Abstract
Key message
Understory dwarf bamboo mitigated soil N competition with co-existing canopy oak trees by foraging in deeper soils and increasing dependence on N forms that differ from those used by canopy trees.
Abstract
Nitrogen (N) competition among co-existing plant species utilizing different mycorrhiza types was explored through the investigation of N sources of oak trees and dwarf bamboo. Vertical distribution of fine roots, soil N pools, δ15N of leaves, and possible soil N sources and nitrate reductase activity (NRA) were all quantified. The fine roots of canopy trees were more concentrated in the surface soils than roots of the understory dwarf bamboo. Soil NH4+ and extractable organic N (EON) content (based on unit weight) decreased from the organic horizon (O horizon) to the deep soils, the size of the NH4+ pool per unit volume increased with soil depth, and the EON was approximately constant. Soil NO3− was not detected at any soil depth or was not significant in value, while NO3− captured by ion-exchange resin (IER) buried at a 10 cm soil depth and net nitrification were observed via laboratory incubation at all soil depths. The δ15N of the NH4+ and EON pools increased with soil depth and the δ15N of NO3− of IER was lower than that of other N forms, except for the δ15N of NH4+ in the O horizon. Furthermore, root NRA tended to be lower in canopy trees than in the understory, implying lower dependency on NO3− by canopy trees. The pattern of root distribution and mycorrhizal fungi association of the understory vegetation (as well as the high root NRA) suggested that dependence on N in deeper soils was higher in understory plants than in canopy trees. These findings indicate that understory vegetation mitigates soil N competition against co-existing canopy trees via the use of alternative N sources.
Similar content being viewed by others
References
Anderson IC, Genney DR, Alexander IJ (2014) Fine-scale diversity and distribution of ectomycorrhizal fungal mycelium in a Scots pine forest. New Phytol 201:1423–1430
Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545
Beevers L, Hageman RH (1969) Nitrate reduction in higher plants. Annu Rev Plant Physiol 20:495–522
Bloom AJ, Burger M, Asensio JSR, Cousins AB (2010) Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903
Brearley FQ (2013) Nitrogen stable isotopes indicate differences in nitrogen cycling between two contrasting Jamaican montane forests. Plant Soil 367:465–476
Cardinael R, Mao Z, Prieto I, Stokes A, Dupraz C, Kim JH, Jourdan C (2015) Competition with winter crops induces deeper rooting of walnut trees in a Mediterranean alley cropping agroforestry system. Plant Soil 391:219–235
Casciotti KL, Sigman DM, Hastings MG, Böhlke JK, Hilkert A (2002) Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal Chem 74:4905–4912
Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiol Rev 22:21–44
Courty PE, Buée M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault MP, Uroz S, Garbaye J (2010) The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biol Biochem 42:679–698
Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L (2015) Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26
Debiasi TV, Calzavara AK, da Silva LM, da Silva JG, Bianchini E, Pimenta JA, Stolf-Moreira R, Aidar MPM, Sodek L, Oliveira HC (2019) Nitrogen metabolism of Neotropical tree seedlings with contrasting ecological characteristics. Acta Physiol Plant 41:131
DeLuca T, Nilsson MC, Zackrisson O (2002) Nitrogen mineralization and phenol accumulation along a fire chronosequence in northern Sweden. Oecologia 133:206–214
Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121–126
Fukuchi S, Obase K, Tamai Y, Yajima T, Miyamoto T (2011) Vegetation and colonization status of mycorrhizal and endophytic fungi in plant species on acidic barren at crater basin of volcano Esan in Hokkaido, Japan. Eurasian J For Res 14:1–11
Fukuzawa K, Shibata H, Takagi K, Nomura M, Kurima N, Fukazawa T, Satoh F, Sasa K (2006) Effects of clear-cutting on nitrogen leaching and fine root dynamics in a cool-temperate forested watershed in northern Japan. For Ecol Manag 225:257–261
Fukuzawa K, Shibata H, Takagi K, Satoh F, Koike T, Sasa K (2013) Temporal variation in fine-root biomass, production and mortality in a cool temperate forest covered with dense understory vegetation in northern Japan. For Ecol Manag 310:700–710
Fukuzawa K, Shibata H, Takagi K, Satoh F, Koike T, Sasa K (2015) Roles of dominant understory Sasa bamboo in carbon and nitrogen dynamics following canopy tree removal in a cool-temperate forest in northern Japan. Plant Species Biol 30:104–115
Gherardi LA, Sala OE, Yahdjian L (2013) Preference for different inorganic nitrogen forms among plant functional types and species of the Patagonian steppe. Oecologia 173:1075–1081
Hiura T (2001) Stochasticity of species assemblage of canopy trees and understorey plants in a temperate secondary forest created by major disturbances. Ecol Res 16:887–893
Hobbie EA, Högberg H (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382
Hobbie EA, Ouimette AP (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95:355–371
Hobbie EA, Macko SA, Williams M (2000) Correlations between foliar delta15N and nitrogen concentrations may indicate plant-mycorrhizal interactions. Oecologia 122:273–283
Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299
Högberg P (1997) Tansley review no. 95 15N natural abundance in soil–plant systems. New Phytol 137:179–203
Holmes RM, McClelland JW, Sigman DM, Fry B, Peterson BJ (1998) Measuring 15N–NH4+ in marine, estuarine and fresh waters: an adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar Chem 60:235–243
Hosokawa N, Isobe K, Urakawa R, Tateno R, Fukuzawa K, Watanabe T, Shibata H (2017) Soil freeze–thaw with root litter alters N transformations during the dormant season in soils under two temperate forests in northern Japan. Soil Biol Biochem 114:270–278
Houlton BZ, Sigman DM, Schuur EA, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA 104:8902–8906
Isobe K, Oka H, Watanabe T, Tateno R, Urakawa R, Liang C, Senoo K, Shibata H (2018) High soil microbial activity in the winter season enhances nitrogen cycling in a cool-temperate deciduous forest. Soil Biol Biochem 124:90–100
IUSS Working group WRB (2015) World reference base for soil resources 2014 (Update 2015), International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome
Kayama M, Koike T (2018) Growth characteristics of dwarf bamboo distributed in the northern part of Japan. In: Abdul Khalil HPS (ed) Bamboo-current and future prospects. IntechOpen, London, pp 185–199
Keeney DR, Nelson DW (1982) Nitrogen—inorganic forms. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis part 2. American Society of Agronomy, Madison, pp 643–698
Koba K, Tokuchi N, Yoshioka T, Hobbie EA, Iwatsubo G (1998) Natural abundance of nitrogen-15 in a forest soil. Soil Sci Soc Am J 62:778–781
Koba K, Hirobe M, Koyama L, Kohzu A, Tokuchi N, Nadelhoffer KJ, Wada E, Takeda H (2003) Natural 15N abundance of plants and soil N in a temperate coniferous forest. Ecosystems 6:457–469
Koba K, Isobe K, Takebayashi Y et al (2010) Delta15N of soil N and plants in a N-saturated, subtropical forest of southern China. Rapid Commun Mass Spectrom 24:2499–2506
Koba K, Fang Y, Mo J et al (2012) The 15N natural abundance of the N lost from an N-saturated subtropical forest in southern China. J Geophys Res 117:G02015
Kohzu A, Matsui K, Yamada T, Sugimoto A, Fujita N (2003) Significance of rooting depth in mire plants: evidence from natural N abundance. Ecol Res 18(3):257–266
Koyama L, Tokuchi N (2003) Effects of NO3− availability on NO3− use in seedlings of three woody shrub species. Tree Physiol 23:281–288
Larsen KS, Michelsen A, Jonasson S, Beier C, Grogan P (2012) Nitrogen uptake during fall, winter and spring differs among plant functional groups in a subarctic heath ecosystem. Ecosystems 15(6):927–939
Lee JA, Stewart GR (1978) Ecological aspects of nitrogen assimilation. Adv Bot Res 6:1–43
Lei TT, Koike T (1998) Functional leaf phenotypes for shaded and open environments of a dominant dwarf bamboo (Sasa senanensis) in northern Japan. Int J Plant Sci 159:812–820
Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620
Liu XY, Koba K, Koyama L et al (2018) Nitrate is an important nitrogen source for Arctic tundra plants. Proc Natl Acad Sci USA 115:3398–3403
Mayor J, Bahram M, Henkel T, Buegger F, Pritsch K, Tedersoo L (2015) Ectomycorrhizal impacts on plant nitrogen nutrition: emerging isotopic patterns, latitudinal variation and hidden mechanisms. Ecol Lett 18:96–107
McIlvin MR, Casciotti KL (2011) Technical updates to the bacterial method for nitrate isotopic analyses. Anal Chem 83:1850–1856
Nadelhoffer K, Shave G, Fry B, Giblin A, Johnson L, McKane R (1996) 15N natural abundances and N use by tundra plants. Oecologia 107:386–394
Nakayama M, Tateno R (2018) Solar radiation strongly influences the quantity of forest tree root exudates. Trees-Struct Funct 32:871–879
Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48
Nordin A, Högberg P, Näsholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132
Obase K, Tamai Y, Yajima T, Miyamoto T (2007) Mycorrhizal associations in woody plant species at the Mt. Usu volcano, Japan. Mycorrhiza 17:209–215
Oliveira HC, da Silva LMI, de Freitas LD, Debiasi TV, Marchiori NM, Aidar MPM, Bianchini E, Pimenta JA, Stolf-Moreira R (2017) Nitrogen use strategies of seedlings from neotropical tree species of distinct successional groups. Plant Physiol Biochem 114:119–127
Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Schmull M, Thomas FM (2000) Morphological and physiological reactions of young deciduous trees (Quercus robur L., Q. petraea [Matt.] Liebl., Fagus sylvatica L.) to waterlogging. Plant Soil 225:227–242
Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Böhlke J (2001) A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73:4145–4153
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
Takahashi M, Higaki A, Nohno M, Kamada M, Okamura Y, Matsui K, Kitani S, Morikawa H (2005) Differential assimilation of nitrogen dioxide by 70 taxa of roadside trees at an urban pollution level. Chemosphere 61:633–639
Takebayashi Y, Koba K, Sasaki Y, Fang Y, Yoh M (2010) The natural abundance of 15N in plant and soil-available N indicates a shift of main plant N resources to NO3− from NH4+ along the N leaching gradient. Rapid Commun Mass Spectrom 24:1001–1008
Tanaka-Oda A, Kenzo T, Inoue Y, Yano M, Koba K, Ichie T (2016) Variation in leaf and soil δ15N in diverse tree species in a lowland dipterocarp rainforest, Malaysia. Trees-Struct Funct 30:509–522
Tateno R, Osada N, Terai M, Tokuchi N, Takeda H (2005) Inorganic nitrogen source utilization by Fagus crenata on different soil types. Trees-Struct Funct 19:477–481
Tateno R, Imada S, Watanabe T, Fukuzawa K, Shibata H (2019) Reduced snow cover changes nitrogen use in canopy and understory vegetation during the subsequent growing season. Plant Soil 438:157–172
Thomas FM, Hilker C (2000) Nitrate reduction in leaves and roots of young pedunculate oaks (Quercus robur) growing on different nitrate concentrations. Environ Exper Bot 43:19–32
Truax B, Lambert F, Gagnon D, Chevrier N (1994) Nitrate reductase and glutamine synthetase activities in relation to growth and nitrogen assimilation in red oak and red ash seedlings: effects of N-forms, N concentration and light intensity. Trees-Struct Funct 9:12–18
Urakawa R, Ohte N, Shibata H et al (2015) Biogeochemical nitrogen properties of forest soils in the Japanese archipelago. Ecol Res 30:1–2
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115
Watanabe T, Fukuzawa K, Shibata H (2013) Temporal changes in litterfall, litter decomposition and their chemical composition in Sasa dwarf bamboo in a natural forest ecosystem of northern Japan. J For Res 18:129–138
Watanabe T, Tateno R, Imada S et al (2019) The effect of a freeze–thaw cycle on dissolved nitrogen dynamics and its relation to dissolved organic matter and soil microbial biomass in the soil of a northern hardwood forest. Biogeochemistry 142:319–338
Acknowledgements
We thank members of the for Hokkaido Forest station, Field Science Education and Research Center, Kyoto University for cooperation and logistics at the field site and laboratory. We also thank to Dr. Keitaro Fukushima and Ms. Chikae Tatsumi and the members of Center for Ecological Research, Kyoto University and FFPRI for isotope measurements. This work was supported by JSPS-KAKENHI (NO. 26292085, 16H04937, and 18H02241). This work was also supported by Joint Usage/Research Grant of Center for Ecological Research, Kyoto University. We would like to thank Editage (http://www.editage.jp) for English language editing.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Des Rochers.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Tateno, R., Nakayama, M., Yano, M. et al. Nitrogen source utilization in co-existing canopy tree and dwarf bamboo in a northern hardwood forest in Japan. Trees 34, 1047–1057 (2020). https://doi.org/10.1007/s00468-020-01980-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-020-01980-1