Scaling foliar respiration in two contrasting forest canopies. Functional Ecology 17, 101–114.
| Scaling foliar respiration in two contrasting forest canopies.Crossref | GoogleScholarGoogle Scholar |
Turnbull MH, Tissue DT, Griffin KL, Richardson SJ, Peltzer DA, Whitehead D (2005) Respiration characteristics in temperate rainforest tree species differ along a long-term soil-development chronosequence. Oecologia 143, 271–279.
| Respiration characteristics in temperate rainforest tree species differ along a long-term soil-development chronosequence.Crossref | GoogleScholarGoogle Scholar | 15657760PubMed |
Valladares F, Gianoli E, Gomez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytologist 176, 749–763.
| Ecological limits to plant phenotypic plasticity.Crossref | GoogleScholarGoogle Scholar | 17997761PubMed |
Walker LR, del Moral R (2003) ‘Primary succession and ecosystem rehabilitation.’ (Cambridge University Press: Cambridge, UK)
Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15, 1–19.
| The fate of phosphorus during pedogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xht1Cltro%3D&md5=3049f6bd0ac3ea992e3224eda5f6c929CAS |
Wardle DA (2002) ‘Communities and ecosystems: linking the aboveground and belowground components.’ (Princeton University Press: Princeton, NJ, USA)
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 |
Watanabe T, Broadley MR, Jansen S, White PJ, Takada J, Satake K, Takamatsu T, Tuah SJ, Osaki M (2007) Evolutionary control of leaf element composition in plants. New Phytologist 174, 516–523.
| Evolutionary control of leaf element composition in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFOktLs%3D&md5=31b61045eee6e8282a78d07403a67dd8CAS | 17447908PubMed |
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 |
Whitehead D, Boelman N, Turnbull M, Griffin K, Tissue D, Barbour M, Hunt J, Richardson S, Peltzer D (2005) Photosynthesis and reflectance indices for rainforest species in ecosystems undergoing progression and retrogression along a soil fertility chronosequence in New Zealand. Oecologia 144, 233–244.
| Photosynthesis and reflectance indices for rainforest species in ecosystems undergoing progression and retrogression along a soil fertility chronosequence in New Zealand.Crossref | GoogleScholarGoogle Scholar | 15891839PubMed |
Wright JP, Sutton-Grier A (2012) Does the leaf economic spectrum hold within local species pools across varying environmental conditions? Functional Ecology 26, 1390–1398.
| Does the leaf economic spectrum hold within local species pools across varying environmental conditions?Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Functional Ecology 17, 10–19.
| Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species.Crossref | GoogleScholarGoogle Scholar |
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, 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.
| Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf life span.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 | 1:CAS:528:DC%2BD2cXjt1Crt74%3D&md5=d60b0f91594517529da250089e292021CAS | 15103368PubMed |
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005a) Assessing the generality of global leaf trait relationships. New Phytologist 166, 485–496.
| Assessing the generality of global leaf trait relationships.Crossref | GoogleScholarGoogle Scholar | 15819912PubMed |
Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets U, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005b) Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography 14, 411–421.
| Modulation of leaf economic traits and trait relationships by climate.Crossref | GoogleScholarGoogle Scholar |