Invasive alien plants increase CH4 emissionsfrom a subtropical tidal estuarine wetland

Chuan Tong • Wei-Qi Wang • Jia-Fang Huang •

Vincent Gauci • Lin-Hai Zhang •

Cong-Sheng Zeng

Received: 8 May 2011 / Accepted: 5 February 2012 / Published online: 22 February 2012

� Springer Science+Business Media B.V. 2012

Abstract Methane (CH4) is an important greenhouse

gas whose emission from the largest source, wetlands

is controlled by a number of environmental variables

amongst which temperature, water-table, the avail-

ability of substrates and the CH4 transport properties of

plants are most prominent and well characterised.

Coastal wetland ecosystems are vulnerable to invasion

by alien plant species which can make a significant

local contribution to altering their species composition.

However the effect of these changes in species

composition on CH4 flux is rarely examined and so is

poorly understood. Spartina alterniflora, a perennial

grass native to North America, has spread rapidly along

the south-east coast of China since its introduction in

1979. From 2002, this rapid invasion has extended to

the tidal marshes of the Min River estuary, an area that,

prior to invasion was dominated by the native plant

Cyperus malaccensis. Here, we compare CH4 flux

from the exotic invasive plant S. alterniflora with

measurements from the aggressive native species

Phragmites australis and the native species C. malacc-

ensis following 3-years of monitoring. CH4 emissions

were measured over entire tidal cycles. Soil CH4

production potentials were estimated for stands of each

of above plants both in situ and in laboratory incuba-

tions. Mean annual CH4 fluxes from S. alterniflora,

P. australis and C. malaccensis dominated stands over

the 3 years were 95.7 (±18.7), 38.9 (±3.26) and 10.9

(±5.26) g m-2 year-1, respectively. Our results dem-

onstrate that recent invasion of the exotic species S.

alterniflora and the increasing presence of the native

plant P. australis has significantly increased CH4

emission from marshes that were previously domi-

nated by the native species C. malaccensis. We also

conclude that higher above ground biomass, higher

CH4 production and more effective plant CH4 transport

of S. alterniflora collectively contribute to its higher

CH4 emission in the Min River estuary.

Keywords Methane emission � Inundation �Plant-mediated transport � Spartina alterniflora �Phragmites australis � Cyperus malaccensis

Introduction

Methane (CH4) is an important greenhouse gas, which

is responsible for approximately 20% of radiative

forcing (IPCC 2007). Biogenic sources account for

more than 70% of total global CH4 emission and the

C. Tong (&) � W.-Q. Wang � J.-F. Huang �L.-H. Zhang � C.-S. Zeng

Research Centre for Wetlands in Sub-tropical Regions,

Key Laboratory of Humid Subtropical Eco-geographical

Process of Ministry of Education, School of Geographical

Sciences, Fujian Normal University, Fuzhou 350007,

China

e-mail: Tongch@fjnu.edu.cn

V. Gauci

Department of Environment, Earth and Ecosystems,

CEPSAR, The Open University, Milton Keynes, UK

123

Biogeochemistry (2012) 111:677–693

DOI 10.1007/s10533-012-9712-5

single largest CH4 source is natural wetlands (IPCC

2007). CH4 emissions from natural wetlands are

strongly influenced by environmental factors which

vary both spatially and temporally. The variability is

related to temperature, topography and vegetation

(Ding et al. 2003; Hirota et al. 2004; Kankaala et al.

2004; Koelbener et al. 2010). Plants act as a key

control on the spatial variability of CH4 flux due to

their influence on CH4 production, oxidation (Hirota

et al. 2004; Koelbener et al. 2010) and, in particular,

on CH4 transport with several studies demonstrating

that aerenchymatous plants are the dominant CH4

emission pathway in these ecosystems (Joabsson and

Christensen 2001; Strom et al. 2005). Coastal and

estuarine wetlands have particularly high net primary

productivity which is known to influence CH4 pro-

duction and several studies have quantified CH4

emissions from these ecosystems (e.g. DeLaune

et al. 1983; Bartlett et al. 1987; Magenheimer et al.

1996; van der Nat and Middelburg 2000; Chang and

Yang 2003).

The invasion of exotic plant species has been

identified as one of the most important problems

facing Earth’s natural ecosystems as invasive alien

species threaten biodiversity, ecosystem structure and

function (Walker and Smith 1997). The impacts of

plant invasion on biogeochemical processes in grass-

land and forest ecosystems have received considerable

attention in recent years especially in studies con-

cerned with above ground and soil nutrient cycling

processes (Ehrenfeld and Scott 2001; David et al.

2004; Bradley et al. 2006; Koutika et al. 2007; Litton

et al. 2008). However, there has been far less work on

the effects of plant invasion on carbon cycling of

estuarine wetland ecosystems (Cheng et al. 2006,

2007; Liao et al. 2007; Zhang et al. 2010) which are

particularly vulnerable to species invasion as 24% of

the world’s most invasive plants are wetland species

(Zedler and Kercher 2004). To our knowledge, no

published research has compared CH4 emissions from

wetlands colonized by exotic invasive species and

native aggressive species with emissions from local

native species.

In China, the area of tidal wetlands has been

estimated at more than 1.2 9 104 km2 (Huang et al.

2006), comprising an important component of the

world’s tidal wetland resource. Spartina alterniflora

(smooth cordgrass) is a native species of brackish

marshes and salt marshes of the Atlantic and Gulf

Coasts of North America. In 1979, S. alterniflora was

deliberately introduced to the Luoyuan Bay on the

Fujian coast, south-east China, and then to the Yangtze

estuary in 1990s. The goal of this introduction was to

increase the protection of coastal banks and to

accelerate sedimentation and land formation (Liao

et al. 2007). S. alterniflora has invaded Scirpus

mariqueter salt marshes in the Yangtze estuary rapidly

(Chung et al. 2004). Indeed, this rapid spread of

S. alterniflora was one of the principal impacts noted

over the past decade affecting native plant communi-

ties in the estuaries and marshlands of south-east

China (Deng et al. 2006). In 2003, S. alterniflora was

designated by the Chinese Environmental Protection

Agency (Chinese Environmental Protection Agency

2003) as one of 16 invasive exotic plants. Information

on CH4 emission from ecosystems invaded by S. alt-

erniflora is therefore urgently needed yet we know of

only two experimental mesocosms studies which

investigated the effects of invasive wetland plant on

CH4 emissions. One in which higher CH4 emissions

were observed from S. alterniflora than from Phrag-

mites australis (common reed) (Cheng et al. 2007),

and another where emissions from S. alterniflora

exceeded those from Suaeda salsa (Zhang et al. 2010).

The Shanyutan wetland is the largest tidal wetland

located in the mouth of the Min River estuary, south-east

China (Fig. 1). In its middle-west part, the native marsh

species Cyperus malaccensis var. bervifolius extends

from the intertidal zone to near the bank. Local historical

records show that S. alterniflora began to invade this

marsh in 2002 and since then it has gradually expanded

its cover from the zone closest to the sea to the intertidal

zone and from about 2004 S. alterniflora has invaded

patches in the C. malaccensis-dominated marsh zone.

P. australis colonized this site about 30–40 years

presumably by dispersal from stands of this species

present in the upper section of the Min River estuary.

Since then it has invaded many part of the marsh

formerly dominated by C. malaccensis. P. australis may

be one of the most widely distributed plants in the world

(Marks and Randall 1993) and is native to China where

it dominates the intertidal zone in many estuarine and

deltaic areas.

We made frequent CH4 flux measurements in the

Shanyutan wetland from 2007 to 2009. The objective

of this study was to extend our knowledge of the

effects of invasive species on CH4 emissions from

tidal estuarine marshes. There were five aspects to the

678 Biogeochemistry (2012) 111:677–693

123

study: first, we tested the hypothesis that invasion of

the native community dominated C. malaccensis by

aggressive species alters the CH4 cycling processes;

second, we examined the seasonal and inter-annual

changes in CH4 flux as determined by the three

different plant species; third, we evaluated the vari-

ations in CH4 flux during exposed and submerged

periods of the tidal cycle, to include three tidal stages

(prior to flooding, during flooding and ebbing, and

after ebbing); fourth, we investigated the effects of

environmental variables on CH4 flux; and finally, in

order to explain any differences in CH4 flux from

stands dominated by each of the three plants, we

measured soil CH4 production potential (both in situ

and in laboratory incubation studies), and also quan-

tified the CH4 flux mediated by each of the three plants

in question both at the individual and population level.

Materials and methods

Site description

This study was conducted within the central-western

portion of the Shanyutan wetland (Longitude,

119�3401200–119�4004000; Latitude, 26�0003600–26�0304200). Climate at the study site is warm and

wet, with a mean annual temperature of 19.6�C and

a mean annual precipitation of 1,350 mm (Zheng

et al. 2006). Within this area there is a mosaic

vegetation landscape dominated by native species

C. malaccensis stands with patches of the alien

invasive plant S. alterniflora, and the native aggres-

sive species P. australis. We selected a C. malacc-

ensis stand, and two stands dominated, respectively,

by S. alterniflora and P. australis. These three

stands were adjacent, and were all pure stands

(monocultures) with clear boundaries between them.

Each of these three observation sites is \20 m apart

and, aside from the plant composition, the area was

otherwise homogenous.

In our study site, tides are considered to be typical

semi-diurnal tides where the soil surface is submerged

for about 7 h over a 24 h cycle. There is normally

between 10 and 150 cm of water above the soil surface

at tide. At other times the soil surface is completely

exposed. The average salinity of the tidal water (May

to December, 2007) was 4.2 ± 2.5%. In December,

2007, the SO42- concentration was 715 ± 55 mg l-1

in tidal water and 250 ± 95 and 395 ± 241 mg l-1 in

Fig. 1 Location of the

study area and sampling site

(filled triangle) in the

Minjiang River estuary

Biogeochemistry (2012) 111:677–693 679

123

the sediment pore water (0–10 and 10–20 cm depth,

respectively).

Total organic carbon (TOC) content of the soil

(0–50 cm) at the study site was measured via wet

combustion of sediments in H2SO4/K2Cr2O7 (Sorrell

et al. 1997; Bai et al. 2005), and there was little

difference between TOC from beneath each of the

three plants stands investigated (Table 1). In 2007, the

aboveground biomass in stands dominated by each of

the three plants was estimated every 2 months. Three

replicate quadrants (50 9 50 cm2) were sampled of

all living biomass for each of the three stands. Biomass

was oven-dried (80�C) to constant mass and weight

(Table 2).

CH4 gas sampling

The enclosed static chamber technique (van den Pol-

van Dasselaar et al. 1999) was used to measure CH4

emissions to the atmosphere at three stages during the

day: (1) exposed prior to flooding (EPF), (2) during

flooding and ebbing (i.e. in the course of a rising and

ebbing tide) (DFE), (3) exposed-after ebb (EAE). In

the study sites, the maximum height of C. malaccensis

is about 1.5 m, and the range of height of P. australis

and S. alterniflora are 1.6–1.8 m. In our study, the

chambers were constructed from three parts; a stain-

less steel bottom collar (50 cm 9 50 cm and 30 cm in

depth) and two PVC chambers (50 cm 9 50 cm in

area) were then positioned to the collar, the middle

chamber being 120 cm tall and the upper chamber,

50 cm tall for P. australis and S. alterniflora stands.

For C. malaccensis stands the middle chamber was

100 cm tall and the upper chamber, 50 cm tall

(Fig. 2). PVC chambers are frequently used for CH4

flux studies (e.g. Magenheimer et al. 1996; van den

Pol-van Dasselaar et al. 1999). The ground collar was

permanently inserted into the marsh sediment, with

2 cm left protruding above the sediment surface. The

chamber was equipped with an electric fan to ensure

complete mixing of the internal air. We controlled air

temperature inside the chambers during the summer

measurements by covering the chamber tops with

cotton quilts. In order to minimize the disturbance of

the measurement sites during sampling, a wooden

access boardwalk was built within the study area.

Monthly CH4 measurements were made from

January 2007 to December 2009 (except in February

of each year). Three replicate chambers were deployed

for the gas sampling. Samples were all taken on the

days between springtide and neap (third or fourth day

after the largest spring tide date, the third or fourth day

Table 1 Total organic carbon contents (g kg-1) in soils

beneath each of the three plant stands (mean ± standard error;

n = 3)

Depth (cm) S. alterniflora P. australis C. malaccensis

0–10 19.48 ± 0.98 20.93 ± 1.27 19.21 ± 0.64

10–20 18.45 ± 1.25 21.89 ± 1.66 18.13 ± 0.74

20–30 18.56 ± 1.75 22.89 ± 2.33 19.36 ± 0.77

30–40 19.69 ± 1.07 22.09 ± 2.66 20.71 ± 0.82

40–50 20.32 ± 0.83 22.51 ± 2.10 21.16 ± 0.54

Table 2 Seasonal changes in above-ground living biomass (g m-2) for each stand (mean ± standard error; n = 3)

Vegetation January March May July September November

S. alterniflora 1650 ± 311 1,256 ± 291 1,345 ± 179 2,389 ± 499 3,037 ± 249 1,496 ± 257

P. australis 0 77 ± 5 696 ± 195 1,525 ± 79 512 ± 107 629 ± 54

C. malaccensis 373 ± 61 256 ± 34 548 ± 109 1,062 ± 130 712 ± 134 578 ± 41

Fig. 2 Static chambers used for measuring CH4 flux from

marshes dominated by the macrophytes, S. alterniflora and

P. australis

680 Biogeochemistry (2012) 111:677–693

123

in each month of the Chinese lunar calendar). These

dates were selected as the sampling sites would all

begin to flood at 10:00 am (Beijing time) to ensure that

diurnal variability was minimized and there was

sufficient time to sample the chamber headspace at

each flooding stage in a single day (EPF, DFE and

EAE), and to ensure that the chambers were not

completely submerged by tidal water. Gas samples

were collected in 100 ml polypropylene syringes

equipped with three-way stopcocks at the same time

of day (between 9:00 and 16:00) on each occasion.

When sampling gas during EPF, the chamber was

enclosed and the first sample (100 ml) of chamber air

was taken at 9:00 (1 h before the beginning of the

flooding), followed by a second and third at 30 min

intervals. When sampling during the DFE stage, the

first gas sample was taken at 10:30 (30 min after

flooding commenced) and then followed by a second

and third sample at 60 min intervals. Finally, when

sampling in EAE, the first sample was taken 1.5 h after

the end of the ebb (about 15:00), followed by a second

and third at 30 min intervals.

Lacunal CH4 gas sampling

Lacunal gas of S. alterniflora and P. australis was

obtained by inserting a 2 ml syringe into the culms of

plants and withdrawing 1.5 ml of the internal plant

atmosphere prior to flooding on September 21, 2009.

We sampled lacunal gas from the first internode from

the culm base to the sixth internode in higher parts of

the culm. We sampled from each internode in 4–5

replicate individual plants for each species. Immedi-

ately after sampling, the contents of the syringe were

injected into a gas chromatograph (GC-2010, Shima-

dzu, Japan, equipped with a FID detector) to determine

CH4 concentrations.

Estimation of CH4 flux

CH4 concentrations were determined using a gas

chromatograph (GC-2010, Shimadzu, Japan) equipped

with an FID detector within 48 h of sampling. The

column and detector temperatures were set at 60 and

130�C, respectively, with nitrogen as the carrier gas at a

flow rate of 20 ml/min, and air and H2 for the FID at flow

rates of 400 and 47 ml/min, respectively. CH4 flux to the

atmosphere was calculated and estimated by a linear

model from changes in gas concentrations (Hirota et al.

2004). The rate of increasing CH4 concentration in the

chamber was determined by linear regression, and data

were rejected if the R2 of the regression was B0.90

(Hirota et al. 2004). In the EPF and EAE stages, the

height of the air volume within the chamber used for

P. australis and S. alterniflora stands was 170 cm

(chamber height), and for the C. malaccensis stand it

was 150 cm. During DFE stage, the internal chamber

water table equilibrated with the rising tide level via

inflow from the middle chamber/collar join. The

average tide level of three sampling times was consid-

ered to be the water height inside the chamber. The

height of the headspace air volume within the chamber

was equal to the difference between the chamber and

water height.

The duration of the two periods of tidal flooding and

ebbing during 24 h averaged around 7 h (3.5 ? 3.5),

and the duration of both before flood and after ebb

periods was 8.5 h. Given the duration of these three

periods, daily CH4 fluxes were calculated as follows

(Eq. 1):

Daily CH4 flux ¼ 8:5� CH4 flux in EPFð Þþ 7� CH4 flux in DFEð Þþ 8:5� CH4 flux in EAEð Þ ð1Þ

Because the sample dates in each month were on

the middle day between neap and spring tides, we

consider measured CH4 fluxes to approximate the

average monthly value thus allowing annual CH4 flux

to be estimated. We consider that calculated daily CH4

flux approximated the average daily CH4 flux in that

month thus allowing annual CH4 flux to be estimated.

Environmental variables measurements

On each sampling date, and for each plant stand, we

measured soil temperature, soil salinity (mS cm-1)

indicated by conductivity (Tamn and Wong 1998) and

Eh (mV) at a depth of 10 cm, and high tide water

height. Temperature and Eh were measured using an

IQ150 instrument (IQ Scientific Instruments, USA),

and soil conductivity was measured using a 2265FS

EC Meter (Spectrum Technologies Inc., USA).

Measurement of in situ and in laboratory CH4

production

We measured CH4 production under each of the three

plant stands at locations near to the above CH4 flux

Biogeochemistry (2012) 111:677–693 681

123

sampling sites in the summer (28–29 July) and winter

(7–8 December) of 2009, i.e. neap tide dates. We used

the CH4 oxidation inhibitor acetylene (C2H2) (Watan-

abe et al. 1995; King 1996) to estimate CH4 production

and oxidation. While King (1996) suggests that

acetylene can inhibit both CH4 oxidation and meth-

anogenesis, such inhibition of methanogenesis tends

to only be reflected in CH4 fluxes of longer incubations

than took place in our short-term study. For each plant

site, the stainless-steel bottom collars (three replicates)

were gently placed and then the PVC chambers were

positioned. To minimize disturbance to the system, the

bottom collars were mounted 3 days prior to sampling.

100 ml of gas in the headspace was sampled beginning

at 9:00 am immediately after closing the chambers,

and then every 20 min for 1 h (a total of four gas

samples were taken). After the final sampling, C2H2

was added to chambers at a headspace concentration

of 3% (King 1996) and left to incubate overnight

(roughly 23 h). The following day, headspace gas was

sampled at 9:00 am. An effort was made to sample pre-

and post-C2H2 treatment at the same time of day to

limit any potential diurnal effects. CH4 concentrations

were determined by GC analysis within 48 h of

sampling. Flux was calculated by linear regressions of

CH4 concentration with time. The post-C2H2 treat-

ment CH4 flux provided a measure of maximum

potential CH4 emission under in situ conditions and

can therefore be considered as an estimate of CH4

production rate. The difference between post and pre-

C2H2 treatment fluxes can be used to estimate rates of

CH4 oxidation.

For process level incubation work surface soil

cores (0–10 cm) (n = 3) were collected in April 2009

from under each of the three stands using stainless–

steel soil tubes. The soil from the three cores was

thoroughly mixed, sealed in plastic bags and refrig-

erated at 4�C prior to analysis. Roots and visible plant

remains were removed manually from the soil sam-

ples and then finely ground in a ball mill. 25 g soil

subsamples were put into 120 ml glass incubation

bottles and distilled water was added to make a 2:1

(water:soil, by volume) slurry. Incubations were

initiated by purging the soil suspension with N2 gas

for 5 min to replace all the oxygen (Wassmann et al.

1998). The samples were then incubated for 1 day at

20�C. 2 ml gas samples were taken using a syringe at

8:00, 14:00 and 20:00 h and CH4 concentration

immediately analyzed.

CH4 flux mediated by plants

To measure CH4 transport and emission of C.

malaccensis we used enclosed static chambers as

previously discussed and clipped the plants within a

treatment group to eliminate plant CH4 transport

(Kelker and Chanton 1997; Ding et al. 2005). The top

growth of C. malaccensis plants within the treatment

groups were clipped, and petroleum jelly was used to

seal the ends to prevent the release of gas from cut

stems. Fluxes were measured from three replicates

each of clipped and unclipped controls.

Because convective CH4 transport occurs in P.

australis (van der Nat et al. 1998), we devised a

‘hanging’ enclosed static chamber (Fig. 3). This

allowed us to minimize any sampling effect on the

CH4 transport process, when directly measuring CH4

transport and emission from single stems of P.

australis and S. alterniflora (Fig. 3). The hanging

chamber cylinder was made of Plexiglas (d = 10 cm).

Four 50 ml samples were manually collected into

100 ml polypropylene syringes equipped with three-

way stopcocks at 10 min intervals. The samples were

then stored in aluminum gas sampling bags.

Fig. 3 Hanging chamber used for gas sampling of CH4

emission mediated by plant transport of S. alterniflora and

P. australis

682 Biogeochemistry (2012) 111:677–693

123

Plant mediated CH4 flux was measured on the 31st

May, 15th July, 10th September and the 8th November

in 2009. CH4 flux mediated by P. australis was not

measured on the 31st May. All treatment sampling was

replicated. Three gas samples were taken during the

low tide stage at same time of the day between 15:00

and 15:30 h on each occasion. Gas sampling usually

lasted half an hour in total (10 min intervals).

For the S. alterniflora and P. australis stands, the

CH4 transport strength at population level was

estimated by multiplying the CH4 transport capacities

of individual plants by plant density. For the C.

malaccensis stand, the CH4 transport of individual

plants were calculated by dividing CH4 transport

capacities of the sampled plant population by plant

density.

Statistics

We tested the significance of observed differences in

methane fluxes among the three plant stands in each

year (2007, 2008 and 2009) by repeated measures

ANOVA, where multiple measurements in a given

plant species through time (11 months) represented

the repeated variables. For each plant stand, the

differences in methane fluxes among three tidal stages

were also tested with repeated measures ANOVA. The

differences in the methane transport capacity of three

plant individuals and populations in each measured

day were examined by a least-significant difference

(LSD) test in One-way ANOVA. All statistical

analyses were performed using SPSS statistical pack-

age (SPSS for Windows13.0).

Results

Seasonal variation of CH4 flux for three tidal stages

In all three plant stands, CH4 flux demonstrated a

distinct seasonal variation during the 2007–2009 study

period (Fig. 4), which is particularly apparent during the

two exposed low tide stages (EPF and EAE). CH4 fluxes

generally reached their maxima during the warm

summer when soil temperature was relatively high.

The lowest CH4 fluxes were mostly observed when soil

temperature was low (i.e. winter—December to Febru-

ary). The largest CH4 flux was 35.3 ± 7.02 and

46.71 ± 10.33 mg m-2 h-1 in EPF and EAE stages

for S. alterniflora stands in the 3 years, for the

P. australis stands, the highest CH4 flux was 40.95 ±

15.05 and 22.10 ± 3.87 mg m-2 h-1 in EPF and EAE

stages and for the C. malaccensis stands, the highest

CH4 flux was only 13.99 ± 5.11 and 17.93 ±

4.57 mg m-2 h-1 in EPF and EAE stages. The lowest

peak tidal water levels (23, 31 and 33 cm) during the

DFE stage were observed on June 2007, July 2008 and

May 2009, each of which corresponded with the peak

in CH4 emission (8.92 ± 4.24, 31.3 ± 9.75 and

6.36 ± 4.13 mg m-2 h-1) from S. alterniflora stands,

8.80 ± 5.63, 9.57 ± 4.14 and 4.19 ± 1.44 mg m-2 h-1

from P. australis stands, and 1.29 ± 0.32, 10.63 ±

4.11 and 0.64 ± 0.39 mg m-2 h-1 from C. malacc-

ensis stands.

Plants invasion, expansion and CH4 flux

The recent invasion of the exotic species S. alterniflora

and the expansion of the native species P. australis had

significantly increased CH4 emissions in ecosystems

previously dominated by the native species C. malacc-

ensis during low tide stages (EPF and EAE) in each year

of the study period (except for P. australis stand in the

EAE stage in 2008 (Fig. 5). However, during tidal

inundation (DFE), only exotic S. alterniflora signifi-

cantly increased CH4 flux when compared with native

C. malaccensis stands, the difference in CH4 flux from

P. australis and C. malaccensis stands were not

significant. CH4 flux from the S. alterniflora stands

were also significantly higher than in P. australis stands

during the EPF and EAE stages with the exception of the

EPF stage in 2009, and in the DFE stage throughout the

3 years when no significant difference was observed.

Influence of tidal inundation on CH4 flux

to atmosphere

Tidal inundation had a significant effect on CH4

emissions (Fig. 5). The effect was most distinct in the

S. alterniflora stands where CH4 emissions were

significantly lower during period of tidal inundation

(DFE) than at low tide (EPF and EAE), however, there

were no significant differences between CH4 fluxes

observed during EPF and EAE. For the C. malaccensis

stands, CH4 emissions in 2007 and 2009, were

significantly lower during DFE than at low tide stages

(EPF and EAE), however, there were no significant

differences between the three tidal stages in 2008. For

Biogeochemistry (2012) 111:677–693 683

123

the P. australis stands, CH4 fluxes in both EPF and

EAE were significantly higher than during DFE in

2007. However, in 2008 and 2009, CH4 fluxes were

only significantly higher in EPF than in DFE.

Estimation of overall annual CH4 flux

to atmosphere

The annual CH4 flux from all three plant stands during the

observation period of 2007–2009 is shown in Table 3.

CH4 flux was highest in 2008. The mean annual CH4 flux

(i.e. the sum of exposed and submerged stages) from

S. alterniflora, P. australis and C. malaccensis stands

during 3 years were 95.65 ± 18.68, 38.90 ± 3.26 and

10.93 ± 5.26 g m-2 year-1, respectively. The percent-

ages of CH4 emissions during the exposed stages in the

total CH4 emissions were 93.5 ± 1.7, 86.7 ± 0.5 and

84.5 ± 3.8% for S. alterniflora, P. australis and C.

malaccensis stands, which indicated that submergence by

tides reduces direct CH4 emissions to the atmosphere.

Lacunal methane

CH4 concentrations within S. alterniflora and P.

australis culms decreased rapidly relative to culm

0

15

30

45

60

75

Jan-2007

Jul-2007

Nov-2007

Apr-2008

Aug-2008

Dec-2008

May-2009

Sep-2009

Dec-2009

CH

4 f

lux

(mg

m-2

h-1

)

0

15

30

45

60

75

CH

4 f

lux

(mg

m-2

h-1

)0

15

30

45

60

75

CH

4 f

lux

(mg

m-2

h-1

) EPF

DFE

EAE

Fig. 4 Seasonal patterns of

CH4 flux from

S. alterniflora, P. australisand C. malaccensis stands at

three tidal stages from 2007

to 2009. Solid circles, opencircles and trianglesrepresent S. alterniflora,

P. australis and

C. malaccensis stands,

respectively

684 Biogeochemistry (2012) 111:677–693

123

height, starting at the culm base (Table 4), the lacunal

CH4 concentrations in the sixth internodes of S.

alterniflora and P. australis culms were only 11.0 and

0.4% of that measured in the first internode of each

species, respectively. Lacunal CH4 concentrations in

all the internodes exceeded ambient levels

(±0.1 lmol l-1), the lacunal CH4 concentrations in

the first internode of S. alterniflora and P. australis

culms were *3 orders of magnitude larger than

ambient levels. Lacunal CH4 concentrations in all the

internodes of the culms of S. alterniflora were higher

than those in the corresponding internodes of P.

australis (Table 4).

Effects of environmental variables on CH4 flux

Exponential models were fitted to the relationship

between soil temperature at 10 cm below the soil

surface and CH4 emissions from three plant stands in

EPF and EAE stages. Although the relationships were

weak (explaining\40% of CH4 flux variation), there

were significant exponential increases in CH4 emis-

sions with soil temperature for three plant stands

(P \ 0.01) (Fig. 6). The relationship between soil

temperature and the CH4 flux from P. australis and C.

malaccensis stands was stronger than that of the S.

alterniflora stand.

0

7

14

21

28

2007 2008 2009

CH

4 f

lux

(mg

m-2

h-1

)

S.alternifloraP.australisC.malaccensis

DFE

a

a a a b ab a ab

b

0

7

14

21

28

2007 2008 2009

CH

4 f

lux

(mg

m-2

h-1

)

S.alternifloraP.australisC.malaccensis

EAE

a

b

a

b

c

a

b

c

b

0

7

14

21

28

2007 2008 2009 C

H4 f

lux

(mg

m-2

h-1

)

S.alternifloraP.australisC.malaccensis

a

b

c b

a a

a

b

c

EPFFig. 5 CH4 flux from

marshes dominated by

S. alterniflora, P. australisand C. malaccensis in three

tidal stages. Values are the

averaged CH4 fluxes of three

tidal stages in all measured

dates in each year, and

represented by

mean ± standard error,

(n = 3). The significance of

differences in CH4 fluxes

among the three plant stands

for each year were tested by

repeated measures ANOVA,

where multiple

measurements in a given

plant species through time

(11 months) represented the

repeated variables (df = 2,

96). CH4 fluxes are

significantly different at

P \ 0.05 if they have no

letters in common

Table 3 Annual budgets for CH4 (g m-2 year-1) from marshes dominated by S. alterniflora, P. australis and C. malaccensis from

2007 to 2009

CH4 flux S. alterniflora P. australis C. malaccensis

2007 2008 2009 2007 2008 2009 2007 2008 2009

CH4 flux in ES 75.40 120.47 70.89 27.89 37.89 35.45 4.36 17.21 5.51

CH4 flux in SS 5.48 12.29 2.43 4.70 5.57 5.19 1.00 4.24 0.48

CH4 flux in (ES ? SS) 80.88 132.76 73.32 32.59 43.46 40.64 5.36 21.45 5.99

ES/(ES ? SS) 93.2% 90.7% 96.7% 85.6% 87.2% 87.2% 81.3% 80.2% 92.0%

Each flux value is the mean of three replicates; ES exposed-stage (EPF ? EAE), sS submerged-stage (DFE), ES ? SS exposed-

stage ? submerged-stage (EPF ? EAE ? DFE), CH4 flux in (ES ? SS): overall annual CH4 flux

Biogeochemistry (2012) 111:677–693 685

123

The correlation coefficients (R) of liner regression

between soil Eh, soil salinity and the CH4 flux from

three plant stands in EPF and EAE stages are shown in

Table 5. Significant correlations between CH4 emis-

sions and these variables were only found in

C. malaccensis and P. australis stands. There was no

significant relationship between soil Eh, soil salinity

and the CH4 flux in the S. alterniflora stand.

Soil CH4 production

The in situ CH4 production rate under S. alterniflora

stands was only significantly higher than that of C.

malaccensis stands in July (Table 6). The in situ CH4

production rate of S. alterniflora stands was significantly

higher than those of P. australis and C. malaccensis

stands in December (Table 6). In laboratory based

anaerobic incubations, the CH4 production potential

(10.7 ± 1.6 ng g-1 h-1) of soil under S. alterniflora

stands was higher than under P. australis stands

(5.3 ± 0.9 ng g-1 h-1) or C. malaccensis stands

(4.5 ± 1.3 ng g-1 h-1), although differences between

P. australis and C. malaccensis stands were small.

CH4 emission mediated by plant transport

Plant type is an important control on CH4 fluxes from

wetland ecosystems. In our study, the CH4 transport

capacity of individual S. alterniflora plants was

significantly higher than that of individual C. malacc-

ensis plants (df = 2, 9; P \ 0.05). For P. australis, the

CH4 transport capacity of individual plants was no

larger than that of C. malaccensis (df = 2, 9;

P [ 0.05) except in September (df = 2, 9; P \ 0.05)

(Fig. 7). At the plant population level, the CH4

transport capacities of S. alterniflora populations were

only significantly higher than in C. malaccensis

Table 4 Lacunal methane concentration (lmol l-1) in the internodes of S. alterniflora and P. australis (mean ± standard error;

n = 3)

Plant Internode 1 Internode 2 Internode 3 Internode 4 Internode 5 Internode 6

S. alterniflora 609.3 ± 112.7 269.2 ± 38.6 491.7 ± 35.3 476.0 ± 81.4 233.5 ± 41.9 66.8 ± 11.5

P. australis 529.0 ± 74.4 50.6 ± 13.7 27.8 ± 4.1 2.1 ± 0.5 2.0 ± 0.7 2.1 ± 0.7

Internode 1 is the first internode from the culm base

YEPF = 0.3053 e0.1235 x

R 2 = 0.3705 ; P <0.01

YEAE = 0.2612 e0.1081 x

R 2 = 0.2866 ; P <0.01

0

20

40

60

80

CH

4 f

lux

(mg

m-2

h-1

)

YEPF = 0.0448 e0.1306 x

R 2 = 0.3402 ; P <0.01

YEAE = 0.0193 e0.1538 x

R 2 = 0.3375 ; P <0.01

0

20

40

60

80

8 15 22 29 36

Soil temperature(°C)

CH

4 f

lux

(mg

m-2

h-1

)

b

c

YEPF = 5.8688e0.0272x

R 2 = 0.0385 ; P <0.05

YEAE = 3.6305 e0.0509 x

R 2 = 0.1124 ; P <0.01

0

20

40

60

80

CH

4 f

lux

(m

g m

-2 h

-1)

a

Fig. 6 Soil temperature control on CH4 flux from the marshes

dominated by S. alterniflora, P. australis and C. malaccensis in

exposed-prior to flooding (EPF) and exposed-after ebbing

(EAE) stages. a S. alterniflora, b P. australis, c C. malaccensis;

open and solid circles represent EPF and EAE, respectively

Table 5 Correlation coefficients of linear regression between

the CH4 fluxes from three plant stands in EPF and EAE, and

measured soil Eh and salinity

R EPF EAE

Eh Salinity Eh Salinity

S. alterniflora -0.152 -0.041 0.078 -0.053

P. australis -0.074 -0.269** -0.032 -0.414**

C.malaccensis

-0.350** -0.319** -0.174* -0.350**

Significance coded: * \0.05, ** \0.01

686 Biogeochemistry (2012) 111:677–693

123

populations in May and November (df = 2, 9;

P \ 0.05), and there were no significant differences

in the CH4 transport capacities between P. australis

and C. malaccensis (df = 2, 9; P [ 0.05).

Discussion

Possible explanation for the effect of S. alterniflora

invasion on enhanced CH4 emission

The invasion of exotic S. alterniflora has significantly

increased CH4 fluxes in marshes previously dominated

by the native species C. malaccensis with the effect

being most prominent during exposed-low tide stages

(Fig. 5). Our findings are consistent with the results of

Cheng et al. (2007) and Zhang et al. (2010). In these two

in vitro experimental mesocosm studies more CH4

emission was observed from brackish S. alterniflora

marsh samples than from those collected in brackish

P. australis marshes in the Yangtze River estuary.

Further, in Jiangsu there was more CH4 emission from

S. alterniflora salt marshes than from S. salsa salt marsh.

Plants can influence CH4 emissions from wetland

ecosystems by altering their production and consump-

tion in and transport from soil (Christensen et al. 2003;

Koelbener et al. 2010). Our laboratory based anaerobic

incubation study reveals a higher CH4 production

potential in soils under S. alterniflora than under

C. malaccensis and even P. australis. In situ measure-

ments also show that the CH4 production rate of

S. alterniflora stands was higher than in C. malaccensis

stands (Table 6). For CH4 production, plants act as an

important source of methanogenic substrate through

excreting labile carbohydrates as exudates and root

debris, where root exudates are likely to be strongly

influenced by plant size (Jones et al. 2004). A high input

of plant root exudates may lead to a stimulation of

Table 6 In situ CH4 production and oxidation (mg CH4 m-2 h-1) in soil under three plant stands

Vegetation 28–29 July 7–8 December

Methane

production

Methane

oxidation

Methane

emission

Methane

production

Methane

oxidation

Methane

emission

S. alterniflora 21.23 ± 11.43 17.02 ± 4.67 4.21 ± 2.23 36.27 ± 8.53 21.13 ± 10.29 15.13 ± 2.96

P. australis 17.05 ± 2.83 9.50 ± 4.09 7.55 ± 1.26 5.29 ± 0.06 2.53 ± 0.34 2.77 ± 0.29

C.malaccensis

9.58 ± 2.05 1.56 ± 0.57 8.01 ± 1.94 3.07 ± 1.44 2.10 ± 1.00 0.97 ± 0.46

The values are means ± standard error of three replicates

A B

Fig. 7 CH4 emissions mediated by plant transport in S. alter-niflora, P. australis and C. malaccensis, A CH4 transport

capacity of individual plants; B CH4 transport capacity of plant

populations, represented by mean ± standard error, (n = 3).

The significances of the differences in CH4 emission among the

three plant stands for each day were tested by least-significant

difference test in One-way ANOVA (df = 2, 9). CH4 emissions

are significantly different at P \ 0.05 if they have no letters in

common

Biogeochemistry (2012) 111:677–693 687

123

methanogenesis and CH4 production (Christensen et al.

2001). Numerous reports demonstrate that CH4 emis-

sions are well correlated with living aboveground

biomass (or net primary production) (Chanton et al.

1997; Greenup et al. 2000; Kutzbach et al. 2004),

however, there are also studies that show no significant

relationship (Joabsson and Christensen 2001). We

found that the exotic invasive species S. alterniflora

had significantly more aboveground biomass than

C. malaccensis and P. australis (F2,51 = 28.89, P \0.001), but there was no significant difference between

P. australis and C. malaccensis (F1,34 = 0.01,

P [ 0.05) in the study site (Table 2), therefore support-

ing the conclusion that live aboveground plant biomass

is a key factor controlling CH4 production and emission

from marshes. King and Reeburgh (2002) found that

carbon assimilated by plants via photosynthesis during14C pulse-labeling turned over rapidly and appeared as

emitted CH4 within 24 h. In the Yangtze estuary, China,

S. alterniflora has been shown to have a higher mean

seasonal net photosynthetic rate than P. australis (Liao

et al. 2007). In our study site, S. alterniflora had a longer

growing season than P. australis and C. malaccensis,

and therefore, we may predict that this species should

capture more atmospheric CO2 and hence produce more

carbohydrates through photosynthesis thus increasing

plant annual net primary productivity (ANPP). We can

therefore conclude that S. alterniflora can fix and then

allocate more carbon to the soil, which in turn results in

more CH4 production and emission compared with the

native species C. malaccensis.

Another important way by which plants can influence

CH4 fluxes is through plant transport. CH4 can be

transported from wetland soil to the atmosphere through

plant aerenchyma tissue found in roots, rhizomes and

living stems (e.g. Verville et al. 1998). Plants provide a

more effective conduit for CH4 transport and so enhance

CH4 emission (Greenup et al. 2000). This herbaceous

plant pathway, where CH4 is emitted from many

wetland species through aerenchyma tissue, may

account for 80–90% of the total gas emitted (Chanton

et al. 2002). The results of our in situ measurements of

CH4 transport capacities in individual plants reveal that

CH4 transport capacity of the S. alterniflora was

significantly higher than that of C. malaccensis. S. alt-

erniflora and P. australis both belong to the perennial

grass family, and C. malaccensis belongs to the

Cyperaceae family. We observed the stems (culms) of

S. alterniflora and P. australis all have obvious lacunae,

however the stems of C. malaccensis have fewer of these

features, which may explain why the CH4 transport

potentials of S. alterniflora and P. australis were higher

than in C. malaccensis. Table 4 demonstrates that

lacunal methane concentrations in the culms of S. alter-

niflora and P. australis were all high. It is, however

difficult to measure methane concentration within the

stems of C. malaccensis. In addition, C. malaccensis

only has full green stems with no ‘leaves’ attached, and

van der Nat et al. (1998) concluded that this feature will

offer a much higher resistance to gas flow than

Phragmites, probably due to the presence of meriste-

matic tissue inside the stems.

As well as altering CH4 production and transport

from wetland soil, vascular plants also transport

oxygen into the rhizosphere to enhance CH4 oxidation

(van der Nat et al. 1998). In situ CH4 oxidation rate in

soils under S. alterniflora stands was rather strong

compared with C. malaccensis stands (Table 6).

According to our observations, S. alterniflora has a

thicker stem and better-developed aerenchyma tissue

than C. malaccensis, which indicates that S. alternifl-

ora may deliver more oxygen into the rhizosphere

compared with C. malaccensis. Although relatively

more oxygen may be brought into the rhizosphere by

S. alterniflora, which further leads to higher rates of

CH4 oxidation under S. alterniflora stands, the final

CH4 emission from S. alterniflora stands was still

larger than that of C. malaccensis in most measure-

ment days (Fig. 4) because this effect was outweighed

by the higher CH4 production measured in the soil of

S. alterniflora stands relative to C. malaccensis stands.

Although bubble ebullition can be an important

pathway of methane release from wetland ecosystems

(with diffusive fluxes often proving to be of negligible

importance), in our study, we only determined the

plant transport path, which generally dominates over

other methane pathways and determines spatial var-

iability in emissions (Gauci et al. 2002). The methane

content within the soil profile is the total amount of

methane present in bubble and dissolved forms. In

C. malaccensis marshes, the monthly averaged dis-

solved methane concentration of the pore water at a

depth of 20 cm was 26.4 lmol l-1 in 2009 (unpub-

lished data). Our chambers were deployed over

relatively long periods in this study, and so it is likely

that observed CH4 fluxes represented a combination of

plant emissions, bubbles and although possibly neg-

ligible diffusion.

688 Biogeochemistry (2012) 111:677–693

123

Taking the above analyses together, we can suggest

that the model of CH4 cycling in S. alterniflora

marshes is as follows: high CH4 production, strong

CH4 oxidation and more effective plant CH4 transport

which, in combination results in higher CH4 emission

compared with native C. malaccensis stand in the Min

River estuary.

CH4 flux from S. alterniflora and P. australis tidal

marshes of the world

Spartina alterniflora is a C4 perennial rhizomatous

grass, native to the Atlantic and Gulf coasts of North

America. Due to it being a dominant plant in estuarine

brackish marshes and salt marshes along the seaboard of

the United States, there are numerous studies reporting

CH4 emissions from Spartina tidal marshes. Bartlett and

Harriss (1993) reviewed CH4 fluxes from S. alterniflora

marshes and found that they fluxes ranged from 0.02 to

6.04 mg m-2 h-1. P. australis is a common species and

may be one of the most widely distributed plants in the

world, however, most of the data on CH4 emission from

P. australis-dominated marshes has focused on fresh

water stands where emissions are reported to amount to

9.13 mg m-2 h-1 in Prairie lake, Nebraska USA (Kim

et al. 1998), 8.58 mg m-2 h-1 in the Scheldt estuary,

The Netherlands (van der Nat and Middelburg 2000)

and 2.51–6.62 mg m-2 h-1 in Lake Vesijarvi, Finland

(Kankaala et al. 2004).

Until this in situ study, there were only two experi-

mental mesocosm studies in China. One compared CH4

emissions from S. alterniflora and P. australis brackish

marshes in the Yangtze estuary (Cheng et al. 2007);

another determined CH4 emissions from S. alterniflora

and S. salsa in coastal salt marsh in Jiangsu (Zhang et al.

2010). Cheng et al. (2007) found that CH4 fluxes from

S. alterniflora mesocosms ranged from 0.16–

0.85 mg m-2 h-1, and Zhang et al. (2010) estimated

that average growing season CH4 fluxes from S. alter-

niflora was 0.88 mg m-2 h-1. In our study, the mean

CH4 emissions over 3-years from S. alterniflora, P.

australis and C. malaccensis dominated stands during

exposed stages were 15.1, 5.91 and 1.59 mg m-2 h-1,

respectively, which is far higher than observed from these

species dominated ecosystems in the earlier mesocosms

studies.

This suggests that mesocosm studies are far

removed from the estuarine environments they were

designed to simulate and so cannot represent actual in

situ CH4 fluxes from S. alterniflora marshes. For

example, in the first study (Cheng et al. 2007)

mesocosms were planted with young ramets of

S. alterniflora or P. australis at a density of about

30 plants m-2, and in the second study (Zhang et al.

2010) mesocosms were only planted with young

individual ramets of S. alterniflora at a plant density of

about 20 plants m-2. These studies contrast with our in

situ study in several respects. Firstly, plant densities

observed in our study where much higher, i.e. plant

densities of S. alterniflora and P. australis marshes

were 257 and 150 plants m-2 (Tong et al. 2011) which

can provide a larger supply of available organic carbon

compounds for methanogenesis, and increase CH4

production and transport. Also, tidal water may carry

some organic carbon particulates to form sediments in

the marsh, which should provide additional substrate

for methanogenesis. Other factors may also play a

role. For example, as a consequence of the above

differences between mesocosms and in situ studies

there may be more methanogens within in situ soils.

Finally, there may also be more non-competitive CH4

production substrates, such as dimethyl sulfide and

trimethylamine, in the natural setting.

CH4 emissions in our study were also large compared

with CH4 fluxes from S. alterniflora salt marshes in the

USA (Bartlett and Harriss 1993). This may be due to

differences in the average salinity of tidal water. SO42-

concentrations in sediment pore water were also rela-

tively low in our study site. In addition, the peak live

aboveground biomass (3.04 kg m-2) of S. alterniflora

marshes in the Min River estuary is greater than that

reported in New Jersey salt marshes, i.e. 0.19 and

0.69 kg m-2 in (Windham and Lathrop 1999; Windham

2001) and in the Delaware Bay, i.e. 1.07 kg m-2

(Gratton and Denno 2005).

CH4 emission in exposed and submerged-tidal

marsh soil environment

Although tide is an important physical process that

influences biogeochemical process in coastal wetlands,

there have been very few attempts to measure CH4

fluxes through the entire tidal cycle. Our results

demonstrate that CH4 emission to the atmosphere from

three plant stands during exposed-stages (prior to

flooding and after ebbing) are all significantly higher

than during the submerged stage (flooding and ebbing)

(Figs. 4, 5). We estimate that over the 3 years for which

Biogeochemistry (2012) 111:677–693 689

123

we have data, S. alterniflora, P. australis and C.

malaccensis stands contributed 93.5, 87.0 and 84.5%,

respectively, of the overall CH4 flux to atmosphere

during exposed-tidal stages. In addition, our investiga-

tion reveals that there was no significant difference in

CH4 flux between the stage prior to flooding and the

stage after ebbing. The result is not consistent with

findings from northern Taiwan by Chang and Yang

(2003), who found that in some months, CH4 flux was

larger before flood, and at other months either no

difference was found, or a larger flux is observed after

ebb.

Kelley et al. (1995) concluded that CH4 emission

was related to water height at the riverbank margin, the

fluxes being greatest when the water level was nearest

the soil surface on both flood and ebb tides. van der

Nat and Middelburg (2000) considered that the CH4

accumulation and emission to the atmosphere from

P. australis marshes increased considerably when the

tidal water level was \8 cm. Overall, our results are

consistent with these studies. CH4 emission from plant

stands are most likely lower during tidal submergence

because plant-mediated CH4 transport is depressed

when plant stems are under tidal water. Kaki et al.

(2001) reported that CH4 transported by P. australis

and Typha latifolia plant is mainly released in the

height range of 0–10 cm above ground. Huang et al.

(2011) also showed that CH4 transported by S.

alterniflora is mainly released in the 0–20 cm height

range above the soils surface. When exposed soils are

flooded with inflowing water, gas diffusion is

restricted as the air space in soil is replaced with

water. Further, inflowing brackish water may dilute

dissolved CH4 in the pore water which may reduce the

release of CH4 (Yamamoto et al. 2009). It is plausible

that transiently stored CH4 in the soil will emit directly

to atmosphere through ebullition when the soils are re-

exposed. It is further possible that increases in water

pressure on flooding will stimulate ejection of air from

soil pores as bubbles.

Measuring CH4 flux during the process of flooding

and ebbing is a challenge, and we considered that a

floating chamber normally used to collect gas samples

from lakes and reservoirs was unsuitable for measure-

ments in estuarine tidal marsh ecosystems (plant ?

soil ? tidal water) during the flooding and ebbing

process. In our study, we measured the CH4 flux emitted

directly into atmosphere during flooding and ebbing

during the middle tide date using a static chamber

method. The water level within the chambers varied

during flooding and ebbing, which may have caused

temporary alteration in atmospheric pressure within the

chamber headspace until water levels inside and outside

the chamber equilibrated. In addition, during flooding

and ebbing stages, dissolved CH4 in water within the

chamber will also have been emitted to the atmosphere,

however distinguishing CH4 emitted from marsh soil

and from tidal water was also a challenge.

Because sampling took place on middle dates

between neap and spring tide dates, the CH4 emission

measured can be considered the average value of CH4

emission in that month, and so annual CH4 emission

can be estimated. However, the tide was not the only

factor influencing CH4 emission, with variations in

temperature, plant biomass and density all influencing

CH4 emissions in each month. These factors may

therefore introduce some uncertainty when estimating

monthly and annual CH4 emissions. Future studies

may mitigate against such variability by increasing the

frequency of measurements around the middle days of

each month.

Environmental controls on CH4 flux

Temperature is known to play an important role in

determining rates of both CH4 production and oxidi-

zation, and is therefore a key environmental variable

controlling CH4 emission. In our study, CH4 emission

increased significantly with soil temperature (Fig. 6),

although temperature could only explain \40% of

CH4 flux variation. The correlation between soil

temperature and CH4 emission in our data was

stronger for C. malaccensis and P. australis stands

(R2 [ 0.3) than for S. alterniflora stands (R2 = 0.04 in

EPF stage, R2 = 0.11 in EAE stage), although the

reasons for observed lower R2 values for the S.

alterniflora stands are not clear.

The response of CH4 emission to temperature is

complex and conflicting results have been obtained

with some studies showing no correlation (Klinger

et al. 1994) whereas the majority of studies report

positive correlations (Bartlett et al. 1992; van der Nat

and Middelburg 2000; Kankaala et al. 2004) and only

one study observed negative correlations (Macdonald

et al. 1998). van der Nat and Middelburg (2000)

suggested that the possible reasons were: (1) temper-

ature enhanced CH4 production rate, but this was

offset by a concurrent increased CH4 oxidization rate;

690 Biogeochemistry (2012) 111:677–693

123

and (2) when substrates are restricted, the effect of

temperature might have a reduced effect. We think

that the responses of methanogens under different

vegetation types and in different climate zones may

vary, and this contributes to the complexity of

relationships between CH4 emission and temperature.

Salinity is also an important environmental factor in

estuarine areas. Some studies show salinity affect-

ing CH4 emission from tidal wetlands. In the Ches-

apeake Bay, Virginia, annual atmospheric CH4 flux

was 5.6 g m-2 year-1 from the most saline site,

22.4 g m-2 year-1 from intermediate site, and

18.2 g m-2 year-1 from the freshest site (Bartlett

et al. 1987). In our study, a significant negative

correlation was only observed between salinity and

CH4 emission in C. malaccensis and P. australis

stands during the exposed stages (Table 5), for

S. alterniflora stands, there was no significant rela-

tionship between soil salinity and CH4 flux. Eh is also

an important factor affecting CH4 emission from

wetlands, however, the relationship between CH4

emission and Eh is also complex, and again variable

results have been found with ranges of Eh where CH4

can be produced from -300 to ?70 mV (Cicerone and

Oremland 1988; Peters and Conrad 1996). Our results

show that the range of Eh where CH4 occurred varied

within a range of -75 to ?155 mV but there was no

significant correlation between CH4 flux and Eh

over the duration of the study for S. alterniflora and

P. australis stands (Table 5).

Acknowledgments We thank Mr. Bo Lei, Chun-qi Zhong,

Zheng-zheng Liu, Lu-ying Lin, Xiao-fei Wan, Yan Ge, Ji Liao,

Shun Yao, Chong-an Chen, and Ms. Hong-yu Yang, for field

assistance and laboratory analysis. This work was financially

supported by the National Science Foundation of China (Grant

No: 40671174, 31000262, 41071148), Key Foundation of

Science and Technology Department of Fujian Province (No.

2010Y0019, 2009R10039-1), and Key Discipline Construction

Foundation for Physical Geography of Fujian Province. We

would sincerely like to thank two anonymous reviewers and

associate editor R Cook for their valuable comments and

suggestions that have improved the manuscript greatly.

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