Midsummer spatial variation in methane efflux fromstands of littoral vegetation in a boreal meso-eutrophiclake

PAULA KANKAALA*, SUVI MAKELA* , IRINA BERGSTROM†, EEVA HUITU*, TIINA KAKI ‡,

ANNE OJALA ‡, MIITTA RANTAKARI †, PIRKKO KORTELAINEN† AND LAURI ARVOLA*

*University of Helsinki, Lammi Biological Station, Lammi, Finland

†Finnish Environment Institute, Helsinki, Finland

‡Department of Ecological and Environmental Sciences, University of Helsinki, Niemenkatu, Lahti, Finland

SUMMARY

1. Spatial variation of methane (CH4) efflux from the littoral zone of a meso-eutrophic

boreal lake was studied with a closed-chamber technique for three summer days in 22

vegetation stands, consisting of three emergent and three floating-leaved species.

2. Between-species differences in CH4 emission were significant. The highest emissions

were measured from the emergent Phragmites australis stands (0.5–1.7 mmol m)2 h)1),

followed by Schoenoplectus lacustris > Equisetum fluviatile > Nuphar lutea > Sparganium

gramineum > Potamogeton natans. Within-species differences between stands were not

significant.

3. In P. australis stands, the stand-specific mean CH4 emission was significantly correlated

with solar radiation, probably indicating the role of effective pressurised ventilation on

CH4 fluxes. The proportion of net primary production emitted as CH4 was significantly

higher in P. australis stands (7.4%) than in stands of S. lacustris and E. fluviatile (both 0.5%).

4. In N. lutea stands, CH4 efflux was negatively correlated with the mean fetch and

positively with the percentage cover of leaves on the water surface. There were no

differences in CH4 efflux between intact N. lutea leaves and those grazed by coleopteran

Galerucella nymphaeae. In S. graminaeum and P. natans stands, CH4 effluxes were not related

to any of the measured environmental variables.

5. For all vegetation stands, the biomass above water level explained about 60% of the

observed spatial variation in CH4 emission, indicating the important role of plants as gas

conduits and producers of substrates for methanogens in the anoxic sediment.

Keywords: boreal lake, littoral vegetation, methane efflux, net ecosystem exchange

Introduction

Methane (CH4) is the major terminal product of the

anaerobic breakdown of organic carbon in freshwater

environments in the absence of alternative electron

acceptors [NO�3 , MnO2, FeO(OH), SO2�

4 ; cf. Capone &

Kiene, 1988]. As a radiatively important trace (RIT)

gas contributing to climate change (Houghton et al.,

2001), the processes leading to CH4 efflux from

natural water-logged areas, i.e. wetlands, as well as

from anthropogenic sources to the atmosphere, have

been intensively studied (reviewed e.g. by Bubier &

Moore, 1994; Segers, 1998; Le Mer & Roger, 2001).

Besides wetlands, the role of freshwater lakes as

sources and sinks of RIT gases (CO2, CH4 and N2O)

has also been recognized. Globally, the majority of

freshwater lakes and rivers are supersaturated with

CO2 because of mineralization of terrestrial organic

Correspondence: Paula Kankaala, University of Helsinki,

Lammi Biological Station, FIN-16900 Lammi, Finland.

E-mail: paula.kankaala@helsinki.fi

Freshwater Biology (2003) 48, 1617–1629

� 2003 Blackwell Publishing Ltd 1617

carbon in aquatic ecosystems (reviewed by Cole et al.,

1994; Cole & Caraco, 2001). High effluxes of CO2 and

CH4 to the atmosphere have been measured from

lakes with high organic matter content in the sediment

(Michmerhuizen, Striegl & McDonald, 1996; Riera,

Schindler & Kratz, 1999; Casper et al., 2000; Kortela-

inen et al., 2000). Methane emissions from littoral

areas in particular have exceeded those commonly

measured from boreal peatlands (Hyvonen et al.,

1998; Nykanen et al., 1998; Juutinen et al., 2001; Kaki,

Ojala & Kankaala, 2001). In northern regions, there are

millions of small shallow postglacial lake basins,

where the littoral zone dominates over the pelagic

(Wetzel, 1990). Thus, the littoral areas of lakes cannot

be omitted in the estimation of boreal carbon balances.

For instance, in Finland, lakes cover about 10% of the

surface area (Raatikainen & Kuusisto, 1990), and the

length of the lake shoreline is about 214 900 km

(unpublished statistics, Finnish Environment Insti-

tute). The shoreline of a Fennoscandian lake is

typically very irregular, with spatial variations in

species composition, density and biomass of littoral

vegetation on a scale of 1–100 m (Toivonen &

Lappalainen, 1980; Rørslett, 1991).

In vegetated littoral areas, the main route of CH4

from the anoxic sediment to the atmosphere goes

through aerenchymal tissues of emergent and float-

ing-leaved plants (Dacey & Klug, 1979; Sebacher,

Harriss & Bartlett, 1985). On the contrary, oxygen

transported by plants supports oxidation of CH4 in

the rhizosphere (King, 1996), and interspecific differ-

ences in the oxidizing capacity of aquatic plants have

been detected (Calhoun & King, 1997; van der Nat &

Middelburg, 1998b). The quality of plant detritus,

especially lignin content, and exposure of growing

sites to erosion by waves, influences long-term

accumulation or decomposition of plant detritus.

Thus, sediment biogeochemistry and CH4 fluxes from

the lake littoral zones may differ considerably within

short (1–50 m) distances (Juutinen et al., 2001; Kaki

et al., 2001).

Methane efflux from lake littoral areas and wet-

lands is commonly studied with a closed-chamber

technique in a few selected areas, where the chambers

are repeatedly placed on the same gas-tight collars

(e.g. Chanton & Whiting, 1995; Livingston & Hutch-

inson, 1995). Usually, solid constructions, such as

boardwalks, are necessary for sampling to avoid

disturbing gas exchange between soil–water–atmo-

sphere interfaces. Although a high temporal resolu-

tion can be achieved with automated sampling (e.g.

Loftfield et al., 1997), studying spatial variation of gas

fluxes in patchy environments with such systems is

difficult and expensive. Our study aimed to determine

how the species composition of macrophytes and

other environmental variables are related to spatial

variation of CH4 efflux in the littoral zone of a boreal

meso-eutrophic lake. A 3-day field study was carried

out on 17–19 July 2001 using an inexpensive design by

which the chambers could be handled from a rowing

boat and moved easily around among the stands of

emergent and floating-leaved vegetation. The samp-

ling period was selected to represent the annual

maximum of plant biomass, which is often found to

coincide with the annual peak of CH4 emissions

(Hyvonen et al., 1998; van der Nat & Middelburg,

2000; Juutinen et al., 2001).

Methods

Study area

Lake Ekojarvi is a small (area 0.74 km2, mean depth

2.4 m, maximum depth 8 m, volume 1.8 km3) head-

water lake in the Kokemaenjoki water course in

Lammi, Southern Finland (Fig. 1). Water samples

from the ice-free periods in 1997 and 1998 suggest

that the lake is mesotrophic; the mean concentrations

of total phosphorus, total nitrogen and chlorophyll a

at 1 m depth were 20, 616 and 12 lg L)1, respectively

(Huitu & Makela, 1999). Because of the polyhumic

character of the water (mean concentration of total

organic carbon 13.5 mg L)1) the Secchi depth of the

lake is only 1.0–1.5 m.

The vegetated littoral zone covers about 14% of

the lake surface, and altogether 19 species have been

observed in its flora of aquatic macrophytes (Huitu

& Makela, 1999). For gas flux studies, we chose 22

stands of aquatic plants, dominated by emergent and

floating-leaved plants (Fig. 1). Four of the stands

were dominated by Phragmites australis (Cav.) Trin.

ex. Steud., two by Schoenoplectus lacustris (L.) Palla,

three by Equisetum fluviatile (L.), six by Nuphar lutea

(L.) Sibth. & Sm., four by Sparganium gramineum

(Georgi) and three by Potamogeton natans (L.). Stands

in the northern part of the lake were chosen for easy

access and to avoid time delays between measure-

ments.

1618 P. Kankaala et al.

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

Methane efflux was studied with a closed-chamber

technique between 9:30 and 15:30 hours solar time

(GMT + 2 h) each day. At least three replicate meas-

urements were made for each measuring site (distance

between replicates <5 m). In the stands of emergent

vegetation, a cylindrical transparent polycarbonate

Equi1

Equi2

Equi3

Nuph2

Nuph1

Phrag1

Potam1

Phrag4

Phrag2

Symbol key

Phrag3

Potam2

Potam3

Nuph5Nuph4

Nuph3Nuph6

Sparg1

Sparg2

Sparg3

Sparg4

Schoe1

Schoe2N

0

km

Mixed Nuphar & Potamogeton

Schoenoplectus lacustris

Phragmites australis

Potamogeton natans

Sparganuim emersum

Nuphar lutea

Sparganium gramineum

Finland

Equisetum fluviatile

0.1 0.2

Care sp.

Measurement site

0 0.5

km

Lake Kuohijärvi

Lake Ekojärvi

Study area

Fig. 1 Study area and vegetation map of stands of emergent and floating-leaved plants in the northern part of Lake Ekojarvi

(61�57¢33¢¢N, 24�11¢46¢¢E). Asterisks indicate the flux measurement sites. For abbreviations of the vegetation stands, see Table 1.

Methane emissions from littoral vegetation 1619

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

chamber (height 1 m, diameter 0.36 m, volume 102 L,

light transmission 86–88% at 400–700 nm) was used

(Fig. 2). The chamber was equipped with a sampling

port and a fan (12 V DC) inside for air circulation. The

chamber hung vertically from an aluminium stan-

chion, which was fitted to the rowlock of the boat. The

shoots of the emergent plants in natural densities

were gently eased into the chamber and the bottom

edge of the chamber was adjusted to be about 10 cm

below the water surface. Care was taken not to disturb

the sediment surface with the chamber or the oars.

Prior to gas sampling, the vent hole on the top cover

of the chamber was closed gas tightly with sticky tape.

For net ecosystem exchange (NEE) of CO2, gas from

the chamber was pumped (2 L min)1) through a 1.2-

m long silicone tube (inner diameter 3 mm, wall

thickness 1 mm) to an LI-6252 CO2 analyser (LI-COR,

Inc., Lincoln, NE, USA). As it is known that gases can

permeate silicone, a check was carried out with test

gases of known CO2 concentration (363 and 103 ppm),

which were fed through a silicone tube as used in the

field and through a copper tube (inner diameter

1 mm, wall thickness 1 mm). This test revealed no

measurable CO2 permeability of the silicone tube

when the measurements were taken simulating in situ

conditions. The changes in CO2 concentration and

temperature inside the chamber (NTC thermistor),

and solar radiation (PAR 400–700 nm) outside the

chamber (LI-1905A 211 quantum sensor connected to

LI-1400 data logger; LI-COR Inc.), were recorded

every 30 s for 3 min. The chamber was then vented for

about 3 min through the vent hole. After closing the

hole, a time series of gas samples (0, 3, 6 and 9 min) for

CH4 analyses was taken through a 0.3-m long silicone

tube into 60-ml syringes (Terumo, Leuven, Belgium),

closed with three-way stopcocks (Luer Lock). The total

sampling time in each stand was usually <1 h; only in

one stand (SCHOESCHOE1) did sampling last 1.2 h. Among

the stands of floating-leaved vegetation, only CH4

fluxes were measured. The measurements in these

stands were made with small transparent floating

chambers (height 0.08 m, diameter 0.26 m, volume

4.1 L). The time series of gas samples (0, 3 and 6 min)

was obtained through a 0.3-m long silicone tube and

temperature inside the chamber was recorded. The

time between replicate samplings among floating-

leaved plants was <10 min. One rower could normally

keep the boat stationary during the sampling; only in

three cases was gas sampling disturbed as the

chamber drifted off the shoots or leaves.

After the gas sampling, the number of shoots

(emergent plants) or leaves (floating-leaved) in the

chamber was counted. For biomass determinations,

the shoots of the emergent plants were cut just above

the sediment surface and the emerged and submerged

parts were separated. For the floating-leaved plants,

only the shoots with leaves rising above the surface

level were taken, and those that did not reach the

water surface were ignored. The plants were dried at

60 �C for 48 h and weighed (precision 0.01 g). Water

Fig. 2 A schematic figure of the polycar-

bonate chamber used in gas flux studies.

(1) Rope to adjust the bottom edge of the

chamber below the water level, (2) vent

hole to be closed prior to gas sampling,

(3) fan connected to a 12 V battery,

(4) sampling port connected with silicone

tube to a pump or a syringe. The tem-

perature probe inside the chamber is not

shown.

1620 P. Kankaala et al.

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

depth at each study site was recorded and the water

temperature was measured at 0.20 m depth and above

the sediment surface (YSI combined probe). Data for

weather variables were obtained from an automatic

weather station (recording at 10 min intervals) situ-

ated 1.5 m above the ground level in an open field

14 km south of Lake Ekojarvi (Potato Research Insti-

tute, Lammi, Finland).

Methane samples were analysed in the laboratory

within 6 h of sampling with an HP 5710A gas

chromatograph (FID, HayeSepQ column: mesh 80/

100; Alltech Inc., Deerfield, IL, USA) equipped with a

0.5-ml loop on a VALCO 10-port valve (VICI, Houston,

TX, USA). Net ecosystem exchange rate was calculated

as a linear decrease in CO2, and CH4 efflux as a linear

increase in CH4 over time. Only those regression

equations with r2 values >0.9 were accepted, and the

results in mmol m)2 h)1 were calculated according to

the ideal gas law. For the emergent vegetation stands

11% (three of 27) and for the floating-leaved vegetation

14% (nine of 63) of the results were rejected because of

an erratic jump in CH4 concentration, probably a result

of ebullition during the sampling period.

For additional information on the stands of floating-

leaved vegetation, the percentage cover of the studied

stands was estimated about 5 days later from five

randomly chosen plots of an area of 0.25 m2. The

length and width of the leaves were measured

(precision 0.5 cm) in each plot, and the leaf surface

area was calculated with geometric formulae accord-

ing to Makela et al. (1992).

Sediment samples from the emission study sites

were taken with steel corers (diameter 4 or 9 cm) from

the uppermost 30-cm sediment layer, where the bulk

of the roots and rhizomes exists. Two cores from each

vegetation stand were pooled, and water content, dry

weight (105 �C) and loss on ignition (LOI % of DW at

550 �C) of the sediment were determined by standard

methods from five subsamples excluding roots and

rhizomes. The exposure of the vegetation stands to

waves was assessed by calculating the mean fetch

(MF, m) in five directions from the shoreline (0�, 45�,90�, 135�, 180�) as described by Cyr (1998).

The efflux results in relation to environmental var-

iables were analysed with CANOCOCANOCO (Ter Braak, 1995)

and SYSTATSYSTAT 9 (SPSS, Inc.) program packages. Principal

component analysis (PCA) was used to summarise and

visualise the major patterns of variation in CH4 emis-

sions and other differences between the vegetation

stands. These variables were shoot/leaf density (m)2),

biomass of plants above the water surface (g m)2),

mean shoot/leaf weight (g), sediment LOI, water depth

(m) and MF (m) (Table 1). The mean values for each

stand were used in the analysis, as the shoots of clonal

plants are connected together via the rhizosphere (cf.

Dacey, 1981). Thus, the CH4 gas transported could not

be related only to the shoots in the chambers. All data

were log-transformed prior to analysis.

Results

Weather conditions and NPP

During the field study the weather conditions were

consistently calm (mean wind speed 1.4 m s)1; range

0.7–2.6 m s)1). The mean air temperature during gas

flux measurements was 23.4, 22.5 and 21.8 �C for the

first, second and third day, respectively (range 20.4–

24.9 �C). The water temperature in the studied veget-

ation stands at 0.2 m depth below water surface varied

between 21.9 and 24.2 �C and at 0.2 m from bottom

between 21.3 and 22.9 �C. In general, the weather was

sunny but, because of occasional clouds, solar radiation

varied between 70 and 1567 lmol m)2 s)1. Throughout

the study period, the NEE of CO2 in the emergent vege-

tation stands was negative. Thus, primary productivity

exceeded the community respiration rate, and results in

Fig. 3 are given as net primary productivity (NPP).

In the stands of P. australis, NPP varied between 0.8

and 9.1 mmol C m)2 h)1 (Fig. 3). A good fit to our

data was given by the following Michaelis–Menten

equation:

NPPðmmol C m�2 h�1Þ ¼ Pmax � I=ðKm þ IÞ;

where NPP is net primary productivity (mmol

C m)2 h)1), Pmax is the maximum rate of productivity

(mmol C m)2 h)1), I is solar radiation (lmol m)2 s)1),

Km is the half-saturation constant, i.e. the solar

radiation where half of the maximal rate of produc-

tion is achieved. Values for Pmax and Km were

19.9 mmol C m)2 h)1 and Km 2269 lmol m)2 s)1,

respectively. In the stands of S. lacustris and

E. fluviatile, NPP was of the same order of magnitude

(1.6–9.2 and 3.0–7.4 mmol C m)2 h)1, respectively) as

measured in P. australis stands, but it was less clearly

related to solar radiation (Fig. 3). In the emergent

vegetation stands studied, NPP was correlated with

neither the density nor the biomass of shoots.

Methane emissions from littoral vegetation 1621

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

CH4 effluxes in relation to environmental variables

Mean CH4 efflux from 22 emergent and floating-

leaved vegetation stands ranged from 0.07 to

1.7 mmol m)2 h)1 (Fig. 4). When the CH4 emissions

were related to environmental variables in the PCA,

the first axis corresponded to shoot biomass and

CH4 efflux, and separated sampling sites with high/

low efflux and high/low shoot biomass per unit

area, and the second axis represented mostly the

proportion of organic matter in sediment (LOI) and

MF (Fig. 5). Axes 1 and 2 had eigenvalues of 0.51

and 0.25, respectively, and accounted for 76.1% of

the total variance in the environmental data. Four

groups of vegetation could be distinguished along

the PCA ordination. The first group was formed by

P. australis (PHRAG)PHRAG) stands, showing high CH4

efflux (mean 0.5–1.7 mmol m)2 h)1; Fig. 4) and high

biomass per plant shoot and per area unit. The

second group was formed by E. fluviatile (EQUIEQUI) and

S. lacustris (SCHOESCHOE) stands. They grew in dense

stands but were more wave-exposed and released

CH4 more slowly than did P. australis stands. The

third group was formed by all N. lutea (NUPHNUPH)

stands. They favoured soft organic sediments and

released CH4 significantly more slowly than P.

australis stands. The fourth group, from which CH4

effluxes were lowest, consisted of P. natans (POTAMPOTAM)

and S. graminaeum (SPARGSPARG) stands.

The differences in CH4 efflux from the stands of

different macrophyte species were further tested with

ANOVAANOVA. Because of large variation within stands

Table 1 Mean ± SE shoot/leaf density m)2, shoot/leaf biomass above water surface (g DW m)2), percentage cover of leaves in

floating-leaved vegetation stands, percentage share of organic matter in the sediment dry weight (LOI), water depth (m) and mean

fetch (m) in vegetation stands on 17–19 July 2001. Number of samples (n) for shoot/leaf density and biomass was the same (given in

parentheses). The location of the stands is shown in Fig. 1

Stand

Shoot/leaf

density (m)2)

Biomass

(g m)2)

Cover

(%)

Sediment

(LOI)

Depth

(m)

Mean

fetch (m)

Phragmites australis

Phrag1 68.8 ± 11.3 (3) 98.0 ± 17.4 42.6 0.51 155

Phrag2 62.2 ± 8.7 (3) 88.2 ± 9.0 35.3 0.42 60

Phrag3 45.8 ± 8.7 (3) 85.4 ± 18.3 5.5 0.56 218

Phrag4 49.1 ± 5.8 (3) 199.8 ± 20.8 90.8 0.50 213

Schoenoplectus lacustris

Schoe1 117.9 ± 20.5(3) 121.5 ± 13.1 2.7 0.48 411

Schoe2 91.7 ± 17.3 (3) 73.8 ± 11.3 9.1 0.91 114

Equisetum fluviatile

Equi1 196.4 ± 15.0(3) 99.6 ± 10.4 13.9 0.83 186

Equi2 108.1 ± 24.7(3) 53.1 ± 18.3 21.1 0.96 214

Equi3 95.0 ± 14.3 (3) 51.3 ± 3.9 7.7 0.60 291

Nuphar lutea

Nuph1 10.4 ± 1.8 (5) 35.0 ± 6.1 26.1 37.4 0.98 151

Nuph2 9.6 ± 2.1 (5) 25.5 ± 5.6 24.2 39.2 1.05 227

Nuph3 11.6 ± 2.1 (5) 10.1 ± 1.0 16.1 37.4 0.78 322

Nuph4 13.6 ± 3.3 (5) 36.8 ± 8.9 35.5 29.4 0.71 37

Nuph5 15.6 ± 1.4 (5) 22.0 ± 1.9 39.0 26.7 0.79 62

Nuph6 8.0 ± 1.1 (5) 9.5 ± 1.3 22.6 21.3 0.63 186

Sparganium gramineum

Sparg1 23.4 ± 5.9 (5) 0.7 ± 0.2 0.8 38.7 0.62 251

Sparg2 100.0 ± 20.7 (5) 10.4 ± 2.2 3.6 23.4 0.62 40

Sparg3 29.3 ± 10.6 (5) 2.2 ± 0.8 1.1 34.4 0.49 188

Sparg4 44.0 ± 8.0 (5) 3.1 ± 0.6 2.0 13.1 0.42 136

Potamogeton natans

Potam1 52.8 ± 12.9 (5) 6.6 ± 1.6 14.5 24.8 0.98 149

Potam2 82.4 ± 4.9 (5) 16.3 ± 1.0 22.6 2.2 0.91 152

Potam3 35.2 ± 7.5 (5) 5.9 ± 1.3 9.6 4.5 0.60 295

LOI, loss on ignition.

1622 P. Kankaala et al.

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(Fig. 4), all observations for each macrophyte species

were first pooled and log-transformed. The CH4

emissions from P. australis stands were significantly

greater than those from any other type of stand,

whereas the CH4 effluxes from P. natans stands were

significantly smaller than those from other stands,

except for stands of S. graminaeum (ANOVAANOVA, Tukey’s

test, P < 0.001, Table 2). This result was not influenced

by the three outlier observations (two for P. australis

and one for P. natans), which were excluded from

ANOVAANOVA, in order better to meet the requirement of

variance homogeneity. No within-species differences

were present in CH4 effluxes, but this result was

probably influenced by the high variation between

replicate measurements and the low number of

observations for each stand. Only stands of N. lutea

showed within-species differences close to signifi-

cance (P ¼ 0.052, n ¼ 18, d.f. ¼ 4).

About 90% of the variation in CH4 efflux in all

stands of emergent macrophytes was explained by the

following multiple regression model:

CH4 effluxðmmol m�2 h�1Þ ¼ 0:221 þ 0:483 � PW

� 0:002 � MF;

where PW is mean dry weight of plant shoots above

water surface (g) and MF is mean fetch (m) of the

growing site (n ¼ 9, r2 ¼ 0.86, P ¼ 0.001). Methane

effluxes were only weakly related to the immediate

measurements of NPP of specific plants in the

chambers. Variation between replicate CH4 emission

measurements was especially high in the PHRAGPHRAG4

stand (Fig. 4), where the measurements were made on

a bright afternoon, following cloudy weather in the

morning. In stands of P. australis, however, a linear

relationship was found between stand-specific mean

values of CH4 effluxes and NPP (r2 ¼ 0.987) as well as

between the mean CH4 emission and mean solar

radiation (r2 ¼ 0.963). Such relationships were not

present in S. lacustris and E. fluviatile stands (Fig. 6).

The proportion (%) of released CH4 to NPP, in units

of carbon, was significantly higher (d.f. ¼ 21, P <

0.001) in P. australis stands (mean ± SE, 7.4 ± 0.5%)

than in stands of S. lacustris and E. fluviatile

(0.5 ± 0.1% in both).

In stands of S. graminaeum and P. natans, CH4

emissions were not related to any of the measured

environmental variables. In N. lutea stands, CH4 efflux

was negatively correlated with the MF (m) of the

0

1

2

3

Phr

ag1

Phr

ag3

CH

4 ef

flux

(mm

ol m

–2 h

–1)

0.00

0.05

0.10

0.15

0.20

Sch

oe1

Equ

i2

Nup

h2

Nup

h4

Nup

h6

Spa

rg1

Pot

am1

Phr

ag2

Phr

ag4

Sch

oe2

Equ

i1

Equ

i3

Nup

h1

Nup

h3

Nup

h5

Spa

rg2

Spa

rg3

Spa

rg4

Pot

am2

Pot

am3

Fig. 4 Mean emission (±SE) of CH4 from vegetation stands in Lake Ekojarvi on 17–19 July 2002. Note the different scale for Phragmites

australis stands.

2

4

6

8

10

0 500 1000 1500 2000

Irradiance (µmol m–2 s–1)

P. australis

S. lacustris

E. fluviatile

NP

P (

mm

ol C

m–2

h–1

)

Fig. 3 Relationship between irradiance (lmol m)2 s)1) and net

primary productivity (NPP; mmol C m)1 h)1) in emergent

vegetation stands. The Michaelis–Menten function is fitted only

to results for Phragmites australis stands. See text for the

parameters of the model.

Methane emissions from littoral vegetation 1623

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

growing site according to the following linear equa-

tion:

CH4 effluxðmmol m�2 h�1Þ ¼ 0:068 � 0:00018MF;

which explained 73% of the variation (n ¼ 6,

P ¼ 0.031). The percentage cover of leaves in the

vegetation stands explained almost as much of the

variation (r2 ¼ 0.692). However, there was a signifi-

cant negative correlation between MF and percentage

cover of leaves (r2 ¼ 0.903) in N. lutea stands and,

thus, the influences of these variables on CH4 efflux

cannot be separated from each other.

The influence of grazing of N. lutea leaves by

its herbivore Galerucella nymphaeae L. (Coleoptera,

Fig. 5 Principal component analysis ordi-

nation of CH4 effluxes and environmental

variables from the vegetation stands in

Lake Ekojarvi. For abbreviations see

Table 1.

Table 2 Mean ± SE of all observations of CH4 efflux from stands of emergent and floating-leaved species (mmol m)2 h)1) in Lake

Ekojarvi on 17–19 July 2001

P. australis S. lacustris E. fluviatile N. lutea S. gramineum P. natans

Mean efflux 1.16 ± 0.33 0.09 ± 0.02 0.07 ± 0.01 0.04 ± 0.01 0.04 ± 0.01 0.02 ± 0.01

n 10 6 8 21 10 17

P. australis 1

S. lacustris <0.001 1

E. fluviatile <0.001 1.0 1

N. lutea <0.001 0.20 0.37 1

S. gramineum <0.001 0.03 0.06 0.72 1

P. natans <0.001 <0.001 <0.001 0.002 0.43 1

Significant differences between species tested with A N O V AA N O V A from log-transformed data and Tukey’s Honest Significant Difference as a

post-hoc test.

P. australis, Phragmites australis; S. lacustris, Schoenoplectus lacustris; E. fluviatile, Equisetum fluviatile; N. lutea, Nuphar lutea;

S. gramineum, Sparganium gramineum; P. natans, Potamogeton natans.

1624 P. Kankaala et al.

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

Chrysomelidae), which was abundant on our study

sites, on CH4 release was tested by separating the

efflux data for intact and heavily perforated leaves, i.e.

those with >10 holes per leaf. The statistical analysis

(Mann–Whitney U test) revealed, however, that per-

forations did not affect CH4 efflux (mean ± SE for

intact leaves 0.039 ± 0.033 mmol m)2 h)1, n ¼ 11; per-

forated leaves 0.035 ± 0.008 mmol m)2 h)1, n ¼ 7;

U ¼ 38.0, P ¼ 0.964).

As indicated by PCA (Fig. 5), including the emer-

gent and floating-leaved vegetation together, CH4

effluxes were significantly correlated with the biomass

of the vegetation stands. This relationship was not

linear but, after a log-transformation of the efflux

values, the assumptions of regression analysis (nor-

mal distribution and homogeneity of variances) were

approximately met. An exponential model:

CH4 effluxðmmol m�2 h�1Þ ¼ 0:02 � e0:024�biom;

where BIOMBIOM refers to dry weight of the biomass (g m)2)

above the water surface, explained 57% of the observed

variation in CH4 efflux (n ¼ 22, P < 0.001). The short

measurement period in similar weather conditions

ensured that the effect of spatial and temporal variation

of temperature (maximum difference above sediment

surface 1.6 �C) on results was negligible.

Discussion

The species composition of emergent and floating-

leaved plant communities had a significant influence

on spatial variation of CH4 effluxes from the veget-

ated littoral zone of Lake Ekojarvi. The highest CH4

efflux was measured from stands of P. australis, which

is known to have a pressurised convective flow

mechanism to transport oxygen effectively to roots

and rhizomes in anoxic sediments and to ventilate

CH4 out from the rhizosphere (Armstrong & Arm-

strong, 1990, 1991; Brix, Sorrell & Orr, 1992; Arke-

bauer et al., 2001; Brix, Sorrell & Lorenzen, 2001;

Strand, 2002). Fluctuations in solar radiation, tem-

perature and relative humidity cause short-term

changes in pressurisation and, thus, influence CH4

flux though plants. Because of the convective flow in

actively growing plants, the daytime CH4 emissions

are usually two to four times higher than those at

night, when CH4 is passed only by diffusion (Kim,

Verma & Billesbach, 1998; van der Nat & Middelburg,

1998a; Brix et al., 2001; Kaki et al., 2001). In a veget-

ation stand, air enters through young, healthy emer-

gent (influx) leaves/shoots and, because of the

pressure difference, air is forced through the aeren-

chymatous tissues to the common rhizome and then

out through older or damaged (efflux) leaves/shoots

(Dacey, 1981; Armstrong & Armstrong, 1991; Allen,

1997). The presence of influx and efflux culms can

explain the somewhat ambiguous observation that, in

stands of P. australis in Lake Ekojarvi, a significant

linear correlation was present between stand-specific

mean CH4 efflux and mean solar radiation, whereas

such a correlation did not exist when these variables

were related to specific plants in the measurement

1

2

3

4

5

0 500 1000 1500 2000

Irradiance (µmol m–2 s–1)

CH

4 ef

flu

x (m

mo

l m–2

h–1

)

P. australis, ssm P. australis, cs S. lacustris, cs E. lacustris, cs

y = 0.293 + 0.001x

r 2 = 0.963

Fig. 6 Relationship between mean irradi-

ance and stand-specific mean efflux of

CH4 in Phragmites australis stands (ssm,

drawn with SE bars) fitted with the linear

model, and chamber-specific CH4 effluxes

(cs) related to irradiance in all emergent

vegetation stands.

Methane emissions from littoral vegetation 1625

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

chambers. Besides the random occurrence of influx or

efflux culms in the chambers, the amount of accumu-

lated CH4 in the rhizomes could have varied and,

thus, affected the measured efflux.

In Lake Ekojarvi, the CH4 efflux from the stands of

two other emergent macrophytes, S. lacustris and E.

fluviatile, was only 3–12% of that measured in daytime

from P. australis stands. Distinct from P. australis,

pressurised convective flow appears not to be the

main mechanism of rhizome ventilation for these

species. This conclusion, based on earlier observations

of insignificant diel variations in CH4 emissions

(Hyvonen et al., 1998; van der Nat & Middelburg,

1998a), is supported by our finding of a lack of

correlation between CH4 emissions and solar radia-

tion. Furthermore, the flow rates in the shoots of

S. lacustris are low, and non-detectable in E. fluviatile,

compared with the high rates in P. australis, Typha

angustifolia, T. latifolia and Sparganium sp. (Strand,

2002). Despite the lack of pressurised ventilation,

E. fluviatile and S. lacustris are able to grow in deeper

waters and on more exposed shores than P. australis

(Toivonen & Lappalainen, 1980; Strand, 2002), which

was also found in Lake Ekojarvi.

According to van der Nat & Middelburg (1998b),

the sediment oxidation capacity of S. lacustris is

greater than that of P. australis. However, CH4

emission from tidal freshwater marshes dominated

by S. lacustris and P. australis was largely determined

by variations in CH4 production rather than variations

in storage and oxidation of CH4 in the sediment (van

der Nat & Middelburg, 1998a, 2000). In Lake Ekojarvi,

organic matter content of the sediment was greater in

sites where P. australis grew with the exception of one

stand, than in those with S. lacustris and E. fluviatile,

but the relationship between CH4 emissions and

organic matter content of the sediment was not clear.

The role of other factors, apart from the organic matter

content of sediment, is also highlighted when compar-

ing the results with those from Lake Paajarvi. In that

lake, the organic matter content of the sediment in

E. fluviatile stands was smaller (5–10% of DW) than

that in the respective stands in Lake Ekojarvi (8–21%

of DW), but the summertime emissions of CH4 were

more than five times greater (0.7–1.8 mmol m)2 h)1;

Hyvonen et al., 1998) than those from Lake Ekojarvi

(0.04–0.12 mmol m)2 h)1). Thus, the organic matter

content of the littoral sediment appears to be a poor

indicator of plant-mediated CH4 effluxes and metha-

nogenic activity in the sediment (L. Lehtinen &

P. Kankaala, unpublished). In the compiled data of

CH4 fluxes from all emergent vegetation stands of

Lake Ekojarvi, mean shoot weight and MF of the site

explained 90% of the spatial variation. This result

indicates the adaptation of P. australis to grow in more

sheltered and anoxic sediments than E. fluviatile and

S. lacustris and, perhaps because of pressurised

ventilation, the CH4 produced in the sediment is

efficiently ventilated to the atmosphere through the

few but tall shoots of P. australis.

In Lake Ekojarvi, the highest CH4 emissions from

N. lutea stands were measured from the most shel-

tered sites with a low MF and the highest cover of

leaves per water surface. This probably indicates

greater anoxia and the more important role of floating

leaves as routes for CH4 flux in the sheltered sites

compared with the more open ones. Dacey (1981)

showed that because of pressurised ventilation the

rate of CH4 flux through Nuphar leaves increased

when they were torn. We could not find any differ-

ences in CH4 effluxes between intact leaves and those

grazed by G. nymphaeae. The identification of intact

leaves as ‘young’ and ‘old’, i.e. influx and efflux

leaves, was not possible by visual observation alone.

However, Kouki (1991) reported from Lake Ridasjarvi

(Southern Finland) that G. nymphae occupied all N.

lutea leaves after emergence, but the proportion of leaf

area eaten varied between 13 and 23%. Thus, if this is

valid also for N. lutea in Lake Ekojarvi, the intact

leaves cannot be regarded as ‘old’. Thus, it seems that

factors other than herbivory by G. nymphae appear to

be more important for CH4 release through N. lutea.

In the stands of S. gramineum and P. natans, CH4

efflux was not related to any of the measured

environmental variables, probably because of spor-

adic ebullition. Heilman & Carlton (2001) observed

that bubbles of gas from submerged floral spikes of

Potamogeton angustifolius Berchtold Presl. represented

19–29% of the total areal CH4 flux in a small meso-

eutrophic lake (Pleasant Lake, MI, U.S.A.) in late

summer and early autumn. In our study, 14% of the

samplings in the floating-leaved vegetation in Lake

Ekojarvi showed ebullitive release of CH4. However,

the bubbles directly from the sediment and those from

the submerged shoots of vegetation could not be

separated.

In Lake Ekojarvi, the variation of plant biomass

above water surface explained about 60% of the

1626 P. Kankaala et al.

� 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 1617–1629

spatial variation in midsummer CH4 efflux in the

vegetated littoral area. This relationship reflected

both the role of plants as gas conduits from the

anoxic sediment and the importance of plants pro-

ducing low-molecular substrates for methanogens

(Dacey & Klug, 1979; Sebacher et al., 1985; Whiting &

Chanton, 1993; Joabsson & Christensen, 2001). In a

large data set from boreal to subtropical wetland

ecosystems, Whiting & Chanton (1993) showed that

CH4 efflux was better correlated with NPP than with

live biomass of vegetation. We measured NPP only

for the emergent vegetation stands and for a short

time period, and thus the role of spatial variation of

NPP cannot be estimated for the whole littoral

vegetation. In our short-term measurements in Lake

Ekojarvi, the proportion of released CH4 to NPP was

significantly higher in P. australis stands (7.4%) than

in S. lacustris and E. fluviatile stands (0.5%). Brix et al.

(2001) estimated that on an annual basis up to 15%

of the net carbon fixed by P. australis wetlands is

released as CH4 to the atmosphere, whereas in the

data set of Whiting & Chanton (1993) this proportion

was 3%.

Our results on the variation in CH4 efflux between

different vegetation stands agree with those of Juuti-

nen et al. (2001) from the littoral zone of a mesotrophic

boreal lake (Heposelka), where the CH4 efflux was

greatest from the permanently flooded Phragmites

and Carex marshes (maximum values 0.7–

0.8 mmol m)2 h)1). In Lake Ekojarvi, CH4 emissions

from P. australis stands were within the range of those

measured in June–September from dense P. australis

stands in the meso-eutrophic boreal Lake Vesijarvi

(midday values 0.4–3.6 mmol m)2 h)1; Kaki et al.,

2001). The chamber technique applied in our study

of the gas flux from emergent macrophytes could be

used only in water deeper than 0.4 m, and thus

vegetation stands higher up in the littoral zone

(mainly Carex spp.) were not included. In this

temporarily flooded littoral zone, the seasonal dynam-

ics of CH4 efflux is greatly affected by changes in

water level, the flux being greatest during the spring

flood (Juutinen et al., 2001).

In conclusion, the spatial variation in CH4 efflux

from the vegetated littoral zone is significantly influ-

enced by the species composition, and perhaps also by

the mode of rhizome ventilation of the emergent and

floating-leaved plants, as well as by the fetch of the

growing site. The significant correlation between the

shoot biomass of macrophytes and CH4 efflux indi-

cates both the role of plants as gas conduits from the

anoxic sediment and the importance of plants produ-

cing substrates for methanogens.

Acknowledgments

The study was supported by the Academy of Finland

(project no. 47099, 47100 and 50389). We thank Merilin

Pienimaki and Beate Bois for help with the field work

and with the laboratory analyses; Seppo Anttila, who

let us use his premises for launching boats and storing

equipment; Paavo Kuisma (Potato Research Institute)

for weather data; the comments of two referees

improved the manuscript.

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