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JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 108, NO. D14, 4421, doi:10.1029/2002JD002989, 2003

Nitrous oxide flux to the atmosphere from the littoral zone of a boreal lake Jari T. Huttunen,1 Sari Juutinen,2 Jukka Alm,3 Tuula Larmola,2 Taina Hammar,4 Jouko Silvola,2 and Pertti J. Martikainen1 Received 27 September 2002; revised 1 April 2003; accepted 7 April 2003; published 26 July 2003.

[1] The surface-atmospheric exchange of nitrous oxide (N2O) was investigated in the

vegetated littoral zone of a eutrophied midboreal lake (Lake Keva¨to¨n, Finland) with a static chamber technique. During a dry summer (three to six samplings per site), the meadow site and two marsh sites in the temporarily flooded eulittoral zone and the Phragmites australis-dominated site in the continuously flooded infralittoral zone had mean daytime N2O-N emissions from 11 ± 7 to 22 ± 7 mg m2 h1, whereas the Nuphar lutea-dominated site in the infralittoral zone had a mean N2O flux close to zero. During a wet summer (13–14 samplings per site), the mean daytime N2O-N fluxes ranged from 4 ± 1 to 15 ± 5 mg m2 h1 at the three eulittoral sites and were negligible at the two infralittoral sites. The littoral zone occupied 26% of the lake area but was estimated to account for most of the N2O emissions from the lake. The studied eulittoral zone, which did not have adjacent nitrogen fertilization, exhibited higher N2O emissions during the summer than seen in northern natural ecosystems in general, including peatlands, forests, and the pelagic regions of lakes. Thus in lake-rich landscapes the littoral zone and other lake-associated wetlands must be considered as potential sources of atmospheric N2O. An assessment of their atmospheric importance requires further data on the N2O fluxes and their regulation in different littoral areas and on the total littoral coverage, neither of which is yet available. INDEX TERMS: 0315 Atmospheric Composition and Structure: Biosphere/atmosphere interactions; 1615 Global Change: Biogeochemical processes (4805); 1803 Hydrology: Anthropogenic effects; 1845 Hydrology: Limnology; 1890 Hydrology: Wetlands; KEYWORDS: boreal lake, global warming, greenhouse gas emission, littoral zone, nitrous oxide flux, wetland Citation: Huttunen, J. T., S. Juutinen, J. Alm, T. Larmola, T. Hammar, J. Silvola, and P. J. Martikainen, Nitrous oxide flux to the atmosphere from the littoral zone of a boreal lake, J. Geophys. Res., 108(D14), 4421, doi:10.1029/2002JD002989, 2003.

1. Introduction [2] Agriculture, fossil fuel combustion, and other human activities have disturbed the global nitrogen (N) cycle by increasing the availability and mobility of N in ecosystems [Vitousek et al., 1997]. As a result, certain aerobic and anaerobic microbial processes in the biosphere, mainly nitrification and denitrification [Davidson and Schimel, 1995], produce more nitrous oxide (N2O), which is then emitted into the atmosphere. N2O is an important atmospheric greenhouse gas [Khalil, 1999] and it may contribute to the loss of stratospheric ozone, especially as the emissions of chlorofluorocarbons (CFCs) are reduced. 1 Department of Environmental Sciences, University of Kuopio, Kuopio, Finland. 2 Department of Biology, University of Joensuu, Joensuu, Finland. 3 Joensuu Research Centre, Finnish Forest Research Institute, Joensuu, Finland. 4 North Savo Regional Environment Centre, Kuopio, Finland.

Copyright 2003 by the American Geophysical Union. 0148-0227/03/2002JD002989

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[3] About one third of the global terrestrial and aquatic N2O emission is considered to be anthropogenic [Seitzinger et al., 2000]. In aquatic ecosystems, N loading can lead to eutrophication and can affect the exchange of N2O between water and the atmosphere. Significant N2O emissions have been measured from N-enriched rivers, as well as estuarine and coastal waters [Seitzinger and Kroeze, 1998; Seitzinger et al., 2000]. Seitzinger et al. [2000] estimated that the annual N2O release from rivers, estuaries, and continental shelves totals 1.9 Tg N. According to Seitzinger et al., over 90% of the estuarine and riverine N2O emission (1.2 Tg N yr1) may be anthropogenic, and 90% of this originates from the Northern midlatitudes, because of heavy N fertilization and high atmospheric N deposition in these regions. Before it enters the streams and rivers, N leached from terrestrial ecosystems comes into contact with the riparian (streamside) ecosystems [Lowrance et al., 1997], where part of the N load is processed to N2O and released to the atmosphere. A recent review by Groffman et al. [2000] showed that the riverine ecosystems are probably ‘‘regional hot spots’’ in N2O production but their global N2O release is unknown. The N-enriched rivers have been included in the recent global

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HUTTUNEN ET AL.: N2O FLUXES FROM THE LITTORAL ZONE

Table 1. Dominating Vegetation and the Carbon (C) and Nitrogen (N) Contents and C/N-Ratios in the Soil/Sediment in the Littoral Zone of Lake Keva¨to¨n Soil/Sediment C and Na Vegetation Zone Meadow

Dominating Species

Depth, cm

Eulittoral Zone Calamagrostis canescens (F.H. Wigg) Roth, Carex acuta L.

Marsh

Carex aquatilis Wahlenb., Calla palustris L., Potentilla palustris (L.) Scop.

Reed

Infralittoral Zone Phragmites australis (Cav.) Trin. ex Steudel

Water lily

Nuphar lutea (L) Sibth. and Sm.

C, %

N, %

C/N

0–2 2 – 10 10 – 20 0–2 2 – 10 10 – 20

42 12 5 25 11 7

2 0.7 0.3 1 0.6 2

21 17 16 18 19 4

0–2 2 – 10 10 – 20 ...

12 12 0.6 NMb

0.6 0.5 0 NM

21 27 ... NM

a

On 15 September 1999, one soil/sediment sample (diameter 7.5 7.5 cm) per site was taken for the measurements of the soil/ sediment C and N contents. The C and N contents were analyzed from the dry soil/sediment with a model 1106 Carlo Erba elemental analyzer (Carlo Erba, Milano, Italy). b Not measured.

estimates of the aquatic N2O emissions, whereas the N2O emissions from inland freshwater lakes are still excluded [Seitzinger and Kroeze, 1998; Seitzinger et al., 2000]. The neglect of lakes and their littoral zones in the ecosystem N2O exchange studies may raise serious uncertainties over estimates of the regional N2O emissions, especially in northern, lake-rich landscapes. For example, in Finland lakes occupy about 10% of the country’s surface area [Raatikainen and Kuusisto, 1990] and in Canada the corresponding figure is 7.6% [Environment Canada, 1998]. The pelagic regions of freshwater lakes and reservoirs are considered only to be minor sources of N2O, although their N2O fluxes have shown extensive variability [Mengis et al., 1997; Huttunen et al., 2000, 2001, 2003]. Instead, similar to the streamside ecosystems [Groffman et al., 2000] and wetlands receiving a high N load [Merbach et al., 2001; Silvan et al., 2002], the lake littoral zones with accelerated N cycling represent potential sites for substantial N2O release. In this study, the seasonal dynamics of N2O fluxes were investigated in the littoral zone of a eutrophied boreal lake, and the fluxes were compared to those previously presented for other natural and managed boreal and temperate ecosystems.

2. Materials and Methods 2.1. Site Description [4] The study area was located on a relatively exposed vegetated shore of Lake Keva¨to¨n (63060N; 27370E), a shallow and highly eutrophic freshwater lake [see Huttunen et al., 2001] in the middle boreal zone in Finland. Lake Keva¨to¨n has received nutrients from intensive agriculture around its catchment, and additionally in the sewage load from a hospital during the period from the 1930s to 1975. The average concentrations of chlorophyll a were 20 and 31 mg l1, total N was 850 and 930 mg l1 and total P was 45 and 51 mg l1 at a depth of 1 m in the water column in the pelagic zone of the lake during the open water periods of 1997 and 1998, respectively (J. T. Huttunen, unpublished data, 1997 – 1998). According to Forsberg and Ryding [1980], the concentrations of 7 – 40 mg l1

for chlorophyll a, 600– 1500 mg l1 for total N, and 25– 100 mg l1 for total P during the open water period indicate a eutrophic state of lakes. Lake Keva¨to¨n is icecovered from mid-November to early May. It has an area of 407 ha, including the infralittoral (continuously flooded littoral) vegetation, and a catchment area of 2400 ha. The lake volume is 0.00932 km3 with mean and maximum depths of 2.3 and 10 m, respectively. Lake Keva¨to¨n has an extensive littoral zone, and the study area formed a 60-m wide transition along its moisture and vegetation gradient. The five study sites were located within four different vegetation zones: (1) a meadow (meadow site) and (2) a sedge marsh (marsh-1 and marsh-2 sites, i.e., upper and lower marsh) in the eulittoral zone (temporarily flooded littoral), and the stands of (3) emergent common reed (reed site) in the upper infralittoral zone and of (4) floating-leaved yellow water lily (water lily site) in the middle infralittoral zone. In the entire lake, the area of flood meadows (meadow and marsh sites) is 39 ha, and the area of emergent aquatic vegetation (reed site) is 41 ha. The floating-leaved vegetation (water lily site) covers 26 ha of the total lake area. The dominating vegetation and the carbon and nitrogen contents of soil/sediment of the sites are presented in Table 1. [5] Soil moisture differed at the study sites between the two studied summer periods. Summer 1997 was extremely dry, whereas summer 1998 was extremely wet. The mean air temperatures in May –October were nearly similar in 1997 and 1998. According to the recordings of precipitation and air temperature between May and October in 1997 and 1998 at the Rissala Airport, located 14 km southeast from Lake Keva¨to¨n, summertime precipitation was 246 and 530 mm, and the mean air temperature was 11.9 and 11.3C, respectively [Finnish Meteorological Institute, 1998, 1999]. At the same location, the long-term (1961 – 1990) precipitation and mean air temperature between May and October were 352 mm and 11.3C [Finnish Meteorological Institute, 1991]. 2.2. N2O Fluxes [6] A boardwalk system was constructed into the study area in June 1997 to avoid the disturbance of soil/sediment

HUTTUNEN ET AL.: N2O FLUXES FROM THE LITTORAL ZONE Table 2. N2O-N Flux Measurements in the Littoral Zone of Lake Keva¨to¨na Date

Total Meadow Marsh-1 Marsh-2 Reed Water Lily Littoral

3 July 1997 21 July 1997 30 July 1997 25 Aug. 1997 16 Sept. 1997 27 Oct. 1997 Total 1997

3 1 2 3 1 3 13

1997 Season 3 2 1 2 2 2 3 3 3 3 3 3 15 15

3 2 3 2 3 ... 13

... ... 3 3 3 ... 9

11 6 12 14 13 9 65

9 June 1997 24 June 1998 30 June 1998 7 July 1998 8 July 1998 13 July 1998 20 July 1998 30 July 1998 3 Aug. 1998 10 Aug. 1998 17 Aug. 1998 19 Aug. 1998 24 Aug. 1998 1 Sept. 1998 7 Sept. 1998 14 Sept. 1998 28 Sept. 1998 6 Oct. 1998 12 Oct. 1998 26 Oct. 1998 Total 1998

3 3 ... 3 ... 3 3 3 ... 3 3 ... ... ... 2 2 2 ... 3 3 36

1998 Season 3 3 ... ... ... ... 3 3 ... ... 3 3 2 3 3 3 ... ... 3 3 2 ... ... ... 3 3 ... 2 2 3 2 2 1 2 1 ... 2 3 3 3 33 36

3 ... ... ... 3 2 3 ... 3 3 ... ... 3 2 3 3 3 ... 2 2 35

... 2 2 ... 2 3 3 ... 3 2 ... 3 3 3 1 ... 3 ... 3 3 36

12 5 2 9 5 14 14 9 6 14 5 3 12 7 12 19 11 1 13 14 176

a Values are the number of individual successful flux measurements (see the text).

during sampling. Aluminum collars (60 60 30 cm) were installed permanently in the ground (at a depth of 20– 25 cm below the soil surface) at the meadow and marsh sites for daytime N2O flux measurements (between 0900 and 1900 UT) with the static, nonsteady state chamber technique [Nyka¨nen et al., 1995, 1998]. At the infralittoral sites, similar collars were hung by height-adjustable wooden frames keeping the lower parts of the collars about 15 cm below the water surface. Three replicate collars were used at each site. The collars had water grooves to ensure a gas-tight connection to the chambers during the measurements. Additional collars with a height of 30 cm were settled upon the permanently installed collars to raise the chambers at the meadow, marsh, and reed sites in order to prevent any possible damage to the vegetation. From each site, the fluxes of N2O were measured 3 – 6 times during the snow-free period in 1997 and 13– 14 times in 1998 (Table 2). The fluxes of N2O were also measured during the winter, on 12 December 1997 and on 17 March and 15 April 1998, using four to six chambers at the meadow site and two chambers at the reed site. The chamber methods used in trace gas exchange studies are described and discussed by Livingston and Hutchinson [1995]. [7] During the N 2O flux measurements, aluminum chambers (60 60 20 cm) were inserted into the water-filled grooves of the collars. In winter, snow was removed from the ground and the chambers were placed onto the ground and padded with snow [Alm et al., 1999].

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Four gas samples were taken at 5 – 8-min intervals from the headspace of the chambers through PVC tubes into 50-ml polypropylene syringes (Terumo Europe, Leuven, Belgium) during the 25 – 30-min measuring period in summer and during the 60-min measuring period in winter. Air was mixed inside the chambers by electrical, brushless fans. The shorter measuring period in summer than in winter was chosen to avoid warming of soils/sediments during the measurements. An average increase of 2C was detected in the chamber air temperatures during the summertime measuring periods, the importance of which for the precision of the flux determination was suggested to be minor compared with that which could be induced if the temperature-dependent microbial activities in the soil were disturbed by a longer measuring period [see Livingston and Hutchinson, 1995]. [8] Gas samples were analyzed for their N2O concentration with a Hewlett-Packard Series II (Hewlett-Packard, Palo Alto, CA) or a Shimadzu GC-14B (Shimadzu Corp., Kyoto, Japan) gas chromatograph, equipped with electron capture detectors (ECD), within 24 hours of sampling. The Hewlett-Packard system has been described by Nyka¨nen et al. [1995, 1998]. In the Shimadzu gas chromatograph, samples were first passed through a glass tube filled with P2O5 to remove water before their loading into a 2-ml loop in a 10-port Shimadzu VLA-1 valve. A column (1.8 m 1/8 inch) was packed with HayeSep Q 80/100 mesh (Hayes Separations, Bandera, TX). Nitrogen (32 ml min1) was used as the carrier gas. The sensitivity of ECD was enhanced by doping it with Ar/CH4 (5% Ar, 95% CH4) at a flow of 2 ml min1. Oxygen was omitted from ECD by bypassing it via an automatic valve. The temperature of ECD was 325C and the temperature of the oven was 40C. The retention time was 2.2 min. Peak areas were integrated with a Shimadzu GLASS-CR 10 program. The Hewlett-Packard and Shimadzu systems had a precision of 0.7 and 0.4% for N2O, respectively. The accuracy of the analyses was maintained by calibrating the gas chromatographs against a standard gas mixture after every 12 samples, which kept the coefficient of variation of the replicated concentration determinations below 1%. The N2O fluxes were calculated from the linear change in the N2O concentrations in the chamber headspace during the measuring periods. The least squares regression lines ‘‘headspace N2O concentration versus time’’ were first visually inspected for abrupt changes in the direction of the flux, resulting from disturbances such as the leakage of the chamber or disturbances of soils/sediments during sampling. For the rest of the data, the linear concentration change (three to four samples) over time was assumed if the r2-value of the regression line was above 0.60. This low limit for r2 was selected to avoid discrimination against low N2O fluxes. Altogether, 26 and 16% of the fluxes were rejected in 1997 and 1998, respectively. Examples of the regression lines from two flux determinations are shown in Figure 1. The detection limit of the chamber measurement for N2O-N was 2 – 4 mg m2 h1. 2.3. Environmental Variables [9] Air temperature inside and outside the chambers was measured with a Fluke 52 K/J thermometer (Fluke Corp., Everett, WA). Soil temperature was determined at the soil/

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Figure 1. The least squares regression lines ‘‘chamber headspace N2O concentration versus time’’ from two N2O flux determinations in September 1998.

but remained below the long-term average in September (Figure 3). During this summer the water tables were continuously at or above the soil surface at the eulittoral sites (Figure 4 and Table 3). In 1998, the monthly average N2O-N fluxes were mostly below 5 mg N2O-N m2 h1, and peak emissions were found only at the meadow and marsh-1 sites (Figure 4), coinciding with the lowest monthly precipitation in September (Figure 3). The seasonal average N2O-N fluxes (mean ± SE) were 15 ± 4, 8 ± 2, and 4 ± 1 mg m2 h1 in 1998 at the meadow, marsh-1, and marsh-2 sites, respectively, and were negligible in the infralittoral zone (Table 3). The monthly soil/sediment surface temperatures were higher in July in 1997 than in 1998, but the decreases in the temperature during rest of the summer season were larger in 1997 (Figure 4). The high mean soil/sediment temperatures in the infralittoral sites in

sediment surface. Soil temperature was not measured during the winter when the soil was frozen. 2.4. Statistical Analyses [10] Nonparametric Spearman correlation coefficients were calculated to study the relations between the N2O fluxes and site moisture and temperature conditions in summer. The correlation analyses were performed separately using the daily values for each site (N = 13– 36) and the seasonal mean values for each chamber (N = 15). An SPSS statistical package (SPSS Inc., release 9.0.1) was used for the statistics.

3. Results 3.1. Temporal and Spatial Patterns of N2O Fluxes and Environmental Variables [11] The summertime littoral N2O-N fluxes had frequency distributions skewed to high values (Figure 2), reflecting seasonal and spatial "hot spots" for N2O release in the study area (see below). The fluxes in the individual measurements ranged from 26 to 140 mg m2 h1 in 1997 (N = 65) and from 19 to 120 mg m2 h1 in 1998 (N = 176). In summer 1997, the mean, standard deviation, and median N2O-N fluxes were 15, 32, and 8 mg m2 h1, respectively. In summer 1998, the corresponding values were 6, 15, and 2 mg m2 h1, respectively. [12] Precipitation was lower in July – August in 1997 than in 1998, being also lower than the long-term (1961 – 1990) average precipitation in these months (Figure 3). This could be seen in lower water table levels in the littoral zone in 1997 (Figure 4 and Table 3). During the dry summer of 1997, the meadow, marsh, and reed sites had their maximum monthly N2O-N emissions (mean ± SE) up to 46 ± 23 mg m2 h1 between July and August (Figure 4), but the spatial variation within all of the sites was large during the entire study (Figure 5). At the eulittoral meadow and marsh sites, and at the reed site in the infralittoral zone, the seasonal mean N2O-N emissions (mean ± SE) ranged from 11 ± 7 to 22 ± 5 mg m2 h1 in 1997, whereas the N2O flux was negligible at the infralittoral water lily site (Table 3). [13] In summer 1998, the monthly rainfall was more than twice the long-term monthly precipitation in June– August

Figure 2. Frequency distributions of N2O fluxes measured during the snow-free seasons of (a) 1997 and (b) 1998 in the littoral zone of Lake Keva¨to¨n.


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Figure 3. Monthly precipitation and mean air temperature in June– October in 1997 and 1998 at the Rissala Airport, located 14 km southeast from Lake Keva¨to¨n [Finnish Meteorological Institute, 1998, 1999], and corresponding long-term averages for the period 1961 – 1990 [Finnish Meteorological Institute, 1991]. 1997 (Table 3) were due to the absence of measurements at these sites in October (Table 2 and Figure 4). 3.2. Relations Between N2O Fluxes and Environmental Variables [14] The importance of the temporarily varying soil moisture and temperature conditions in the N2O fluxes was studied by correlating the daily fluxes with the corresponding water table levels and soil/sediment temperatures. These correlations were calculated separately for the five littoral study sites. The daily N2O flux correlated significantly ( p < 0.05) with the water table level or the soil/sediment surface temperature only at the marsh-1 site. There the daily N2O flux was positively related to soil temperature (Spearman Rank correlation coefficient r = 0.713, N = 15) in 1997 and negatively to the water table level (r = 0.573, N = 33) in 1998. The effects of these factors on the spatial variation in the N2O fluxes within the littoral zone were assessed using the seasonal average fluxes, water table levels, and soil/sediment temperatures from each chamber locations (i.e., 15 microsites) in the correlation analyses. In 1998, the mean summertime N2O flux correlated negatively with the mean water table level (r = 0.713, p = 0.003, N = 15), but in 1997 this relation was not statistically significant (r = 0.493, p = 0.062, N = 15). The seasonal mean N2O flux did not correlate significantly with the mean soil/sediment surface temperature (not shown). 3.3. Winter N2O Fluxes [15] The N2O-N fluxes varied from 7 to 4 mg m2 h1 in the individual wintertime chamber measurements.

The N2O-N fluxes were negligible in winter, averaging (mean ± SE) 1 ± 0.4 and 0 ± 2 mg m2 h1 at the marsh and reed sites, respectively.

4. Discussion 4.1. Littoral N2O Emissions and Their Atmospheric Importance [16] The present sparse data hint at the potential importance of boreal littoral regions and lake-associated wetlands in the total atmospheric N2O load. In this study, the summer N2O-N fluxes in the driest part of the littoral zone (meadow and marsh sites), and at the reed site, ranged from 11 ± 7 to 22 ± 5 mg m2 h1 during the dry summer 1997, and even higher mean summertime N2O-N fluxes, 16-27 mg m2 h1, have been reported for temporarily flooded meadow and swamp sites in midboreal eutrophied Lake Postilampi, Finland [Huttunen et al., 2000]. These emission rates match or are higher than the N2O emissions from various wetlands, forest and aquatic ecosystems in the boreal and temperate regions (Table 4). The littoral sites, however, showed lower N2O emissions than those reported for fertilized agricultural soils (Table 4). [17] The average winter N2O fluxes were negligible, corresponding to natural peatlands in Finland where the wintertime N2O emissions have been found to be small [Alm et al., 1999]. In drained Finnish peatlands the N2O release during wintertime has contributed up to 28% of the annual emissions [Alm et al., 1999]. However, our measurements did not include the freezing-thawing periods in spring

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Figure 4. Monthly average soil/sediment temperatures, water table levels (negative below the soil surface), and N2O fluxes in the littoral zone of Lake Keva¨to¨n. The error bars are standard errors of the mean.

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Table 3. Statistics of the N2O-N Fluxes, Water Table Levels, and Soil/Sediment Surface Temperatures in the Snow-Free Periods of 1997 and 1998 in the Littoral Zone of Lake Keva¨to¨n N2O-N Flux, mg m2 h1 Site

Mean ± SE

b

Min.

Max.

Water Table, cma N

c

Mean ± SE

Soil/Sediment Temperature, C

Min.

Max.

N

Mean ± SE

53 8 7 0 23

2 1 0 32 60

14 16 15 13 9

14 15 15 19 18

± ± ± ± ±

3 2 3 2 1

0 11 7 48 83

25 50 45 76 113

37 33 33 36 39

14 14 12 16 14

± ± ± ± ±

1 1 1 1 1

Min.

Max.

N

1 0 0 13 13

30 30 30 27 23

13 16 15 10 9

4 3 5 5 5

22 22 28 22 18

37 30 34 25 18

1997 Meadow Marsh-1 Marsh-2 Reed Water lily

21 ± 12 19 ± 10 11 ± 7 22 ± 5 1 ± 5

18 18 23 3 26

140 140 93 59 20

13 15 15 13 9

19 ± 4 2 ± 1 2 ± 1 18 ± 3 47 ± 6

Meadow Marsh-1 Marsh-2 Reed Water lily

15 ± 4 8±2 4±1 1±1 1±2

11 8 17 19 14

120 54 15 16 37

36 33 36 35 36

10 ± 1 25 ± 2 22 ± 2 64 ± 1 100 ± 1

1998

a

Negative below the soil surface. SE, the standard error of the mean. c N, the number of individual measurements. b

and autumn, when high N2O emissions have been measured from various terrestrial environments [e.g., Wagner-Riddle et al., 1996; Huttunen et al., 2002; Martikainen et al., 2002; Schu¨rmann et al., 2002]. For example, in farmed mineral and organic soils in Finland, the winter N2O release has accounted for an average of 57% of the annual emissions [Martikainen et al., 2002]. In an alfalfa field in Ontario, Canada, the N2O emissions between October and February were approximated to account for 50% of the annual emissions [Wagner-Riddle et al., 1996], whereas in some alpine soils in Switzerland [Schu¨rmann et al., 2002] and in spruce and beech plantations in Germany [Papen and Butterbach-Bahl, 1999] even more N2O was released during the winter than in summer. The possible episodic N2O emissions during freezing and thawing of soils [e.g., Papen and Butterbach-Bahl, 1999] or diel short-term variations in the flux [e.g., Maljanen et al., 2002], neither of which is easily obtained with the manual chamber techniques, must be further assessed in the littoral wetlands with automated chambers [Maljanen et al., 2002]. The micrometeorological techniques, although being nonintrusive compared to the use of the chambers, are not applicable in the narrow littoral zones such as our study area (width 60 m). The fetch in the littoral zone between the land and the open water area would be too small, and on the other hand, information of the spatial flux heterogeneity (see above) cannot be attained by micrometeorological measurements. In fact, in the simultaneous N2O flux measurements by the chamber and micrometeorological techniques, the results have agreed satisfactorily [Smith et al., 1994; Christensen et al., 1996; Laville et al., 1999]. 4.2. Regulation of N2O Fluxes [18] Aerobic nitrification and anaerobic denitrification are the major processes producing N2O in soils/sediments, whereas N2O can be consumed by denitrification in highly anoxic conditions [Davidson and Schimel, 1995]. Our data, however, could not differentiate between the importance of nitrification and denitrification in the littoral N2O production, and thus, a following speculation of possible reasons for the high N2O emissions during summer droughts must be viewed with care. The high N2O emissions during the dry summer 1997 could be a result of enhanced N turnover

and nitrification rates in the aerobic soil/sediment surface, and/or of enhanced denitrification due to increased nitrate supply into anaerobic, denitrifying microsites in the soils. In the wet summer 1998, nitrification in the surface soil/

Figure 5. Variation in the monthly average N2O fluxes between 15 chambers in the littoral zone of Lake Keva¨to¨n during the snow-free periods of 1997 and 1998. Individual bars at each month correspond to the monthly N2O fluxes from chambers 1 to 15. The chambers with accepted fluxes are presented in parentheses for each month. ND, not determined.

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Table 4. Mean N2O-N Fluxes From Some Boreal and Temperate Ecosystems Ecosystems

Location

Mean Flux, mg N2O N m2 h1

Na

Seasonb

Referencesc

0.8 – 5.3 0.1 – 25 0.8 – 25 0.4 – 1.3 2.1 – 270 9.1 – 47 14 – 180

9 8 10 15 1 2 2

summer summer summer annual summer annual annual

1 1 2 3 4 5 5

Wetlands Peatlands, natural Peatlands, drained Peatlands, natural Various wetlands, natural Restored peatland buffer zone Drained fen grassland, control Drained fen grassland, fertilized

Finland Finland Finland Ontario, Canada Finland Germany Germany

Freshwater lakes and reservoirs Freshwater lakes, oligo-mesotrophic Freshwater lakes, eutrophic and aerated Hudson River Platte River

Finland Switzerland Switzerland New York, USA Colorado, USA

2.1 – 8.2 0.3 – 24 9.5 – 19 6.4 62d

9 4 2 1 1

summer annual annual annual annual

6 7 7 8 9

Mixed forest Mixed forest Deciduous forest Deciduous forests Deciduous forest Coniferous forests Coniferous forest Deciduous forest Coniferous forest Deciduous forest

Forestse Sweden Ontario, Canada Saskatchewan, Canada Saskatchewan, Canada New York, USA Northeastern USA Germany Germany Switzerland Switzerland

0.8 – 1.4 0.4 4.4 – 5.7 0.03 – 0.4 0.8 – 4.1 1.1 – 2.1 16 58 0.8 – 6.7 9.0 – 10

1 1 1 2 1 5 1 1 1 1

annual summer summer annual summer summer annual annual summer summer

10 11 12 13 14 15 16 16 17 17

Organic agricultural soils Mineral agricultural soils Afforested organic soils Cropped soils, fertilized Pasture/hay land Bare agricultural soil Bare agricultural soil, manured Agricultural soils, cultivated Pastureland

Agricultural Land Finland 42 – 420 Finland 17 – 90 Finland 21 – 120 Saskatchewan, Canada 1.9 – 27 Saskatchewan, Canada 0.5 Ontario, Canada 42 Ontario, Canada 83 Ontario, Canada 16 – 72 Switzerland 5.5 – 15

2 2 3 3 2 1 1 2 1

annual annual summer annual annual annual annual annual summer

18 18 19 13 13 20 20 20 17

Lakes and Rivers

a

N, the number of studied ecosystems with a varying number of subsites; see the references for the detailed site description. See the references for the detailed study period. References are as follows: 1, Regina et al. [1996]; 2, Huttunen et al. [2002]; 3, Schiller and Hastie [1994]; 4, Silvan et al. [2002]; 5, Merbach et al. [2001]; 6, Huttunen et al. [2003]; 7, Mengis et al. [1997]; 8, Cole and Caraco [2001]; 9, McMahon and Dennehy [1999]; 10, Klemedtsson et al. [1997]; 11, Schiller and Hastie [1996]; 12, Simpson et al. [1997]; 13, Corre et al. [1999]; 14, McHale et al. [1998]; 15, Castro et al. [1993]; 16, Papen and Butterbach-Bahl [1999]; 17, Schu¨rmann et al. [2002]; 18, Martikainen et al. [2002]; 19, Maljanen et al. [2001]; 20, Wagner-Riddle et al. [1996]. d Median value. e All forest sites represent natural/control sites of the studies. b c

sediment layers could be limited by the lack of oxygen, which then would limit the nitrate supply for denitrification. On the other hand, the wetter conditions in 1998 could favor anoxia and reduction of nitrate and N2O to N2, limiting the N2O release. However, the proportion of produced N2O increases both in nitrification and denitrification at low oxygen concentrations [Davidson and Schimel, 1995], thus the summertime lowering of the water table levels increasing the volume of modestly aerated soil could increase the proportion of N2O production in either of these processes. Nonetheless, the N2O production was most probably limited at our littoral study sites by nitrate availability. In the rural areas of the boreal zone, atmospheric N deposition is usually low and the leaching of N forms a major source of N into aquatic ecosystems, especially in agricultural and forested catchments [Rekolainen, 1989; Cooke and Prepas, 1998; Mannio et al., 2000]. At the meadow and swamp sites in Lake Postilampi, where there are higher N2O emissions [Huttunen et al., 2000], nitrogen leaching was probably

higher as a result of more intensive fertilization in the surrounding area. Laboratory studies with littoral sediments taken close to the meadow and marsh sites in Lake Keva¨to¨n have suggested that the littoral N2O production is limited by low nitrate availability, due to low nitrification activity [Liikanen et al., 2003]. The vegetated sediment cores incubated in this glasshouse experiment with the water table levels at 0 or 15 cm did not show increases in the N2O fluxes following ammonium fertilization (3 g of NH4+-N m2), but exhibited from ten- to hundredfold increases in the N2O release after nitrate addition (3 g of 2 NO 3 -N m ). The mean N2O-N flux from the cores before the extra N was added was 16 mg m2 h1, being similar to those we found from the eulittoral zone in this field study. The laboratory experiment, however, could not judge that nitrification was not changed in the littoral zone during summer drought, since the sediment temperature (average 16C) was lower in the laboratory than in the field during the large emissions in 1997.


[19] In general, the N2O release from wetlands depends on the complex interactions of the N transformation processes [Davidson and Schimel, 1995; Groffman et al., 2000]. For example, in nutrient-rich boreal peatlands the long-term lowering of the water table by ditching has increased the N2O emissions, and this has been associated with the enhanced oxygen availability and the increase in N mineralization in the surface peat, whereas in nutrient-poor peatlands draining did not increase the N 2 O fluxes [Martikainen et al., 1993; Regina et al., 1996]. The shortterm lowering of the water table in laboratory, simulating a summer drought, also has increased N2O release from peat soils [Aerts and Ludwig, 1997; Regina et al., 1998; Dowrick et al., 1999]. In peat cores from a mid-Welsh mire, UK, the increased N2O emissions following a drought were suggested to have been due to the increased N2O:N2 production ratio during denitrification in the saturated, but not totally water-logged conditions [Dowrick et al., 1999]. There could be several possible reasons for the high summertime N2O emissions from the littoral sites in our study, and the further assessment of the littoral N2O exchange should include studies on the nitrogen transformations along the littoral vegetation gradients. As suggested for the assessment of N2O fluxes in natural and constructed riparian ecosystems [Groffman et al., 2000], the N2O:N2 production ratio during denitrification could also be among the key factors to understand the littoral N2O dynamics and their atmospheric importance. The N in leaching and runoff that enters the littoral zone and is not removed from the system to the atmosphere as N2 or N2O, nor is retained into the vegetation, microbes, or soils and sediments, can fuel the N2O production in the N-receiving aquatic ecosystems, including lakes, rivers, and estuarine areas. 4.3. Contribution of the Littoral Zone to Total N2O Emissions From Lakes [20] In Lake Keva¨to¨n, where the vegetated littoral zone covers 26% of the lake area, the littoral zone is the main source of N2O to the atmosphere. The eulittoral meadow and marsh sites released N2O-N from 0.3 ± 0.1 to 0.5 ± 0.3 and from 0.09 ± 0.02 to 0.4 ± 0.2 kg ha1, respectively, during the summer seasons (150 days assumed). These constitute a substantial summertime N2O-N emissions, ranging from 21 ± 6 to 30 ± 17 kg in the flood meadows and from 6 ± 2 to 28 ± 15 kg in the marsh vegetation, in contrast to the negligible N2O fluxes in the pelagic zone of the lake. Nitrous oxide accumulates in the water column of Lake Keva¨to¨n during the winter, leading to N2O-N release of 0.003 – 0.015 kg ha1 following the spring ice melt [Huttunen et al., 2001, also unpublished data, 1997 – 1999]. During two open water periods, minor total N2O-N uptake, averaging 0.006 and 0.025 kg ha1, can be estimated for the pelagic zone based on the monthly measurements at three sites with floating static chambers [Huttunen et al., 2003]. The pelagic N2O-N emissions from the open water area of the lake (324 ha) can then be approximated to range from 1 to 5 kg at spring ice melt, and from 2 to 8 kg during the open water period. [21] It is not currently possible to estimate the total N2O emissions from the littoral regions of boreal lakes, because there are no data, which encompass the total littoral wetland area. However, since there is a shoreline of 190,000 km in

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the Finnish lakes [Kuusisto, 1987], this implies that these littoral N2O emissions could have at least a regional importance in the N2O emissions in the boreal zone. Because the N2O emissions are consistently higher from wetlands receiving a high nitrate load (Table 4) [Merbach et al., 2001; Silvan et al., 2002] than at the presented littoral sites, the increasing eutrophication of northern lakes [Intergovernmental Panel on Climate Change, 1996] possibly will increase their littoral N2O emissions in the future. [22] Acknowledgments. Eija Konttinen (y), Kaisa Ma¨ntynen, Irma Nihtila¨-Ma¨kela¨, Heikki Païvinen, Raimo Asikainen, Markku Virnes, Kalle Maaranen, Tarja Niskanen, and Henna Harju are thanked for technical assistance. We would like to thank the Tiihonen family for all their support during the field campaigns. The valuable suggestions of the reviewers are greatly appreciated. This work was financially supported by the Maj and Tor Nessling Foundation, the Finnish Cultural Foundation, the Niilo Helander Foundation, and the Academy of Finland.

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J. Alm, Joensuu Research Centre, Finnish Forest Research Institute, P. O. Box 68, FIN-80101 Joensuu, Finland. T. Hammar, North Savo Regional Environment Centre, P. O. Box 1049, FIN-70701 Kuopio, Finland. J. T. Huttunen and P. J. Martikainen, Department of Environmental Sciences, University of Kuopio, Bioteknia 2, P. O. Box 1627, FIN-70211 Kuopio, Finland. ( [email protected]) S. Juutinen, T. Larmola, and J. Silvola, Department of Biology, University of Joensuu, P. O. Box 111, FIN-80101 Joensuu, Finland.