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Inundation strongly stimulates nitrous oxide emissions from stems of the upland tree Fagus sylvatica and the riparian tree Alnus glutinosa

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Abstract

Background and aims

Nitrous oxide (N2O) and methane (CH4) can be emitted from surfaces of riparian plants. Data on the emission of these greenhouse gases by upland trees are scarce. We quantified CH4 and N2O emissions from stems of Fagus sylvatica, an upland tree, and Alnus glutinosa, a riparian tree.

Methods

The gas fluxes were investigated in mesocosms under non-flooded control conditions and during a flooding period using static chamber systems and gas chromatographic analyses.

Results

Despite differences in the presence of an aerenchyma system, both tree species emitted N2O and CH4 from the stems. Flooding caused a dramatic transient increase of N2O stem emissions by factors of 740 (A. glutinosa) and even 14,230 (F. sylvatica). Stem emissions of CH4 were low and even deposition was determined (F. sylvatica controls). The results suggest that CH4 was transported mainly through the aerenchyma, whereas N2O transport occurred in the xylem sap.

Conclusions

For the first time it has been demonstrated that upland trees such as F. sylvatica clearly significantly emit N2O from their stems despite lacking an aerenchyma. If this result is confirmed in adult trees, upland forests may constitute a new and significant source of atmospheric N2O.

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References

  • Anderson B, Bartlett K, Frolking S, Hayhoe K, Jenkins J, Salas W (2010) Methane and nitrous oxide emissions from natural sources. United States Environmental Protection Agency, Office of Atmospheric Programs, Washington

    Google Scholar 

  • Aulakh MS, Wassmann R, Rennenberg H (2000) Methane emissions from rice fields - quantification, mechanisms, role of management, and mitigation options. Adv Agron 70:193–260

    Article  CAS  Google Scholar 

  • Azam F, Müller C, Weiske A, Benckiser G, Ottow JCG (2002) Nitrification and denitrification as sources of atmospheric nitrous oxide – role of oxidizable carbon and applied nitrogen. Biol Fertil Soils 35:54–61

    Article  CAS  Google Scholar 

  • Bohn TJ, Lettenmaier DP, Sathulur K, Bowling LC, Podest E, McDonald KC, Friborg T (2007) Methane emissions from western Siberian wetlands: heterogeneity and sensitivity to climate change. Environ Res Lett 2:1–9

    Article  Google Scholar 

  • Bosse U, Frenzel P (1997) Activity and distribution of methane-oxidizing bacteria in flooded rice soil mesocosms and in rice plants (Oryza sativa). Appl Environ Microbiol 63:1199–1207

    PubMed  CAS  Google Scholar 

  • Bremner JM, Blackmer AM (1978) Nitrous oxide: emission from soils during nitrification of fertilizer nitrogen. Science 199:295–296

    Article  PubMed  CAS  Google Scholar 

  • Brüggemann N, Meier R, Steigner D, Zimmer I, Louis S, Schnitzler JP (2009) Nonmicrobial aerobic methane emission from poplar shoot cultures under low-light conditions. New Phytol 182:912–918

    Article  PubMed  Google Scholar 

  • Buchel HB, Grosse W (1990) Localization of the porous partition responsible for pressurized gas transport in Alnus glutinosa (L.) Gaertn. Tree Physiol 6:247–256

    Article  PubMed  Google Scholar 

  • Butterbach-Bahl K, Papen H, Rennenberg H (1997) Impact of gas transport through rice cultivars on methane emission from rice paddy fields. Plant Cell Environ 20:1175–1183

    Article  CAS  Google Scholar 

  • Butterbach-Bahl K, Papen H, Rennenberg H (2000) Scanning electron microscopy analysis of the aerenchyma in two rice cultivars. Phyton Ann Rei Bot 40:43–55

    Google Scholar 

  • Cai Z, Xing G, Yan X, Xu H, Tsuruta H, Yagi K, Minami K (1997) Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilisers and water management. Plant Soil 196:7–14

    Article  CAS  Google Scholar 

  • Chang C, Janzen HH, Cho CM, Nakonechny EM (1998) Nitrous oxide emission through plants. Soil Sci Soc Am J 62:35–38

    Article  CAS  Google Scholar 

  • Chen X, Boeckx P, Shen S, Van Cleemput O (1999) Emission of N2O from rye grass (Lolium perenne L.). Biol Fertil Soils 28:393–396

    Article  CAS  Google Scholar 

  • Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R et al (2007) Regional climate projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (ed) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and New York, pp 872–879

  • Claessens H, Oosterbaan A, Savill P, Rondeux J (2010) A review of the characteristics of black alder (Alnus glutinosa (L.) Gaertn.) and their implications for silvicultural practices. Forestry 83:163–175

    Article  Google Scholar 

  • Denier van der Gon HAC, Neue HU (1996) Oxidation of methane in the rhizosphere of rice plants. Biol Fertil Soils 22:359–366

    Article  CAS  Google Scholar 

  • Dick J, Skiba U, Munro R, Deans D (2006) Effect of N-fixing and non N-fixing trees and crops on NO and N2O emissions from Senegalese soils. J Biogeogr 33:416–423

    Article  Google Scholar 

  • Dueck TA, de Visser R, Poorter H, Persijn S, Gorissen A, de Visser W, Schapendonk A, Verhagen J, Snel J, Harren FJM et al (2007) No evidence for substantial aerobic methane emission by terrestrial plants: a 13C-labelling approach. New Phytol 175:29–35

    Article  PubMed  CAS  Google Scholar 

  • FAO (Food and Agriculture Organization of the United Nations) (2006) World reference base for soil resources 2006. A framework for international classification, correlation and communication, 2nd edn. World Soil Resources Reports 103, Rome

  • Ferner E, Rennenberg H, Kreuzwieser J (2012) Effect of fl ooding on C metabolism of fl ood-tolerant (Quercus robur) and non-tolerant (Fagus sylvatica) tree species. Tree Physiol 32:135–145

    Article  PubMed  CAS  Google Scholar 

  • Forsteinrichtung Stadtwald Freiburg (2011) Städtisches Forstamt Freiburg im Breisgau

  • Forster P, Ramaswamy V, Artaxo P, Berntsen T, Betts R, Fahey DW, Haywood J, Lean J, Lowe DC, Myhre G et al (2007) Changes in atmospheric constituents and in radiative forcing. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and New York, pp 137–153

  • Frenzel P, Rudolph J (1998) Methane emission from a wetland plant: the role of CH4 oxidation in Eriophorum. Plant Soil 202:27–32

    Article  CAS  Google Scholar 

  • García LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105:657–663

    Article  Google Scholar 

  • Gauci V, Gowing DJG, Hornibrook ERC, Davis JM, Dise NB (2010) Woody stem methane emission in mature wetland alder trees. Atmos Environ 44:2157–2160

    Article  CAS  Google Scholar 

  • Einrichtungswerk Landkreis Rastatt - Gemeindewald Steinmauern (2009) Landratsamt Rastatt and Regierungspräsidium Freiburg, Abteilung 8, Forstdirektion

  • Geßler A, Keitel C, Kreuzwieser J, Matyssek R, Seiler W, Rennenberg H (2007) Potential risks for European beech (Fagus sylvatica L.) in a changing climate. Trees 21:1–11

    Article  Google Scholar 

  • Gilbert B, Frenzel P (1995) Methanotrophic bacteria in the rhizosphere of rice mesocosms and their effect on porewater methane concentration and methane emission. Biol Fertil Soils 20:93–100

    Article  CAS  Google Scholar 

  • Hefting MM, Bobbink R, de Caluwe H (2003) Nitrous oxide emission and denitrification in chronically nitrate-loaded riparian buffer zones. J Environ Qual 32:1194–1203

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann G, Thun R, Herrmann R, Knickmann E (1991) Methodenbuch Band 1, Die Untersuchung von Böden, 4th edn. VDLUFA-Verlag, Darmstadt

    Google Scholar 

  • Keppler F, Hamilton JTG, Brass M, Röckmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191

    Article  PubMed  CAS  Google Scholar 

  • Keppler F, Hamilton JTG, McRoberts WC, Vigano I, Braß M, Röckmann T (2008) Methoxyl groups of plant pectin as a precursor compound for atmospheric methane: evidence from deuterium labelling studies. New Phytol 178:808–814

    Article  PubMed  CAS  Google Scholar 

  • Kreuzwieser J, Fürniss S, Rennenberg H (2002) Impact of waterlogging on the N-metabolism of flood tolerant and non-tolerant tree species. Plant Cell Environ 25:1039–1049

    Article  Google Scholar 

  • Kreuzwieser J, Buchholz J, Rennenberg H (2003) Emission of methane and nitrous oxide by Australian mangrove ecosystems. Plant Biology 5:423–431

    Article  CAS  Google Scholar 

  • Kreuzwieser J, Papadopoulou E, Rennenberg H (2004) Interaction of flooding with carbon metabolism of forest trees. Plant Biology 6:299–306

    Article  PubMed  CAS  Google Scholar 

  • Kroeze C, Mosier A, Bouwman L (1999) Closing the global N2O budget: a retrospective analysis 1500–1994. Glob Biogeochem Cycles 13:1–8

    Article  CAS  Google Scholar 

  • Lelieveld J, Crutzen P, Dentener FJ (1998) Changing concentration, lifetime and climate forcing of atmospheric methane. Tellus 50B:128–150

    CAS  Google Scholar 

  • Li C (2007) Quantifying greenhouse gas emissions from soils: scientific basis and modeling approach. Soil Sci Plant Nutr 53:344–352

    Article  CAS  Google Scholar 

  • Mander U, Lohmus K, Teiter S, Uri V, Augustin J (2008) Gaseous nitrogen and carbon fluxes in riparian alder stands. Boreal Env Res 13:231–241

    CAS  Google Scholar 

  • Matthews E, Fung I (1987) Methane emission from natural wetlands: global distribution, area, and environmental characteristics of sources. Glob Biogeochem Cycles 1:61–86

    Article  CAS  Google Scholar 

  • McBain MC, Warland JS, McBride RA, Wagner-Riddle C (2004) Laboratory-scale measurements of N2O and CH4 emissions from hybrid poplars (Populus deltoids x Populus nigra). Waste Manag Res 22:454–465

    Article  PubMed  CAS  Google Scholar 

  • McLeod AR, Fry SC, Loake GJ, Messenger DJ, Reay DS, Smith KA, Yun BW (2008) Ultraviolet radiation drives methane emissions from terrestrial plant pectins. New Phytol 180:124–132

    Article  PubMed  CAS  Google Scholar 

  • Nisbet RER, Fisher R, Nimmo RH, Bendall DS, Crill PM, Gallego-Sala AV, Hornibrook ERC, López-Juez E, Lowry D, Nisbet PBR et al (2009) Emission of methane from plants. Proc Roy Soc B Biol Sci 276:1347–1354

    Article  CAS  Google Scholar 

  • Nouchi I, Mariko S, Aoki K (1990) Mechanism of methane transport from the rhizosphere to the atmosphere through rice plants. Plant Physiol 94:59–66

    Article  PubMed  CAS  Google Scholar 

  • Pihlatie M, Ambus P, Rinne J, Pilegaard K, Vesala T (2005) Plant-mediated nitrous oxide emissions from beech (Fagus sylvatica) leaves. New Phytol 168:93–98

    Article  PubMed  CAS  Google Scholar 

  • Pinay G, Roques L, Fabre A (1993) Spatial and temporal patterns of denitrification in a riparian forest. J Appl Ecol 30:581–591

    Article  Google Scholar 

  • Prendergast-Miller MT, Baggs EM, Johnson D (2011) Nitrous oxide production by the ectomycorrhizal fungi Paxillus involutus and Tylospora fibrillosa. FEMS Microbiol Lett 316:31–35

    Article  PubMed  CAS  Google Scholar 

  • Pritsch K, Munch JC, Buscot F (1997) Morphological and anatomical characterisation of black alder Alnus glutinosa (L.) Gaertn. ectomycorrhizas. Mycorrhiza 7:201–216

    Article  Google Scholar 

  • Purvaja R, Ramesh R, Frenzel P (2004) Plant-mediated methane emission from an Indian mangrove. Glob Change Biol 10:1825–1834

    Article  Google Scholar 

  • Raghoebarsing AA, Smolders AJP, Schmid MC, Rijpstra WIC, Wolters-Arts M, Derksen J, Jetten MSM, Schouten S, Sinninghe Damste JS, Lamers LPM et al (2005) Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature 436:1153–1156

    Article  PubMed  CAS  Google Scholar 

  • Rice AL, Butenhoff CL, Shearer MJ, Teama D, Rosenstiel TN, Khalil MAK (2010) Emissions of anaerobically produced methane by trees. Geophys Res Lett 37:1–5

    Article  Google Scholar 

  • Rudaz AO, Davidson EA, Firestone MK (1991) Sources of nitrous oxide production following wetting of dry soil. FEMS Microbiol Ecol 85:117–124

    CAS  Google Scholar 

  • Rusch H, Rennenberg H (1998) Black alder (Alnus Glutinosa (L.) Gaertn.) trees mediate methane and nitrous oxide emission from the soil to the atmosphere. Plant Soil 201:1–7

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Silver WL, Herman DJ, Firestone MK (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82:2410–2416

    Article  Google Scholar 

  • Smart DR, Bloom AJ (2001) Wheat leaves emit nitrous oxide during nitrate assimilation. Proc Natl Acad Sci USA 98:7875–7878

    Article  PubMed  CAS  Google Scholar 

  • Smith KA (1990) Greenhouse gas fluxes between land surfaces and the atmosphere. Prog Phys Geogr 14:349–372

    Article  Google Scholar 

  • Smith CJ, Patrick WH Jr (1983) Nitrous oxide emission as affected by alternate anaerobic and aerobic conditions from soil suspensions enriched with ammonium sulfate. Soil Biol Biochem 15:693–697

    Article  CAS  Google Scholar 

  • Smith KA, Ball T, Conen F, Dobbie KE, Massheder J, Rey A (2003) Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur J Soil Sci 54:779–791

    Article  Google Scholar 

  • Sorz J, Hietz P (2006) Gas diffusion through wood: implications for oxygen supply. Trees 20:34–41

    Article  Google Scholar 

  • Sponagel H, Grottenthaler W, Hartmann KJ, Hartwich R, Janetzko P, Joisten H, Kühn D, Sabel KJ, Traidl R (2005) 5.6.13.4.1. Feinboden. In: Sponagel H, Grottenthaler W, Hartmann KJ, Hartwich R, Janetzko P, Joisten H, Kühn D, Sabel KJ, Traidl R (eds) Bodenkundliche Kartieranleitung. Ad-hoc-Arbeitsgruppe Boden der Staatlichen Geologischen Dienste und der Bundesanstalt für Geowissenschaften und Rohstoffe, E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, pp 141–148

  • Struwe S, Kjoller A (1989) Field determination of denitrification in water-logged forest soils. FEMS Microbiol Ecol 62:71–78

    Article  Google Scholar 

  • Templer PH, Silver WL, Pett-Ridge J, DeAngelis KM, Firestone MK (2008) Plant and microbial controls on nitrogen retention and loss in a humid tropical forest. Ecology 89:3030–3040

    Article  Google Scholar 

  • Terazawa K, Ishizuka S, Sakata T, Yamada K, Takahashi M (2007) Methane emissions from stems of Fraxinus mandshurica var. japonica trees in a floodplain forest. Soil Biol Biochem 39:2689–2692

    Article  CAS  Google Scholar 

  • Toda H, Yagi K, Yoh M, Takeuchi M (1994) Measurement of methane and nitrous oxide emissions from the peatlands in Northern Quèbec, Canada. Proc NIPR Symp Polar Biol 7:237–242

    Google Scholar 

  • Vigano I, van Weelden H, Holzinger R, Keppler F, McLeod A, Röckmann T (2008) Effect of UV radiation and temperature on the emission of methane from plant biomass and structural components. Biogeosciences 5:937–947

    Article  CAS  Google Scholar 

  • Wang ZP, Han XG, Wang GG, Song Y, Gulledge J (2008) Aerobic methane emission from plants in the Inner Mongolia steppe. Environ Sci Technol 42:62–68

    Article  PubMed  CAS  Google Scholar 

  • Wassmann R, Aulakh MS (2000) The role of rice plants in regulating mechanisms of methane emissions. Biol Fertil Soils 31:20–29

    Article  CAS  Google Scholar 

  • Yan X, Shi S, Du L, Xing G (2000) Pathways of N2O emission from rice paddy soil. Soil Biol Biochem 32:437–440

    Article  CAS  Google Scholar 

  • Yu KW, Wang ZP, Chen GX (1997) Nitrous oxide and methane transport through rice plants. Biol Fertil Soils 24:341–343

    Article  CAS  Google Scholar 

  • Zeikus JG, Ward JC (1974) Methane formation in living trees: a microbial origin. Science 184:1181–1183

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Boeckx P, Chen G, Van Cleemput O (2000) Nitrous oxide emission from herbicide-treated soybean. Biol Fertil Soils 32:173–176

    Article  Google Scholar 

  • Zvára K (1998) 7 Nĕkolik výběrů. In: Zvára K (ed) Biostatistika. Karolinum, Praha, pp 115–145

    Google Scholar 

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Acknowledgments

The present study was partially funded by DAAD (German Academic Exchange System), which is gratefully acknowledged. We would like to thank Dr. Helmer Schack-Kirchner for the soil type identification and Michael Rienks for technical support.

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Correspondence to Jürgen Kreuzwieser.

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Construction of a mesocosm for experiments with Alnus glutinosa and Fagus sylvatica (JPEG 143 kb)

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Construction of a stem chamber for the determination of nitrous oxide and methane emission rates from stems of Alnus glutinosa and Fagus sylvatica (JPEG 57 kb)

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Machacova, K., Papen, H., Kreuzwieser, J. et al. Inundation strongly stimulates nitrous oxide emissions from stems of the upland tree Fagus sylvatica and the riparian tree Alnus glutinosa . Plant Soil 364, 287–301 (2013). https://doi.org/10.1007/s11104-012-1359-4

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