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Title: Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees

Abstract

Summary Plant functional traits have revealed trade‐offs related to life‐history adaptations, geographical distributions, and ecosystem processes. Fine roots are essential in plant resource acquisition and play an important role in soil carbon cycling. Nonetheless, root trait variation is still poorly quantified and rarely related to the rest of the plant. We examined chemical and morphological traits of 34 temperate arbuscular mycorrhizal tree species, representing three main angiosperm clades (super‐orders asterid, magnoliid and rosid). We tested to what extent fine root chemical and morphological traits were correlated similarly to the leaf economical spectrum ( LES ) or were structured by ancestral affiliations among species. Root traits did not display the same trade‐offs as leaves (e.g. specific root length was not correlated with root N, whereas specific leaf area was correlated with leaf N). Moreover, 75% of below‐ground traits were phylogenetically structured according to Pagel's λ and Abouheif's C mean autocorrelation tests, as opposed to 28% of above‐ground traits. Magnoliids showed thicker, less branched roots than asterids or rosids, but rosid roots exhibited lower N and higher non‐acid‐hydrolysable (e.g. lignin) content than other species. In contrast, leaf traits did not differ significantly among super‐orders. At the whole‐tree level, chemical traits such asmore » nitrogen tissue content and lignin content were correlated between above and below‐ground organs. The distribution of root traits in woody temperate trees was better explained by shared ancestry than by the nutrient content and structural trade‐offs expected by the LES hypothesis. Root chemistry and morphology differed substantially among species belonging to different super‐orders, suggesting deep divergences in resource acquisition strategies among major angiosperm groups. Although we found partial support for the idea of whole‐plant integration based on corresponding nitrogen content across all organs (i.e. a plant economics spectrum), our study stresses phylogenetic affiliation as the primary driver of root trait distributions among angiosperms, a pattern that could be easily overlooked based solely on above‐ground observations.« less

Authors:
 [1];  [2];  [1];
  1. Department of Biological Sciences Kent State University Kent OH 44242 USA
  2. Department of Biological Sciences Kent State University Kent OH 44242 USA, The Holden Arboretum 9500 Sperry Rd Kirtland OH 44094 USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1401599
Grant/Contract Number:  
DE‐SC000433
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Functional Ecology
Additional Journal Information:
Journal Name: Functional Ecology Journal Volume: 29 Journal Issue: 6; Journal ID: ISSN 0269-8463
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Valverde‐Barrantes, Oscar J., Smemo, Kurt A., Blackwood, Christopher B., and Norden, ed., Natalia. Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees. United Kingdom: N. p., 2014. Web. doi:10.1111/1365-2435.12384.
Valverde‐Barrantes, Oscar J., Smemo, Kurt A., Blackwood, Christopher B., & Norden, ed., Natalia. Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees. United Kingdom. https://doi.org/10.1111/1365-2435.12384
Valverde‐Barrantes, Oscar J., Smemo, Kurt A., Blackwood, Christopher B., and Norden, ed., Natalia. Tue . "Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees". United Kingdom. https://doi.org/10.1111/1365-2435.12384.
@article{osti_1401599,
title = {Fine root morphology is phylogenetically structured, but nitrogen is related to the plant economics spectrum in temperate trees},
author = {Valverde‐Barrantes, Oscar J. and Smemo, Kurt A. and Blackwood, Christopher B. and Norden, ed., Natalia},
abstractNote = {Summary Plant functional traits have revealed trade‐offs related to life‐history adaptations, geographical distributions, and ecosystem processes. Fine roots are essential in plant resource acquisition and play an important role in soil carbon cycling. Nonetheless, root trait variation is still poorly quantified and rarely related to the rest of the plant. We examined chemical and morphological traits of 34 temperate arbuscular mycorrhizal tree species, representing three main angiosperm clades (super‐orders asterid, magnoliid and rosid). We tested to what extent fine root chemical and morphological traits were correlated similarly to the leaf economical spectrum ( LES ) or were structured by ancestral affiliations among species. Root traits did not display the same trade‐offs as leaves (e.g. specific root length was not correlated with root N, whereas specific leaf area was correlated with leaf N). Moreover, 75% of below‐ground traits were phylogenetically structured according to Pagel's λ and Abouheif's C mean autocorrelation tests, as opposed to 28% of above‐ground traits. Magnoliids showed thicker, less branched roots than asterids or rosids, but rosid roots exhibited lower N and higher non‐acid‐hydrolysable (e.g. lignin) content than other species. In contrast, leaf traits did not differ significantly among super‐orders. At the whole‐tree level, chemical traits such as nitrogen tissue content and lignin content were correlated between above and below‐ground organs. The distribution of root traits in woody temperate trees was better explained by shared ancestry than by the nutrient content and structural trade‐offs expected by the LES hypothesis. Root chemistry and morphology differed substantially among species belonging to different super‐orders, suggesting deep divergences in resource acquisition strategies among major angiosperm groups. Although we found partial support for the idea of whole‐plant integration based on corresponding nitrogen content across all organs (i.e. a plant economics spectrum), our study stresses phylogenetic affiliation as the primary driver of root trait distributions among angiosperms, a pattern that could be easily overlooked based solely on above‐ground observations.},
doi = {10.1111/1365-2435.12384},
journal = {Functional Ecology},
number = 6,
volume = 29,
place = {United Kingdom},
year = {Tue Dec 23 00:00:00 EST 2014},
month = {Tue Dec 23 00:00:00 EST 2014}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1111/1365-2435.12384

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Works referenced in this record:

The ecophysiology of early angiosperms: Early angiosperm ecophysiology
journal, January 2007


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
  • DOI: 10.1111/geb.12048

Ephemeral root modules in Fraxinus mandshurica
journal, September 2010


Co-Inertia Analysis and the Linking of Ecological data Tables
journal, November 2003

  • Dray, Stéphane; Chessel, Daniel; Thioulouse, Jean
  • Ecology, Vol. 84, Issue 11
  • DOI: 10.1890/03-0178

Size-Correction and Principal Components for Interspecific Comparative Studies
journal, December 2009


Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications
journal, February 2011


Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis
journal, August 2011


Controls on long-term root and leaf litter decomposition in neotropical forests
journal, May 2009


Coevolution of roots and mycorrhizas of land plants
journal, May 2002


Evolution of root endosymbiosis with bacteria: how novel are nodules?
journal, February 2009


Functional distinctiveness of major plant lineages
journal, February 2014

  • Cornwell, William K.; Westoby, Mark; Falster, Daniel S.
  • Journal of Ecology, Vol. 102, Issue 2
  • DOI: 10.1111/1365-2745.12208

The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species
journal, November 2009


Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species
journal, June 2004


A multi-trait test of the leaf-height-seed plant strategy scheme with 133 species from a pine forest flora
journal, November 2009


Comparisons of Structure and life span in Roots and Leaves Among Temperate Trees
journal, August 2006


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
  • DOI: 10.1016/j.tree.2010.11.011

Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts
journal, September 1999

  • Ackerly, David D.; Reich, Peter B.
  • American Journal of Botany, Vol. 86, Issue 9
  • DOI: 10.2307/2656775

Cenozoic climate change shaped the evolutionary ecophysiology of the Cupressaceae conifers
journal, May 2012

  • Pittermann, J.; Stuart, S. A.; Dawson, T. E.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 24
  • DOI: 10.1073/pnas.1114378109

Angiosperm leaf vein evolution was physiologically and environmentally transformative
journal, February 2009

  • Boyce, C. Kevin; Brodribb, Tim J.; Feild, Taylor S.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1663
  • DOI: 10.1098/rspb.2008.1919

The hidden cost of transpiration
journal, March 2010

  • Beerling, David J.; Franks, Peter J.
  • Nature, Vol. 464, Issue 7288
  • DOI: 10.1038/464495a

The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto
journal, February 2014


Functional traits, productivity and effects on nitrogen cycling of 33 grassland species
journal, October 2002


Linking leaf and root trait syndromes among 39 grassland and savannah species
journal, April 2005


Atmospheric carbon dioxide linked with Mesozoic and early Cenozoic climate change
journal, December 2007

  • Fletcher, Benjamin J.; Brentnall, Stuart J.; Anderson, Clive W.
  • Nature Geoscience, Vol. 1, Issue 1
  • DOI: 10.1038/ngeo.2007.29

Structure and organization of a northern New England salt marsh plant community
journal, January 2004


Multi-trait interactions, not phylogeny, fine-tune leaf size reduction with increasing altitude
journal, January 2011

  • Milla, Rubén; Reich, Peter B.
  • Annals of Botany, Vol. 107, Issue 3
  • DOI: 10.1093/aob/mcq261

Do we need an Extended Evolutionary Synthesis?
journal, December 2007


The Evolution of Plant Functional Variation: Traits, Spectra, and Strategies
journal, May 2003

  • Reich, P. B.; Wright, I. J.; Cavender‐Bares, J.
  • International Journal of Plant Sciences, Vol. 164, Issue S3
  • DOI: 10.1086/374368

Reconciling plant strategy theories of Grime and Tilman
journal, July 2005


Fine root Architecture of nine North American Trees
journal, May 2002


How to measure and test phylogenetic signal: How to measure and test phylogenetic signal
journal, April 2012


The relationship between stem and branch wood specific gravity and the ability of each measure to predict leaf area
journal, April 2008

  • Swenson, Nathan G.; Enquist, Brian J.
  • American Journal of Botany, Vol. 95, Issue 4
  • DOI: 10.3732/ajb.95.4.516

Decoupled leaf and stem economics in rain forest trees: Decoupled leaf and stem economics spectra
journal, August 2010


Consequences of climate change on the tree of life in Europe
journal, February 2011

  • Thuiller, Wilfried; Lavergne, Sébastien; Roquet, Cristina
  • Nature, Vol. 470, Issue 7335
  • DOI: 10.1038/nature09705

Drought sensitivity shapes species distribution patterns in tropical forests
journal, May 2007

  • Engelbrecht, Bettina M. J.; Comita, Liza S.; Condit, Richard
  • Nature, Vol. 447, Issue 7140
  • DOI: 10.1038/nature05747

Regulation of Respiration In Vivo
book, January 2005


A comparison of methods for determining proximate carbon fractions of forest litter
journal, February 1990

  • Ryan, Michael G.; Melillo, Jerry M.; Ricca, Andrea
  • Canadian Journal of Forest Research, Vol. 20, Issue 2
  • DOI: 10.1139/x90-023

Plasticity in above- and belowground resource acquisition traits in response to single and multiple environmental factors in three tree species
journal, March 2013

  • Freschet, Grégoire T.; Bellingham, Peter J.; Lyver, Philip O'B.
  • Ecology and Evolution, Vol. 3, Issue 4
  • DOI: 10.1002/ece3.520

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
  • DOI: 10.1093/aob/mcr297

Linking root traits to potential growth rate in six temperate tree species
journal, June 2002


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
  • DOI: 10.1086/665823

Leaf, stem and root tissue strategies across 758 Neotropical tree species
journal, July 2012


phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package
journal, December 2011


adephylo: new tools for investigating the phylogenetic signal in biological traits
journal, June 2010


Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants
journal, August 2008


Land-plant ecology on the basis of functional traits
journal, May 2006


Evidence of the ‘plant economics spectrum’ in a subarctic flora
journal, March 2010


The worldwide leaf economics spectrum
journal, April 2004

  • Wright, Ian J.; Reich, Peter B.; Westoby, Mark
  • Nature, Vol. 428, Issue 6985
  • DOI: 10.1038/nature02403

Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms
journal, March 2009


Phylogenetic distribution and evolution of mycorrhizas in land plants
journal, May 2006


From tropics to tundra: Global convergence in plant functioning
journal, December 1997

  • Reich, P. B.; Walters, M. B.; Ellsworth, D. S.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 25
  • DOI: 10.1073/pnas.94.25.13730

The distribution of below-ground traits is explained by intrinsic species differences and intraspecific plasticity in response to root neighbours
journal, June 2013

  • Valverde-Barrantes, Oscar J.; Smemo, Kurt A.; Feinstein, Larry M.
  • Journal of Ecology, Vol. 101, Issue 4
  • DOI: 10.1111/1365-2745.12087

Phylogenies and the Comparative Method
journal, January 1985

  • Felsenstein, Joseph
  • The American Naturalist, Vol. 125, Issue 1
  • DOI: 10.1086/284325

A phylogenetic perspective on the distribution of plant diversity
journal, August 2008

  • Donoghue, M. J.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1
  • DOI: 10.1073/pnas.0801962105

Independent Evolution of Leaf and Root Traits within and among Temperate Grassland Plant Communities
journal, June 2011


Predicting fine root lifespan from plant functional traits in temperate trees
journal, June 2012


Let the concept of trait be functional!
journal, May 2007


Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages: Selectivity in AMF-plant associations
journal, May 2011


Fine root decomposition rates do not mirror those of leaf litter among temperate tree species
journal, October 2009


Inferring the historical patterns of biological evolution
journal, October 1999


The earliest fossil evidence of the Hamamelidaceae: Late Cretaceous (Turonian) inflorescences and fruits of Altingioideae
journal, May 2001

  • Zhou, Zhe-kun; Crepet, William L.; Nixon, Kevin C.
  • American Journal of Botany, Vol. 88, Issue 5
  • DOI: 10.2307/2657028

Modulation of leaf economic traits and trait relationships by climate: Modulation of leaf traits by climate
journal, August 2005


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
  • DOI: 10.1016/j.jtbi.2010.03.038

The leaf size/number trade-off in herbaceous angiosperms
journal, October 2009

  • Whitman, T.; Aarssen, L. W.
  • Journal of Plant Ecology, Vol. 3, Issue 1
  • DOI: 10.1093/jpe/rtp018

A survey of micorrhizal infection in an amazonian rain forest
journal, September 1980


Specific leaf area and leaf dry matter content as alternative predictors of plant strategies
journal, July 1999


Fine root morphological adaptations in Scots pine, Norway spruce and silver birch along a latitudinal gradient in boreal forests
journal, November 2007


Functional Traits and Niche-Based Tree Community Assembly in an Amazonian Forest
journal, October 2008


Co-inertia analysis: an alternative method for studying species-environment relationships
journal, June 1994


Coordination between leaf and stem traits related to leaf carbon gain and hydraulics across 32 drought-tolerant angiosperms
journal, February 2008


Relations of Environmental Change to Angiosperm Evolution During the Late Cretaceous and Tertiary
book, January 1997


A handbook of protocols for standardised and easy measurement of plant functional traits worldwide
journal, January 2003

  • Cornelissen, J. H. C.; Lavorel, S.; Garnier, E.
  • Australian Journal of Botany, Vol. 51, Issue 4
  • DOI: 10.1071/BT02124

Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species
journal, April 2014


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
  • DOI: 10.1111/nph.12842

Wood anatomy and wood density in shrubs: Responses to varying aridity along transcontinental transects
journal, August 2009

  • Martínez-Cabrera, Hugo I.; Jones, Cynthia S.; Espino, Susana
  • American Journal of Botany, Vol. 96, Issue 8
  • DOI: 10.3732/ajb.0800237

Architectural analysis of plant root systems 1. Architectural correlates of exploitation efficiency
journal, July 1991


Tree species fine-root demography parallels habitat specialization across a sandhill soil resource gradient
journal, July 2009

  • Espeleta, Javier F.; West, Jason B.; Donovan, Lisa A.
  • Ecology, Vol. 90, Issue 7
  • DOI: 10.1890/08-0056.1

Patterns in root trait variation among 25 co-existing North American forest species
journal, March 2009


APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004


Comparative anatomy of roots and mycorrhizae of common Ontario trees
journal, March 1990

  • Brundrett, Mark; Murase, Gracia; Kendrick, Bryce
  • Canadian Journal of Botany, Vol. 68, Issue 3
  • DOI: 10.1139/b90-076

Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil
journal, January 2007

  • Zangaro, Waldemar; Nishidate, Fabio Rodrigo; Vandresen, Julia
  • Journal of Tropical Ecology, Vol. 23, Issue 1
  • DOI: 10.1017/S0266467406003713

Integrated Screening Validates Primary Axes of Specialisation in Plants
journal, June 1997

  • Grime, J. P.; Thompson, K.; Hunt, R.
  • Oikos, Vol. 79, Issue 2
  • DOI: 10.2307/3546011

Picante: R tools for integrating phylogenies and ecology
journal, April 2010


Phylogenetic biome conservatism on a global scale
journal, February 2009

  • Crisp, Michael D.; Arroyo, Mary T. K.; Cook, Lyn G.
  • Nature, Vol. 458, Issue 7239
  • DOI: 10.1038/nature07764