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 »
- Authors:
-
- Pennsylvania State Univ., University Park, PA (United States)
- 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.:
- Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division
- 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. https://doi.org/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. https://doi.org/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. As a result, 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 = {Thu May 25 00:00:00 EDT 2017},
month = {Thu May 25 00:00:00 EDT 2017}
}
Web of Science
Works referenced in this record:
Foraging strategies in trees of different root morphology: the role of root lifespan
journal, September 2013
- Adams, T. S.; McCormack, M. L.; Eissenstat, D. M.
- Tree Physiology, Vol. 33, Issue 9
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
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
Plant Competition Underground
journal, November 1997
- Casper, Brenda B.; Jackson, Robert B.
- Annual Review of Ecology and Systematics, Vol. 28, Issue 1
Belowground carbon trade among tall trees in a temperate forest
journal, April 2016
- Klein, T.; Siegwolf, R. T. W.; Korner, C.
- Science, Vol. 352, Issue 6283
Disproportionate abundance between ectomycorrhizal root tips and their associated mycelia: Ectomycorrhizal root tips and their associated mycelia
journal, November 2006
- Kjøller, Rasmus
- FEMS Microbiology Ecology, Vol. 58, Issue 2
Multiple Multilocus DNA Barcodes from the Plastid Genome Discriminate Plant Species Equally Well
journal, July 2008
- Fazekas, Aron J.; Burgess, Kevin S.; Kesanakurti, Prasad R.
- PLoS ONE, Vol. 3, Issue 7
Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs
journal, March 2004
- Treonis, Amy M.; Ostle, Nick J.; Stott, Andrew W.
- Soil Biology and Biochemistry, Vol. 36, Issue 3
Long-term disadvantages of selective root placement: root proliferation and shoot biomass of two perennial grass species in a 2-year experiment
journal, October 2001
- Fransen, Bart; De Kroon, Hans
- Journal of Ecology, Vol. 89, Issue 5
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
The structure and function of the vegetative mycelium of ectomycorrhizal plants. VI. Activities of nutrient mobilizing enzymes in birch litter colonized by Paxillus involutus (Fr.) Fr.
journal, July 1995
- Bending, Gary D.; Read, David J.
- New Phytologist, Vol. 130, Issue 3
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
Influence of Mycorrhizal Infection on Competition for Phosphorus and Potassium by two Grasses
journal, July 1977
- Fitter, A. H.
- New Phytologist, Vol. 79, Issue 1
Root foraging traits and competitive ability in heterogeneous soils
journal, April 2007
- Rajaniemi, Tara K.
- Oecologia, Vol. 153, Issue 1
A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi
journal, July 1990
- McGONIGLE, T. P.; Miller, M. H.; Evans, D. G.
- New Phytologist, Vol. 115, Issue 3
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
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
Biomass and morphology of fine roots in temperate broad-leaved forests differing in tree species diversity: is there evidence of below-ground overyielding?
journal, May 2009
- Meinen, Catharina; Hertel, Dietrich; Leuschner, Christoph
- Oecologia, Vol. 161, Issue 1
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
Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species
journal, April 2015
- Liu, Bitao; Li, Hongbo; Zhu, Biao
- New Phytologist, Vol. 208, Issue 1
Root–Root Interactions: Towards A Rhizosphere Framework
journal, March 2016
- Mommer, Liesje; Kirkegaard, John; van Ruijven, Jasper
- Trends in Plant Science, Vol. 21, Issue 3
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
Determinants of Soil Microbial Communities: Effects of Agricultural Management, Season, and Soil Type on Phospholipid Fatty Acid Profiles
journal, July 1998
- Bossio, D. A.; Scow, K. M.; Gunapala, N.
- Microbial Ecology, Vol. 36, Issue 1
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
Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field
journal, September 2001
- Wallander, Hakan; Nilsson, Lars Ola; Hagerberg, David
- New Phytologist, Vol. 151, Issue 3
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
Soil insects alter fine root demography in peach (Prunus persica)
journal, March 2002
- Wells, C. E.; Glenn, D. M.; Eissenstat, D. M.
- Plant, Cell and Environment, Vol. 25, Issue 3
Seasonal Timing of Root Growth in Favorable Microsites
journal, June 1988
- Eissenstat, David M.; Caldwell, Martyn M.
- Ecology, Vol. 69, Issue 3
Are competitive interactions influenced by spatial nutrient heterogeneity and root foraging behavior?
journal, May 2002
- Bliss, Kristin M.; Jones, Robert H.; Mitchell, Robert J.
- New Phytologist, Vol. 154, Issue 2
Interspecific competition impacts on the morphology and distribution of fine roots in European beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) Karst.)
journal, September 2005
- Bolte, A.; Villanueva, I.
- European Journal of Forest Research, Vol. 125, Issue 1
First come, first served: grasses have a head start on forbs with prompt nutrient patch occupation
journal, July 2009
- Šmilauerová, Marie; Šmilauer, Petr
- Plant and Soil, Vol. 328, Issue 1-2
Plants Integrate Information About Nutrients and Neighbors
journal, June 2010
- Cahill, J. F.; McNickle, G. G.; Haag, J. J.
- Science, Vol. 328, Issue 5986
Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory?
journal, September 2011
- Mommer, Liesje; van Ruijven, Jasper; Jansen, Corien
- Functional Ecology, Vol. 26, Issue 1
Contrasting root behaviour in two grass species: a test of functionality in dynamic heterogeneous conditions
journal, March 2011
- Mommer, Liesje; Visser, Eric J. W.; van Ruijven, Jasper
- Plant and Soil, Vol. 344, Issue 1-2
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
The plastic plant: root responses to heterogeneous supplies of nutrients
journal, April 2004
- Hodge, Angela
- New Phytologist, Vol. 162, Issue 1
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
Root Competition: Towards a Mechanistic Understanding
book, January 2003
- de Kroon, H.; Mommer, L.; Nishiwaki, A.
- Root Ecology
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
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
A Review of Forest Gap Models
journal, January 2001
- Bugmann, Harald
- Climatic Change, Vol. 51, Issue 3/4, p. 259-305
Evolutionarily Stable Strategy Carbon Allocation to Foliage, Wood, and Fine Roots in Trees Competing for Light and Nitrogen: An Analytically Tractable, Individual-Based Model and Quantitative Comparisons to Data
journal, February 2011
- Dybzinski, Ray; Farrior, Caroline; Wolf, Adam
- The American Naturalist, Vol. 177, Issue 2
Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete
journal, July 1999
- Hodge, A.; Robinson, D.; Griffiths, B. S.
- Plant, Cell and Environment, Vol. 22, Issue 7
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
In situ high-frequency observations of mycorrhizas
journal, June 2013
- Allen, Michael F.; Kitajima, Kuni
- New Phytologist, Vol. 200, Issue 1
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
Resource and non-resource root competition effects of grasses on early- versus late-successional trees
journal, May 2009
- Messier, Christian; Coll, Lluis; Poitras-Larivière, Amélie
- Journal of Ecology, Vol. 97, Issue 3
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
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
Burrowing by badgers (Meles meles) and foxes (Vulpes vulpes) changes soil conditions and vegetation in a European temperate forest
journal, November 2013
- Kurek, Przemysław; Kapusta, Paweł; Holeksa, Jan
- Ecological Research, Vol. 29, Issue 1
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
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
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)
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)
Works referencing / citing this record:
Fine root responses to temporal nutrient heterogeneity and competition in seedlings of two tree species with different rooting strategies
journal, February 2018
- Wang, Peng; Shu, Meng; Mou, Pu
- Ecology and Evolution, Vol. 8, Issue 6
Root diameter predicts the extramatrical hyphal exploration distance of the ectomycorrhizal fungal community
journal, April 2018
- Chen, Weile; Eissenstat, David M.; Koide, Roger T.
- Ecosphere, Vol. 9, Issue 4
Influences of plant interspecific competition and arbuscular mycorrhizal fungi on nitrogen form preference of an invasive plant
journal, October 2019
- Huangfu, Chaohe; Li, Keli; Hui, Dafeng
- Biogeochemistry, Vol. 145, Issue 3
Linkage of root morphology to anatomy with increasing nitrogen availability in six temperate tree species
journal, February 2018
- Wang, Wenna; Wang, Yan; Hoch, Günter
- Plant and Soil, Vol. 425, Issue 1-2
Competition between Zea mays genotypes with different root morphological and physiological traits is dependent on phosphorus forms and supply patterns
journal, March 2018
- Li, Hongbo; Zhang, Deshan; Wang, Xinxin
- Plant and Soil, Vol. 434, Issue 1-2
Roots and arbuscular mycorrhizal fungi are independent in nutrient foraging across subtropical tree species
journal, June 2019
- Liu, Bitao; Li, Liang; Rengel, Zed
- Plant and Soil, Vol. 442, Issue 1-2
Effects of morphology and stand structure on root biomass and length differed between absorptive and transport roots in temperate trees
journal, July 2019
- Wang, Yanan; Gao, Guoqiang; Wang, Na
- Plant and Soil, Vol. 442, Issue 1-2
The Responses of Forest Fine Root Biomass/Necromass Ratio to Environmental Factors Depend on Mycorrhizal Type and Latitudinal Region
journal, May 2018
- Wang, Cunguo; Chen, Zhao; Yin, Hong
- Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 5
Theory predicts plants grow roots to compete with only their closest neighbours
journal, October 2019
- Farrior, Caroline E.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1912
Plants maximize competition while minimizing competitors belowground: a theoretical analysis of incentives for root competition in space
posted_content, September 2018
- Farrior, Caroline E.
Nutrient foraging by mycorrhizas: From species functional traits to ecosystem processes
journal, January 2018
- Chen, Weile; Koide, Roger T.; Eissenstat, David M.
- Functional Ecology, Vol. 32, Issue 4
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
Distinct fine‐root responses to precipitation changes in herbaceous and woody plants: a meta‐analysis
journal, November 2019
- Wang, Peng; Huang, Kailing; Hu, Shuijin
- New Phytologist, Vol. 225, Issue 4
Susquehanna Shale Hills Critical Zone Observatory: Shale Hills in the Context of Shaver's Creek Watershed
journal, January 2018
- Brantley, Susan L.; White, Tim; West, Nicole
- Vadose Zone Journal, Vol. 17, Issue 1
Soil and Tree Nutrient Status of High Elevation Mixed Red Spruce (Picea rubens Sarg.) and Broadleaf Deciduous Forests
journal, December 2019
- Crim, Philip M.; McDonald, Louis M.; Cumming, Jonathan R.
- Soil Systems, Vol. 3, Issue 4
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)
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)