Foliar trait contrasts between African forest and savanna trees: genetic versus environmental effects
Franziska Schrodt A O , Tomas F. Domingues B P , Ted R. Feldpausch A Q , Gustavo Saiz C , Carlos Alberto Quesada D , Michael Schwarz E , F. Yoko Ishida D F , Halidou Compaore G , Adamo Diallo H , Gloria Djagbletey I , Fidele Hien G , Bonaventure Sonké K , Herman Toedoumg K , Loius Zapfack K , Pierre Hiernaux J , Eric Mougin J , Michael. I. Bird L , John Grace B , Simon L. Lewis A M , Elmar M. Veenendaal N and Jon Lloyd F R SA School of Geography, University of Leeds, LS2 9JT, UK.
B School of Geosciences, University of Edinburgh, EH8 9XP, Scotland, UK.
C Karlsruhe Institute of Technology, Institute of Meteorology and Climate Research, 82467, Garmisch-Partenkirchen, Germany.
D Instituto Nacional de Pesquisas da Amazonia, Manaus, Cx Postal 2223 – CEP 69080-971, Brazil.
E Fieldwork Assistance, PSF 101022, 07710, Jena, Germany.
F School of Tropical and Marine Sciences and Centre for Terrestrial Environmental and Sustainability Sciences, James Cook University, Cairns, Qld 4870, Australia.
G Institut de l’Environnement et de Recherches Agricoles, 04 BP 8645, Ouagadougou, Burkina Faso.
H Centre National des Semences Forestières, BP 2682, Ouagadougou, Burkina Faso.
I Ecosystem and Climate Change Division, Forestry Research Institute of Ghana, PO Box UP 63 KNUST Kumasi, Ghana.
J Géosciences Environnement Toulouse, Observatoire Midi-Pyrénées, 14, avenue Edouard Belin - 31400 Toulouse, France.
K Plant Systematic and Ecology Laboratory, Department of Biology, Higher Teachers’ Training College, University of Yaounde, PO Box 047, Yaounde Cameroon.
L School of Earth and Environmental Sciences and Centre for Terrestrial Environmental and Sustainability Sciences, James Cook University, Cairns, Qld 4870, Australia.
M Department of Geography, University College London, WC1E 6BT, UK.
N Centre for Ecosystem Studies, University of Wageningen, PO Box 47, 6700AA, Wageningen, Netherlands.
O Present address: Max Planck Institute for Biogeochemsitry, Postfach 10 0164 , 07701 Jena, Germany and iDiv, German Centre for Integrative Biodiversity Research, Halle-Jena-Leipzig, Deutscher Platz 5e,04103 Leipzig, Germany.
P Present address: Universidade de São Paulo, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto, Av Bandeirantes, 3900 , CEP 14040-901 , Bairro Monte Alegre , Ribeirão Preto, SP, Brazil.
Q Present address: College of Life and Environmental Sciences, University of Exeter, EX4 4RJ, UK.
R Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, SL6 7PY, UK.
S Corresponding author. Email: jonathan.lloyd@imperial.ac.uk
Functional Plant Biology 42(1) 63-83 https://doi.org/10.1071/FP14040
Submitted: 31 January 2014 Accepted: 9 July 2014 Published: 6 November 2014
Journal Compilation © CSIRO Publishing 2015 Open Access CC BY-NC-ND
Abstract
Variations in leaf mass per unit area (Ma) and foliar concentrations of N, P, C, K, Mg and Ca were determined for 365 trees growing in 23 plots along a West African precipitation gradient ranging from 0.29 to 1.62 m a–1. Contrary to previous studies, no marked increase in Ma with declining precipitation was observed, but savanna tree foliar [N] tended to be higher at the drier sites (mass basis). Generally, Ma was slightly higher and [N] slightly lower for forest vs savanna trees with most of this difference attributable to differences in soil chemistry. No systematic variations in [P], [Mg] and [Ca] with precipitation or between trees of forest vs savanna stands were observed. We did, however, find a marked increase in foliar [K] of savanna trees as precipitation declined, with savanna trees also having a significantly lower [K] than those of nearby forest. These differences were not related to differences in soil nutrient status and were accompanied by systematic changes in [C] of opposite sign. We suggest an important but as yet unidentified role for K in the adaption of savanna species to periods of limited water availability; with foliar [K] being also an important factor differentiating tree species adapted to forest vs savanna soils within the ‘zone of transition’ of Western Africa.
Additional keywords: foliar cations, leaf mass per unit area, leaf physiology, nitrogen, phenology, phosphorus, potassium, plant functional traits, tropical, West Africa, zone of transition.
References
Anderson MJ (2001) A new method for non‐parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Anderson MJ (2006) Distance‐based tests for homogeneity of multivariate dispersions. Biometrics 62, 245–253.
| Distance‐based tests for homogeneity of multivariate dispersions.Crossref | GoogleScholarGoogle Scholar | 16542252PubMed |
Aranibar JN, Otter L, Macko SA, Feral CJ, Epstein HE, Dowty PR, Eckardt F, Shugart HH, Swap RJ (2004) Nitrogen cycling in the soil–plant system along a precipitation gradient in the Kalahari sands. Global Change Biology 10, 359–373.
| Nitrogen cycling in the soil–plant system along a precipitation gradient in the Kalahari sands.Crossref | GoogleScholarGoogle Scholar |
Arbonnier M (2004) ‘Trees, shrubs and lianas of West African dry zones.’ (Editions Quae: Paris)
Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecology Letters 15, 393–405.
| The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis.Crossref | GoogleScholarGoogle Scholar | 22435987PubMed |
Battie-Laclau P, Laclau J-P, Beri C, Mietton L, Muniz MRA, Arenque BC, De Cassia Piccolo M, Jordan-Meille L, Bouillet J-P, Nouvellon Y (2014) Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant, Cell & Environment 37, 70–81.
| Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyjurbE&md5=a1063670eefe0db2b8cc818ab32c96feCAS |
Brodribb TJ, Holbrook NM, Gutiérrez MV (2002) Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees. Plant, Cell & Environment 25, 1435–1444.
| Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees.Crossref | GoogleScholarGoogle Scholar |
Buckley R, Wasson R, Gubb A (1987) Phosphorus and potassium status of arid timefield soils in central Australia and Southern Africa, and biogeographic implications. Journal of Arid Environments 13, 211–216.
Buckley TN, Miller JD, Farquhar GD (2002) The mathematics of linked optimisation for water and nitrogen use in a canopy. Silva Fennica 36, 639–669.
Cernusak LA, Hutley LB, Beringer J, Holtum JA, Turner BL (2011) Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia. Agricultural and Forest Meteorology 151, 1462–1470.
| Photosynthetic physiology of eucalypts along a sub-continental rainfall gradient in northern Australia.Crossref | GoogleScholarGoogle Scholar |
Chabot BF, Hicks DJ (1982) The ecology of leaf life spans. Annual Review of Ecology and Systematics 13, 229–259.
| The ecology of leaf life spans.Crossref | GoogleScholarGoogle Scholar |
Chave J, Navarrete D, Almeida S, Álvarez E, Aragão LEOC, Bonal D, Châtelet P, Silva-Espejo JE, Goret JY, von Hildebrand P, Jiménez E, Patiño S, Peñuela MC, Phillips OL, Stevenson P, Malhi Y (2010) Regional and seasonal patterns of litterfall in tropical South America. Biogeosciences 7, 43–55.
| Regional and seasonal patterns of litterfall in tropical South America.Crossref | GoogleScholarGoogle Scholar |
Cochrane TT (1989) Chemical properties of native savanna and forest soils in central Brazil. Soil Science Society of America Journal 53, 139–141.
| Chemical properties of native savanna and forest soils in central Brazil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhslahsbw%3D&md5=224f2f89c49bd2a1de153489f8470743CAS |
Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecological Monographs 69, 569–588.
| Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients.Crossref | GoogleScholarGoogle Scholar |
De Bie S, Ketner P, Paasse M, Geerling C (1998) Woody plant phenology in the West Africa savanna. Journal of Biogeography 25, 883–900.
| Woody plant phenology in the West Africa savanna.Crossref | GoogleScholarGoogle Scholar |
Devineau J-L (1999) Seasonal rhythms and phenological plasticity of savanna woody species in a fallow farming system (south-west Burkina Faso). Journal of Tropical Ecology 15, 497–513.
| Seasonal rhythms and phenological plasticity of savanna woody species in a fallow farming system (south-west Burkina Faso).Crossref | GoogleScholarGoogle Scholar |
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=a4fec222ad092583d2d52fd4335039e5CAS |
Flury B (1988) ‘Common principal components and related multivariate models.’ (Wiley: New York)
Fonseca CR, Overton JMC, 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, Patiño 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 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 |
Fyllas NM, Quesada CA, Lloyd J (2012) Deriving plant functional types for Amazonian forests for use in vegetation dynamics models. Perspectives in Plant Ecology, Evolution and Systematics 14, 97–110.
| Deriving plant functional types for Amazonian forests for use in vegetation dynamics models.Crossref | GoogleScholarGoogle Scholar |
Galwey NW (2006) ‘Introduction to mixed modelling: beyond regression and analysis of variance.’ (Wiley: Chichester, UK)
Gee GS, Bauder JW (1986) Particle-size analysis. In ‘Methods in soil analysis. Part 1. Physical and mineralogical methods’. (Ed. A Kluite) pp. 383–409. (SSSA and ASA: Madison, WI, USA)
Gotsch S, Geiger E, Franco A, Goldstein G, Meinzer F, Hoffmann W (2010) Allocation to leaf area and sapwood area affects water relations of co-occurring savanna and forest trees. Oecologia 163, 291–301.
| Allocation to leaf area and sapwood area affects water relations of co-occurring savanna and forest trees.Crossref | GoogleScholarGoogle Scholar | 20058025PubMed |
Gower JC (1971) A general coefficient of similarity and some of its properties. Biometrics 27, 857–871.
| A general coefficient of similarity and some of its properties.Crossref | GoogleScholarGoogle Scholar |
Hall NM, Peyrillé P (2006) Dynamics of the West African monsoon. Journal de Physique. IV 139, 81–99.
| Dynamics of the West African monsoon.Crossref | GoogleScholarGoogle Scholar |
Hao G-Y, Hoffmann WA, Scholz FG, Bucci SJ, Meinzer FC, Franco AC, Cao K-F, Goldstein G (2008) Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155, 405–415.
| Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems.Crossref | GoogleScholarGoogle Scholar | 18049826PubMed |
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
| Very high resolution interpolated climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |
Hoffmann WA, Franco AC (2003) Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts. Journal of Ecology 91, 475–484.
| Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts.Crossref | GoogleScholarGoogle Scholar |
Hoffmann W, Franco A, Moreira M, Haridasan M (2005a) Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees. Functional Ecology 19, 932–940.
| Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees.Crossref | GoogleScholarGoogle Scholar |
Hoffmann WA, Franco AC, Moreira MZ, Haridasan M (2005b) Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees. Functional Ecology 19, 932–940.
| Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees.Crossref | GoogleScholarGoogle Scholar |
Hoffmann WA, Adasme R, Haridasan M, de Carvalho MT, Geiger EL, Pereira MAB, Gotsch SG, Franco AC (2009) Tree topkill, not mortality, governs the dynamics of savanna–forest boundaries under frequent fire in central Brazil. Ecology 90, 1326–1337.
| Tree topkill, not mortality, governs the dynamics of savanna–forest boundaries under frequent fire in central Brazil.Crossref | GoogleScholarGoogle Scholar | 19537552PubMed |
Hoffmann WA, Geiger EL, Gotsch SG, Rossatto DR, Silva LC, Lau OL, Haridasan M, Franco AC (2012) Ecological thresholds at the savanna‐forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes. Ecology Letters 15, 759–768.
| Ecological thresholds at the savanna‐forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes.Crossref | GoogleScholarGoogle Scholar | 22554474PubMed |
Ishida A, Nakano T, Yazaki K, Matsuki S, Koike N, Lauenstein DL, Shimizu M, Yamashita N (2008) Coordination between leaf and stem traits related to leaf carbon gain and hydraulics across 32 drought-tolerant angiosperms. Oecologia 156, 193–202.
| Coordination between leaf and stem traits related to leaf carbon gain and hydraulics across 32 drought-tolerant angiosperms.Crossref | GoogleScholarGoogle Scholar | 18297313PubMed |
Legendre P, Legendre L (2012) ‘Numerical ecology.’ (Elsevier: Amsterdam)
Lehmann CER, Archibald SA, Hoffmann WA, Bond WJ (2011) Deciphering the distribution of the savanna biome. New Phytologist 191, 197–209.
| Deciphering the distribution of the savanna biome.Crossref | GoogleScholarGoogle Scholar |
Leigh RA, Wyn Jones RG (1984) A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell. New Phytologist 97, 1–13.
| A hypothesis relating critical potassium concentrations for growth to the distribution and function of this ion in the plant cell.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXksFequrY%3D&md5=9addfbf16ccdc106f02ae44e3e0a0f89CAS |
Lloyd J, Goulden M, Ometto JP, Fyllas NM, Quesada CA, Patino S (2009) Ecophysiology of forest and savanna vegetation. In ‘Amazonia and climate change’. (Eds M Keller, J Gash, P Silva Dias.) pp. 463–484. (American Geophysical Union: Washington DC)
Lloyd J, Patiño S, Paiva RQ, Nardoto GB, Quesada CA, Santos AJB, Baker TR, Brand WA, Hilke I, Gielmann H, Raessler M, Luizão FJ, Martinelli LA, Mercado LM (2010) Optimisation of photosynthetic carbon gain and within-canopy gradients of associated foliar traits for Amazon forest trees. Biogeosciences 7, 1833–1859.
| Optimisation of photosynthetic carbon gain and within-canopy gradients of associated foliar traits for Amazon forest trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtl2ksrvM&md5=1e9e64d73f4356acd83bbb8ba532ef17CAS |
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 | 1:CAS:528:DC%2BC3sXpvFars7s%3D&md5=c33fa5f049c4def6cb639927b43df02aCAS | 23621613PubMed |
Midgley GF, Aranibar JN, Mantlana KB, Macko S (2004) Photosynthetic and gas exchange characteristics of dominant woody plants on a moisture gradient in an African savanna. Global Change Biology 10, 309–317.
| Photosynthetic and gas exchange characteristics of dominant woody plants on a moisture gradient in an African savanna.Crossref | GoogleScholarGoogle Scholar |
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara R, Simpson GL, Solymos P, Stevens M, Wagner H (2012) ‘vegan: community ecology package. R package.’ ver. 2.0–2. 2011. Available at http://CRAN.R-project.org/package=vegan
Osnas JL, 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 | 1:CAS:528:DC%2BC3sXntVGjsLg%3D&md5=bc26f0852a9b362d8778afe01a8cee33CAS | 23539179PubMed |
Patiño S, Fyllas NM, Baker TR, Paiva R, Quesada CA, Santos AJB, Schwarz M, ter Steege H, Phillips OL, Lloyd J (2012) Coordination of physiological and structural traits in Amazon forest trees. Biogeosciences 9, 775–801.
| Coordination of physiological and structural traits in Amazon forest trees.Crossref | GoogleScholarGoogle Scholar |
Pella E (1990) Elemental organic analysis. Part 2. State of the art. American Laboratory 22, 28–32.
Phillips PC, Arnold SJ (1999) Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy. Evolution 53, 1506–1515.
| Hierarchical comparison of genetic variance-covariance matrices. I. Using the Flury hierarchy.Crossref | GoogleScholarGoogle Scholar |
Pinheiro JC, Bates DM (2000) ‘Mixed effects models in S and S-PLUS.’ (Springer-Verlag: Berlin)
Pleysier JL, Juo ASR (1980) A single-extraction method using silver-thiourea for measuring exchangeable cations and effective CEC in soils with variable charges. Soil Science 129, 205–211.
Pinheiro J, Bates D, DebRoy S, Sarkar D (2011) ‘R Development Core Team. nlme: linear and nonlinear mixed effects models. R package ver. 3.1–98.’ (R Foundation for Statistical Computing: Vienna)
Poorter H, Villar R (1997) The fate of acquired carbon in plants: chemical composition and construction costs. In ‘Plant resource allocation’. (Eds FA Bazzaz, J Grace) pp. 39–72. (Academic Press: San Diego, CA, USA)
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 |
Poupon H (1979) Etude de la phénologie de la strate ligneuse aFété Olé (Sénégal septentrional) de 1971 a1977. Bulletin de l’Institut Fondamental d’Afrique Noire, Tome 41, 44–85.
Quesada CA, Lloyd J, Schwarz M, Patiño S, Baker TR, Czimczik C, Fyllas NM, Martinelli L, Nardoto GB, Schmerler J, Santos AJB, Hodnett MG, Herrera R, Luizão FJ, Arneth A, Lloyd G, Dezzeo N, Hilke I, Kuhlmann I, Raessler M, Brand WA, Geilmann H, Moraes Filho JO, Carvalho FP, Araujo Filho RN, Chaves JE, Cruz Junior 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 | 1:CAS:528:DC%2BC3cXhtV2rtLrL&md5=df1f7abba5e21cd6816dd45a3b06332eCAS |
Quesada CA, Lloyd J, Anderson LO, Fyllas NM, Schwarz M, Czimczik CI (2011) Soils of Amazonia with particular reference to the RAINFOR sites. Biogeosciences 8, 1415–1440.
| Soils of Amazonia with particular reference to the RAINFOR sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12rt7nI&md5=39f76ca0c32a95c332c801703ac569a6CAS |
R-Development-Core-Team (2012) ‘R: a language and environment for statistical computing.’ Available at http://www.R-project.org/
Ratnam J, Bond WJ, Fensham RJ, Hoffmann WA, Archibald S, Lehmann CE, Anderson MT, Higgins SI, Sankaran M (2011) When is a ‘forest’a savanna, and why does it matter? Global Ecology and Biogeography 20, 653–660.
| When is a ‘forest’a savanna, and why does it matter?Crossref | GoogleScholarGoogle Scholar |
Ratter J (1992) Transition between cerrado and forest vegetation in Brazil. In ‘Nature and dynamics of forest-savanna boundaries’. (Eds P Furley, J Proctor, JA Ratter) pp. 417–430. (Chapman and Hall: London)
Rossatto DR, Hoffmann WA, Franco AC (2009) Differences in growth patterns between co-occurring forest and savanna trees affect the forest–savanna boundary. Functional Ecology 23, 689–698.
| Differences in growth patterns between co-occurring forest and savanna trees affect the forest–savanna boundary.Crossref | GoogleScholarGoogle Scholar |
Saiz G, Bird MI, Domingues TF, Schrodt F, Schwarz M, Feldpausch TR, Veenendaal EM, Djagbletey G, Hien F, Compaore H, Diallo A, Lloyd J (2012) Variation in soil carbon stocks and their determinants across a precipitation gradient in West Africa. Global Change Biology 18, 1670–1683.
| Variation in soil carbon stocks and their determinants across a precipitation gradient in West Africa.Crossref | GoogleScholarGoogle Scholar |
Schulze E-D, Williams RJ, Farquhar GD, Schulze W, Langridge J, Miller JM, Walker BH (1998) Carbon and nitrogen isotope discrimination and nitrogen nutrition of trees along a rainfall gradient in northern Australia. Functional Plant Biology 25, 413–425.
Thompson J, Viana J, Proctor J, Ratter J (1992) Contrasting forest-savanna boundaries on Maraca Island, Roraima, Brazil. In ‘Nature and dynamics of forest-savanna boundaries’.’ (Eds P Furley, J Proctor, JA Ratter) pp. 367–391. (Chapman and Hall: London)
Torello-Raventos M, Feldpausch TR, Veenendaal E, Schrodt F, Saiz G, Domingues TF, Djagbletey G, Ford A, Kemp J, Marimon BS, Marimon BH, Lenza E, Ratter JA, Maracahipes L, Sasaki D, Sonke B, Zapfack L, Taedoumg H, Villarroel D, Schwarz M, Quesada CA, Ishida FY, Nardoto GB, Affum-Baffoe K, Arroyo L, Bowman DMJS, Compaore H, Davies K, Diallo A, Fyllas NM, Gilpin M, Hien F, Johnson M, Killeen TJ, Metcalfe D, Miranda HS, Steininger M, Thomson J, Sykora K, Mougin E, Hiernaux P, Bird MI, Grace J, Lewis SL, Phillips OL, Lloyd J (2013) On the delineation of tropical vegetation types with an emphasis on forest/savanna transitions. Plant Ecology & Diversity 6, 101–137.
| On the delineation of tropical vegetation types with an emphasis on forest/savanna transitions.Crossref | GoogleScholarGoogle Scholar |
Veenendaal E, Torello-Raventos M, Feldpausch T, Domingues TF, Gerard FF, Schrodt F, Saiz G, Quesada CA, Djagbletey G, Ford A, Kemp J, Marimon BS, Marimon Junior BH, Lenza E, Ratter JA, Maracahipes L, Sasaki D, Sonké B, Zapfack L, Villarroel D, Schwarz M, Ishida FY, Gilpin M, Nardoto GB, Affum-Baffoe K, Arroyo L, Bloomfield K, Gjeca G, Compaore H, Davies K, Diallo A, Fyllas NM, Gignoux J, Hien F, Johnson M, Mougin E, Hiernaux P, Killeen TJ, Metcalfe D, Miranda HS, Steininger M, Sykora K, Bird MI, Grace J, Lewis SL, Phillips OL, Lloyd J (2014) Structural, physiognomic and aboveground biomass variation in savanna-forest transition zones on three continents. How different are co-occurring savanna and forest formations? Biogeosciences Discussions 11, 4591–4636.
| Structural, physiognomic and aboveground biomass variation in savanna-forest transition zones on three continents. How different are co-occurring savanna and forest formations?Crossref | GoogleScholarGoogle Scholar |
Villar R, Ruiz Robleto J, de Jong Y, Poorter H (2006) Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families. Plant, Cell & Environment 29, 1629–1643.
| Differences in construction costs and chemical composition between deciduous and evergreen woody species are small as compared to differences among families.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlSmtbg%3D&md5=a314f9d9d2006b4bbf7f8c6ed25408b5CAS |
Walter H, Mueller-Dombois D (1971) ‘Ecology of tropical and subtropical vegetation.’ (Oliver & Boyd: Edinburgh, UK)
Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3– an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3, 257–259.
| smatr 3– an R package for estimation and inference about allometric lines.Crossref | GoogleScholarGoogle Scholar |
Wei H, Wu B, Yang W, Luo T (2011) Low rainfall-induced shift in leaf trait relationship within species along a semi-arid sandy land transect in northern China. Plant Biology 13, 85–92.
| Low rainfall-induced shift in leaf trait relationship within species along a semi-arid sandy land transect in northern China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOjsr4%3D&md5=d909e99dc6ebdd67e8525f1ba36f9323CAS | 21143729PubMed |
Williams LJ, Bunyavejchewin S, Baker PJ (2008) Deciduousness in a seasonal tropical forest in western Thailand: interannual and intraspecific variation in timing, duration and environmental cues. Oecologia 155, 571–582.
| Deciduousness in a seasonal tropical forest in western Thailand: interannual and intraspecific variation in timing, duration and environmental cues.Crossref | GoogleScholarGoogle Scholar | 18188604PubMed |
Wood SN (2006) ‘Generalized additive models: an introduction with R.’ (CRC Press: Boca Raton, FL, USA)
Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society. Series B, Statistical Methodology 73, 3–36.
| Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models.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, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) 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 |