Plant and Soil201: 1–7, 1998.© 1998Kluwer Academic Publishers. Printed in the Netherlands.

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Black alder (Alnus Glutinosa(L.) Gaertn.) trees mediate methane andnitrous oxide emission from the soil to the atmosphere

H. Rusch1,2 and H. Rennenberg1,3

1Fraunhofer-Institute for Atmospheric Environmental Research, Kreuzeckbahnstrasse 19, 82467 Garmisch-Partenkirchen, Germany.2Present address: Krieseby 1, 24354 Rieseby, Germany.3Corresponding author;permanent address: Institut für Forstbotanik und Baumphysiologie, Professur für Baumphysiologie, Albert-Ludwigs-Universität Freiburg, Am Flughafen 17, 79085 Freiburg i. Br., Germany∗

Received 30 October 1997. Accepted in revised form 11 February 1998

Key words:alder,Alnus glutinosa, methane, nitrous oxide, trace gas flux

Abstract

Three-year-old seedlings of black alder (Alnus glutinosa(L.) Gaertn.), a common European wetland tree species,were grown in native soil taken from an alder swamp. Fluxes of methane (CH4) and nitrous oxide (N2O) betweenthe tree stem and the atmosphere were determined under controlled conditions. Both CH4 and N2O were emittedthrough the bark of the stem into the atmosphere when the root zone exhibited ‘higher-than-ambient’ CH4 and N2Ogas mixing ratios. Flooding of the soil caused a decreased N2O emission but an increased CH4 efflux from the stem.Immediately after flooding of the soil, N2O was emitted from the seedlings’ bark at a rate of 350µmol N2O m−2

h−1 whereas CH4 flux could not be detected. After more than 40 days of flooding CH4 fluxes up to 3750µmolCH4 m−2 h−1 from the stem were measured, while N2O emission had decreased below the limit of detection. Gasefflux decreased with increasing stem height and correlated with gas mixing ratios in the soil, indicating diffusionthrough the aerenchyma as the major path of gas transport. From these results it is assumed that woody specieswith aerenchyma can serve as conduits for soil-derived trace gases into the atmosphere, to date only shown forherbaceous plants. This, yet unidentified, ‘woody plant pathway’ contributes to the total greenhouse gas sourcestrength of wetlands.

Introduction

As a morphological adaptation to flooding conditions,wetland plants possess aerenchyma. This air-filled tis-sue is required to aerate the roots of wetland plantsand constitutes the major pathway for the flux of O2through plants (Grosse and Schröder, 1986; Justin andArmstrong, 1987; Perata and Alpi, 1993; Schröder,1989). This pathway is also a means for soil-bornegases to escape in the opposite direction, i.e. from theroot zone to the shoot and into the atmosphere.

Gases that have been shown to escape into the at-mosphere via aerenchyma of wetland plants are: (1)methane (e.g. Sebacher et al., 1985; Schimel, 1995),(2) nitrous oxide and (3) dinitrogen (Mosier et al.,

∗ FAX No: 7612038302. E-mail: here@sun2.ruf.uni-freiburg.de

1990; Reddy et al., 1989), (4) carbon monoxide (Con-rad et al., 1988), (5) hydrogen (Schütz et al., 1988),and (6) carbon dioxide (e.g. Thomas et al., 1996). The‘plant pathway’ may make up more than 90% of totalemission of soil-borne gases as has been shown forCH4 emission from rice paddies (Holzapfel-Pschornand Seiler, 1986; Schütz et al., 1989) and wetlandsdominated byCarex spec. (Whiting and Chanton,1992). Other pathways of CH4 exchange between thesoil and the atmosphere, i.e. the release of gas bub-bles (Keller and Stallard, 1994) and diffusion at thesoil/water-atmosphere interface (Barber et al., 1988;Schütz et al., 1991), appear to be of minor importance.

Whereas the role of wetland plants as conduits forCH4 has been investigated for numerous herbaceousspecies (for a review see Schütz et al., 1991; Singhand Singh, 1995), the flux of nitrogen both as N2 and

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N2O from the root zone into the atmosphere has sofar been shown for only a few species including rice(Oryza sativaL.) (Mosier et al., 1990; Reddy et al.,1989), Pontederia cordataL. and Juncus effususL.(Reddy et al., 1989). Plant-mediated efflux of soil-derived gases is assumed to be of minor importancefor total gas emissions of ecosystems with low vegeta-tion like Sphagnumspec. – dominating bogs or heathwhere plants have no or only small roots (Thomaset al., 1996). Thus, depending on the soil and theplant community, the plant pathway may or may notcontribute to the total gas source strength of wetlandecosystems. For most natural ecosystems the contri-bution of plant-mediated gas efflux to total emission isunknown.

So far only herbaceous wetland species have beenidentified as paths for gas transport from the root zoneinto the atmosphere. Schütz et al. (1991) discussed apotential gas efflux out of the trunks of woody speciesvia the lenticels, but actual data on trees as conduitsfor soil-borne trace gases have not been published todate. Trees and shrubs make up a large percentageof wetland biomass, especially in riverine ecosystemspermanently or temporarily flooded. Similar to wet-land herbs, these woody plants exhibit morphologicaland physiological adaptations to wetland conditions,among them aerenchyma formation (Perata and Alpi,1993; Schröder, 1989).

Therefore, in the present study the question hasbeen addressed as to whether aerenchymous woodyplants mediate gas transport from the root zone viathe shoot into the atmosphere. We decided to inves-tigate fluxes of the greenhouse gases CH4 and N2O(IPCC, 1994) because wetlands are considered strongsources of CH4 and, to a lesser extent, N2O (Ciceroneand Oremland, 1988; Martikainen et al., 1993, 1995;Schütz et al., 1990). Black alder (Alnus glutinosa(L.) Gaertn.) was selected for these studies becauseaerenchyma formation and oxygen transport of thisEuropean wetland species is well documented (Grosseand Schröder, 1986; Schröder, 1989).

Material and methods

Plant material

Two-year-old seedlings of black alder were obtainedfrom a tree nursery (Baumschule Handel, Tutzing,Germany) and planted in 15-L pots containing soilfrom an alder swamp (top layer, 0–30 cm) on Lake Be-lau in Northern Germany (54◦6′ N, 10◦14′ E) taken in

Figure 1. Root fumigation chamber used for N2O and CH4 trans-port studies.

spring. Plants were left in the field and were kept well-watered during the summer, using tap water withoutaddition of nutrients. The seedlings were not wateredduring winter, and the roots were protected from freez-ing damage by covering the pots with wood chips.Watering was resumed in April of the following year.At this time the 3-year-old seedlings had reached astem height of approximately 2 m and a diameterof 2.5 cm at soil level. Plants were moved to thelaboratory a few days before the experiments werestarted to allow adaptation to indoor conditions. Af-ter holes in the bottom of the pots had been closed,the plants were watered to achieve waterlogged con-ditions. Twigs were cut off at their base up to a stemheight of 40 cm, on average four twigs per plant, tofacilitate mounting of the chambers on the plants. Toprevent effects on gas flux, the cut ends were sealedwith grease. Light intensity was maintained at 200µmol m−2s−1 PPFD (photosynthetic photon flux den-sity) at the top of the canopy and at about a tenth ofthis value at soil level, representing the conditions of aforest understorey. Air temperature was kept at 20± 2◦C.

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Figure 2. Static chamber for the determination of N2O and CH4efflux from the stem.

Root fumigation chamber

In order to expose bare roots of intact plants to N2Oor CH4, a root fumigation chamber similar to that de-scribed by Huss-Danell (1978) was construced (Figure1). For this purpose two perspex lids were fitted ona perspex cylinder (35 cm high, i.d. 12 cm) with O-rings. A hole was drilled in the centre of the top lidwide enough to hold the stem base, and the top lid wascut in two pieces. Edges of the lid were smoothed andfitted with rubber seals. The entire root was rinsed withtap water to remove the soil and was inserted into thechamber in such a way that the stem base was lined upwith the top lid. The two parts of the top lid were in-serted from left and right, and the remaining openingsin the top lid were sealed with an inert sealing material(Teroson, Teroson GmbH, Heidelberg, Germany). Thebottom of the chamber was covered with water beforefumigation started to achieve a saturated atmosphereonce the chamber was sealed. Up to several mL of pureCH4 and N2O (Messer-Griesheim, Olching, Germany)were injected into the chamber through the septum ofa 1/4" fitting.

Stem chambers

Gas flux out of stems of alder seedlings was measuredwith static chambers. For their design perspex cylin-ders (i.d. 12 cm) and lids fitted with O-rings were used(Figure 2). Two holes were drilled wide enough to fitthe stem, and the cylinder was cut in two parts acrossthe holes to attach the chamber horizontally to the stem(Figure 2). The cut edges of the cylinder were fitted

with rubber seals, and the two parts of the chamberwere held in place with four steel springs attached tosmall screws. The remaining openings of the cham-ber were sealed with Teroson. One of the lids wasequipped with a fan and two 1/4" fittings. The fan waspowered by a 24 V electric motor with a magnet oneither side of the lid. Each chamber enclosed 12 cm ofthe stem. Three chambers were attached on top of eachother, starting at the stem base, thus enclosing stem ar-eas between 0–12 cm, 14–26 cm, and 28–40 cm abovesoil, respectively. In control experiments high mixingratios of N2O and CH4 had been injected into emptychambers. Mixing ratios had remained constant over afew hours, showing that the chambers were gas-tight.

Soil air samples

The mixing ratios of CH4 and N2O were monitoredwith the sampling device developed by Bodenbender(1997). This device is essentially a rectangular-shapedpost made from perspex (35 cm long, 9 cm wide,5 cm deep) with small holes (18 mm diameter) as‘chambers’ spaced 4 cm apart along its whole length.These chambers were covered with a teflon mem-brane (PTFE, 12.5µm thick; Bachhofer, Reutlingen,Germany) which allowed gas exchange but excludedwater from entering. The sampling device was insertedinto the soil and withdrawn after a minimum of 3 days.This allowed equilibration between the gas mixing ra-tios of the soil air and the chambers. Air samples wereimmediately taken from the chambers after removal ofthe sampling device from the soil.

Gas analysis

The static chambers mounted on the stem of the plantswere flushed for a few minutes with pressurised air,closed, and gas samples were withdrawn every tenminutes during the subsequent half hour with a 100-µL gas-tight syringe (Hamilton, Bonaduz, Switzer-land) and immediately analysed. Mixing ratios of N2Owere determined with a gas chromatograph equippedwith a hayesep-N column (60–80 mesh, 3 m× 1/8")and an electron capture detector (Perkin-Elmer, modelGC 8500, carrier gas helium with a flow rate of 40mL min−1, injector and column temperature 60◦C,detector temperature 350◦C). Analysis of CH4 mix-ing ratios was performed with a gas chromatographequipped with a molecular sieve (60–80 mesh, 1.5 m× 1/4"; WGA, Pfungstadt, Germany) and a flame ion-isation detector (Shimadzu, model GC-8AIF, carriergas N2 at a flow rate of 50 mL min−1, injector and

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column temperature 100◦C, detector temperature 150◦C).

Experimental procedures

Two different sets of experiments were performed.The first set involved rinsing the soil from the plantroots and subsequently exposing the bare roots to avariety of mixing ratios of both N2O and CH4 in thefumigation chamber and measuring the gas efflux outoff the stem at the same time. For the second set ofexperiments, plants were left rooted in the swamp soilin the 15-L pots (in situ). The soil was waterlogged,and mixing ratios of N2O and CH4 in the soil air aswell as the gas efflux out of the stem were monitoredover a time course of several weeks.

The data obtained in these two experimental ap-proaches cannot be compared directly, because the gasmixing ratio in the fumigation chamber represents thegas mixing ratio at the site of gas entry into the roots.In the in situ experiments the gas mixing ratio mea-sured in soil air at a certain depth is an integrated valuethat may be significantly different from the gas mixingratio at the site of gas entry into the roots.

Data analysis and statistics

Determinations of flux rates were performed in tripli-cate. Gas mixing ratios were plotted against time, andflow rates were calculated from the slope of linear re-gression lines (n = 4). Flux rates were normalised forthe stem surface area that was enclosed in the staticchamber. The root fumigation experiments were per-formed with two alder seedlings, and gas flux ratesof each of the gases were pooled. The pooled datawere used to calculate the relationship between the gasmixing ratios in the root zone and stem gas efflux ratesusing linear regression.

Results and discussion

Zeikus and Ward (1974) assessed specimens ofUlmusamericanaL., Salix nigra L., andPopulus deltoidesBartr. in the field that showed decaying heartwood.When the trees were ‘tapped’ 1 m above ground levelwith a cork borer the escaping gas could be ignited,suggesting that methanogenic bacteria present in thewood were the source for the high CH4 partial pres-sure in the wood. In the present investigation of alderseedlings with healthy wood no such gas flux from thestems could be observed. If the emissions observed

Figure 3. Efflux of N2O and CH4 from the stem of three-year-oldalder seedlings after fumigation of the root zone. Roots of twoseedlings of black alder (stem height c. 2 m, root length c. 20 cm,stem diameter at stem base 2.0 cm, stem diameter at 40 cm abovesoil 1.0 cm) were rinsed to remove adhering soil and were fumi-gated with different mixing ratios of N2O and CH4 in a gas-tightchamber. Gas efflux out of the stem area 0–12 cm above soil wasmeasured using a static chamber technique. Air samples were takenfrom the chamber at regular intervals and mixing ratios of N2O andCH4 were determined. Flux rates were calculated from the slopes oflinear regression lines of gas mixing ratios plotted vs. time and werenormalised for the stem surface area enclosed by the chamber. Datafrom experiments with two trees were pooled and used for linearregression analyses of stem efflux rates versus root gas mixing ratio.

in the present studies had been caused by bacteria inthe trees, gas would have been emitted from the stemsalso at ambient gas mixing ratios (0.31 ppm for N2Oand 1.71 ppm for CH4; IPCC, 1994) in the root zone.Because such emissions were not found (Figure 3), thepresent study deals with a phenomenon different fromthat of Zeikus and Ward (1974), i.e. the flux of soil-borne CH4 and N2O from the root through the woodyplant to the shoot.

In the present study, N2O as well as CH4 wereemitted from the stem surface of alder seedlings both

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Figure 4. Time-course of the efflux of N2O and CH4 from thestem of alder seedlings and of gas mixing ratios in soil air. Over atime-course of 40 days after flooding flux rates of N2O and CH4 outof the stem area 0–12 cm above soil were measured at the indicatedtimes using the static chamber technique. Flux rates were calculatedfrom the slopes of linear regression lines of gas mixing ratios plottedvs. time. Rates below the limit of detection of the experimentalset-up (c. 2µmol N2O m−2 h−1and c. 4µmol CH4 m−2 h−1,respectively) were set to zero. Flux rates were related to the stemsurface area enclosed in the static chamber. Soil air was collectedat different depths and the mixing ratios of N2O and CH4 weredetermined. Experiments were performed at air temperatures of 20◦C ± 2 ◦C. Vertical bars represent the standard deviation of meansof three replicate measurements. Similar results were obtained intwo independent experiments.

after fumigation of roots with higher-than-ambient gasmixing ratios (Figure 3) andin situ at higher mixingratios of these gases in natural soil air (Figure 4). Dur-ing in situ experiments distinct time-courses of both,flux rates and soil air gas mixing ratios were observed(Figure 4). When trees were assayed immediately af-ter flooding of the soil, N2O was emitted from theseedlings’ bark at a rate of 350µmol N2O m−2 h−1

whereas CH4 flux could not be detected. However,after more than 40 days of flooding CH4 fluxes up to3750µmol CH4 m−2 h−1 from the stem were mea-sured, while N2O emission had decreased below thelimit of detection (Figure 4). Gas efflux rates corre-sponded to initially high but decreasing soil air mixingratios of N2O and initially low but rising CH4 mixingratios as a consequence of flooding. Gas mixing ratiosin the soil air were highest at a depth of 9 cm withmaximum values of 35 ppm N2O and 4800 ppm CH4(Figure 4). Literature data on soil air gas mixing ra-tios from other investigations are sparse. Thomas et al.(1996) determined a mixing ratio of 190± 5 ppm CH4

at 15 cm depth and 10◦C in peat monoliths, but didnot address the effect of altered water status on CH4mixing ratios in soil air.

The high stem efflux rates observed illustrate thesignificance which the plant pathway may have forthe emission of N2O and CH4 from wetland ecosys-tems. In wetland soils N2O as well as N2 are excretedinto the soil by anaerobic denitrifiers in considerableamounts, but the release of the gases from floodedwetlands is thought to be low (Goodroad and Keeney,1984; Martikainen et al., 1995; Terry et al., 1981).This may be caused by a complete reduction of ni-trate to N2 (Terry et al., 1981) or by water acting asa diffusion barrier. This diffusion barrier may be cir-cumvented by plant-mediated transport (Mosier et al.,1990; Reddy et al., 1989). On the other hand, wet-land soils turn into sinks for CH4 at low water tableswith aerobic conditions (Martikainen et al., 1993) dueto CH4 oxidation by methanotrophic microorganisms(Cicerone and Oremland, 1988). This oxidation in theupper soil layers may be bypassed by plant-mediatedtransport, but part of the CH4 produced may still beoxidized in the aerobic zone of the rhizosphere.

We found a linear relationship of both CH4 andN2O efflux out of the stem with the respective gasmixing ratio in the root fumigation chamber (Figure3). This finding is strong evidence that the mode oftransport of these gases was mainly by diffusion, aconclusion also supported by the apparent decrease ofstem gas efflux with increasing stem height (Figure5). Thermo-osmosis, an active mode of gas transportin plants extensively investigated for oxygen trans-port in black alder (Schröder, 1989), is unlikely tocontribute to the emission of CH4 and N2O observedin the present study, since light intensity in the stemarea was kept at c. 20µmol m−2 s−1 which is toolow to generate the temperature difference between thestem and the outside air necessary for thermo-osmosis(Schröder, 1989).

Schröder (1989) investigated black alder seedlingsand identified wood as the main site for transport ofa tracer gas from the shoot into the root. Diffusionrates of the tracer depended on the porosity of the stemtissue and the size of the tree. Highest rates were foundin leaf-covered plants that were exposed for prolongedperiods to flooding during spring or summer. In thepresent study the porosity of stems of flooded blackalder seedlings was sufficiently large to allow a linearincrease of diffusion rates even up to gas mixing ratiosabout a factor of 5000 above ambient, both for N2Oand CH4 (Figure 3).

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Figure 5. Relative flux rates of N2O and CH4 from different stemsegments of alder seedlings. For plant material and experimentalconditions see legend to Figure 4. Flux rates of N2O and CH4 outof the stems of five alder seedlings growing in native swamp soilwere measured 0–12 cm, 14–26 cm, and 28–40 cm above soil, us-ing a static chamber technique. Flux rates were calculated from theslopes of linear regression lines of gas mixing ratios plotted vs. time.Emission rates out of the lowest stem area analysed (0–12 cm abovesoil) were set 100%. Efflux rates out of the other stem areas wereexpressed as relative flux rates± standard error. Relative flux ratesof N2O and CH4 out of given stem areas (14–26 cm above soil or28–40 cm above soil) were not significantly different atp < 0.05.

Our data indicate that N2O efflux out of the stemwas significantly higher than CH4 efflux at given mix-ing ratios in the fumigation chamber. For example,at mixing ratios of 2000 ppm in the root zone fluxrates of N2O out of the stem were 165µmol m−2 h−1

versus 78µmol m−2 h−1 for CH4 (Figure 3). A sim-ilar observation was made in thein situ experiments.Maximum N2O mixing ratios in the soil were 35 ppmcompared to a 140-fold higher maximum CH4 mixingratio; still the corresponding flux rates of the two gasesdiffered only by a factor of 10 (Figure 4). This strik-ing difference might have been caused by an extensiveCH4 oxidation in the root zone of alder trees. Thepresence of methane-oxidising microorganisms in therhizosphere of wetland plants has been demonstratedrepeatedly (Denier van der Gon and Neue, 1996; Ger-ard and Chanton, 1993; Schipper and Reddy, 1996).Methane oxidation by methanotrophs in aerobic soilsurface layers may make up more than 90% of theCH4 produced in some ecosystems (Frenzel et al.,1990; Sundh et al., 1995). The reduction of N2O to N2

by denitrifying microorganisms was most likely sup-pressed in the aerobic part of the rhizosphere (Reddyet al., 1989), thus resulting in relatively high rates ofN2O efflux.

In conclusion, seedlings of black alder, a flood-tolerant tree species that forms aerenchyma underflooding conditions (Schröder, 1989), serve as path-way for CH4 and N2O from the root zone via the shootinto the atmosphere. It is very likely that this is alsotrue for more mature black alder trees, because (1) in-creased rooting depth will increase the requirement foraerenchyma formation to facilitate sufficient oxygentransport to the roots and (2) increased exploitation ofthe soil by the roots will enhanced trace gas flux intothe aerenchyma of the roots. We therefore propose thatsimilar fluxes through trees under field conditions arelikely to occur and are mainly driven by the existenceand features of the aerenchyma and by the gas mixingratios in the rhizosphere. For example, aerenchymaformation in response to flooding has been found ina number of wetland tree species includingCyperuspapyrusL. (Li and Jones, 1995) and seedlings ofAlnusjaponica (Yamamoto et al., 1995a),Fraxinus mand-shuricaRupr.var. japonicaMaxim. (Yamamoto et al.,1995b),Taxodium distichum(L.) Rich. var. distichum(Kludze et al., 1994),Alnus rubraBong. (Harrington,1987), and even flood-tolerantPinus spec. (Topa andMcLeod, 1986), suggesting that these species mayalso be potential conduits for trace gases of micro-bial origin in the root zone. Plant-mediated gas fluxesneed to be included in laboratory and field measure-ments to avoid an underestimation of total emissionsof soil-borne gases in ecosystems with a high densityof large annual plants as well as aerenchymous shrubsand trees.

Acknowledgements

This study was funded by the Bundesministerium fürBildung, Wissenschaft, Forschung und Technologie aspart of the ‘Ökoystemforschung im Bereich der Born-höveder Seenkette’ which is gratefully acknowledged.

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Section editor: F R Minchin