title: Quantification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organisms in a boreal pine forest.
abstract: *The flux of carbon from tree photosynthesis through roots to ectomycorrhizal (ECM) fungi and other soil organisms is assumed to vary with season and with edaphic factors such as nitrogen availability, but these effects have not been quantified directly in the field. *To address this deficiency, we conducted high temporal-resolution tracing of (13)C from canopy photosynthesis to different groups of soil organisms in a young boreal Pinus sylvestris forest. *There was a 500% higher below-ground allocation of plant C in the late (August) season compared with the early season (June). Labelled C was primarily found in fungal fatty acid biomarkers (and rarely in bacterial biomarkers), and in Collembola, but not in Acari and Enchytraeidae. The production of sporocarps of ECM fungi was totally dependent on allocation of recent photosynthate in the late season. There was no short-term (2 wk) effect of additions of N to the soil, but after 1 yr, there was a 60% reduction of below-ground C allocation to soil biota. *Thus, organisms in forest soils, and their roles in ecosystem functions, appear highly sensitive to plant physiological responses to two major aspects of global change: changes in seasonal weather patterns and N eutrophication.
authors.affiliation: Department of Forest Ecology and Management, Swedish University of Agricultural Sciences (SLU), SE-901 83 Umeå, Sweden.
authors.forename: Mona N
authors.initials: MN
authors.lastname: Högberg
authors.affiliation: Departamento de Ecología y Biología Animal, Universidad de Vigo, 36310 Vigo, Spain.|Centre for Ecology and Hydrology, Lancaster Environment Centre, Lancaster LA1 4AP, UK.
authors.forename: Maria J I
authors.initials: MJI
authors.lastname: Briones
authors.affiliation: Department of Forest Ecology and Management, Swedish University of Agricultural Sciences (SLU), SE-901 83 Umeå, Sweden.
authors.forename: Sonja G
authors.initials: SG
authors.lastname: Keel
authors.affiliation: Department of Forest Ecology and Management, Swedish University of Agricultural Sciences (SLU), SE-901 83 Umeå, Sweden.
authors.forename: Daniel B
authors.initials: DB
authors.lastname: Metcalfe
authors.affiliation: Department of Plant Physiology and Umeå Plant Science Centre, University of Umeå, SE-901 87 Umeå, Sweden.
authors.forename: Catherine
authors.initials: C
authors.lastname: Campbell
authors.affiliation: Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, UK.
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Midwood
authors.affiliation: Macaulay Land Use Research Institute, Craigiebuckler, Aberdeen AB15 8QH, UK.
authors.forename: Barry
authors.initials: B
authors.lastname: Thornton
authors.affiliation: Department of Plant Physiology and Umeå Plant Science Centre, University of Umeå, SE-901 87 Umeå, Sweden.
authors.forename: Vaughan
authors.initials: V
authors.lastname: Hurry
authors.affiliation: Southern Swedish Forest Research Centre, SLU, PO Box 49, SE-230 53 Alnarp, Sweden.
authors.forename: Sune
authors.initials: S
authors.lastname: Linder
authors.affiliation: Department of Forest Ecology and Management, Swedish University of Agricultural Sciences (SLU), SE-901 83 Umeå, Sweden.
authors.forename: Torgny
authors.initials: T
authors.lastname: Näsholm
authors.affiliation: Department of Forest Ecology and Management, Swedish University of Agricultural Sciences (SLU), SE-901 83 Umeå, Sweden.
authors.forename: Peter
authors.initials: P
authors.lastname: Högberg
mesh_terms: D002244:Carbon / Q000378:metabolism*; D002245:Carbon Dioxide / Q000378:metabolism; D017753:Ecosystem; D007553:Isotope Labeling; D013058:Mass Spectrometry; D038821:Mycorrhizae / Q000502:physiology*; D009584:Nitrogen / Q000378:metabolism*; D028223:Pinus / Q000382:microbiology*; D012621:Seasons; D012988:Soil Microbiology; D013548:Sweden; D014197:Trees / Q000378:metabolism*
chemical_list: D002245:Carbon Dioxide; D002244:Carbon; D009584:Nitrogen
references.citation: Aber J, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I. 1998. Nitrogen saturation in temperate forest ecosystems - hypotheses revisited. Bioscience 48: 921-934.
references.citation: Bahn M, Schmitt M, Siegwolf R, Richter A, Brüggemann N. 2009. Does photosynthesis affect grassland soil-respired CO2 and its carbon isotope composition on a diurnal timescale? New Phytologist 182: 451-460.
references.citation: Berg B, McClaugherty C. 2003. Plant litter decomposition, humus formation, carbon sequestration. Berlin, Germany: Springer.
references.citation: Carbone MS, Czimczik CI, McDuffee KE, Trumbore SE. 2007. Allocation and residence times of photosynthetic products in a boreal forest using a low-level 14C pulse-chase labelling technique. Global Change Biology 13: 466-477.
references.citation: Dise NB, Wright RF. 1995. Nitrogen leaching from European forests in relation to nitrogen deposition. Forest Ecology and Management 71: 153-162.
references.citation: Frostegård Å, Bååth E. 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22: 59-65.
references.citation: Gange AC, Gange EG, Sparks TH, Boddy L. 2007. Rapid and recent changes in fungal fruting patterns. Science 316: 71.
references.citation: Hansen J, Türk R, Vogg G, Heim R, Beck E. 1997. Conifer carbohydrate physiology: updating classical views. In: Rennenberg H, Eschrich W, Ziegler H, eds. Trees - contributions to modern tree physiology. Leiden, the Netherlands: Backhuys, 97-108.
references.citation: Hanson PJ, Edwards NT, Garten CT, Andrews JA. 2000. Separating root and microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48: 115-146.
references.citation: van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundsröm US. 2005. The carbon we do not see - the impact of low molecular weight compounds on carbon dynamics in forest soils: a review. Soil Biology and Biochemistry 37: 1-13.
references.citation: Heinemeyer A, Hartley IP, Evans SP, Carreira de la Fuentes JA, Ineson P. 2007. Forest soil CO2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Global Change Biology 13: 1786-1797.
references.citation: Hermans C, Hammond JP, White PJ, Verbruggen N. 2006. How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11: 610-617.
references.citation: Hobbie EA, Weber NS, Trappe JM, van Klinken GJ. 2002. Using radiocarbon to determine the mycorrhizal status of fungi. New Phytologist 156: 129-136.
references.citation: Högberg MN, Chen Y, Högberg P. 2007a. Gross nitrogen mineralisation and fungi-to-bacteria ratios are negatively correlated in boreal forests. Biology and Fertility of Soils 44: 363-366.
references.citation: Högberg MN, Högberg P. 2002. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytologist 154: 791-795.
references.citation: Högberg P, Högberg MN, Göttlicher SG, Betson NR, Keel SG, Metcalfe DB, Campbell C, Schindlbacher A, Hurry V, Lundmark T et al. 2008. High temporal resolution tracing of photosynthate carbon from the tree canopy to forest soil microorganisms. New Phytologist 177: 220-228.
references.citation: Högberg MN, Högberg P, Myrold DD. 2007b. Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150: 590-601.
references.citation: Högberg MN, Myrold DD, Giesler R, Högberg P. 2006. Contrasting patterns of soil N cycling in model ecosystems of Fennoscandian boreal forests. Oecologia 147: 96-107.
references.citation: Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ. 2001. Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411: 789-792.
references.citation: Högberg P, Read DJ. 2006. Towards a more plant physiological perspective on soil ecology. Trends in Ecology and Evolution 21: 548-554.
references.citation: Horwath WR, Pregitzer KS, Paul EA. 1994. 14C allocation in tree-soil systems. Tree Physiology 14: 1163-1176.
references.citation: Johnson D, Krsek M, Wellington EMH, Stott AW, Cole L, Bardgett RD, Read DJ, Leake JR. 2005. Soil invertebrates disrupt carbon flow through fungal networks. Science 309: 1047.
references.citation: Kagawa A, Sugimoto A, Maximow TC. 2006. Seasonal course of translocation, storage and remobilization of 13C pulse-labeled photoassimilate in naturally growing Larix gmelinii saplings. New Phytologist 171: 793-804.
references.citation: Körner C, Asshoff R, Bignucolo O, Hättenschwiler S, Keel SG, Pelaez-Riedl S, Pepin S, Siegwolf RTW, Zotz G. 2005. Carbon flux and growth in mature deciduous forest exposed to elevated CO2. Science 309: 1360-1362.
references.citation: Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D. 2006. Carbon fluxes from plants through soil organisms determined by field 13CO2 pulse-labelling in an upland grassland. Applied Soil Ecology 33: 152-175.
references.citation: Lin GH, Ehleringer JR, Rygiewicz PT, Johnson MG, Tingey DT. 1999. Elevated CO2 and temperature impacts on different components of soil CO2 efflux in Douglas-fir terracosms. Global Change Biology 5: 157-168.
references.citation: Mäkelä A, Valentine HT, Helmisaari HS. 2008. Optimal co-allocation of carbon and nitrogen in a forest stand at steady state. New Phytologist 180: 114-123.
references.citation: Matamala R, Gonzalez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH. 2003. Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302: 1385-1387.
references.citation: Neufeld JD, Wagner M, Murrel JC. 2007. Who eats what, where and when? Isotope labelling experiments are coming of age ISME Journal 1: 103-110.
references.citation: 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 Phytologist 158: 409-416.
references.citation: O′Connor FB. 1955. Extraction of enchytraid worms from a coniferous forest soil. Nature 175: 815-816.
references.citation: Olsson P, Linder S, Giesler R, Högberg P. 2005. Fertilization of boreal forest reduces both autotrophic and heterotrophic soil respiration. Global Change Biology 11: 1745-1753.
references.citation: Ostle N, Briones MJI, Ineson P, Cole L, Staddon P, Sleep D. 2007. Isotopic detection of recent photosynthate carbon flow into grassland rhizosphere fauna. Soil Biology and Biochemistry 39: 768-777.
references.citation: Ostle N, Ineson P, Benham D, Sleep D. 2000. Carbon assimilation and turnover in grassland vegetation using an in situ13CO2 pulse labelling system. Rapid Communications in Mass Spectrometry 14: 1345-1350.
references.citation: Paterson E, Gebbing T, Abel C, Sim A, Telfer G. 2007. Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytologist 173: 600-610.
references.citation: Plain C, Gerant D, Maillard P, Dannoura M, Dong Y, Zeller B, Priault P, Parent F, Epron D. 2009. Tracing of recently assimilated carbon in respiration at high temporal resolution in the field with a tunable diaode laser absorption spectrometer after in situ 13CO2 pulse labelling of 20-year-old beech trees. Tree Physiology 29: 1433-1445.
references.citation: Pollierer MM, Langel R, Körner C, Maraun M, Scheu S. 2007. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecology Letters 10: 729-736.
references.citation: Salminen J, Haimi J. 2001. Life history and spatial distribution of the enchytraeid worm Cognettia sphagnetorum (Oligochaeta) in metal-polluted soil: belowground sink-source population dynamics. Environmental Toxicology & Chemistry 20: 1993-1999.
references.citation: Schimel DS. 1995. Terrestrial ecosystems and the carbon-cycle. Global Change Biology 1: 77-91.
references.citation: Siira-Pietikäinen A, Penttinen R, Huhta V. 2008. Oribatid mites (Acari: Oribatida) in boreal forest floor and decaying wood. Pedobiologia 52: 111-118.
references.citation: Smith SE, Read DJ. 2008. Mycorrhizal symbiosis, 3 rd edn . London, UK: Academic Press.
references.citation: Söderström B, Read DJ. 1987. Respiratory activity of intact and excised ectomycorrhizal mycelial systems growing in unsterilised soil. Soil Biology and Biochemistry 19: 231-236.
references.citation: Staddon PL. 2004. Carbon isotopes in functional soil ecology. Trends in Ecology and Evolution 19: 148-154.
references.citation: Steinmann K, Siegwolf RTW, Saurer M, Körner C. 2004. Carbon fluxes to the soil in a mature temperate forest assessed by 13C isotope tracing. Oecologia 141: 489-501.
references.citation: Subke J-A, Vallack HW, Magnusson T, Keel SG, Metcalfe DB, Högberg P, Ineson P. 2009. Short-term dynamics of abiotic and biotic soil 13CO2 effluxes after in situ13CO2 pulse labelling of boreal pine forest. New Phytologist 183: 349-357.
references.citation: Tunlid A, White DC. 1992. Biochemical analysis of biomass, community structure, nutritional status, and metabolic activity of microbial communities in soil. In: Stotzky G, Bollag J-M, eds. Soil biochemistry. New York, NY, USA: Marcel Dekker, 229-261.
references.citation: Vance ED, Brookes PC, Jenkinson DS. 1987. An extraction method for measuring microbial biomass C. Soil Biology and Biochemistry 19: 703-707.
references.citation: Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman GD. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7: 737-750.
references.citation: Wallenda T, Kottke I. 1998. Nitrogen deposition and ectomycorrhizas. New Phytologist 139: 169-187.
references.citation: Wardle DA, Klironomos JN, Setälä H, van der Putten WH, Wall DH. 2004. Ecological linkages between aboveground and belowground biota. Science 304: 1629-1633.
references.citation: Waring RH, Running SW 1998. Forest ecosystems. Analysis at multiple scales, 2 nd edn . San Diego, CA, USA: Academic Press.
references.citation: Wessels JGH. 1993. Fruiting in higher fungi. Advances in Microbial Physiology 34: 147-202.
references.citation: Yarwood SA, Myrold DD, Högberg MN. 2009. Termination of below-ground C allocation by trees alters soil fungal and bacterial communities in a boreal forest. FEMS Microbiology Ecology 70: 151-162.