Abstract
Background and aims
Spatially segregating root systems is a fundamental mechanism by which plants can avoid competition for resources. Understory roots contribute substantially to total forest fine-root biomass, but the strategy of function-based fine root placement between trees and understory species at the plant community level is unknown. The aim of this study was to determine the differences between trees and understory plants in the deployment of fine roots.
Methods
We collected fine roots of trees and understory species in two subtropical coniferous forests, sorted the fine roots into absorptive and transport roots, determined the vertical placement of these two types of fine roots, and examined the abiotic and biotic factors that may regulate the horizontal allocation of fine roots.
Results
We found that the contribution of absorptive shrub roots to absorptive roots of the woody plants was higher than the contribution of total shrub fine roots to the total fine roots of the woody plants in the topsoil. Understory plants allocated a greater proportion of their absorptive roots to transport roots (RatioA/T) and more total fine-root biomass than trees in the topsoil. Trees had a lower RatioA/T in the topsoil; but increased their contribution of fine-root biomass to the total fine-root biomass and RatioA/T with depth. The proliferation of shrub fine roots in the topsoil was affected more by soil structure (rock-fragment content and bulk density) than by nearby stems, and the growth of tree fine roots was inhibited by nearby dense and/or large stems.
Conclusions
Our results provide evidence of an elaborate differentiation of root deployment between trees and understory plants. The roots of understory plants dominated the topsoil by possessing a higher branching capacity of absorptive roots than trees, filling the readily occupied macropores and being less affected by nearby stems. Trees enhance their resource foraging towards deeper soil by increasing their advantage of occupying soil volume and branching capacity of absorptive roots with depth. We also suggested that the roots of understory plants may affect ecosystemic carbon and nutrients cycling more than expected because of the disproportionately higher investment of absorptive roots in the topsoil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aschehoug ET, Callaway RM (2014) Morphological variability in tree root architecture indirectly affects coexistence among competitors in the understory. Ecology 95:1731–1736. https://doi.org/10.1890/13-1749.1
Bakker MR, Augusto L, Achat DL (2006) Fine root distribution of trees and understory in mature stands of maritime pine (Pinus pinaster) on dry and humid sites. Plant Soil 286:37–51. https://doi.org/10.1007/s11104-006-9024-4
Barnes PW, Archer S (1999) Tree-shrub interactions in a subtropical savanna parkland: competition or facilitation? J Veg Sci 10:525–536. https://doi.org/10.2307/3237187
Bolte A, Villanueva I (2006) Interspecific competition impacts on the morphology and distribution of fine roots in European beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) karst.). Eur J For Res 125:15–26. https://doi.org/10.1007/s10342-005-0075-5
Brassard BW, Chen HYH, Bergeron Y, Paré D (2011) Differences in fine root productivity between mixed- and single- species stands. Funct Ecol 25:238–246. https://doi.org/10.1111/j.1365-2435.2010.01769.x
Brassard BW, Chen HYH, Cavard X, Laganière J, Reich PB, Bergeron Y, Paré D, Yuan Z (2013) Tree species diversity increases fine root productivity through increased soil volume filling. J Ecol 101:210–219. https://doi.org/10.1111/1365-2745.12023
Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965. https://doi.org/10.1890/0012-9658(1997)078[1958:CAFASA]2.0.CO;2
Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570. https://doi.org/10.1146/annurev.ecolsys.28.1.545
Chen HYH, Brassard BW (2013) Intrinsic and extrinsic controls of fine root lifespan. Crit Rev Plant Sci 32:151–161. https://doi.org/10.1080/07352689.2012.734742
Chen WJ, Zhang QF, Cihlar J, Bauhus J, Price DT (2004) Estimating fine-root biomass and production of boreal and cool temperate forests using aboveground measurements: a new approach. Plant Soil 265:31–46. https://doi.org/10.1007/s11104-005-8503-3
Comas LH, Eissenstat DM (2009) Patterns in root trait variation among 25 co-existing North American forest species. New Phytol 182:919–928. https://doi.org/10.1111/j.1469-8137.2009.02799.x
Curt T, Lucot E, Bouchaud M (2001) Douglas-fir root biomass and rooting profile in relation to soils in amid-elevation area (Beaujolais mounts, France). Plant Soil 233:109–125. https://doi.org/10.1023/A:1010333308738
Diochon A, Kellman L, Beltrami H (2009) Looking deeper: an investigation of soil carbon losses following harvesting from a managed northeastern red spruce (Picea rubens Sarg.) forest chronosequence. For Ecol Manag 257:413–420. https://doi.org/10.1016/j.foreco.2008.09.015
Eissenstat DM (1992) Costs and benefits of constructing roots of small diameter. J Plant Nutr 15:763–782. https://doi.org/10.1080/01904169209364361
Eissenstat DM, Yanai RD (1997) The ecology of root lifespan. Adv Ecol Res 27:1–60. https://doi.org/10.1016/S0065-2504(08)60005-7
Epron D, Osawa A (2017) Fine roots: when anisotropy matters. Tree Physiol 37:693–696. https://doi.org/10.1093/treephys/tpx063
Fan PP, Guo DL (2010) Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil. Oecologia 163:509–515. https://doi.org/10.1007/s00442-009-1541-4
Fiès JC, Louvigny ND, Chanzy A (2002) The role of stones in soil water retention. Eur J Soil Sci 53:95–404. https://doi.org/10.1046/j.1365-2389.2002.00431.x
Finér L, Helmisaari HS, Lõhmus K, Majdi H, Brunner I, Børja I, Eldhuset T, Godbold D, Grebenc T, Konôpka B, Kraigher H, Möttönen MR, Ohashi M, Oleksyn J, Ostonen I, Uri V, Vanguelova E (2007) Variation in fine root biomass of three European tree species: beech (Fagus sylvatica L.), Norway spruce (Picea abies L. karst.) and scots pine (Pinus sylvestris L.). Plant Biosyst 141:394–405. https://doi.org/10.1080/11263500701625897
Finér L, Ohashi M, Noguchi K, Hirano Y (2011) Factors causing variation in fine root biomass in forest ecosystems. For Ecol Manag 261:265–277. https://doi.org/10.1016/j.foreco.2010.10.016
Frazer GW, Canham CD, Lertzman KP (1999) Gap light analyzer (GLA), version 2.0: imaging software to extract canopy structure and gap light transmission indices from true-color fisheye photographs. Copyright 1999: Simon Fraser University, Burnaby, BC, and the Institute of Ecosystem Studies, Millbrook, New York; (http://www.rem.sfu.ca/forestry/index.htm or http://www.ecostudies.org)
Freschet GT, Valverde-Barrantes OJ, Tucher CM, Craine JM, McCormack ML, Fort F, Blackwood CB, Urban-Mead KR, Iversen CM, Bonis A, Comas LH, Cornelissen JHC, Dong M, Guo DL, Hobbie SE, Holdaway RJ, Kembel SW, Makita N, Onipchenko VG, Picon-Cochard C, Reich PB, de la Riva EG, Smith SW, Soudzilovskaia NA, Tjoelker MG, Wardle DA, Roumet C (2017) Climate, soil and plant functional types as drivers of global fine-root trait variation. J Ecol 105:1182–1196. https://doi.org/10.1111/1365-2745.12769
Fu XL, Wang JL, Di YB, Wang HM (2015a) Differences in fine-root biomass of trees and understory vegetation among stand types in subtropical forests. PLoS One 10:e0128894. https://doi.org/10.1371/journal.pone.0128894
Fu XL, Yang FT, Wang JL, Di YB, Dai XQ, Zhang XY, Wang HM (2015b) Understory vegetation leads to changes in soil acidity and in microbial communities 27 years after reforestation. Sci Total Environ 502:280–286. https://doi.org/10.1016/j.scitotenv.2014.09.018
Fu XL, Wang JL, Wang HM, Dai XQ, Yang FT, Zhao M (2016) Response of the fine root production, phenology, and turnover rate of six shrub species from a subtropical forest to a soil moisture gradient and shading. Plant Soil 399:135–146. https://doi.org/10.1007/s11104-015-2686-z
Gargiulo L, Mele G, Terribile F (2016) Effect of rock fragments on soil porosity: a laboratory experiment with two physically degraded soils. Eur J Soil Sci 67:597–604. https://doi.org/10.1111/ejss.12370
Godbold DL, Fritz HW, Jentschke G, Meesenburg H, Rademacher P (2003) Root turnover and root necromass accumulation of Norway spuce (Picea abies) are affected by soil acidity. Tree Physiol 23:915–921. https://doi.org/10.1093/treephys/23.13.915
Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in along leaf pine forest. Oecologia 140:450–457. https://doi.org/10.1007/s00442-004-1596-1
Guo DL, Mitchell RJ, Withington JM, Fan PP, Hendricks JJ (2008) Endogenous and exogenous controls of root life span, mortality and nitrogen flux in a longleaf pine forest: root branch order predominates. J Ecol 96:737–745. https://doi.org/10.1111/j.1365-2745.2008.01385.x
Gwenzi W, Veneklaas EJ, Holmes KW, Bleby TM, Phillips IR, Hinz C (2011) Spatial analysis of fine root distribution on a recently constructed ecosystem in a water-limited environment. Plant Soil 344:255–272. https://doi.org/10.1007/s11104-011-0744-8
Hansson K, Helmisaari H, Sah SP, Lange H (2013) Fine root production and turnover of tree and understorey vegetation in scots pine, silver birch and Norway spruce stands in SW Sweden. For Ecol Manag 309:58–65. https://doi.org/10.1016/j.foreco.2013.01.022
Helmisaari HS, Makkonen K, Kellomäki S, Valtonen E, Mälkönen E (2002) Below- and above-ground biomass, production and nitrogen use in scots pine stand in eastern Finland. For Ecol Manag 165:317–326. https://doi.org/10.1016/S0378-1127(01)00648-X
Helmisaari HS, Derome J, Nöjd P, Kukkola M (2007) Fine root biomass in relation to site and stand characteristics in Norway spruce and scots pine stands. Tree Physiol 27:1493–1504. https://doi.org/10.1093/treephys/tpn042
Helmisaari HS, Saarsalmi A, Kukkola M (2009) Effects of wood ash and nitrogen fertilization on fine root biomass and soil and foliage nutrients in a Norway spruce stand in Finland. Plant Soil 314:121–132. https://doi.org/10.1007/s11104-008-9711-4
Hendrick RL, Pregitzer KS (1997) The relationship between fine root demography and the soil environment in northern hardwood forests. Ecoscience 4:99–105. https://doi.org/10.1080/11956860.1997.11682383
Hendricks JJ, Nadelhoffer KJ, Aber JD (1993) Assessing the role of fine roots in carbon and nutrient cycling. Trends Ecol Evol 8:174–178. https://doi.org/10.1016/0169-5347(93)90143-D
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x
Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411. https://doi.org/10.1007/BF00333714
Jentschke G, Drexhage M, Fritz HW, Fritz E, Schella B, Lee DH, Gruber F, Heimann J, Kuhr M, Schmidt J, Schmidt S, Zimmermann R, Godbold DL (2001) Does soil acidity reduce subsoil rooting in Norway spruce (Picea abies)? Plant Soil 237:91–108. https://doi.org/10.1023/A:1013305712465
Khetdan C, Chittamart N, Tawornpruek S, Kongkaew T, Onsamrarn W, Garré S (2017) Influence of rock fragments on hydraulic properties of Ultisols in Ratchaburi Province, Thailand. Geoderma Regional 10:21–28. https://doi.org/10.1016/j.geodrs.2017.04.001
Kou L, Jiang L, Fu X, Dai X, Wang H, Li S (2018) Nitrogen deposition increases root production and turnover but slows root decomposition in Pinus elliottii plantations. New Phytol 218:1450–1461. https://doi.org/10.1111/nph.15066
Leuschner C, Hertel D (2003) Fine root biomass of temperate forests in relation to soil acidity and fertility, climate, age and species. Progress Bot 64:405–438. https://doi.org/10.1007/978-3-642-55819-1_16
Leuschner C, Hertel D, Coner H, Buttner V (2001) Root competition between beech and oak: a hypothesis. Oecologia 126:276–284. https://doi.org/10.1007/s004420000507
Leuschner C, Hertel D, Schmid I, Koch O, Muhs A, Holscher D (2004) Stand fine root biomass and fine root morphology in old growth beech forests as a function of precipitation and soil fertility. Plant Soil 258:43–56. https://doi.org/10.1023/B:PLSO.0000016508.20173.80
Liu BT, Li H, Zhu B, Koide RT, Eissenstat DM, Guo DL (2015) Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species. New Phytol 208:125–136. https://doi.org/10.1111/nph.13434
Liu B, He J, Zeng F, Lei J, Arndt SK (2016) Life span and structure of ephemeral root modules of different functional groups from a desert system. New Phytol 211:103–112. https://doi.org/10.1111/nph.13880
Liu Y, Wang GL, Yu KX, Li P, **ao L, Liu GB (2018) A new method to optimize root order classification based on the diameter interval of fine root. Sci Rep 8. https://doi.org/10.1038/s41598-018-21248-6
Ma Z, Chen HYH (2016) Effects of species diversity on fine root productivity in diverse ecosystems: a global meta-analysis. Glob Ecol Biogeogr 25:1387–1396. https://doi.org/10.1111/geb.12488
Ma Z, Chen HYH (2017) Effects of species diversity on fine root productivity increase with stand development and associated mechanisms in a boreal forest. J Ecol 105:237–245. https://doi.org/10.1111/1365-2745.12667
Makita N, Hirano Y, Dannoura M, Kominami Y, Mizoguchi T, Ishii H, Kanazawa Y (2009) Fine root morphological traits determine variation in root respiration of Quercus serrata. Tree Physiol 29:579–585. https://doi.org/10.1007/s11104-006-6638-5
Makita N, Hirano Y, Mizoguchi T, Kominami Y, Dannoura M, Ishii H, Finer L, Kanazawa Y (2011) Very fine roots respond to soil depth: biomass allocation, morphology, and physiology in a broad-leaved temperate forest. Ecol Res 26:95–104. https://doi.org/10.1007/s11284-010-0764-5
Materechera SA, Alston AM, Kirby JM, Dexter AR (1992) Influence of root diameter on the penetration of seminal roots into a compacted subsoil. Plant Soil 144:297–303. https://doi.org/10.1007/BF00012888
McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2014) Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology 95:2224–2235. https://doi.org/10.1890/13-1942.1
McCormack ML, Dickie IA, Eissenstat DM, Guo DL, Helmisaari HS, Hobbie EA, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB, Leppalammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518. https://doi.org/10.1111/nph.13363
McMinn RG (1963) Characteristics of Douglas-fir root system. Can J Bot 41:105–122. https://doi.org/10.1139/b63-010
Millikin CS, Bledsoe CS (1999) Biomass and distribution of fine and coarse roots from blue oak (Quercus douglasii) trees in the northern Sierra Nevada foothills of California. Plant Soil 214:27–38. https://doi.org/10.1023/A:1004653932675
Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405. https://doi.org/10.1034/j.1600-0706.2003.12010.x
Moreno G, Cubera E (2008) Impact of stand density on water status and leaf gas exchange in Quercus ilex. For Ecol Manag 254:74–84. https://doi.org/10.1016/j.foreco.2007.07.029
Nilsson MC, Wardle DA (2005) Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Front Ecol Environ 3:421–428. https://doi.org/10.1890/1540-9295(2005)003[0421:UVAAFE]2.0.CO;2
Noguchi K, Sakata T, Mizoguchi T, Takahashi M (2005) Estimating the production and mortality of fine roots in a Japanese cedar (Cryptomeria japonica D. Don) plantation using a minirhizotron technique. J For Res 10:435–441. https://doi.org/10.1007/s10310-005-0163-x
Norby RJ, Ledford J, Reilly CD, Miller NE, O’Neill EG (2004) Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment. PNAS 101:9689–9693. https://doi.org/10.1073/pnas.0403491101
Nuszdorfer FC (1981) Bulk density. Taxonamic classification of humus forms in ecosystems of British Columbia. Edited by Klinka K, green RN, Trowbridge R, Lowe LE, min BC. For Land Manage Rep 8:49–51
Pregitzer KS (2008) Tree root architecture-form and function. New Phytol 180:562–564. https://doi.org/10.1111/j.1469-8137.2008.02648.x
Pregitzer KS, Kubiske ME, Yu CK, Hendrick RL (1997) Relationships among root branch order, carbon, and nitrogen in four temperate species. Oecologia 111:302–308. https://doi.org/10.1007/s004420050239
Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309. https://doi.org/10.2307/3100029
Rolo V, Moreno G (2012) Interspecific competition induces asymmetrical rooting profile adjustments in shrub-encroached open oak woodlands. Trees 26:997–1006. https://doi.org/10.1007/s00468-012-0677-8
Ruess RW, Hendrick RL, Burton AJ, Pregitzer KS, Sveinbjornssön B, Allen MF, Maurer GE (2003) Coupling fine root dynamics with ecosystem carbon cycling in black spruce forest of interior Alaska. Ecol Monogr 73:643–662. https://doi.org/10.1890/02-4032
Sauer TJ, Logsdon SD (2002) Hydraulic and physical properties of stony soils in a small watershed. Soil Sci Soc Am J 66:1947–1956. https://doi.org/10.2136/sssaj2002.1947
Sitch S, Smith B, Prentice IC, Arneth A, Bondeau A, Cramer W, Kaplan JO, Levis S, Lucht W, Sykes MT, Thonicke K, Venevsky S (2003) Evaluation of ecosystem dynamics, plant geography and terrestrial carbon cycling in the LPJ dynamic global vegetation model. Glob Chang Biol 9:161–185. https://doi.org/10.1046/j.1365-2486.2003.00569.x
Sun T, Dong L, Mao Z, Li Y (2015) Fine root dynamics of trees and understorey vegetation in a chronosequence of Betula platyphylla stands. For Ecol Manag 346:1–9. https://doi.org/10.1016/j.foreco.2015.02.035
Szota C, Veneklaas EJ, Koch JM, Lambers H (2007) Root architecture of jarrah (Eucalyptus marginata) trees in relation to post-mining deep rip** in Western Australia. Restor Ecol 15:65–73. https://doi.org/10.1111/j.1526-100X.2007.00294.x
Wang Y, Dong X, Wang H, Wang Z, Gu J (2015) Root tip morphology, anatomy, chemistry and potential hydraulic conductivity vary with soil depth in three temperate hardwood species. Tree Physiol 36:99–108. https://doi.org/10.1093/treephys/tpv094
Warrick AW (2002) Soil physics companion. CRC Press, Boca Raton
Yanai RD, Park BB, Hamburg SP (2006) The vertical and horizontal distribution of roots in northern hardwood stands of varying age. Can J For Res 36:450–459. https://doi.org/10.1139/x05-254
Yang FT, Feng ZM, Wang HM, Dai XQ, Fu XL (2017) Deep soil water extraction helps to drought avoidance but shallow soil water uptake during dry season controls the inter-annual variation in tree growth in four subtropical plantations. Agric For Meteorol 234:106–114. https://doi.org/10.1016/j.agrformet.2016.12.020
Yuan ZY, Chen HYH (2010) Fine root biomass, production, turnover rates, and nutrient contents in boreal Forest ecosystems in relation to species, climate, fertility, and stand age: literature review and meta-analyses. Crit Rev Plant Sci 29:204–221. https://doi.org/10.1080/07352689.2010.483579
Zhou ZC, Shangguan ZP (2007) Vertical distribution of fine roots in relation to soil factors in Pinus tabulaeformis Carr. Forest of the loess plateau of China. Plant Soil 291:119–129. https://doi.org/10.1007/s11104-006-9179-z
Acknowledgements
We thank Fengting Yang, ** Chen, Chuanpeng Cheng, Yuebao Di, MingjieXu, Xueli Mo, Zebing Du for help during field sampling and root sorting. This work was funded by the National Natural Science Foundations of China (31730014, 41671224), and the National Key Research and Development Program of China (2016YFD0600202).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Amandine Erktan
Rights and permissions
About this article
Cite this article
Jiang, P., Wang, H., Fu, X. et al. Elaborate differences between trees and understory plants in the deployment of fine roots. Plant Soil 431, 433–447 (2018). https://doi.org/10.1007/s11104-018-3778-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3778-3