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Title: Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests

Abstract

Plants compete for nutrients using a range of strategies. We investigated nutrient foraging within nutrient hot-spots simultaneously available to plant species with diverse root traits. We hypothesized that there would be more root proliferation by thin-root species than by thick-root species, and that root proliferation by thin-root species would limit root proliferation by thick-root species. We conducted a root ingrowth experiment in a temperate forest in eastern USA where root systems of different tree species could interact. Tree species varied in the thickness of their absorptive roots, and were associated with either ectomycorrhizal (EM) or arbuscular mycorrhizal (AM) fungi. Thus, there were thin- and thick-root AM and thin- and thick-root EM plant functional groups. Half the ingrowth cores were amended with organic nutrients (dried green leaves). Relative root length abundance, the proportion of total root length in a given soil volume occupied by a particular plant functional group, was calculated for the original root population and ingrowth roots after 6 months. The shift in relative root length abundance from original to ingrowth roots was positive in thin-root species but negative in thick-root species (p < .001), especially in unamended patches (AM: +6% vs. -7%; EM: +8% vs. -9%). Being thin-rootedmore » may thus allow a species to more rapidly recolonize soil after a disturbance, which may influence competition for nutrients. Moreover, we observed that nutrient additions amplified the shift in root length abundance of thin over thick roots in AM trees (+13% vs. -14%), but not in EM trees (+1% vs -3%). In contrast, phospholipid fatty acid biomarkers suggested that EM fungal hyphae strongly proliferated in nutrient hot-spots whereas AM fungal hyphae exhibited only modest proliferation. We found no evidence that when growing in the shared patch, the proliferation of thin roots inhibited the growth of thick roots. Synthesis. Knowledge of root morphology and mycorrhizal type of co-existing tree species may improve prediction of patch exploitation and nutrient acquisition in heterogeneous soils.« less

Authors:
 [1];  [2]; ORCiD logo [1]
  1. Pennsylvania State Univ., University Park, PA (United States)
  2. Pennsylvania State Univ., University Park, PA (United States); Brigham Young Univ., Provo, UT (United States)
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23). Climate and Environmental Sciences Division; USDOE Office of Science (SC)
Contributing Org.:
NSF
OSTI Identifier:
1419620
Alternate Identifier(s):
OSTI ID: 1411152
Grant/Contract Number:  
SC0012003
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Ecology
Additional Journal Information:
Journal Volume: 106; Journal Issue: 1; Journal ID: ISSN 0022-0477
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; arbuscular mycorrhiza; ectomycorrhiza; ingrowth; nutrient foraging; plant–soil interactions; resource exploitation; root competition; root length density; root proliferation; soil heterogeneity

Citation Formats

Chen, Weile, Koide, Roger T., and Eissenstat, David M. Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests. United States: N. p., 2017. Web. doi:10.1111/1365-2745.12800.
Chen, Weile, Koide, Roger T., & Eissenstat, David M. Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests. United States. doi:10.1111/1365-2745.12800.
Chen, Weile, Koide, Roger T., and Eissenstat, David M. Thu . "Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests". United States. doi:10.1111/1365-2745.12800. https://www.osti.gov/servlets/purl/1419620.
@article{osti_1419620,
title = {Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests},
author = {Chen, Weile and Koide, Roger T. and Eissenstat, David M.},
abstractNote = {Plants compete for nutrients using a range of strategies. We investigated nutrient foraging within nutrient hot-spots simultaneously available to plant species with diverse root traits. We hypothesized that there would be more root proliferation by thin-root species than by thick-root species, and that root proliferation by thin-root species would limit root proliferation by thick-root species. We conducted a root ingrowth experiment in a temperate forest in eastern USA where root systems of different tree species could interact. Tree species varied in the thickness of their absorptive roots, and were associated with either ectomycorrhizal (EM) or arbuscular mycorrhizal (AM) fungi. Thus, there were thin- and thick-root AM and thin- and thick-root EM plant functional groups. Half the ingrowth cores were amended with organic nutrients (dried green leaves). Relative root length abundance, the proportion of total root length in a given soil volume occupied by a particular plant functional group, was calculated for the original root population and ingrowth roots after 6 months. The shift in relative root length abundance from original to ingrowth roots was positive in thin-root species but negative in thick-root species (p < .001), especially in unamended patches (AM: +6% vs. -7%; EM: +8% vs. -9%). Being thin-rooted may thus allow a species to more rapidly recolonize soil after a disturbance, which may influence competition for nutrients. Moreover, we observed that nutrient additions amplified the shift in root length abundance of thin over thick roots in AM trees (+13% vs. -14%), but not in EM trees (+1% vs -3%). In contrast, phospholipid fatty acid biomarkers suggested that EM fungal hyphae strongly proliferated in nutrient hot-spots whereas AM fungal hyphae exhibited only modest proliferation. We found no evidence that when growing in the shared patch, the proliferation of thin roots inhibited the growth of thick roots. Synthesis. Knowledge of root morphology and mycorrhizal type of co-existing tree species may improve prediction of patch exploitation and nutrient acquisition in heterogeneous soils.},
doi = {10.1111/1365-2745.12800},
journal = {Journal of Ecology},
number = 1,
volume = 106,
place = {United States},
year = {2017},
month = {5}
}

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Works referenced in this record:

Foraging strategies in trees of different root morphology: the role of root lifespan
journal, September 2013


Mycorrhizal fungi and roots are complementary in foraging within nutrient patches
journal, September 2016

  • Cheng, Lei; Chen, Weile; Adams, Thomas S.
  • Ecology, Vol. 97, Issue 10
  • DOI: 10.1002/ecy.1514

Variability in aboveground carbon driven by slope aspect and curvature in an eastern deciduous forest, USA
journal, February 2017

  • Smith, Lauren A.; Eissenstat, David M.; Kaye, Margot W.
  • Canadian Journal of Forest Research, Vol. 47, Issue 2
  • DOI: 10.1139/cjfr-2016-0147

Plant Competition Underground
journal, November 1997


Belowground carbon trade among tall trees in a temperate forest
journal, April 2016


Multiple Multilocus DNA Barcodes from the Plastid Genome Discriminate Plant Species Equally Well
journal, July 2008


Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs
journal, March 2004


Rapid fine root disappearance in a pine woodland: a substantial carbon flux
journal, December 2002

  • Stevens, Glen N.; Jones, Robert H.; Mitchell, Robert J.
  • Canadian Journal of Forest Research, Vol. 32, Issue 12
  • DOI: 10.1139/x02-135

Reliance on shallow soil water in a mixed-hardwood forest in central Pennsylvania
journal, November 2015

  • Gaines, Katie P.; Stanley, Jane W.; Meinzer, Frederick C.
  • Tree Physiology, Vol. 36, Issue 4
  • DOI: 10.1093/treephys/tpv113

Root foraging traits and competitive ability in heterogeneous soils
journal, April 2007


A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi
journal, July 1990


Plant root proliferation in nitrogen–rich patches confers competitive advantage
journal, March 1999

  • Robinson, David; Hodge, Angela; Griffiths, Bryan S.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 266, Issue 1418
  • DOI: 10.1098/rspb.1999.0656

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


Toward Understanding the Consequences of soil Heterogeneity for Plant Populations and Communities
journal, September 2003

  • Hutchings, Michael J.; John, Elizabeth A.; Wijesinghe, Dushyantha K.
  • Ecology, Vol. 84, Issue 9
  • DOI: 10.1890/02-0290

Root–Root Interactions: Towards A Rhizosphere Framework
journal, March 2016


Soil Nutrient Heterogeneity Alters Competition Between two Perennial Grass Species
journal, September 2001


Nutrient foraging behaviour of four co-occurring perennial grassland plant species alone does not predict behaviour with neighbours
journal, August 2015

  • McNickle, Gordon G.; Deyholos, Michael K.; Cahill, James F.
  • Functional Ecology, Vol. 30, Issue 3
  • DOI: 10.1111/1365-2435.12508

Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field
journal, September 2001


Complementary plant nutrient-acquisition strategies promote growth of neighbour species
journal, March 2014

  • Teste, Francois P.; Veneklaas, Erik J.; Dixon, Kingsley W.
  • Functional Ecology, Vol. 28, Issue 4
  • DOI: 10.1111/1365-2435.12270

Soil insects alter fine root demography in peach (Prunus persica)
journal, March 2002


Seasonal Timing of Root Growth in Favorable Microsites
journal, June 1988

  • Eissenstat, David M.; Caldwell, Martyn M.
  • Ecology, Vol. 69, Issue 3
  • DOI: 10.2307/1941037

Are competitive interactions influenced by spatial nutrient heterogeneity and root foraging behavior?
journal, May 2002


First come, first served: grasses have a head start on forbs with prompt nutrient patch occupation
journal, July 2009


Plants Integrate Information About Nutrients and Neighbors
journal, June 2010


Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory?
journal, September 2011


Contrasting root behaviour in two grass species: a test of functionality in dynamic heterogeneous conditions
journal, March 2011


Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands
journal, January 2017

  • Teste, François P.; Kardol, Paul; Turner, Benjamin L.
  • Science, Vol. 355, Issue 6321
  • DOI: 10.1126/science.aai8291

The plastic plant: root responses to heterogeneous supplies of nutrients
journal, April 2004


The Microscale Distribution of Neighbouring Plant Roots in Fertile Soil Microsites
journal, January 1991

  • Caldwell, M. M.; Manwaring, J. H.; Durham, S. L.
  • Functional Ecology, Vol. 5, Issue 6
  • DOI: 10.2307/2389539

Exploitation of Phosphate from Fertile Soil Microsites by Three Great Basin Perennials when in Competition
journal, January 1991

  • Caldwell, M. M.; Manwaring, J. H.; Jackson, R. B.
  • Functional Ecology, Vol. 5, Issue 6
  • DOI: 10.2307/2389538

Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors
journal, November 2015

  • Shah, Firoz; Nicolás, César; Bentzer, Johan
  • New Phytologist, Vol. 209, Issue 4
  • DOI: 10.1111/nph.13722

Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete
journal, July 1999


Aggregated and complementary: symmetric proliferation, overyielding, and mass effects explain fine-root biomass in soil patches in a diverse temperate deciduous forest landscape
journal, November 2014

  • Valverde-Barrantes, Oscar J.; Smemo, Kurt A.; Feinstein, Larry M.
  • New Phytologist, Vol. 205, Issue 2
  • DOI: 10.1111/nph.13179

In situ high-frequency observations of mycorrhizas
journal, June 2013

  • Allen, Michael F.; Kitajima, Kuni
  • New Phytologist, Vol. 200, Issue 1
  • DOI: 10.1111/nph.12363

Invasive Root Growth into Disturbed Soil of Two Tussock Grasses that Differ in Competitive Effectiveness
journal, January 1989

  • Eissenstat, D. M.; Caldwell, M. M.
  • Functional Ecology, Vol. 3, Issue 3
  • DOI: 10.2307/2389375

Resource and non-resource root competition effects of grasses on early- versus late-successional trees
journal, May 2009


Co-occurring grassland species vary in their responses to fine-scale soil heterogeneity
journal, July 2016

  • Tamme, Riin; Gazol, Antonio; Price, Jodi N.
  • Journal of Vegetation Science, Vol. 27, Issue 5
  • DOI: 10.1111/jvs.12431

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
  • DOI: 10.1111/nph.13451

Burrowing by badgers (Meles meles) and foxes (Vulpes vulpes) changes soil conditions and vegetation in a European temperate forest
journal, November 2013


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
  • DOI: 10.1073/pnas.1601006113

Data from: Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests
dataset, April 2017

  • Chen, Weile; Koide, Roger T.; Eissenstat, David M.
  • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1111/1365-2745.12800, 1 XLSX file (33.13 Kb)
  • DOI: 10.5061/dryad.bh88s

Soil Nutrient Heterogeneity Alters Competition between Two Perennial Grass Species
journal, September 2001

  • Fransen, Bart; de Kroon, Hans; Berendse, Frank
  • Ecology, Vol. 82, Issue 9
  • DOI: 10.2307/2679934

    Works referencing / citing this record:

    Data from: Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests
    dataset, April 2017

    • Chen, Weile; Koide, Roger T.; Eissenstat, David M.
    • Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1111/1365-2745.12800, 1 XLSX file (33.13 Kb)
    • DOI: 10.5061/dryad.bh88s

    Mycorrhizal fungi and roots are complementary in foraging within nutrient patches
    journal, September 2016

    • Cheng, Lei; Chen, Weile; Adams, Thomas S.
    • Ecology, Vol. 97, Issue 10
    • DOI: 10.1002/ecy.1514

    Root foraging traits and competitive ability in heterogeneous soils
    journal, April 2007


    First come, first served: grasses have a head start on forbs with prompt nutrient patch occupation
    journal, July 2009


    Contrasting root behaviour in two grass species: a test of functionality in dynamic heterogeneous conditions
    journal, March 2011


    Burrowing by badgers (Meles meles) and foxes (Vulpes vulpes) changes soil conditions and vegetation in a European temperate forest
    journal, November 2013


    Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs
    journal, March 2004


    Root–Root Interactions: Towards A Rhizosphere Framework
    journal, March 2016


    Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field
    journal, September 2001


    Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete
    journal, July 1999


    Soil insects alter fine root demography in peach (Prunus persica)
    journal, March 2002


    Are competitive interactions influenced by spatial nutrient heterogeneity and root foraging behavior?
    journal, May 2002


    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
    • DOI: 10.1073/pnas.1601006113

    Foraging strategies in trees of different root morphology: the role of root lifespan
    journal, September 2013


    Reliance on shallow soil water in a mixed-hardwood forest in central Pennsylvania
    journal, November 2015

    • Gaines, Katie P.; Stanley, Jane W.; Meinzer, Frederick C.
    • Tree Physiology, Vol. 36, Issue 4
    • DOI: 10.1093/treephys/tpv113

    Plant root proliferation in nitrogen–rich patches confers competitive advantage
    journal, March 1999

    • Robinson, David; Hodge, Angela; Griffiths, Bryan S.
    • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 266, Issue 1418
    • DOI: 10.1098/rspb.1999.0656

    Complementary plant nutrient-acquisition strategies promote growth of neighbour species
    journal, March 2014

    • Teste, Francois P.; Veneklaas, Erik J.; Dixon, Kingsley W.
    • Functional Ecology, Vol. 28, Issue 4
    • DOI: 10.1111/1365-2435.12270

    Nutrient foraging behaviour of four co-occurring perennial grassland plant species alone does not predict behaviour with neighbours
    journal, August 2015

    • McNickle, Gordon G.; Deyholos, Michael K.; Cahill, James F.
    • Functional Ecology, Vol. 30, Issue 3
    • DOI: 10.1111/1365-2435.12508

    Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes
    journal, May 2019

    • Tedersoo, Leho; Bahram, Mohammad
    • Biological Reviews, Vol. 94, Issue 5
    • DOI: 10.1111/brv.12538

    Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory?
    journal, September 2011


    Resource and non-resource root competition effects of grasses on early- versus late-successional trees
    journal, May 2009


    A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi
    journal, July 1990


    The plastic plant: root responses to heterogeneous supplies of nutrients
    journal, April 2004


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


    Co-occurring grassland species vary in their responses to fine-scale soil heterogeneity
    journal, July 2016

    • Tamme, Riin; Gazol, Antonio; Price, Jodi N.
    • Journal of Vegetation Science, Vol. 27, Issue 5
    • DOI: 10.1111/jvs.12431

    In situ high-frequency observations of mycorrhizas
    journal, June 2013

    • Allen, Michael F.; Kitajima, Kuni
    • New Phytologist, Vol. 200, Issue 1
    • DOI: 10.1111/nph.12363

    Aggregated and complementary: symmetric proliferation, overyielding, and mass effects explain fine-root biomass in soil patches in a diverse temperate deciduous forest landscape
    journal, November 2014

    • Valverde-Barrantes, Oscar J.; Smemo, Kurt A.; Feinstein, Larry M.
    • New Phytologist, Vol. 205, Issue 2
    • DOI: 10.1111/nph.13179

    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
    • DOI: 10.1111/nph.13451

    Ectomycorrhizal fungi decompose soil organic matter using oxidative mechanisms adapted from saprotrophic ancestors
    journal, November 2015

    • Shah, Firoz; Nicolás, César; Bentzer, Johan
    • New Phytologist, Vol. 209, Issue 4
    • DOI: 10.1111/nph.13722

    Plants Integrate Information About Nutrients and Neighbors
    journal, June 2010


    Belowground carbon trade among tall trees in a temperate forest
    journal, April 2016


    Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands
    journal, January 2017

    • Teste, François P.; Kardol, Paul; Turner, Benjamin L.
    • Science, Vol. 355, Issue 6321
    • DOI: 10.1126/science.aai8291

    Variability in aboveground carbon driven by slope aspect and curvature in an eastern deciduous forest, USA
    journal, February 2017

    • Smith, Lauren A.; Eissenstat, David M.; Kaye, Margot W.
    • Canadian Journal of Forest Research, Vol. 47, Issue 2
    • DOI: 10.1139/cjfr-2016-0147

    Rapid fine root disappearance in a pine woodland: a substantial carbon flux
    journal, December 2002

    • Stevens, Glen N.; Jones, Robert H.; Mitchell, Robert J.
    • Canadian Journal of Forest Research, Vol. 32, Issue 12
    • DOI: 10.1139/x02-135

    Plant Competition Underground
    journal, November 1997


    Multiple Multilocus DNA Barcodes from the Plastid Genome Discriminate Plant Species Equally Well
    journal, July 2008


    Toward Understanding the Consequences of soil Heterogeneity for Plant Populations and Communities
    journal, September 2003

    • Hutchings, Michael J.; John, Elizabeth A.; Wijesinghe, Dushyantha K.
    • Ecology, Vol. 84, Issue 9
    • DOI: 10.1890/02-0290

    Seasonal Timing of Root Growth in Favorable Microsites
    journal, June 1988

    • Eissenstat, David M.; Caldwell, Martyn M.
    • Ecology, Vol. 69, Issue 3
    • DOI: 10.2307/1941037

    Invasive Root Growth into Disturbed Soil of Two Tussock Grasses that Differ in Competitive Effectiveness
    journal, January 1989

    • Eissenstat, D. M.; Caldwell, M. M.
    • Functional Ecology, Vol. 3, Issue 3
    • DOI: 10.2307/2389375

    Exploitation of Phosphate from Fertile Soil Microsites by Three Great Basin Perennials when in Competition
    journal, January 1991

    • Caldwell, M. M.; Manwaring, J. H.; Jackson, R. B.
    • Functional Ecology, Vol. 5, Issue 6
    • DOI: 10.2307/2389538

    The Microscale Distribution of Neighbouring Plant Roots in Fertile Soil Microsites
    journal, January 1991

    • Caldwell, M. M.; Manwaring, J. H.; Durham, S. L.
    • Functional Ecology, Vol. 5, Issue 6
    • DOI: 10.2307/2389539

    Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes
    journal, May 2019

    • Tedersoo, Leho; Bahram, Mohammad
    • Biological Reviews, Vol. 94, Issue 5
    • DOI: 10.1111/brv.12538