Abstract
Purpose
The lack of synchronous studies on fine roots and fungal hyphae makes it difficult to gain insight into changes in how mycorrhizal trees search for nutrients under reduced precipitation and increased nitrogen deposition.
Methods
We applied a modified version of the ingrowth bag approach to estimate the community-level responses of fine roots and fungal hyphae to long-term changes in nitrogen and water availability in a mixed mature forest.
Results
Water reduction, nitrogen addition and the two treatments applied in combination decreased root length density, root biomass and fungal hyphal length density, with the lowest values occurring in the combined treatment. Compared with fine roots in the control treatment, fine roots in the water reduction treatment had a thinner diameter, lower branching intensity and a greater specific root length. Fungal hyphae in the combined treatment had significantly greater diameters than in the control treatment at 0–10 cm soil depths. Root length density, root biomass, root branching intensity and hyphal length density significantly decreased with increasing soil depth. In contrast, hyphal diameter increased with increasing soil depth. Fungal hyphal length density was positively related to root length density but negatively related to hyphal diameter.
Conclusion
Forest fine roots and fungal hyphae respond plastically to soil water and nitrogen availability. An integrative and simultaneous understanding of both root and hyphal trait plasticity can provide better insights into the resource acquisition strategies of trees experiencing environmental changes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Data used in this article will be available as part of the Fine-Root Ecology Database.
References
Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297. https://doi.org/10.2136/vzj2006.0068
Allen MF (2009) Water relations in the mycorrhizosphere. In: Lüttge U, Beyschlag W, Büdel B, Francis D (eds) Progress in botany. Springer, Berlin, pp 257–276. https://doi.org/10.1007/978-3-540-68421-3_12
Bååth E, Söderström B (1979) The significance of hyphal diameter in calculation of fungal biovolume. Oikos 11–14. https://doi.org/10.2307/3544505
Bae K, Fahey TJ, Yanai RD, Fisk M (2015) Soil nitrogen availability affects belowground carbon allocation and soil respiration in northern hardwood forests of New Hampshire. Ecosystems 18:1179–1191. https://doi.org/10.1007/s10021-015-9892-7
Baier R, Ingenhaag J, Blaschke H, Göttlein A, Agerer R (2006) Vertical distribution of an ectomycorrhizal community in upper soil horizons of a young Norway spruce (Picea abies [L.] Karst.) stand of the Bavarian Limestone Alps. Mycorrhiza 16:197–206. https://doi.org/10.1007/s00572-006-0035-z
Brunner I et al (2013) Fine-root turnover rates of European forests revisited: an analysis of data from sequential coring and ingrowth cores. Plant Soil 362:357–372. https://doi.org/10.1007/s11104-012-1313-5
Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. https://doi.org/10.3389/fpls.2015.00547
Brunner I, Herzog C, Galiano L, Gessler A (2019) Plasticity of fine-root traits under long-term irrigation of a water-limited Scots pine forest. Front Plant Sci 10:701. https://doi.org/10.3389/fpls.2019.00701
Chen W, Koide RT, Adams TS, DeForest JL, Cheng L, Eissenstat DM (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proc Natl Acad Sci USA 113:8741–8746. https://doi.org/10.1073/pnas.1601006113
Cheng L et al (2016) Mycorrhizal fungi and roots are complementary in foraging within nutrient patches. Ecology 2815–2823. https://doi.org/10.1002/ecy.1514
Dai L et al (2013) Effects of climate change on biomass carbon sequestration in old-growth forest ecosystems on Changbai Mountain in Northeast China. For Ecol Manage 300:106–116. https://doi.org/10.1016/j.foreco.2012.06.046
Dickie IA, Xu B, Koide RT (2002) Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytol 156:527–535. https://doi.org/10.1046/j.1469-8137.2002.00535.x
Essene AL, Shek KL, Lewis JD, Peay KG, McGuire KL (2017) Soil type has a stronger role than dipterocarp host species in shaping the ectomycorrhizal fungal community in a Bornean lowland tropical rain forest. Front Plant Sci 8(1):1828. https://doi.org/10.3389/fpls.2017.01828
Fabião A, Persson HÅ, Steen E (1985) Growth dynamics of superficial roots in Portuguese plantations of Eucalyptus globulus Labill. studied with a mesh bag technique. Plant Soil 83:233–242. https://doi.org/10.1007/BF02184295
Flower-Ellis JGK, Persson H (1980) Investigation of structural properties and dynamics of scots pine stands. Ecol Bull:125–138
Fort F, Freschet GT (2020) Plant ecological indicator values as predictors of fine-root trait variations. J Ecol 108:1565–1577. https://doi.org/10.1111/1365-2745.13368
Freschet GT et al (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
Friese CF, Allen MF (1991) The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia 83:409–418. https://doi.org/10.1080/00275514.1991.12026030
Geng S, Chen Z, Ma S, Feng Y, Zhang L, Zhang J, Han S (2020) Throughfall reduction diminished the enhancing effect of N addition on soil N leaching loss in an old, temperate forest. Environ Pollut 261:114090. https://doi.org/10.1016/j.envpol.2020.114090
Gu J, Xu Y, Dong X, Wang H, Wang Z (2014) Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species. Tree Physiol 34:415–425. https://doi.org/10.1093/treephys/tpu019
Guo W et al (2018) Effects of nitrogen addition on mycorrhizal fungi community structure and diversity of emopenPinus koraiensisemclose and emopenFraxinus mandshuricaemclose in Changbai Mountain. Ecol Environ Sci 27:10–17
Hagenbo A, Piñuela Y, Castaño C, MartínezdeAragón J, de Miguel S, Alday JG, Bonet JA (2021) Production and turnover of mycorrhizal soil mycelium relate to variation in drought conditions in Mediterranean emopenPinus pinasteremclose, emopenPinus sylvestrisemclose and emopenQuercus ilexemclose forests. New Phytol 230(4):1609–1622. https://doi.org/10.1111/nph.17012
Harpole WS, Potts DL, Suding KN (2007) Ecosystem responses to water and nitrogen amendment in a California grassland. Glob Chang Biol 13:2341–2348. https://doi.org/10.1111/j.1365-2486.2007.01447.x
Hasibeder R, Fuchslueger L, Richter A, Bahn M (2014) Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytol 205:1117–1127. https://doi.org/10.1111/nph.17012
Hunt GA, Fogel R (1983) Fungal hyphal dynamics in a western Oregon Douglas-fir stand. Soil Biol Biochem 15:641–649. https://doi.org/10.1016/0038-0717(83)90027-5
Joslin JD, Wolfe MH, Hanson PJ (2000) Effects of altered water regimes on forest root systems. New Phytol 147:117–129. https://doi.org/10.1046/j.1469-8137.2000.00692.x
Juniper S, Abbott L (2006) Soil salinity delays germination and limits growth of hyphae from propagules of arbuscular mycorrhizal fungi. Mycorrhiza 16:371–379. https://doi.org/10.1007/s00572-006-0046-9
Kårén O, Nylund J-E (1997) Effects of ammonium sulphate on the community structure and biomass of ectomycorrhizal fungi in a Norway spruce stand in southwestern Sweden. Can J Bot 75:1628–1642. https://doi.org/10.1139/b97-875
Lü CQ, Tian HQ (2007) Spatial and temporal patterns of nitrogen deposition in China: synthesis of observational data. J Geophys Res 112:D22S05. https://doi.org/10.1029/2006JD007990
Lilleskov EA, Kuyper TW, Bidartondo MI, Hobbie EA (2019) Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: a review. Environ Pollut 246:148–162
Majdi H, Persson H (1995) Effects of ammonium sulphate application on the chemistry of bulk soil, rhizosphere, fine roots and fine-root distribution in a Picea abies (L.) Karst Stand. Plant Soil 168:151–160. https://doi.org/10.1007/BF00029323
Majdi H, Truus L, Johansson U, Nylund J-E, Wallander H (2008) Effects of slash retention and wood ash addition on fine root biomass and production and fungal mycelium in a Norway spruce stand in SW Sweden. For Ecol Manage 255:2109–2117. https://doi.org/10.1016/j.foreco.2007.12.017
McCormack M, Iversen C (2019) Physical and functional constraints on viable belowground acquisition strategies. Front Plant Sci 10:1215. https://doi.org/10.3389/fpls.2019.01215
McCormack ML, Kaproth MA, Cavender-Bares J, Carlson E, Hipp AL, Han Y, Kennedy PG (2020) Climate and phylogenetic history structure morphological and architectural trait variation among fine-root orders. New Phytol 228(6):1824–1834. https://doi.org/10.1111/nph.16804
McGuire KL, Allison SD, Fierer N, Treseder KK (2013) Ectomycorrhizal-dominated boreal and tropical forests have distinct fungal communities, but analogous spatial patterns across soil horizons. PLoS ONE 8:e68278. https://doi.org/10.1371/journal.pone.0068278
Meier I, Leuschner C (2008) Belowground drought response of European beech: fine root biomass and carbon partitioning in 14 mature stands across a precipitation gradient. Glob Chang Biol 14:2081–2095. https://doi.org/10.1111/j.1365-2486.2008.01634.x
Nadelhoffer KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147:131–139. https://doi.org/10.1046/j.1469-8137.2000.00677.x
Neumann J, Matzner E (2013) Biomass of extramatrical ectomycorrhizal mycelium and fine roots in a young Norway spruce stand-a study using ingrowth bags with different substrates. Plant Soil 371:435–466. https://doi.org/10.1007/s11104-013-1701-5
Nilsson LO, Wallander H (2003) Production of external mycelium by ectomycorrhizal fungi in a norway spruce forest was reduced in response to nitrogen fertilization. New Phytol 158:409–416. https://doi.org/10.1046/j.1469-8137.2003.00728.x
Osono T (2015) Hyphal length in the forest floor and soil of subtropical, temperate, and subalpine forests. J For Res 20:69–76. https://doi.org/10.1007/s10310-014-0461-2
Ostonen I et al (2007) Specific root length as an indicator of environmental change. Plant Biosyst 141:426–442. https://doi.org/10.1080/11263500701626069
Parrent JL, Vilgalys R (2007) Biomass and compositional responses of ectomycorrhizal fungal hyphae to elevated CO2 and nitrogen fertilization. New Phytol 176:164–174. https://doi.org/10.1111/j.1469-8137.2007.02155.x
Persson H (1983) The distribution and productivity of fine roots in boreal forests. Plant Soil 71:87–101. https://doi.org/10.1007/BF02182644
Persson H, Ahlström K, Clemensson-Lindell A (1997) Fine-root response to nitrogen manipulation in three Norway spruce catchment areas. Stapfia 50:309–316
Persson H, Ahlström K, Clemensson-Lindell A (1998) Nitrogen addition and removal at Gårdsjön-effects on fine-root growth and fine-root chemistry. For Ecol Manage 101:199–205
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/10.1890/0012-9615(2002)072[0293:FRAONN]2.0.CO;2
Schäfer H, Ataka M, Dannoura M, Osawa A (2018) Evidence for the coupling of extraradical mycorrhizal hyphae production to plant C assimilation in Japanese warm-temperate forest of arbuscular mycorrhizal and ectomycorrhizal tree species. Eur J Soil Biol 88:73–79. https://doi.org/10.1016/j.ejsobi.2018.07.002
Sims SE, Hendricks JJ, Mitchell RJ, Kuehn KA, Pecot SD (2007) Nitrogen decreases and precipitation increases ectomycorrhizal extramatrical mycelia production in a longleaf pine forest. Mycorrhiza 17:299–309. https://doi.org/10.1007/s00572-007-0105-x
Sylvia DM (1992) Quantification of external hyphae of vesicular-arbuscular mycorrhizal fungi. In: Norris JR, Read DJ, Varma AK (eds) Methods in microbiology, vol 24. Academic Press, pp 53–65. https://doi.org/10.1016/S0580-9517(08)70086-2
Valliere JM, Allen EB (2016) Interactive effects of nitrogen deposition and drought-stress on plant-soil feedbacks of Artemisia californica seedlings. Plant Soil 403:277–290. https://doi.org/10.1007/s11104-015-2776-y
Vogt K, Persson H (1991) Measuring growth and development of roots. In: Lassoie JP, Hinckley TM (eds) Techniques and approaches in forest tree ecophysiology. CRC Press, Boca Raton, pp 477–501
Wallander H (2006) External mycorrhizal mycelia–the importance of quantification in natural ecosystems. New Phytol 171:240–242
Wallander H, Ekblad A, Bergh J (2011) Growth and carbon sequestration by ectomycorrhizal fungi in intensively fertilized Norway spruce forests For Ecol. Manage 262:999–1007. https://doi.org/10.1016/j.foreco.2011.05.035
Wallander H, Göransson H, Rosengren U (2004) Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139:89–97. https://doi.org/10.1007/s00442-003-1477-z
Wallander H, Nilsson LO, Hagerberg D, Bååth E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151:753–760. https://doi.org/10.1046/j.0028-646x.2001.00199.x
Wang CK (2006) Biomass allometric equations for 10 co-occurring tree species in Chinese temperate forests. For Ecol Manage 222:9–16. https://doi.org/10.1016/j.foreco.2005.10.074
Wang C et al (2017) Six-year nitrogen–water interaction shifts the frequency distribution and size inequality of the first-order roots of Fraxinus mandschurica in a mixed mature Pinus koraiensis forest. Front Plant Sci 8:1691. https://doi.org/10.3389/fpls.2017.01691
Wang C, Han S, Zhou Y, Zhang J, Zheng X, Dai G, Li M-H (2016) Fine root growth and contribution to soil carbon in a mixed mature Pinus koraiensis forest. Plant Soil 400:275–284. https://doi.org/10.1007/s11104-015-2724-x
Wang C, Zong S, Li M-H (2019a) The contrasting responses of mycorrhizal fungal mycelium associated with woody plants to multiple environmental factors. Forests 10:973. https://doi.org/10.3390/f10110973
Wang CG, Han SJ, Zhou YM, Yan CF, Cheng XB, Zheng XB, Li MH (2012) Responses of fine roots and soil N availability to short-term nitrogen fertilization in a broad-leaved Korean pine mixed forest in northeastern China. PLoS ONE 7:e31042. https://doi.org/10.1371/journal.pone.0031042
Wang W, Mo Q, Han X, Hui D, Shen W (2019b) Fine root dynamics responses to nitrogen addition depend on root order, soil layer, and experimental duration in a subtropical forest. Biol Fertility Soils 55:723–736
Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3–an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259. https://doi.org/10.1111/j.2041-210X.2011.00153.x
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291
Weemstra M, Kiorapostolou N, van Ruijven J, Mommer L, de Vries J, Sterck F (2020) The role of fine-root mass, specific root length and lifespan in tree performance: a whole-tree exploration. Funct Ecol 34:575–585. https://doi.org/10.1111/1365-2435.13520
Yan G et al (2019) Nitrogen deposition and decreased precipitation altered nutrient foraging strategies of three temperate trees by affecting root and mycorrhizal traits. Catena 181:104094. https://doi.org/10.1016/j.catena.2019.104094
Yu D et al (2011) Climatic effects on radial growth of major tree species on Changbai Mountain. Ann For Sci 68:921. https://doi.org/10.1007/s13595-011-0098-7
Zadworny M, McCormack ML, Żytkowiak R, Karolewski P, Mucha J, Oleksyn J (2017) Patterns of structural and defense investments in fine roots of Scots pine (Pinus sylvestris L.) across a strong temperature and latitudinal gradient in Europe. Glob Chang Biol 23:1218–1231. https://doi.org/10.1111/gcb.13514
Zhang X et al (2020) Effects of long-term nitrogen addition and decreased precipitation on the fine root morphology and anatomy of the main tree species in a temperate forest For Ecol. Manage 455:117664. https://doi.org/10.1016/j.foreco.2019.117664
Zhang Z, Yuan Y, Liu Q, Yin H (2019) Plant nitrogen acquisition from inorganic and organic sources via root and mycelia pathways in ectomycorrhizal alpine forests. Soil Biol Biochem 136:107517. https://doi.org/10.1016/j.soilbio.2019.06.013
Zheng J, Guo R, Li D, Zhang J, Han S (2017) Nitrogen addition, drought and mixture effects on litter decomposition and nitrogen immobilization in a temperate forest. Plant Soil 416(1–2):165–179. https://doi.org/10.1007/s11104-017-3202-4
Zou Y, Zhang D, Liu C, Wu Q (2019) Relationship between mycorrhizae and root hairs Pakistan. J Bot 51:727–733. https://doi.org/10.30848/PJB2019-2(39)
Acknowledgements
We thank Dr. Melissa Dawes for help editing the manuscript and Lufu Zhao, Fenghua Wang and Fuxian Liu for their assistance in the field and laboratory. This work was supported by the National Key R&D Program of China (Grant No. 2019YFA0607301) and the Natural Science Foundation of China (Grant Nos. 41971052, U19A2023 and 31500354).
Funding
This work was supported by the National Key R&D Program of China (Grant no. 2019YFA0607301) and the Natural Science Foundation of China (Grant nos. 41971052, U19A2023 and 31500354).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by CW, IB, WG, ZC and M-HL. The first draft of the manuscript was written by CW and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Responsible Editor: Michael Luke McCormack.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, C., Brunner, I., Guo, W. et al. Effects of long-term water reduction and nitrogen addition on fine roots and fungal hyphae in a mixed mature Pinus koraiensis forest. Plant Soil 467, 451–463 (2021). https://doi.org/10.1007/s11104-021-05092-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-05092-8