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Nitrogen uptake and nitrogen use efficiency above and below ground along a topographic gradient of soil nitrogen availability

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Abstract

Nitrogen (N) uptake and nitrogen use efficiency (NUE) are closely related through feedback mechanisms to soil N availability and N cycling in forested ecosystems. We investigated N uptake and NUE not only at the leaf, litterfall, and aboveground levels but also belowground and whole stand levels along a topographic gradient of soil N availability in a cool temperate deciduous forest in Japan. In this study, we addressed how whole stand level N uptake and NUE affect C and N cycling in forested ecosystems. At the leaf, litterfall, and aboveground levels, N uptake decreased and NUE increased with decreasing soil N availability. This pattern resulted from decreasing leaf N concentrations and increasing N resorption efficiencies as soil N availability declined. Low N concentrations in litterfall may have resulted in little soil N being available to plants, due to microbial immobilization. In contrast, when belowground components were included, N uptake and NUE were not correlated with soil N availability. This was mainly due to higher levels of fine root production when soil N availability was low. Higher fine root allocation can result in a high input of detritus to decomposer systems and, thus, contribute to accumulation of soil organic matter and immobilization by microbes, which may result in further soil N availability decline. Our results suggest that allocation to the fine root rather than whole stand level NUE is important for C and N cycling in forested ecosystems, as is the feedback mechanism in which litterfall level NUE shifts with changes in the N concentration of litterfall.

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References

  • Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  CAS  Google Scholar 

  • Aerts R, de Caluwe H (1994) Nitrogen use efficiency of Carex species in relation to nitrogen supply. Ecology 75:2362–2372

    Google Scholar 

  • Aerts R, Bakker C, de Caluwe H (1992) Root turnover as determinant of the cycling of C, N, and P in a dry heathland ecosystem. Biogeochemistry 15:175–190

    Article  CAS  Google Scholar 

  • Aikawa T, Tateno R, Takeda H (2002) Leaf phenology along a slope in a cool temperate deciduous forest. For Res, Kyoto 74:21–33 (in Japanese with English summary)

    Google Scholar 

  • Berendse F, Aerts R (1987) Nitrogen-use efficiency: a biologically meaningful definition? Funct Ecol 1:293–296

    Google Scholar 

  • Birk EM, Vitousek PM (1986) Nitrogen availability and nitrogen use efficiency in loblolly pine stands. Ecology 67:69–79

    Article  Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • Eckstein RL, Karlsson PS, Weih M (1999) Leaf life span and nutrient resorption as determinants of plant nutrient conservation in temperate-arctic region. New Phytol 143:177–189

    Article  Google Scholar 

  • Edwards NT, Harris WF (1977) Carbon cycling in a mixed deciduous forest floor. Ecology 58:431–437

    Article  CAS  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  PubMed  Google Scholar 

  • Enoki T, Kawaguchi H, Iwatsubo G (1997) Nutrient-uptake and nutrient-use efficiency of Pinus hunbergii Parl. along a topographical gradient of soil nutrient availability. Ecol Res 12:191–199

    Article  CAS  Google Scholar 

  • Finzi AC, van Breemen N, Canham CD (1998) Canopy tree–soil interactions within temperate forests: species effects on carbon and nitrogen. Ecol Appl 8:440–446

    Google Scholar 

  • Finzi AC, Norby RJ, Calfapietra C, Gallet-Budynek A, Gielen B, Holmes WE, Hoosbeek MR, Iversen CM, Jackson RB, Kubiske ME, Ledford J, Liberloo M, Oren R, Polle A, Pritchard S, Zak DR, Schlesinger WH, Ceulemans R (2007) Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proc Natl Acad Sci USA 104:14014–14019

    Article  CAS  PubMed  Google Scholar 

  • Franklin O, McMurtrie RE, Iversen CM, Crous KY, Finzi AC, Tissue DT, Ellsworth DS, Oren R, Norby RJ (2009) Forest fine-root production and nitrogen use under elevated CO2: contrasting responses in evergreen and deciduous trees explained by a common principle. Glob Change Biol 15:132–144

    Article  Google Scholar 

  • Fukasawa Y, Osono T, Takeda H (2005) Small-scale variation in chemical property within logs of Japanese beech in relation to spatial distribution and decay ability of fungi. Mycoscience 46:209–214

    Article  CAS  Google Scholar 

  • Garten CT Jr, Huston MA, Thoms CA (1994) Topographic variation of soil nitrogen dynamics at Walker Branch watershed, Tennessee. For Sci 40:497–512

    Google Scholar 

  • Giesler R, Högberg M, Högberg P (1998) Soil chemistry and plants in Fennoscandian boreal forest as exemplified by a local gradient. Ecology 79:119–137

    Article  Google Scholar 

  • Gower ST, Vogt KA, Grier CC (1992) Carbon dynamics of Rocky Mountain Douglas-fir: influence of water and nutrient availability. Ecol Monogr 62:43–65

    Article  Google Scholar 

  • Grier CC, Vogt KA, Keyes MR, Edmonds RL (1981) Biomass distribution and above- and below-ground production in young and mature Abies amabilis zone ecosystems of the Washington Cascades. Can J For Res 11:155–167

    Article  Google Scholar 

  • Harris WF, Kinerson RS Jr, Edwards NT (1977) Comparison of belowground biomass of natural deciduous forest and loblolly pine plantations. Pedobiologia 17:369–381

    Google Scholar 

  • Hendrick RL, Pregitzer KS (1993) The dynamics of fine root length, biomass, and nitrogen content in two northern hardwood ecosystems. Can J For Res 23:2507–2520

    Article  Google Scholar 

  • Hendricks JJ, Nadelhoffer KJ, Aber JD (1993) Assessing the role of fine roots in carbon and nutrient cycling. Trends Ecol Evol 8:174–178

    Article  Google Scholar 

  • Hendricks JJ, Hendrick RL, Wilson CA, Mitchell RJ, Pecot SD, Guo D (2006) Assessing the patterns and controls of fine root dynamics: an empirical test and methodological review. J Ecol 94:57

    Article  Google Scholar 

  • Hirose T (1971) Nitrogen turnover and dry-matter production of a Solidago altissima population. Jpn J Ecol 21:18–32

    Google Scholar 

  • Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–339

    Article  Google Scholar 

  • Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522

    Article  Google Scholar 

  • Hobbie SE, Reich PB, Oleksyn J, Ogdahl M, Zytkowiak R, Hale C, Karolewski P (2006) Tree species effects on decomposition and forest floor dynamics in a common garden. Ecology 87:2288–2297

    Article  PubMed  Google Scholar 

  • Iversen CM, Ledford J, Norby RJ (2008) CO2 enrichment increases carbon and nitrogen input from fine roots in a deciduous forest. New Phytol 179:837–847

    Article  CAS  PubMed  Google Scholar 

  • John B, Pandey HN, Tripathi RS (2001) Vertical distribution and seasonal changes of fine and coarse root mass in Pinus kesiya Royle Ex. Gordon forest of three different ages. Acta Oecol 22:293–300

    Article  Google Scholar 

  • Keyes MR, Grier CC (1981) Above- and below-ground net production in 40-year-old Douglas-fir stands on low and high productivity sites. Can J For Res 11:599–605

    Article  Google Scholar 

  • Knops JMH, Wedin D, Tilman D (2001) Biodiversity and decomposition in experimental grassland ecosystems. Oecologia 126:429–433

    Article  Google Scholar 

  • Lichter J, Billings SA, Ziegler SE, Aindh D, Ryals R, Finzi AC, Jackson RB, Stemmler EA, Schlesinger WH (2008) Soil carbon sequestration in a pine forest after 9 years of atmospheric CO2 enrichment. Glob Change Biol 14:2910–2922

    Article  Google Scholar 

  • Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig A, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Article  Google Scholar 

  • Masaki T, Suzuki W, Niiyama K, Iida S, Tanaka T (1992) Community structure of a species-rich temperate forest, Ogawa Forest Reserve, central Japan. Vegetatio 98:97–111

    Google Scholar 

  • McClaugherty CA, Aber JD, Melillo JM (1982) The role of fine root in the organic matter and nitrogen budgets of two forested ecosystems. Ecology 63:1481–1490

    Article  Google Scholar 

  • Meier CE, Grier CC, Cole DW (1985) Below- and aboveground N and P use by Abies amabilis stands. Ecology 66:1928–1942

    Article  Google Scholar 

  • Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ (2000) The potential effects of nitrogen deposition on fine-root production in forest ecosystems. New Phytol 147:131–139

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ, Aber JD, Melillo JM (1985) Fine root, net primary production, and soil nitrogen availability: a new hypothesis. Ecology 66:1377–1390

    Article  Google Scholar 

  • Nambiar EKS (1987) Do nutrients retranslocate from fine roots? Can J For Res 17:913–918

    Article  Google Scholar 

  • Ogino K (1977) A beech forest in Ashiu: its increment and net production. In: Shidei T, Kira T (eds) Primary productivity of Japanese forest. JIBP Synthesis, vol 16. University of Tokyo Press, Tokyo, Japan, pp 172–186

    Google Scholar 

  • Osada N, Tateno R, Hyodo F, Takeda H (2004) Changes in crown architecture with tree height in two deciduous tree species: developmental constraints or plastic response to the competition for light? For Ecol Manag 188:337–347

    Article  Google Scholar 

  • Osono T, Takeda H (2001) Organic chemical and nutrient dynamics in decomposing beech leaf litter in relation to fungal ingrowth and succession during 3-year decomposition processes in a cool temperate deciduous forest in Japan. Ecol Res 16:649–670

    Article  CAS  Google Scholar 

  • Osono T, Takeda H (2005) Decomposition of organic chemical components in relation to nitrogen dynamics in leaf litter of 14 tree species in a cool temperate forest. Ecol Res 20:41–49

    Article  CAS  Google Scholar 

  • Pastor J, Aber JD, McClaugherty CA (1984) Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65:256–268

    Article  CAS  Google Scholar 

  • Reich PB, Grigal DF, Aber JD, Gower ST (1997) Nitrogen mineralization and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78:335–347

    Article  Google Scholar 

  • Reich PB, Walters MB, Tjoelker MG, Vanderklein D, Buschena C (1998) Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Funct Ecol 12:395–405

    Article  Google Scholar 

  • Shaver GR, Melillo JM (1984) Nutrient budgets of marsh plants: efficiency concepts and relation to availability. Ecology 65:1491–1510

    Article  Google Scholar 

  • Silla F, Escudero A (2004) Nitrogen-use efficiency: trade-offs between N productivity and mean residence time at organ, plant and population levels. Funct Ecol 18:511–521

    Article  Google Scholar 

  • Steele SJ, Gower ST, Vogel JG, Norman JM (1997) Root mass, net primary production and turnover in aspen, jack pine and black spruce forests in Saskatchewan and Manitoba, Canada. Tree Physiol 17:577–587

    CAS  PubMed  Google Scholar 

  • Takeda H, Abe T (2001) Templates of food–habitat resources for the organization of soil animals in temperate and tropical forests. Ecol Res 16:961–973

    Article  Google Scholar 

  • Takeda H, Ishida Y, Tsutsumi T (1987) Decomposition of leaf litter in relation to litter quality and site conditions. Memories of the College of Agriculture, Kyoto University 130:17–38

    Google Scholar 

  • Tateno R, Kawaguchi H (2002) Differences in nitrogen use efficiency between leaves from canopy and subcanopy trees. Ecol Res 17:695–704

    Article  Google Scholar 

  • Tateno R, Takeda H (2003) Forest structure and tree species distribution in relation to topography-mediated heterogeneity of soil nitrogen and light at forest floor. Ecol Res 18:559–571

    Article  Google Scholar 

  • Tateno R, Morozumi S, Takeda H (2003) Interspecific comparison of leaf area loss caused by insect herbivores in relation to leaf properties in a cool temperate deciduous broad-leaved forest. Jpn J For Environ 45:29–33

    Google Scholar 

  • Tateno R, Hishi T, Takeda H (2004) Above- and belowground biomass and net primary production in a cool-temperate deciduous forest in relation to topographical changes in soil nitrogen. For Ecol Manag 193:297–306

    Article  Google Scholar 

  • Tateno R, Osada N, Terai M, Tokuchi N, Takeda H (2005a) Inorganic nitrogen source utilization by Fagus crenata on different soil types. Trees 19:477–481

    Article  Google Scholar 

  • Tateno R, Aikawa T, Takeda H (2005b) Leaf-fall phenology along a topography-mediated environmental gradient in a cool–temperate deciduous broad-leaved forest in Japan. J For Res 10:269–274

    Article  Google Scholar 

  • van Breemen N, Finzi AC (1998) Plant–soil interactions: ecological aspects and evolutionary implications. Biogeochemistry 42:1–19

    Article  Google Scholar 

  • Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572

    Article  Google Scholar 

  • Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298

    Article  CAS  Google Scholar 

  • Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13:87–115

    Article  Google Scholar 

  • Vogt KA, Grier CC, Vogt DJ (1986) Production, turnover, and nutrient dynamics of above- and belowground detritus of world forests. Adv Ecol Res 15:303–377

    Article  Google Scholar 

  • Yasumura Y, Hikosaka K, Matsui K, Hirose T (2002) Leaf-level nitrogen-use efficiency of canopy and understorey species in a beech forest. Funct Ecol 16:826–834

    Article  Google Scholar 

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Acknowledgments

We would like to thank Kyoto University Ashiu Forest Research Station for supporting for our study. We wish to thank Noriyuki Osada, Takashi Osono, Sachie Morozumi, Reiji Fujimaki, Takuo Hishi, Hiroyuki Ishii, Takanobu Aikawa, and the members of Laboratory of Forest Ecology, Graduate School of Agriculture, Kyoto University, for their very helpful suggestions on the manuscript and for assistance with fieldwork. This study was partly supported by a grant of (11213205 and 20780120) from the Japan Society for the Promotion of Science.

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Authors and Affiliations

  1. Graduate School of Agriculture, Kyoto University, Kyoto, 6068502, Japan

    Ryunosuke Tateno & Hiroshi Takeda

  2. Faculty of Agriculture, Kagoshima University, Kagoshima, 8900065, Japan

    Ryunosuke Tateno

  3. Faculty of Science and Engineering, Doshisha University, Kyotanabe, 6100321, Japan

    Hiroshi Takeda

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  1. Ryunosuke Tateno
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Correspondence to Ryunosuke Tateno.

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Communicated by Jason Kaye.

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Tateno, R., Takeda, H. Nitrogen uptake and nitrogen use efficiency above and below ground along a topographic gradient of soil nitrogen availability. Oecologia 163, 793–804 (2010). https://doi.org/10.1007/s00442-009-1561-0

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