Exotic Spartina alterniflora invasion alters ecosystem-atmosphere exchange of CH4 and N2 O and carbon sequestration in a coastal salt marsh in China

Exotic Spartina alterniflora invasion alters ecosystem–atmosphere exchange of CH4 and N2O and carbonsequestration in a coastal salt marsh in ChinaJUN J I YUAN1 , 2 , WE IX IN D ING 1 , DEYAN L IU 1 , HO JEONG KANG3 , CHR I S FREEMAN4 ,

J IAN X IANG 1 , 2 and YONGXIN LIN1 , 2

1State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008,

China, 2University of Chinese Academy of Sciences, Beijing 10049, China, 3School of Civil and Environmental Engineering, Yonsei

University, Seoul 120–749, Korea, 4School of Biological Sciences, Bangor University, Gwynedd LL57 2UW, UK

Abstract

Coastal salt marshes are sensitive to global climate change and may play an important role in mitigating global

warming. To evaluate the impacts of Spartina alterniflora invasion on global warming potential (GWP) in Chinese

coastal areas, we measured CH4 and N2O fluxes and soil organic carbon sequestration rates along a transect of coastal

wetlands in Jiangsu province, China, including open water; bare tidal flat; and invasive S. alterniflora, native Suaeda

salsa, and Phragmites australis marshes. Annual CH4 emissions were estimated as 2.81, 4.16, 4.88, 10.79, and 16.98 kg

CH4 ha�1 for open water, bare tidal flat, and P. australis, S. salsa, and S. alterniflora marshes, respectively, indicating

that S. alterniflora invasion increased CH4 emissions by 57–505%. In contrast, negative N2O fluxes were found to be

significantly and negatively correlated (P < 0.001) with net ecosystem CO2 exchange during the growing season in S.

alterniflora and P. australis marshes. Annual N2O emissions were 0.24, 0.38, and 0.56 kg N2O ha�1 in open water, bare

tidal flat and S. salsa marsh, respectively, compared with -0.51 kg N2O ha�1 for S. alterniflora marsh and �0.25 kg

N2O ha�1 for P. australis marsh. The carbon sequestration rate of S. alterniflora marsh amounted to 3.16 Mg

C ha�1 yr�1 in the top 100 cm soil profile, a value that was 2.63- to 8.78-fold higher than in native plant marshes. The

estimated GWP was 1.78, �0.60, �4.09, and �1.14 Mg CO2eq ha�1 yr�1 in open water, bare tidal flat, P. australis

marsh and S. salsa marsh, respectively, but dropped to �11.30 Mg CO2eq ha�1 yr�1 in S. alterniflora marsh. Our

results indicate that although S. alterniflora invasion stimulates CH4 emissions, it can efficiently mitigate increases in

atmospheric CO2 and N2O along the coast of China.

Keywords: atmospheric N2O consumption, carbon sequestration, GWP, N-limit, Spartina alterniflora invasion, sulfate

Received 31 May 2014 and accepted 30 September 2014

Introduction

The steady increase in atmospheric concentrations of

greenhouse gases (GHGs) has led to a warming of

Earth’s surface and other climate changes since the pre-

industrial era (IPCC (Intergovernmental Panel on Cli-

mate Change), 2007). Natural wetlands play a critically

important role in governing the rate of increase of GHG

concentrations because of their large soil carbon (C)

and nitrogen (N) pools, high CH4 and considerable

N2O emissions (Song et al., 2009). Like freshwater wet-

lands, tidal salt marshes, and other coastal wetlands

have high primary productivity (Liao et al., 2008) and

contain ~10% of the global soil C (Schlesinger, 1995).

Tidal salt marshes show higher C sequestration poten-

tials compared with terrestrial forests and peatlands

due to their ability to bury locally produced organic C,

and trap sediment and associated organic C (Chmura,

2011). Unlike other wetlands, salt marshes have been

suggested to be more valuable C sinks than other eco-

systems because of their relatively low CH4 and N2O

emissions (Livesley & Andrusiak, 2012). Despite their

importance, salt marshes are among the ecosystems

that are most threatened by and vulnerable to human

activities and climate change, including sea-level rise,

eutrophication, and exotic plant invasion (Kirwan et al.,

2010; Deegan et al., 2012).

As two significant elements of global change, exotic

plant invasion and climate change are major pressing

environmental problems that may threaten the sustain-

ability of global ecosystems (Tamura & Tharayil, 2014).

Furthermore, these two global changes are predicted to

interact, with climate change facilitating a massive

range expansion of many exotic species over the com-

ing decades (Dawson et al., 2012). However, the poten-

tial for plant invasions to participate in feedback loops

that affect climate change by regulating sequestration

of soil organic C (SOC), and CH4 and N2O emissions in

invaded ecosystems has not been extensively studied.Correspondence: Weixin Ding, tel. +86 25 8688 1527,

fax +86 25 8688 1000, e-mail: [email protected]

1© 2014 John Wiley & Sons Ltd

Global Change Biology (2014), doi: 10.1111/gcb.12797

Global Change Biology

In natural ecosystems, the dominant plant species

regulate net primary production, litter quantity and

chemistries, and the timing of the litter inputs (Ehren-

feld et al., 2001; Allison & Vitousek, 2004). The physical

and physiological traits of the primary producers that

regulate the initial C assimilation directly and indirectly

influence the abundance and metabolism of soil biota

that conduct C and N cycles (Hawkes et al., 2005; De

Deyn et al., 2008). In general, most invasive plants have

higher resource acquisition (Tharayil et al., 2009) and

resource-use efficiencies (Funk & Vitousek, 2007), and

thus have higher net primary productivity compared

with native plants (Liao et al., 2008). This in turn

increases soil C stock in the invaded ecosystems (Wol-

kovich et al., 2010), despite the potential destabilization

of native soil C stocks (Tamura & Tharayil, 2014). In

most wetlands, the photosynthetically fixed C serves as

the source of substrates for methanogenesis (Kuzyakov,

2002; Str€om et al., 2012). There is a direct species-depen-

dent linkage between plant production and substrate

availability for CH4 production (Joabsson & Christen-

sen, 2001), and plant invasion has the potential to affect

CH4 emission rates. Additionally, most invasive plants

exhibit distinct litter chemistries from those of native

species. These chemically different inputs alter the C

cycling and methanogen community composition, and

could have disproportionate impacts on CH4 emissions

in wetlands (Yuan et al., 2014). Plant invasion can also

alter the various components of ecosystem N cycles.

Hawkes et al. (2005) showed that exotic grasses dou-

bled gross nitrification rates in part by increasing the

abundance and changing the composition of ammonia-

oxidizing bacteria in soil, and subsequently altered eco-

system N budgets. Therefore, the N2O fluxes associated

with invaded ecotypes could also be distinct from those

associated with native ecotypes.

Spartina alterniflora is a C4 plant native to North

America and was intentionally introduced to China in

1979 for coastal erosion control and sediment stabiliza-

tion (Qin & Zhong, 1992). Spartina alterniflora can prop-

agate via seed, rhizomes or vegetative fragments, and

thus has rapidly expanded by replacing native species

such as Suaeda salsa and Phragmites australis, becoming

one of the dominant plants in the land-water ecotone

(An et al., 2007). Invasive S. alterniflora has a higher net

primary productivity than native plants, and leads to

increased C stocks in biomass and soils (Liao et al.,

2008). This change in marsh ecosystem structure may

potentially stimulate CH4 emissions. In mesocosm

experiments, Zhang et al. (2010a) reported a 63%

increase in CH4 emissions following S. alterniflora inva-

sion mainly due to the higher biomass and density

compared with native plants (Cheng et al., 2007). How-

ever, there is little information on the invasive effects of

S. alterniflora on in situ CH4 emissions. Spartina alternifl-

ora invasion also increased N stocks and accelerated N

cycling in a salt marsh (Liao et al., 2008); however, the

response of N2O emissions to such a N increase

remains unexplored. In particular, anthropogenic N

inputs (e.g., fertilization, N deposition, and aquacul-

ture) have caused eutrophication of Chinese coastal

waters (Cui et al., 2013). Exotic plant species are sug-

gested to be better able to capitalize on increased avail-

ability of resources. Thus, it could be postulated that

invasive S. alterniflora could exert an undue influence

on CH4 and N2O emissions because of the continuous

availability of high-reactivity N (primarily as NO3�) in

the water (Deegan et al., 2012).

In this study, we carried out field measurements of

CH4 and N2O emissions from a coastal salt marsh

undergoing rapid S. alterniflora invasion in Jiangsu

Province, China. We also estimated the net soil C bal-

ance based on changes in SOC storage in the top

100 cm soil profile over the period 1995–2011. The

objectives of this study were (i) to determine the

patterns and magnitudes of CH4 and N2O fluxes; (ii)

to assess the effect of exotic S. alterniflora invasion on

GHG exchange rates; and (iii) to understand whether

the coastal marsh is a net C sink or source, and

gain insight into the complete GHG accounting of

the global warming potential (GWP) along the coast

of China.

Materials and methods

Study site and long-term experimental design

The study site is located in a coastal salt marsh in the buffer

zone of Yancheng National Nature Reserve (33°220N,

120°420E), Yancheng city, Jiangsu Province, China (Fig. 1a).

The climate is warm temperate, with a mean annual air tem-

perature of 12.6 °C and a mean annual precipitation of

1040 mm. Tides in this region are semidiurnal with an ampli-

tude of 2–3 m and the sea water salinity ranges from 30.0& to

32.0&. S. alterniflora was intentionally introduced in 1982 from

the United States (Qin & Zhong, 1992) and has rapidly spread

by replacing native P. australis and S. salsa, resulting in a sub-

stantial shift in plant zonation across the marsh landscape.

Coastal wetlands in the area are composed of five zones

(Fig. 1b). Open water is located on the lowest part, namely,

the subtidal zone and tidal channels, and exposed only during

extreme low tides or full moon events. The bare tidal flat and

S. alterniflora marsh are located on the lower and middle

regions of the intertidal zone, respectively, which is regularly

inundated semidiurnally. S. salsa marsh is in the irregularly

flooded high intertidal zone and is inundated only when the

tidal level is higher than the mean high water spring tide. P.

australis marsh is in the rarely flooded supralittoral zone and

is inundated only when storm and heavy rainfall events

occur.

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

2 J . YUAN et al.

A long-term experimental transect from near shore to the

lowland area ~300 m in width and ~2000 m in length was

established in 2008. For gas sampling, three 5 m2 plots were

randomly established within each site (open water, bare tidal

flat, S. salsa marsh, S. alterniflora marsh, and P. australis marsh)

along this transect in November 2011. The S. alterniflora site

was selected where S. alterniflora replaced S. salsa in 2002. The

open water site was established in a tidal channel where a

sluice had been built up to reduce water-level fluctuations.

Wooden boardwalks were installed in each plot for the mea-

surement of GHG emissions. For estimating SOC sequestra-

tion rate, a chronosequence with different invasion times was

identified within the S. alterniflora community based on the

analysis of Thematic Mapper satellite images (Figure S1).

Measurement of GHG fluxes

The static closed chamber technique was used to measure the

GHG fluxes (Figure S2). In the bare tidal flat and S. alterniflora,

S. salsa, and P. australis marshes, PVC chamber collars with a

water-filled channel (50 cm 9 50 cm 9 20 cm) were installed

along the boardwalk and inserted into the soil ~20 cm deep.

In the open water site, a specially designed system, which

included four stainless steel pegs for fixing the whole system

and adjustable crossbars for raising or lowering the chamber

collars with the fluctuation of water level, was installed along

the boardwalks to minimize the influence of wave impact.

Three PVC chamber collars were placed on the crossbars. If

necessary, the crossbars together with the chamber collars

were adjusted to the best position 1 day before sampling.

GHG fluxes were measured using transparent, open-ended

Plexiglass chambers equipped with a dry battery-driven fan.

The chamber volume was 25 l in the open water site and 125 l

in the other sites or 250 l in the S. alterniflora and P. australis

marshes as plants grew higher than the allowed height for the

125 l chamber.

Samples were taken twice weekly during the growing sea-

son from April to October and weekly during the nongrowing

season from November to March. Sampling was done at

08:00–10:00 hours local time to minimize diurnal variation in

flux patterns. Chambers were tightly fitted atop the collars by

inserting the flange of the chamber into the water trough at

the upper end of the chamber collars. Each time, four samples

of the chamber air were manually pulled into 50 ml syringes

at 0, 10, 20, and 30 min after closure, and injected into 22 ml

pre-evacuated vials fitted with butyl rubber stoppers for

analysis. The air temperature inside the chamber was simulta-

neously measured with a mercury thermometer. GHG concen-

trations were determined using a gas chromatograph (Agilent

7890, Santa Clara, CA, USA) equipped with a flame ionization

detector for CO2 and CH4 and a 63Ni electron capture detector

for N2O. CO2 and CH4 gas standards were provided by the

National Research Center for Certified Reference Materials,

Beijing, China. The N2O gas standard was provided by the

National Institute for Agro-Environmental Sciences, Japan.

The precision for GHG concentrations was �0.5% based on

(a)

(b)

Fig. 1 Location of the experimental site in the buffer zone of Yancheng National Nature Reserve, Jiangsu Province, China (a) and a

gas sampling transect of the coast including open water, bare tidal flat, and Spartina alterniflora, Suaeda salsa and Phragmites australis

marshes (b).

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

SPARTINA ALTERNIFLORA INVASION AND CLIMATE CHANGE 3

repeated measurements of standard samples. GHG fluxes

were calculated using a linear least squares fit to the four

points in the time series of concentration for each plot (Dataset

see Tables S1, S2, and S3). Net ecosystem CO2 exchange (NEE)

was equivalent to the inverse of CO2 flux (Figure S3). Fluxes

were omitted if the slope of the linear fitting had R2 < 0.90.

The minimum detectable fluxes for CO2, CH4, and N2O

were � 6.06 mg CO2 m�2 h�1, �0.06 mg CH4 m�2 h�1, and

�3.25 lg N2O m�2 h�1, respectively, for samples taken using

the 125 L chamber. Cumulative CH4 and N2O emissions in

the entire year and during the growing and nongrowing sea-

sons were calculated from the emissions between every two

adjacent measurements.

Auxiliary measurements

The water table and the soil and water temperature at 10 cm

depth were measured simultaneously with gas sampling at

each plot. A perforated PVC pipe 6 cm in diameter was

installed in each plot down to 70 cm depth, and a pressure

sensor (TS203, Danrui Sensor, Kunshan, China) was built

inside the PVC pipe to monitor the fluctuation of the water

table. The water table in the open water site was directly

measured by a straightedge. The temperature of the sea

water and soil at 10 cm depth was measured using a portable

digital thermometer (JM624, Jinming Instrument, Tianjin,

China).

Measurement of plant and soil characteristics

Aboveground biomass, height, and stem density of plants

were monitored on 22 September 2012. Three 50 cm2 sampling

quadrats were randomly established in each site. Plants in

each quadrat were clipped at the soil surface, washed care-

fully with distilled water and oven dried for 24 h at 70 °C.Height and stem density were determined.

Soil samples from the gas sampling sites were taken from

the 0–20 cm layer in each quadrat using a 2.5-cm-diameter

stainless steel sampler and stored at 4 °C in a cool box for

transport. A subsample (~200 g) was air dried for analysis of

soil properties. Concentrations of SOC and total nitrogen (TN)

were determined by the wet oxidation redox titration method

and micro-Kjeldahl method, respectively (Carter, 1993). To

measure dissolved organic carbon (DOC), 50 g fresh soil (on

an oven-dried basis) was incubated with 100 mL deionized

water for 30 min on an end-over-end shaker at 25 °C, andthen centrifuged at 4 000 rpm for 25 min at 4 °C (Yuan et al.,

2014). Supernatants were filtered through a 0.45 lm mem-

brane filter (Whatman, Clifton, NJ, USA) and analyzed on a

Shimadzu C analyzer (TOC Vcph, Shimadzu, Kyoto, Japan).

Sulfate (SO42�) in extracts was analyzed using a DX-120 Ion

Chromatograph (Dionex, Camberley, UK) fitted with a Dionex

IonPac AS19 separation column (4 mm 9 250 mm) with its

corresponding AG19 (4 mm 9 50 mm) guard column and a

conductivity detector. A 5 g fresh soil subsample (on an oven

dried basis) from each sample was extracted with 50 mL 2 M

KCl, shaken at 200 c.p.m. for 60 min and then filtered. Soil

NH4+ and NO3

� concentrations in the filtrate were determined

colorimetrically with a Segmented Flow Analyser (SAN++,Skalar, Breda, the Netherlands) (Ma et al., 2010).

Estimates of SOC sequestration rate and net GWP

Soil organic C sequestration rate was calculated based on the

rate of increase of SOC density in the top 100 cm soil profile.

Profile soils in the S. alterniflora marsh were collected in tripli-

cate in June 2011 along a chronosequence that S. alterniflora

invaded in 2011, 2010, 2007, 1999, and 1995. Soil profiles for

the bare tidal flat, and S. salsa and P. australis marshes were

collected in triplicate in 2003, 2007, and 2011. The soil profiles

were divided into 10-cm-thick horizontal layers for sampling.

Bulk density was measured simultaneously by the core

method (Culley, 1993).

Soil organic C density (SOCD, Mg C ha�1) in the 100 cm

profile was calculated by bulk density and SOC concentration

(Tables S4 and S5):

SOCD ¼X

ðSOCi � BDi �HiÞ � 10�1 ð1Þ

where SOCi, BDi, and Hi are the SOC concentration (g C kg�1),

bulk density (g cm�3), and the thickness (10 cm) of the soil

layer i, respectively. The rate of increase of SOC density

(SOCSR, Mg C ha�1 yr�1) was calculated as follows:

SOCSR ¼ ðSOCD0 � SOCDtÞ=t ð2Þwhere SOCD0 and SOCDt are the SOC densities in the bare

tidal flat, and S. salsa and P. australis marshes measured in

2003 and 2011, respectively, or in the marsh invaded by S. alt-

erniflora in 2011 and 1995, respectively; t is the difference in

the invasion time or interval between two measurement times

(year).

The global warming potential over a 100-year time horizon

(GWP, Mg CO2eq ha�1 yr�1) in the bare tidal flat, and S. al-

terniflora, S. salsa, and P. australis marshes was calculated by

the following equation (IPCC (Intergovernmental Panel on

Climate Change), 2007):

GWP ¼ CH4 � 25þN2O� 298� SOCSR� 44=12 ð3Þand for the open water:

GWP ¼ CH4 � 25þN2O�þCO2 � 1 ð4Þwhere CH4, N2O, and CO2 denote emission rates of CH4 (Mg

CH4 ha�1 yr�1), N2O (Mg N2O ha�1 yr�1) and CO2 (Mg

CO2 ha�1 yr�1), respectively.

Statistical analysis

Statistical analyses were conducted using SPSS 11.0 (SPSS Inc,

Chicago, IL, USA) unless otherwise stated. Analysis of vari-

ance (ANOVA) with a Tukey’s honestly significant difference test

was used to compare soil properties, plant characteristics, and

CH4 and N2O emissions among the sites. All dependent vari-

ables were evaluated for normality and were log-transformed

to normalize the distributions if necessary prior to statistical

analysis. Multiple regressions were used to identify the key

drivers of GHG fluxes in each site. Spearman’s nonparametric

rank correlation was used to describe relationships between

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

4 J . YUAN et al.

annual GHG emissions and soil or plant characteristics. The

quality of fit of the linear equations was judged statistically by

the coefficient of determination, R2, and its statistical signifi-

cance was determined by Fisher’s F test. The significance of

the regression coefficients was tested by Student’s t-test.

Results

Plant and soil characteristics

The aboveground biomass of S. alterniflora was

1.70 kg m�2, which was 2.15 and 4.16 times that of S.

salsa and P. australis, respectively, despite the fact that

P. australis had the highest height and S. salsa had the

highest stem density (Table 1).

Soil organic C and TN concentrations in S. alterniflora

marsh were 2.50–10.19 and 2.05–7.53 times, respec-

tively, those of other sites. The two unvegetated sites

had the lowest SOC and TN concentrations. DOC con-

centration showed a similar pattern and was up to

1.07 g C kg�1 in S. alterniflora marsh, a value that was

3.34–7.13 times that in other sites. The salinity and sul-

fate concentration in soils were 3.16–16.06& and 0.25–1.22 g SO4

2� kg�1, respectively, and showed an order

of S. alterniflora > open water sediments > bare tidal flat

> S. salsa > P. australis. The highest NH4+ concentration

was observed in S. alterniflora marsh, and the lowest

was in the unvegetated sites. The lowest NO3� concen-

tration was measured in S. alterniflora marsh, which

was significantly (P < 0.05) lower than that in other

sites except open water. No significant difference was

found in the NH4+ and NO3

� concentrations between

the S. salsa and P. australis marshes (Table 2).

Climate dynamics, soil temperature, and hydrologicalconditions

The average annual air temperature in 2012 was

15.1 °C, 2.5 °C higher than the long-term (30-year)

value (Fig. 2). Precipitation was 836 mm, of which 70%

fell during the growing season. Mean annual soil and

water temperatures at 10 cm depth were 18.47 °C and

20.12 °C in the bare tidal flat and open water sites,

respectively, which were significantly (P < 0.05) higher

than those in the vegetated sites (17.30–17.53 °C).Owing to the elevation gradient, the water table was

ranked as follows: open water > bare tidal flat > S. alt-

erniflora > S. salsa > P. australis. The annual mean water

table ranged from �40.38 (P. australis) to 133.26 cm

(open water).

Methane fluxes

The CH4 flux showed an apparent temporal pattern

in all five sites (Fig. 3). The lowest flux was 0.01–0.04 mg CH4 m�2 h�1, which was observed in Janu-

ary or February, and there was no significant differ-

ence among the five sites. CH4 fluxes peaked in July

for S. salsa marsh, August for open water and P. aus-

tralis marsh, and September for bare tidal flat and S.

alterniflora marsh. The highest flux was 0.62 mg

CH4 m�2 h�1 in S. alterniflora marsh, which was sig-

nificantly (P < 0.05) higher than in other sites. The

mean CH4 flux showed an order of S. alterniflora

(0.19 mg CH4 m�2 h�1) > P. australis (0.12 mg

CH4 m�2 h�1) > S. salsa (0.06 mg CH4 m�2 h�1) >bare tidal flat (0.05 mg CH4 m�2 h�1) > open water

(0.03 mg CH4 m�2 h�1). The CH4 flux was signifi-

cantly correlated with soil and water temperature in

all sites, and was significantly correlated with the

water table in all sites except open water (Table 3). A

multiple regression equation including both variables

was established; these two factors accounted for 16.3–66.4% of the temporal variation of the CH4 flux, of

which soil temperature explained 16.3–57.8%, while

the water table explained only 1.7–8.7%.

Annual CH4 emissions were distinct among sites and

the lowest emissions were measured in the unvegetated

sites, ranging from 2.81 to 4.16 kg CH4 ha�1 (Fig. 4).

However, values were not significantly different from

that in S. salsa marsh. The highest annual CH4 emission

was estimated as 16.98 kg CH4 ha�1 in S. alterniflora

marsh. In P. australis and S. salsa marshes, the annual

CH4 emissions were 10.79 and 4.88 kg CH4 ha�1,

respectively, and were significantly (P < 0.05) different

from each other. During the growing season, cumula-

tive CH4 emissions accounted for 72.5–83.7% of annual

CH4 emissions in the vegetated sites, compared with

64.8–71.7% in the unvegetated sites.

When the data from the five sites were combined for

analysis, annual CH4 emissions were significantly

(P < 0.05) correlated with SOC or TN and marginally

(P < 0.10) correlated with DOC, but not with soil

Table 1 Plant characteristics in the coastal marsh

Site

Aboveground

biomass

(kg m�2)

Stem

density

(stem m�2) Height (m)

P. australis 0.79 � 0.18b 46 � 6c 2.32 � 0.23a

S. salsa 0.41 � 0.05c 804 � 140a 0.48 � 0.04c

S. alterniflora 1.70 � 0.11a 112 � 10b 1.85 � 0.16b

F value 84.72 79.71 103.5

P value <0.001 <0.001 <0.001

Mean � standard deviation (n = 3).

Values within the same column followed by different letters

indicate significant differences at P < 0.05.

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

SPARTINA ALTERNIFLORA INVASION AND CLIMATE CHANGE 5

Table 2 Soil characteristics in the coastal salt marsh

Site

SOC

(g C kg�1) TN (g N kg�1)

DOC

(g C kg�1) Salinity (&)

Sulfate

(g SO42� kg�1)

NH4+

(mg N kg�1)

NO3�

(mg N kg�1)

P. australis 5.42 � 0.50b 0.55 � 0.04b 0.23 � 0.01bc 3.16 � 0.64d 0.25 � 0.09bc 3.61 � 0.59b 0.86 � 0.19a

S. salsa 3.95 � 0.25c 0.40 � 0.02c 0.32 � 0.02b 7.75 � 0.94c 0.47 � 0.07b 3.18 � 0.25bc 1.14 � 0.35a

S.

alterniflora

13.55 � 0.42a 1.13 � 0.03a 1.07 � 0.12a 16.06 � 0.67a 1.22 � 0.25a 6.12 � 0.53a 0.27 � 0.07b

Bare tidal

flat

1.88 � 0.33d 0.20 � 0.01d 0.15 � 0.04c 9.96 � 0.33c 0.51 � 0.05bc 1.81 � 0.57c 0.86 � 0.10a

Open water 1.33 � 0.17d 0.15 � 0.04d 0.18 � 0.02bc 13.49 � 1.43b 0.57 � 0.02c 1.83 � 0.59c 0.25 � 0.00b

F value 586.41 629.8 143.8 97.36 26.44 34.37 13.32

P value <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001

Mean � standard deviation (n = 3).

Values within the same column followed by different letters indicate significant differences at P < 0.05.

SOC, soil organic carbon; TN, total nitrogen; DOC, dissolved organic carbon.

(a)

(b)

(c)

(d)

Fig. 2 Temporal variation of air temperature and precipitation (a), highest tidal level and tidal level at 9:00 am (b), soil or water tem-

perature at 10 cm depth (c), and water table (d) in the coastal salt marsh. Standard deviations are not shown for figure clarity.

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

6 J . YUAN et al.

salinity, sulfate concentration, mean soil and water

temperature, or water table (Table 4). Furthermore,

annual CH4 emissions decreased exponentially with

the ratio of SO42� to DOC when the data measured in

the 15 plots of the five sites was integrated for analysis

(Fig. 5). In the vegetated sites, annual CH4 emissions

were also marginally (P < 0.10) correlated with above-

ground biomass, but not with stem density.

Table 3 Multiple linear regressions of CH4 flux (FCH4, mg CH4 m�2 h�1) and N2O flux (FN2O, lg N2O m�2 h�1) against water

table (WT) and soil and water temperature at 10 cm depth (T) in the coastal salt marshes

Gas Site Regression Equation R2

Partial R2

Temperature (°C) Water table (cm)

CH4 P. australis FCH4 = 0.0070T + 0.0013WT + 0.0723 0.664*** 0.578*** 0.087***

S. salsa FCH4 = 0.0019T + 0.0005WT + 0.0410 0.483*** 0.424*** 0.059**

S. alterniflora FCH4 = 0.0127T + 0.0024WT + 0.0408 0.592*** 0.554*** 0.017*

Bare tidal flat FCH4 = 0.0014T + 0.0005WT + 0.0331 0.416*** 0.346*** 0.069**

Open water FCH4 = 0.0007T + 0.0202 0.163*** 0.163*** 0.004

N2O P. australis FN2O = �0.834T + 10.159 0.588*** 0.588*** –

S. salsa FN2O = 0.105T + 4.765 0.088* 0.088* –

S. alterniflora FN2O = �0.953T + 8.393 0.517*** 0.517*** –

Bare tidal flat FN2O = 0.096T + 2.693 0.236*** 0.236*** –

Open water FN2O = 0.073T + 1.405 0.222*** 0.222*** –

*P < 0.05, **P < 0.01 and ***P < 0.001.

Fig. 3 Temporal variation of CH4 and N2O fluxes in the coastal

salt marsh. Standard deviations are not shown for figure clarity.

Fig. 4 Cumulative CH4 and N2O emissions from the coastal salt

marsh over the entire year and during the growing or non-

growing season. Different letters indicate significant differences

among the sites at P < 0.05. The growing season and non-grow-

ing season denoted the period from April to October and

November to March, respectively.

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

SPARTINA ALTERNIFLORA INVASION AND CLIMATE CHANGE 7

Nitrous oxide fluxes

N2O fluxes were at a low level throughout the year,

ranging from 0.89 to 7.80, 0.83 to 8.52, �29.24 to

14.81, 0.68 to 14.09, and �26.43 to 9.48 lg N2O

m�2 h�1 for open water, bare tidal flat, and S. alter-

niflora, S. salsa and P. australis marshes, respectively

(Fig. 3). Open water, bare tidal flat, and S. salsa

marsh showed weak emissions; however, mean N2O

fluxes during the growing season were significantly

(P < 0.05) higher than during the nongrowing season.

In contrast, although S. alterniflora and P. australis

marshes were also a source of N2O during the non-

growing season, they showed consumption of atmo-

spheric N2O during the growing season. The N2O

flux was positively (P < 0.05) correlated with soil and

water temperature in open water, bare tidal flat, and

S. salsa marsh; in contrast, there was a negative corre-

lation in S. alterniflora and P. australis marshes

(Table 3). It should be noted that N2O flux was sig-

nificantly (P < 0.05) negatively correlated with NEE

in S. alterniflora and P. australis marshes (Fig. 6).

During the growing season, cumulative N2O emis-

sions in S. alterniflora and P. australis marshes was

�0.57 and �0.38 kg N2O ha�1, respectively, which

resulted in these marshes becoming a sink of atmo-

spheric N2O, with annual N2O sink of �0.51 and

�0.25 kg N2O ha�1, respectively. Significant (P < 0.05)

differences in annual N2O emissions were ranked as S.

salsa > bare tidal flat ≥ open water > P. australis > S. alt-

erniflora (Fig. 4). Annual N2O emissions were margin-

ally (P < 0.10) and negatively correlated with SOC and

TN, but not with NH4+ or NO3

� (Table 4).

Carbon sequestration and net GWP

The SOC density in the top 100 cm soil profile mea-

sured in 2011 was estimated as 18.2 Mg C ha�1 for bare

tidal flat, 37.1 Mg C ha�1 for S. salsa marsh and 29.0 Mg

C ha�1 for P. australis marsh, and varied from 16.2 to

66.7 Mg C ha�1 in S. alterniflora marsh with 0–16 years

colonization. The highest SOC density in the marsh

invaded by S. alterniflora in 1995 was 1.80–3.67 times

that in bare tidal flat, S. salsa marsh and P. australis

marsh. The estimated SOC sequestration rate was 0.22,

Table 4 Correlation coefficients between annual CH4 or N2O emission and soil or plant characteristics in the coastal marsh

Gas SOC TN DOC Salinity Sulfate NH4+ NO3

�Soil/water

temperature

Water

table

Aboveground

biomass†

Stem

density†

CH4 0.963** 0.973** 0.866 0.205 0.642 0.957* �0.326 �0.683 �0.484 0.976 �0.816

N2O �0.816 �0.824 �0.705 �0.206 �0.527 �0.792 0.545 0.393 0.225 �0.867 0.951

*P < 0.05 and **P < 0.01.

†Data in the unvegetated sites were not included for analysis (n = 3).

Fig. 6 Relationship between N2O flux and net ecosystem CO2

exchange (NEE) in the S. alterniflora and P. australis marshes.Fig. 5 Relationship between annual CH4 emission and ratio of

SO2�4 to DOC in the fifteen plots of five measurement sites.

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

8 J . YUAN et al.

1.19, and 0.36 Mg C ha�1 yr�1 in bare tidal flat, S. salsa

marsh, and P. australis marsh during the period 2003–2011, respectively, whereas it was up to 3.16 Mg

C ha�1 yr�1 in S. alterniflora marsh (Fig. 7).

The estimated GWP in bare tidal flat, and S. alternifl-

ora, S. salsa, and P. australis marshes was �0.60, �11.30,

�4.09, and �1.14 Mg CO2eq ha�1 yr�1, respectively

(Fig. 8), indicating that the coastal marsh ecosystem,

regardless of the presence of plants, has a negative

GWP. S. alterniflora marsh showed the largest negative

GWP, primarily due to the high SOC sequestration rate

and, to a lesser extent, the uptake of atmospheric N2O.

In contrast, the GWP of open water site was 1.78 Mg

CO2eq ha�1 yr�1, and CH4, N2O, and CO2 emissions

contributed 3.9, 4.1, and 92.0%, respectively.

Discussion

Effect of S. alterniflora invasion on CH4 emissions

The 1.57- to 6.05-fold higher annual CH4 emissions in S.

alterniflora marsh compared with open water, bare tidal

flat, and native plant marshes indicate that S. alterniflora

invasion has dramatically stimulated CH4 emissions

along the coast of China. Our finding is consistent with

Cheng et al. (2007) and Zhang et al. (2010a) who

observed higher CH4 emissions from S. alterniflora

marsh than from P. australis and S. salsa marshes in

mesocosm studies. However, the CH4 emissions mea-

sured in this study were approximately half those mea-

sured in their studies and were substantially lower

than emissions reported previously for freshwater wet-

lands (Kang & Freeman, 2002; Chen et al., 2013). We

found that annual CH4 emissions were significantly

related to SOC and marginally related to DOC, which

accounted for 92.7% and 74.9%, respectively, of the spa-

tial variation of CH4 emissions among the five sites. Mi-

namikawa et al. (2005) also attributed differences in

CH4 emissions from five paddy fields to variations in

SOC. In this study, however, the 3.65-fold higher DOC

concentration in S. alterniflora marsh increased CH4

emissions only by 67% compared with P. australis

marsh, indicating that increased DOC in S. alterniflora

marsh was not efficiently converted into CH4 and the

marked accumulation of SOC did not induce large CH4

emissions. Interestingly, European P. australis haplo-

type invasion on the east coast of the United States has

not stimulated CH4 emissions compared with native S.

alterniflora, despite having more than double the above-

ground biomass, because of the similarity in below-

ground biomass and SOC storage for both species

(Emery & Fulweiler, 2014).

The concentration and quality of SOC or DOC can

affect CH4 emissions by changing both the supply of

methanogenic substrates and the abundance and com-

munity structure of methanogenic archaea in wetlands

(Wagner et al., 2005). Many researchers have noted that

labile organic compounds in the form of plant exudates

act as substrates for methanogenesis (e.g., Freeman

et al., 2002). Str€om et al. (2005, 2012), for example, found

Fig. 7 Relationship between SOC density in the top 100 cm soil

profile and the S. alterniflora invasion time or interval of the

measurement time in bare tidal flat, S. salsa marsh and P. aus-

tralis marsh.

Fig. 8 Global warming potential (GWP) estimated by annual

CH4 and N2O emissions as well as SOC sequestration potential

in bare tidal flat, S. alterniflora marsh, S. salsa marsh and P. aus-

tralis marsh, or annual CO2 emission in open water site.

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

SPARTINA ALTERNIFLORA INVASION AND CLIMATE CHANGE 9

that root exudates were the major source of substrate

(mainly acetate) for methanogens in peatlands,

although organic compounds from exudates accounted

for approximately 10% of total DOC in soil (Fischer

et al., 2007). Ding et al. (2002) and Liu et al. (2014) sug-

gest that the source of substrates for methanogenesis

depends on the species specific to a given wetland.

They found that substrates were derived primarily

from plant litters in Carex lasiocarpa marsh, but from ex-

udates in Calamagrostis angustifolia marsh. Yuan et al.

(2014) demonstrated that CH4 was primarily produced

by obligate acetotrophic methanogens in bare tidal flat,

but by facultative methanogens using ‘noncompetitive’

substrates such as trimethylamine in S. alterniflora

marsh. S. alterniflora absorbs sulfate from tidal water to

achieve osmoregulation (Cavalieri & Huang, 1981),

resulting in the synchronous accumulation of sulfate

and SOC after senescing. Sulfate-reducing bacteria have

been noted to outcompete acetotrophic or facultative

methanogens for acetate unless sulfate concentrations

are depleted to lower than 1 mM (King, 1984), an effect

widely observed in peatlands (Dowrick et al., 2006). In

this study, the sulfate concentration in S. alterniflora

marsh amounted to 12.71 mM, and CH4 emissions

were negatively related to the ratio of SO42� to DOC.

Thus, it is likely that the low increase in CH4 emissions

in S. alterniflora marsh was primarily due to a limited

increase of ‘noncompetitive’ substrates.

CH4 fluxes were significantly correlated with soil and

water temperature in all sites. Previous studies have

shown that high temperatures increase CH4 production

due to increased substrate supply following a stimula-

tion of SOC degradation and plant growth, and/or an

increased abundance of methanogenic archaea (Gan

et al., 2012; Kim et al., 2012). However, we found that

the CH4 flux peak in S. alterniflora marsh was not com-

pletely consistent with the maximum soil temperature

and occurred in September. Wang & Lee (1994) demon-

strated that the highest concentrations of aliphatic

amines in soils appeared when S. alterniflora began to

senesce. The coincidence of the CH4 flux peak at the

time of S. alterniflora senescence further suggests that

‘noncompetitive’ substrates play a key role in CH4

emissions in S. alterniflora marsh. It should be noted

that, the hydrologic setting of S. alternifora is different

than S. salsa and P. australis, with S. alternifora located

in sediments with higher mean water (Fig. 1b). So the

greater CH4 emissions from S. alternifora could also be

(partly) explained by their being located in a more satu-

rated soil environment.

The annual CH4 emissions from S. alterniflora marsh

were close to the value (12.5 kg CH4 ha�1) measured

for a Virginia coastal salt marsh (Bartlett et al., 1985),

but much lower than those measured for many estuar-

ies (Poffenbarger et al., 2011). For example, Tong et al.

(2012) reported annual emissions of 956.5 kg CH4 ha�1

from the estuary of Mingjiang River, China where tidal

water salinity was 4.2& and pore water sulfate concen-

tration was as low as 2.60 mM. Poffenbarger et al.

(2011) attributed spatial differences in CH4 emissions to

the discrepancy of tidal water salinity and sulfate con-

centration. However, Keller et al. (2009) found CH4

emissions from brackish marshes were not greatly dif-

ferent from those from freshwater marshes, if not

higher, despite sulfate concentrations in brackish

marshes being generally higher than the threshold for

suppressing hydrogenotrophic and acetotrophic metha-

nogenesis. Clearly, further study is required to evaluate

differences in substrate type and the dominant species

of methanogens in S. alterniflora estuarine marshes with

low salinity.

Annual CH4 emissions from open sea water

amounted to 2.81 kg CH4 ha�1, which is greater than

the value (0.09 kg CH4 ha�1) for open ocean (Holmes

et al., 2000), but only slightly higher than the 0.56–1.22 kg CH4 ha�1 for European shelf areas (Bange,

2006) and close to the data (1.87–3.10 kg CH4 ha�1) for

shelf regions of the Black Sea (Amouroux et al., 2002).

These findings indicate that CH4 emissions from coastal

waters do not differ significantly around the world.

CH4 in the marine environment mainly originates from

organic matter in sediments at shallow depths (Shakh-

ova & Semiletov, 2007). Zhang et al. (2004) measured

higher CH4 concentrations in benthic waters and high

CH4 fluxes from the organic C-rich sediments in the

North East China Sea. Jayakumar et al. (2001) attributed

high CH4 saturations in the coastal waters of the Ara-

bian Sea to the copious supply of organic C from land

as well as direct CH4 inputs from coastal wetlands

through runoff. Therefore, the increased C inputs due

to S. alterniflora invasion might stimulate CH4 emissions

in open water.

Effect of S. alterniflora invasion on N2O emissions

Coastal areas have been recognized as a major marine

contributor to atmospheric N2O (Nevison et al., 1995;

Bange, 2006). Seitzinger & Kroeze (1998) reported that

~1.00% of the N input was converted to N2O in estuar-

ies, similar to the current default emission factor of

1.00% per unit N input defined by IPCC (Intergovern-

mental Panel on Climate Change) (2006) in agricultural

soils. In this study, however, P. australis and particu-

larly S. alterniflora marshes consumed atmospheric

N2O, as observed in the Scirpus mariqueter estuarine

marsh of Yangtze River (Yu et al., 2012) and in a Japa-

nese lagoon marsh (Hirota et al., 2007). In general, salt

marshes are recognized as N-limited ecosystems for the

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

10 J . YUAN et al.

growth of microorganisms and plants, and such a con-

straint would be more severe for S. alterniflora and P.

australis with larger primary production due to their

larger N demand (Delaune et al., 1989). Wetland plants

outcompete microorganisms such as nitrifiers and den-

itrifiers for mineral N; thus denitrifiers have to use N2O

as the only electron acceptor when soil NO3� is below

the threshold of ~1 mg N kg�1 (Ryden, 1983). Although

NO3‒ concentration in coastal waters of the study region

increased 3.54 times from 1997 to 2006 (Song, 2010) and

annual N loading was estimated as 68.4 kg N ha�1

(Wan et al., 2003), NO3� concentration in soils was close

to or below the threshold for denitrifers. Our findings

suggest that salt marshes could efficiently lower

anthropogenic N loading without stimulating N2O

emissions.

It has been found that ammonia-oxidizing bacteria

and archaea can utilize NH4+ at concentrations as low

as 1 lM and 130 nM, respectively (Bollmann et al.,

2002; Martens-Habbena et al., 2009). These values are

much lower than the concentrations measured in this

study. Thus, we infer that the extremely low NO3� con-

centrations were primarily derived from low nitrifica-

tion rates in marsh soils probably due to anaerobic

condition (Jenkins & Kemp, 1984). Coupled nitrifica-

tion-denitrification has been suggested to be the major

pathway for N loss in wetlands (Moseman-Valtierra

et al., 2011). The photosynthesis of S. alterniflora and P.

australis could stimulate coupled nitrification-denitrifi-

cation by supplying O2 to nitrifiers in the rhizosphere

via aerenchymateous tissue, thereby stimulating nitrifi-

cation and providing NO3� to denitriers (An & Joye,

2001). In turn, the stimulated denitrifiers would con-

sume N2O during hypoxic conditions due to the NO3�

limitation. In this study, the negative relationship

between NEE and N2O flux in S. alterniflora and P. aus-

tralis marshes indicated that plant photosynthates as

root exudates and debris might play a key role in N2O

consumption by facilitating the activities of denitrifiers.

Jørgensen et al. (2012) showed that the N2O consump-

tion rate in the root layer soil was 5- to 6-fold greater

than that in the soil below the main root zone in a Dan-

ish Phalaris arundinacea wetland. Further study is

required to understand the actual mechanism of N2O

consumption in coastal marshes.

The net N2O emissions in open water, bare tidal flat,

and S. salsa marsh were in contrast with those in S. alt-

erniflora and P. australis marshes. These were close to

the reported emission (0.48 kg N2O ha�1) for Louisi-

ana’s gulf coastal marsh (Smith et al., 1983), and were

slightly higher than the reported annual sea-to-air

value (0.06–0.16 kg N2O ha�1) for the North Pacific

(Popp et al., 2002), but were lower than the emission

(19.64–40.68 kg N2O ha�1) from the open water area of

various European estuaries (Bange, 2006). Clearly, the

current eutrophication status does not appear to

increase N2O emissions along the coast of China. A sig-

nificant relationship between N2O flux and soil temper-

ature indicates that higher temperatures are conducive

to N2O emissions (Chapuis-Lardy et al., 2007). The sur-

face seawater columns and top layer of the sandy bare

tidal flat are generally oxic (Rosenkranz et al., 2006),

while macrobenthic (e.g., crabs) activities in S. salsa

marsh have been suggested to enhance O2 transport

into the sediment by bioturbation (Dollhopf et al.,

2005). Hence, aerobic water and soil surfaces and

higher temperatures could accelerate soil organic N

mineralization and stimulate N2O production through

nitrification. Interestingly, the highest NO3� concentra-

tion was in S. salsa marsh and was slightly higher than

the threshold for net N2O consumption. It is likely that

the denitrification potential in open water, bare tidal

flat and S. salsa marsh was low due to low SOC concen-

trations and a low or absent supply of plant photosyn-

thates (Wang et al., 2007; Sun et al., 2013).

Effect of S. alterniflora invasion on C sequestration andGWP

Our results showed that S. alterniflora invasion effec-

tively increased C sequestration. The estimated SOC

sequestration rate in S. alterniflora marsh was 2.63- to

8.78-fold higher than in native plant marshes (Fig. 7),

and was higher than the value (0.08–0.38 Mg

C ha�1 yr�1) for peat ecosystems (Belyea & Warner,

1996) and the global average (2.10 Mg C ha�1 yr�1) in

mangrove and salt marshes (Choi et al., 2001; Chmura

et al., 2003). It was also higher than those in other eco-

systems, such as farmland (0.15 Mg C ha�1 yr�1) and

preserved old-growth forest of China (0.06 Mg

C ha�1 yr�1) (Xie et al., 2007).

The accumulation of SOC has been suggested to

result from either higher primary production and less

decomposition, and/or an input of residues with high

chemical resistance to decay (Baldock & Skjemstad,

2000). The highest SOC sequestration rate in S. alternifl-

ora marsh was primarily the result of greater inputs of

C through plant litters and roots, and their being

located in a more saturated and presumably more

anaerobic environment. Our results showed that the

aboveground biomass of S. alterniflora was 1.15- to 3.16-

fold greater than that of native plants, while the root

biomass of S. alterniflora was about fivefold greater than

S. salsa (Zhang et al., 2010b). As belowground biomass

(roots and rhizomes) of S. alterniflora was three- to

five-fold greater than aboveground biomass (Roman &

Daiber, 1984; Liao et al., 2008), Zhang et al. (2010b) con-

cluded that belowground biomass has a more impor-

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

SPARTINA ALTERNIFLORA INVASION AND CLIMATE CHANGE 11

tant role in SOC accumulation. Meanwhile, S. alternifl-

ora litter has a high C/N ratio and a high Na content

relative to S. salsa, and is thought to be resistant to

decay and facilitate higher SOC sequestration (Yang

et al., 2009). Although the aboveground biomass of P.

australis was only second to that of S. alterniflora, SOC

sequestration rate was lowest among the vegetated

sites. Therefore, the differences in primary productivity

could not fully explain this variability. P. australis

marsh was located in the highest region and was less

flooded by tides. In contrast, S. salsa and particularly S.

alterniflora were situated in the lower region where tidal

flooding frequently occurred. Therefore, the sediment

deposition rates were distinct among the sites. Liu et al.

(2010) estimated that the sediment deposition rate was

2.20 and 3.00 cm yr�1 in S. salsa and S. alterniflora

marshes, respectively, but only 1.00 cm yr�1 in bare

tidal flat and 1.50 cm yr�1 in P. australis marsh over the

period 1986–2007. Sediment deposition not only input-

ted organic C directly, but also, more importantly, bur-

ied plant-derived organic materials, resulting in the fast

accumulation of SOC by slowing their turnover

(Chmura et al., 2003; Choi & Wang, 2004).

A positive GWP value for open sea water indicated

that seawater-flooded coast is a potential GHG source.

In contrast, the intertidal and supralittoral zones effec-

tively suppress the increase of atmospheric GHGs

mainly by sequestering C in soils. S. alterniflora showed

the highest potential for mitigating climate warming,

which was 2.76–9.94 times that for native plants. In

China, S. alterniflora had spread to an area of 34 451 ha

by 2007 (Zuo et al., 2012), which accounted for 3.54% of

the national coastal wetlands (Niu et al., 2012). The esti-

mated net consumption of atmospheric GHGs could

reach 0.39 Tg CO2eq yr�1 in S. alterniflora marsh ecosys-

tem of China.

In conclusion, despite sulfate-accumulation-sup-

pressed CH4 production, S. alterniflora invasion along

the coast of China still stimulated CH4 emissions com-

pared with open water, bare tidal flat, and native P. aus-

tralis and S. salsa marshes. This is because higher

primary productivity and the consequent elevation of

SOC supplied more substrates for methanogensis. Low

N2O emissions were also observed in open water, bare

tidal flat and native S. salsa marsh, and in contrast, net

consumption of atmospheric N2O occurred in S. alter-

niflora and P. australis marshes. This indicated that salt

marshes, especially under S. alterniflora invasion, could

efficiently cut down anthropogenic N loading without

stimulating N2O emissions. SOC sequestration rate

amounted to 3.16 Mg C ha�1 yr�1 in S. alterniflora

marsh, which was 2.63 to 8.78 times that of native plant

marshes. Our results suggest that S. alterniflora invasion

along the coast of China could efficiently mitigate GHG

emissions by strongly sequestering atmospheric CO2

and, to a lesser extent, consuming atmospheric N2O

compared with native plants.

Acknowledgements

This work was supported by the strategic priority research pro-gram of the Chinese Academy of Sciences (XDA05020501),National Basic Research Program of China (2012CB417102), andNatural Science Foundation of China (41171190, 40725003). H.Kang is grateful to ERC (2013-067218).

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Supporting Information

Additional Supporting Information may be found in theonline version of this article:

Figure S1. Sampling sites for measurement of SOC seques-tration rate in the coastal wetlands.Figure S2. Closed chamber systems for measurement ofgreenhouse gases from salt marshes (a) and the open water(b). 1 - marsh soil or sediment, 2 - PVC chamber collar, 3 -water-filled channel, 4 - plant, 5 - plexiglass cylindricalchamber, 6 - fan, 7 - thermometer, 8 - silicon septum, 9 -stainless steel pegs, 10 - locking recess, 11 - crossbar and 12 -water column.Figure S3. Temporal variation of carbon dioxide (CO2)fluxes in a coastal salt marsh measured by the transparentchamber.Table S1. Dataset of the CH4 fluxes (mg CH4 m�2 h�1) inthe coastal salt marsh measured in 2012.Table S2. Dataset of the N2O fluxes (µg N2O m�2 h�1) inthe coastal salt marsh measured in 2012.Table S3. Dataset of the CO2 fluxes (mg CO2 m�2 h�1) inthe coastal salt marsh measured in 2012.Table S4. Soil bulk density (g cm�3) in the top 100 cm pro-file of a coastal salt marsh.Table S5. Soil organic carbon concentration (g C kg�1) inthe top 100 cm profile of a coastal salt marsh.

© 2014 John Wiley & Sons Ltd, Global Change Biology, doi: 10.1111/gcb.12797

14 J . YUAN et al.