A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine‐root tissues in seed plants
Abstract
Summary Fine‐root traits play key roles in ecosystem processes, but the drivers of fine‐root trait diversity remain poorly understood. The plant economic spectrum ( PES ) hypothesis predicts that leaf and root traits evolved in coordination. Mycorrhizal association type, plant growth form and climate may also affect root traits. However, the extent to which these controls are confounded with phylogenetic structuring remains unclear. Here we compiled information about root and leaf traits for > 600 species. Using phylogenetic relatedness, climatic ranges, growth form and mycorrhizal associations, we quantified the importance of these factors in the global distribution of fine‐root traits. Phylogenetic structuring accounts for most of the variation for all traits excepting root tissue density, with root diameter and nitrogen concentration showing the strongest phylogenetic signal and specific root length showing intermediate values. Climate was the second most important factor, whereas mycorrhizal type had little effect. Substantial trait coordination occurred between leaves and roots, but the strength varied between growth forms and clades. Our analyses provide evidence that the integration of roots and leaves in the PES requires better accounting of the variation in traits across phylogenetic clades. Inclusion of phylogenetic information provides a powerful framework for predictions of belowground functionalmore »
- Authors:
-
- International Center of Tropical Botany Florida International University Miami FL 33199 USA, Department of Biological Sciences Kent State University Kent OH 44242 USA
- Centre d'Ecologie Fonctionnelle et Evolutive UMR 5175 (CNRS – Université de Montpellier – Université Paul‐Valéry Montpellier – EPHE) Montpellier 34293 France
- Department of Biological Sciences Kent State University Kent OH 44242 USA
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1373826
- Grant/Contract Number:
- DE‐SC0004335; SC0004335
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Name: New Phytologist Journal Volume: 215 Journal Issue: 4; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Valverde‐Barrantes, Oscar J., Freschet, Grégoire T., Roumet, Catherine, and Blackwood, Christopher B. A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine‐root tissues in seed plants. United Kingdom: N. p., 2017.
Web. doi:10.1111/nph.14571.
Valverde‐Barrantes, Oscar J., Freschet, Grégoire T., Roumet, Catherine, & Blackwood, Christopher B. A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine‐root tissues in seed plants. United Kingdom. https://doi.org/10.1111/nph.14571
Valverde‐Barrantes, Oscar J., Freschet, Grégoire T., Roumet, Catherine, and Blackwood, Christopher B. Tue .
"A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine‐root tissues in seed plants". United Kingdom. https://doi.org/10.1111/nph.14571.
@article{osti_1373826,
title = {A worldview of root traits: the influence of ancestry, growth form, climate and mycorrhizal association on the functional trait variation of fine‐root tissues in seed plants},
author = {Valverde‐Barrantes, Oscar J. and Freschet, Grégoire T. and Roumet, Catherine and Blackwood, Christopher B.},
abstractNote = {Summary Fine‐root traits play key roles in ecosystem processes, but the drivers of fine‐root trait diversity remain poorly understood. The plant economic spectrum ( PES ) hypothesis predicts that leaf and root traits evolved in coordination. Mycorrhizal association type, plant growth form and climate may also affect root traits. However, the extent to which these controls are confounded with phylogenetic structuring remains unclear. Here we compiled information about root and leaf traits for > 600 species. Using phylogenetic relatedness, climatic ranges, growth form and mycorrhizal associations, we quantified the importance of these factors in the global distribution of fine‐root traits. Phylogenetic structuring accounts for most of the variation for all traits excepting root tissue density, with root diameter and nitrogen concentration showing the strongest phylogenetic signal and specific root length showing intermediate values. Climate was the second most important factor, whereas mycorrhizal type had little effect. Substantial trait coordination occurred between leaves and roots, but the strength varied between growth forms and clades. Our analyses provide evidence that the integration of roots and leaves in the PES requires better accounting of the variation in traits across phylogenetic clades. Inclusion of phylogenetic information provides a powerful framework for predictions of belowground functional traits at global scales.},
doi = {10.1111/nph.14571},
journal = {New Phytologist},
number = 4,
volume = 215,
place = {United Kingdom},
year = {Tue Apr 25 00:00:00 EDT 2017},
month = {Tue Apr 25 00:00:00 EDT 2017}
}
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Works referenced in this record:
Variation of first-order root traits across climatic gradients and evolutionary trends in geological time: Root trait variation and evolution
journal, February 2013
- Chen, Weile; Zeng, Hui; Eissenstat, David M.
- Global Ecology and Biogeography, Vol. 22, Issue 7
Co-variations in litter decomposition, leaf traits and plant growth in species from a Mediterranean old-field succession
journal, February 2006
- Kazakou, E.; Vile, D.; Shipley, B.
- Functional Ecology, Vol. 20, Issue 1
Using functional traits and phylogenetic trees to examine the assembly of tropical tree communities
journal, March 2012
- Baraloto, Christopher; Hardy, Olivier J.; Paine, C. E. Timothy
- Journal of Ecology, Vol. 100, Issue 3
Forward Selection of Explanatory Variables
journal, September 2008
- Blanchet, F. Guillaume; Legendre, Pierre; Borcard, Daniel
- Ecology, Vol. 89, Issue 9
Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms
journal, February 2016
- Valverde-Barrantes, Oscar J.; Horning, Amber L.; Smemo, Kurt A.
- Plant and Soil, Vol. 404, Issue 1-2
Decomposition of the finest root branching orders: linking belowground dynamics to fine-root function and structure
journal, February 2011
- Goebel, Marc; Hobbie, Sarah E.; Bulaj, Bartosz
- Ecological Monographs, Vol. 81, Issue 1
Three keys to the radiation of angiosperms into freezing environments
journal, December 2013
- Zanne, Amy E.; Tank, David C.; Cornwell, William K.
- Nature, Vol. 506, Issue 7486
Phylogenetic Constraints Do Not Explain the Rarity of Nitrogen-Fixing Trees in Late-Successional Temperate Forests
journal, August 2010
- Menge, Duncan N. L.; DeNoyer, Jeanne L.; Lichstein, Jeremy W.
- PLoS ONE, Vol. 5, Issue 8
Plant traits and decomposition: are the relationships for roots comparable to those for leaves?
journal, December 2011
- Birouste, Marine; Kazakou, Elena; Blanchard, Alain
- Annals of Botany, Vol. 109, Issue 2
Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes
journal, March 2015
- McCormack, M. Luke; Dickie, Ian A.; Eissenstat, David M.
- New Phytologist, Vol. 207, Issue 3
Evolutionary Patterns and Biogeochemical Significance of Angiosperm Root Traits
journal, July 2012
- Comas, L. H.; Mueller, K. E.; Taylor, L. L.
- International Journal of Plant Sciences, Vol. 173, Issue 6
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package
journal, December 2011
- Revell, Liam J.
- Methods in Ecology and Evolution, Vol. 3, Issue 2
Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants
journal, August 2008
- Reich, Peter B.; Tjoelker, Mark G.; Pregitzer, Kurt S.
- Ecology Letters, Vol. 11, Issue 8
Variation of the Linkage of Root Function with Root Branch Order
journal, February 2013
- Long, Yingqian; Kong, Deliang; Chen, Zhengxia
- PLoS ONE, Vol. 8, Issue 2
Evidence of the ‘plant economics spectrum’ in a subarctic flora
journal, March 2010
- Freschet, Grégoire T.; Cornelissen, Johannes H. C.; van Logtestijn, Richard S. P.
- Journal of Ecology, Vol. 98, Issue 2
Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum
journal, March 2016
- Kramer-Walter, Kris R.; Bellingham, Peter J.; Millar, Timothy R.
- Journal of Ecology, Vol. 104, Issue 5
Specific root length as an indicator of environmental change
journal, November 2007
- Ostonen, I.; Püttsepp, Ü.; Biel, C.
- Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, Vol. 141, Issue 3
The worldwide leaf economics spectrum
journal, April 2004
- Wright, Ian J.; Reich, Peter B.; Westoby, Mark
- Nature, Vol. 428, Issue 6985
Relating root structure and anatomy to whole-plant functioning in 14 herbaceous Mediterranean species
journal, November 2006
- Hummel, Irène; Vile, Denis; Violle, Cyrille
- New Phytologist, Vol. 173, Issue 2
Phylogenies and the Comparative Method
journal, January 1985
- Felsenstein, Joseph
- The American Naturalist, Vol. 125, Issue 1
Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy
journal, January 2016
- Roumet, Catherine; Birouste, Marine; Picon-Cochard, Catherine
- New Phytologist, Vol. 210, Issue 3
Coevolution of roots and mycorrhizas of land plants
journal, May 2002
- Brundrett, Mark C.
- New Phytologist, Vol. 154, Issue 2
Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies
journal, July 2014
- Comas, Louise H.; Callahan, Hilary S.; Midford, Peter E.
- Ecology and Evolution, Vol. 4, Issue 15
Independent Evolution of Leaf and Root Traits within and among Temperate Grassland Plant Communities
journal, June 2011
- Kembel, Steven W.; Cahill, James F.
- PLoS ONE, Vol. 6, Issue 6
Predicting fine root lifespan from plant functional traits in temperate trees
journal, June 2012
- Luke McCormack, M.; Adams, Thomas S.; Smithwick, Erica A. H.
- New Phytologist, Vol. 195, Issue 4
Fine root decomposition rates do not mirror those of leaf litter among temperate tree species
journal, October 2009
- Hobbie, Sarah E.; Oleksyn, Jacek; Eissenstat, David M.
- Oecologia, Vol. 162, Issue 2
Inferring the historical patterns of biological evolution
journal, October 1999
- Pagel, Mark
- Nature, Vol. 401, Issue 6756
Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology
journal, June 2013
- Hempel, Stefan; Götzenberger, Lars; Kühn, Ingolf
- Ecology, Vol. 94, Issue 6
Functional distinctiveness of major plant lineages
journal, February 2014
- Cornwell, William K.; Westoby, Mark; Falster, Daniel S.
- Journal of Ecology, Vol. 102, Issue 2
Below‐ground frontiers in trait‐based plant ecology
journal, October 2016
- Laliberté, Etienne
- New Phytologist, Vol. 213, Issue 4
A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution
journal, January 2012
- de Boer, Hugo Jan; Eppinga, Maarten B.; Wassen, Martin J.
- Nature Communications, Vol. 3, Issue 1
Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum: Commentary on Kramer-Walter et al . (2016)
journal, August 2016
- Valverde-Barrantes, Oscar J.; Blackwood, Christopher B.
- Journal of Ecology, Vol. 104, Issue 5
Towards a multidimensional root trait framework: a tree root review
journal, May 2016
- Weemstra, Monique; Mommer, Liesje; Visser, Eric J. W.
- New Phytologist, Vol. 211, Issue 4
Fitting Linear Mixed-Effects Models Using lme4
journal, January 2015
- Bates, Douglas; Mächler, Martin; Bolker, Ben
- Journal of Statistical Software, Vol. 67, Issue 1
A global Fine-Root Ecology Database to address below-ground challenges in plant ecology
journal, February 2017
- Iversen, Colleen M.; McCormack, M. Luke; Powell, A. Shafer
- New Phytologist, Vol. 215, Issue 1, p. 15-26
Carbon allocation in forest ecosystems
journal, October 2007
- Litton, Creighton M.; Raich, James W.; Ryan, Michael G.
- Global Change Biology, Vol. 13, Issue 10
The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests
journal, April 2013
- Phillips, Richard P.; Brzostek, Edward; Midgley, Meghan G.
- New Phytologist, Vol. 199, Issue 1
Comparisons of Structure and life span in Roots and Leaves Among Temperate Trees
journal, August 2006
- Withington, Jennifer M.; Reich, Peter B.; Oleksyn, Jacek
- Ecological Monographs, Vol. 76, Issue 3
The evolution of the worldwide leaf economics spectrum
journal, February 2011
- Donovan, Lisa A.; Maherali, Hafiz; Caruso, Christina M.
- Trends in Ecology & Evolution, Vol. 26, Issue 2
Impacts of individual tree species on carbon dynamics in a moist tropical forest environment
journal, June 2010
- Russell, Ann E.; Raich, James W.; Arrieta, Ricardo Bedoya
- Ecological Applications, Vol. 20, Issue 4
Modulation of leaf economic traits and trait relationships by climate: Modulation of leaf traits by climate
journal, August 2005
- Wright, Ian J.; Reich, Peter B.; Cornelissen, Johannes H. C.
- Global Ecology and Biogeography, Vol. 14, Issue 5
Putting phylogeny into the analysis of biological traits: A methodological approach
journal, June 2010
- Jombart, Thibaut; Pavoine, Sandrine; Devillard, Sébastien
- Journal of Theoretical Biology, Vol. 264, Issue 3
Linking litter decomposition of above- and below-ground organs to plant-soil feedbacks worldwide
journal, June 2013
- Freschet, Grégoire T.; Cornwell, William K.; Wardle, David A.
- Journal of Ecology, Vol. 101, Issue 4
Global patterns in the vulnerability of ecosystems to vegetation shifts due to climate change: Global vulnerability to climate change
journal, June 2010
- Gonzalez, Patrick; Neilson, Ronald P.; Lenihan, James M.
- Global Ecology and Biogeography, Vol. 19, Issue 6
Avoiding inaccuracies in tree calibration and phylogenetic community analysis using Phylocom 4.2
journal, May 2013
- Gastauer, Markus; Meira-Neto, João Augusto Alves
- Ecological Informatics, Vol. 15
Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis
journal, February 2009
- Brundrett, Mark C.
- Plant and Soil, Vol. 320, Issue 1-2
Phylomatic: tree assembly for applied phylogenetics
journal, March 2005
- Webb, Campbell O.; Donoghue, Michael J.
- Molecular Ecology Notes, Vol. 5, Issue 1
Explaining within-community variation in plant biomass allocation: a balance between organ biomass and morphology above vs below ground?
journal, January 2015
- Freschet, Grégoire T.; Kichenin, Emilie; Wardle, David A.
- Journal of Vegetation Science, Vol. 26, Issue 3
The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto
journal, February 2014
- Reich, Peter B.
- Journal of Ecology, Vol. 102, Issue 2
Linking leaf and root trait syndromes among 39 grassland and savannah species
journal, April 2005
- Tjoelker, M. G.; Craine, J. M.; Wedin, D.
- New Phytologist, Vol. 167, Issue 2
Fundamental Trade-Offs Generating the Worldwide leaf Economics Spectrum
journal, March 2006
- Shipley, Bill; Lechowicz, Martin J.; Wright, Ian
- Ecology, Vol. 87, Issue 3
Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species
journal, April 2014
- Gu, J.; Xu, Y.; Dong, X.
- Tree Physiology, Vol. 34, Issue 4
Leading dimensions in absorptive root trait variation across 96 subtropical forest species
journal, May 2014
- Kong, Deliang; Ma, Chengen; Zhang, Qian
- New Phytologist, Vol. 203, Issue 3
Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees
journal, December 2014
- Valverde-Barrantes, Oscar J.; Smemo, Kurt A.; Blackwood, Christopher B.
- Functional Ecology, Vol. 29, Issue 6
Going underground: root traits as drivers of ecosystem processes
journal, December 2014
- Bardgett, Richard D.; Mommer, Liesje; De Vries, Franciska T.
- Trends in Ecology & Evolution, Vol. 29, Issue 12
Phylogenetic and Growth Form Variation in the Scaling of Nitrogen and Phosphorus in the Seed Plants
journal, October 2006
- Kerkhoff, Andrew J.; Fagan, William F.; Elser, James J.
- The American Naturalist, Vol. 168, Issue 4
References
book, January 2012
- Legendre, Pierre; Legendre, Louis
- Developments in Environmental Modelling
The Importance of Tissue Density for Growth and Life Span of Leaves and Roots: A Comparison of Five Ecologically Contrasting Grasses
journal, December 1996
- Ryser, P.
- Functional Ecology, Vol. 10, Issue 6
Do ectomycorrhizal and arbuscular mycorrhizal temperate tree species systematically differ in root order-related fine root morphology and biomass?
journal, February 2015
- Kubisch, Petra; Hertel, Dietrich; Leuschner, Christoph
- Frontiers in Plant Science, Vol. 6
Patterns in root trait variation among 25 co-existing North American forest species
journal, March 2009
- Comas, L. H.; Eissenstat, D. M.
- New Phytologist, Vol. 182, Issue 4
Global response patterns of terrestrial plant species to nitrogen addition
journal, July 2008
- Xia, Jianyang; Wan, Shiqiang
- New Phytologist, Vol. 179, Issue 2
An evolutionary perspective on leaf economics: phylogenetics of leaf mass per area in vascular plants
journal, July 2014
- Flores, Olivier; Garnier, Eric; Wright, Ian J.
- Ecology and Evolution, Vol. 4, Issue 14
Fine root Architecture of nine North American Trees
journal, May 2002
- Pregitzer, Kurt S.; DeForest, Jared L.; Burton, Andrew J.
- Ecological Monographs, Vol. 72, Issue 2
Species- and community-level patterns in fine root traits along a 120 000-year soil chronosequence in temperate rain forest: Root trait shifts along soil chronosequence
journal, March 2011
- Holdaway, Robert J.; Richardson, Sarah J.; Dickie, Ian A.
- Journal of Ecology, Vol. 99, Issue 4
APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004
- Paradis, E.; Claude, J.; Strimmer, K.
- Bioinformatics, Vol. 20, Issue 2
How to measure and test phylogenetic signal: How to measure and test phylogenetic signal
journal, April 2012
- Münkemüller, Tamara; Lavergne, Sébastien; Bzeznik, Bruno
- Methods in Ecology and Evolution, Vol. 3, Issue 4
The nutrient absorption–transportation hypothesis: optimizing structural traits in absorptive roots
journal, November 2016
- Kong, Deliang; Wang, Junjian; Zeng, Hui
- New Phytologist, Vol. 213, Issue 4
The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients
journal, May 2001
- Craine, J. M.; Froehle, J.; Tilman, D. G.
- Oikos, Vol. 93, Issue 2
Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control: Tansley review
journal, November 2011
- Poorter, Hendrik; Niklas, Karl J.; Reich, Peter B.
- New Phytologist, Vol. 193, Issue 1
Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest
journal, May 2015
- Eissenstat, David M.; Kucharski, Joshua M.; Zadworny, Marcin
- New Phytologist, Vol. 208, Issue 1
Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species
journal, November 2008
- Guo, Dali; Xia, Mengxue; Wei, Xing
- New Phytologist, Vol. 180, Issue 3
Testing for Phylogenetic Signal in Comparative Data: Behavioral Traits are more Labile
journal, April 2003
- Blomberg, Simon P.; Garland, Theodore; Ives, Anthony R.
- Evolution, Vol. 57, Issue 4
Picante: R tools for integrating phylogenies and ecology
journal, April 2010
- Kembel, S. W.; Cowan, P. D.; Helmus, M. R.
- Bioinformatics, Vol. 26, Issue 11
Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change
journal, December 2008
- Williams, Stephen E.; Shoo, Luke P.; Isaac, Joanne L.
- PLoS Biology, Vol. 6, Issue 12
Which is a better predictor of plant traits: temperature or precipitation?
journal, May 2014
- Moles, Angela T.; Perkins, Sarah E.; Laffan, Shawn W.
- Journal of Vegetation Science, Vol. 25, Issue 5
No globally consistent effect of ectomycorrhizal status on foliar traits
journal, September 2012
- Koele, Nina; Dickie, Ian A.; Oleksyn, Jacek
- New Phytologist, Vol. 196, Issue 3
Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees
journal, July 2016
- Chen, Weile; Koide, Roger T.; Adams, Thomas S.
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 31
Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation
journal, March 2007
- Swenson, N. G.; Enquist, B. J.
- American Journal of Botany, Vol. 94, Issue 3
Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis
journal, November 2016
- Maherali, Hafiz; Oberle, Brad; Stevens, Peter F.
- The American Naturalist, Vol. 188, Issue 5