Sulfur storage changed by exotic Spartina alterniflora in coastal saltmarshes of China

e c o l o g i c a l e n g i n e e r i n g 3 5 ( 2 0 0 9 ) 536–543

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Sulfur storage changed by exotic Spartina alterniflora in coastal saltmarshes of China Changfang Zhou a,b,c , Shuqing An a,c,∗ , Zifa Deng a , Daqiang Yin c , Yingbiao Zhi a , Zhiyi Sun a , Hui Zhao a , Luxian Zhou a , Chao Fang a , Chen Qian a a

Institute of Wetland Ecology, School of Life Science, Nanjing University, Nanjing 210093, PR China Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK c State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing 210093, PR China b

a r t i c l e

i n f o

a b s t r a c t

Article history:

For the purpose of ecological engineering, Spartina alterniflora was introduced to China in

Received 23 August 2007

1979 and now covers about 112,000 ha of China’s coastal lands. It was hypothesized that

Received in revised form

S. alterniflora could actively change the habitat environment, thus facilitating its compe-

14 January 2008

tition over native species. In Yancheng Nature Reserve, sulfur storage of sediments and

Accepted 17 January 2008

plant tissues was compared among marshes dominated by the exotic S. alterniflora and adjacent native Suaeda salsa and Phragmites australis and bare mudflat. Results showed that the S. alterniflora marsh contained the highest content of water-soluble, adsorbed, carbonate-

Keywords:

occluded and total sulfur in the sediment. The sulfur levels were higher in the center than

Biogeochemistry

at the edges of the S. alterniflora marsh. Native marshes showed no significant difference

Salt marsh

in sediment sulfur levels. With greater biomass and higher tissue sulfur concentrations,

Spartina alterniflora

plant sulfur storage of S. alterniflora vegetation was also larger than those of the native

Sulfur

vegetations. Because higher concentrations of sulfur increase the competitive advantage

Vegetation alteration

of S. alterniflora over native halophytes, the results of the research showing that S. alterniflora increased marsh sulfur storage may shed light on the mechanism of expansion of monospecific vegetation in coastal China. © 2008 Elsevier B.V. All rights reserved.

1.

Introduction

Smooth cordgrass (Spartina alterniflora) is a rhizomatous perennial C4 grass, characterized by high productivity and acting as a foundation species in the intertidal coastal zone (Stribling, 1997; Normile, 2004). Native to the Atlantic and Gulf coastal marshes of North America, the species has been found flourishing on the Pacific coast of America (Daehler and Strong, 1996; Taylor et al., 2004; Civille et al., 2005), Brazil (Netto and Lana, 1997, 1999), England, New Zealand, Australia, Tasmania

and the Netherlands (Ayres et al., 2004). The species usually forms dense stands and plays an important role in coastal protection and erosion control (Chung et al., 2004; Strong and Ayres, in press). For the purpose of ecological engineering, S. alterniflora was introduced to China in 1979 (Xu and Zhuo, 1985; Chung et al., 2004). During the next 25 years, the species experienced a rapid expansion over Chinese coasts. It now covers a total area of about 112,000 ha, and is distributed from Tianjin City (117.20◦ E, 39.13◦ N) in the north to Guangxi Province (109.12◦ E, 21.49◦ N)

∗ Corresponding author at: Institute of Wetland Ecology, School of Life Science, Nanjing University, Nanjing 210093, PR China. Tel.: +86 25 83594560; fax: +86 25 83594560. E-mail address: [email protected] (S. An). 0925-8574/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2008.01.004

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in the south (Zhang et al., 2004), with Jiangsu Province having the largest population of 13,700 ha (An et al., 2007; Zhang et al., 2004). It was suggested that the rapid expansion of S. alterniflora in China was attributed to suitable climate, sediment, and marine hydrodynamics (Normile, 2004; Zhang et al., 2004). However, efforts are still needed before a full understanding of its mechanisms can be reached. Recent evidence suggests that plant species can exert strong control over their soil environment and thus influence interactions with other plant species (Sherman et al., 1998; Ehrenfeld, 2003; Allison and Vitousek, 2004). It has been reported that S. alterniflora accelerates soil development of salt marshes (Netto and Lana, 1997), increases organic matter of the sediment (Gao et al., 2005), changes carbon and nitrogen cycling of the coast (Tyler and Grosholz, 2003), modifies habitat conditions and facilitates the establishment and persistence of cobble beach plant communities (Bruno and Kennedy, 2000), and has other ecosystem effects (Crooks, 2002; Levin et al., 2006). Sulfur, like nitrogen, phosphorus and potassium, is essential nutrition for all plants (Thompson et al., 1986; Itanna, 2005). However, as coastal environments are usually enriched with this element, studies on sulfur have often focused on its toxicity to animals and plants (Weeks et al., 2002; Holmer et al., 2003). S. alterniflora is an exception, as supported by the following evidences. Seliskar et al. (2004) found through lab experiments that S. alterniflora was more tolerant to sulfide than Spartina patens, Setaria magna, Atriplex triangularis and P. australis. They also found that sulfide levels between 0.4 and 0.9 mM would favor seedling establishment of S. alterniflora over P. australis, while at 0.9 mM, S. alterniflora seedlings would have the decided advantage (Seliskar et al., 2004). Chambers et al. (1998) found through both lab study and field investigation that S. alterniflora was better adapted to sulfidic soil conditions than P. australis, thus restricting the distribution of the latter in tidal salt marshes. Stribling (1997) also suggested that the adaptation of S. alterniflora to high salinity was correlated to a high sulfate requirement, and sulfate deficiency might limit S. alterniflora distribution in low salinity marshes. S. alterniflora may contain some special forms of sulfur, as its total sulfur content is higher than for most plants, with measured concentrations of up to 1.2% (Stribling, 1997). Since seawater contains sulfate, activities of S. alterniflora that concentrate sulfur could have a substantial influence on the chemistry of substrates where this plant invades as well as where it grows naturally (Derry and Murray, 2004). Aiming to uncover the mechanism of rapid expansion of S. alterniflora in China and the means by which large areas of monospecific vegetation can be maintained, it has been hypothesized that S. alterniflora can positively promote the accumulation of sulfur compounds in sediments, thus inhibiting growth of native species that are less tolerant of the conditions ensuing from high sulfur concentrations in the sediment. To test the hypothesis, we set up a field investigation at Yancheng National Nature Reserve in Jiangsu Province, the largest beach wetland reserve in China. The sulfur compounds were compared in sediments of the exotic S. alterniflora marsh, adjacent native S. salsa marsh, P. australis marsh and bare mudflat, and also determined the sulfur contained in tissues of

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the three dominant species, S. alterniflora, S. Salsa and P. australis. This research may shed light on the reasons for the rapid expansion of monospecific vegetation in China, and may also help in a better evaluation of the influence of S. alterniflora expansion on Chinese coastal ecosystems.

2.

Materials and methods

2.1.

Site description

The study site was set in the core area of Yancheng Nature Reserve (Fig. 1). The reserve is on the west Pacific coast (119◦ 29 E to 121◦ 16 E, 32◦ 20 N to 34◦ 37 N) in the transition belt between north subtropical and warm-temperate zones, with annual solar radiation about 502.42 kJ cm−2 and rainfall about 1000 mm (Zhou et al., 2003; Zhu et al., 2004). It is on an aggrading mudflat, controlled by standard semi-diurnal tides, with a tidal range 2.5–4.0 m on average (Ren, 1986; Zhu et al., 2004). Seawater salinity here is 2.95–3.22%. Sand contained in the seawater averages 2.209 g l−1 at the flood and 1.156 g l−1 during ebb tides (Ren, 1986). The Reserve was established in 1984, and was recognized as part of the “International Network of Biosphere Reserves” in 1993 and as a “Wetland of International Importance” (no. 1156) of the Ramsar Convention in 2002. It is the first and largest beach wetland reserve in China, and offers the world’s largest winter habitat for the endangered Grus japonensis (Zhou et al., 2003). S. alterniflora was introduced to Yancheng Nature Reserve in 1983 (Xu and Zhuo, 1985), and it spread widely in the intertidal zone during the next 20 years (Zhang et al., 2004). S. salsa is one of the main native halophytes in the tidal zone and grows

Fig. 1 – Sample locations in Yancheng Natural Reserve.

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to the landward side of the S. alterniflora vegetation. Next most abundant is P. australis, which grows above S. salsa. The three species overlap very little in distribution, and typical widths of S. alterniflora, S. salsa and P. australis are about 1.5, 4.8 and 0.5 km, respectively, in the sampling site. A bare mudflat of several kilometers in width appears in front of S. alterniflora vegetation at low ebb. Due to strict management of the reserve and few human disturbances, the extent of all three vegetation zones has grown since the establishment of the reserve.

2.2.

Sample collection and analyses

Field sampling was carried out from 30 October to 4 November 2004. Three parallel sample transects (T1 –T3 ) were labeled from seaward to upland, each about 7 km long, and with a distance of 200 m between them (Fig. 1). On each transect, five locations of equal distance were marked, numbered from seaward to landward, within monospecific vegetation of S. alterniflora, S. salsa or P. australis. One location (S0 ) 200 m out from the seaside margin of the S. alterniflora vegetation was also marked on the bare mudflat as the control. In each location, soil from three separate plots, 5 cm × 5 cm in area and 30 cm in depth and 10 m apart, was dug out and combined for soil analysis. Plants with root and rhizomes within three separate plots, 50 cm × 50 cm in area and 30 cm in depth, were also collected and mixed for biomass analysis. For the middle transect T2 , another three individual plants were randomly dug out in each location for analysis of sulfur concentrations in plant tissues. Soil samples taken back to the lab were air-dried, ground and passed through a 0.15-mm sieve, with remaining plant residue in the soil being removed. The methods of Blanchar (1986) and Shan et al. (1992) in extracting sulfur compounds were referenced. One-gram soil from each sample was transferred into a 50 ml centrifuge tube, to which 10 ml H2 O was added, it was shaken for 30 min and centrifuged at 10,000 rpm for 10 min. The supernatant was collected for analysis of water-soluble sulfur. The residual soil in the tube was washed with 5 ml H2 O, then 10 ml NaH2 PO4 was added, and it was shaken for 30 min and centrifuged again at 10,000 rpm for 10 min. The supernatant was collected for analysis of adsorbed sulfur. The residual soil was washed again with 5 ml H2 O, to which 20 ml 1N HCl was added, it was shaken for 1 h and also centrifuged at 10,000 rpm for 10 min. The supernatant was collected for analysis of carbonate-occluded sulfur. Sulfur contents in the three supernatants were analyzed with inductively coupled plasma-atomic emission spectroscopy (ICP-AES, JY38S). Another 0.1 g soil of each sample was put in a small porcelain crucible, mixed with 0.25 g NaHCO3 and 0.01 g Ag2 O, heated at 550 ◦ C for 3 h in a muffle furnace. The ash was transferred into a centrifuge tube, to which 6 ml H2 O was added, it was shaken for 3 h at 37 ◦ C and centrifuged at 4000 rpm for 10 min. Total sulfur content in supernatant was analyzed with ICP-AES (Blanchar, 1986; Zhao et al., 1998). For plant sulfur storage analysis, biomass production per unit area marsh was first determined, as plant materials were rinsed with distilled water, divided in above- and underground tissues, dried at 65 ◦ C for 60 h and weighed. For measurement of sulfur concentrations in plant tissues, plants were

also rinsed with distilled water, divided in above- and underground tissues, then dried at 65 ◦ C for 24 h, ground and passed through a 0.25-mm sieve, and dried at 65 ◦ C for another 24 h. Then, 0.5 g tissue for each sample was put in a tube, to which 5 ml HNO3 was added, it was covered with a funnel and stood for more than 30 min, then digested at 150 ◦ C for 30–45 min, cooled 5 min, then 2 ml HClO4 was added and it was digested at 215 ◦ C for 2 h after fumes from HNO3 had evolved. The funnel was removed 15 min before the end of digestion. The tube was cooled, after added 30 ml H2 O, it was heated to boiling, mixed while hot, then cooled, diluted to 50 ml and mixed again. A small portion of the digest was centrifuged in a 1.5-ml disposable tube for 3 min with 12,000 rpm, then sulfur concentration in supernatant was measured by ICP-AES (Blanchar, 1986; Li et al., 2001). Plant sulfur storage per unit area marsh was estimated as sulfur concentration in underground tissue × underground biomass + sulfur concentration in aboveground tissue × aboveground biomass. Statistics of the data were performed by SPSS 13.0. One-way ANOVAs, with Duncan tests when variances were homogeneous, but with Tamhane tests when variances were heterogeneous, were performed at 0.05 level among different salt marshes or among different locations within the same marsh. Correlations between sediment total sulfur storage and plant sulfur storage were calculated by Pearson two-tailed tests.

3.

Results

3.1. Sulfur contents differed among sediments of the four marshes The S. alterniflora marsh contained the highest sulfur contents (Table 1), as water-soluble and adsorbed sulfur in S. alterniflora marsh (24.06 ± 2.64 and 28.43 ± 1.39 ␮gS g−1 soil) were significantly higher than those in bare mudflat (15.08 ± 1.31 and 20.59 ± 1.27 ␮gS g−1 soil) and P. australis (13.10 ± 0.88 and 22.37 ± 0.71 ␮gS g−1 soil) marsh (P < 0.05), while carbonateoccluded sulfur in S. alterniflora marsh (358.48 ± 16.90 ␮gS g−1 soil) was significantly higher than that in bare mudflat (294.13 ± 20.42 ␮gS g−1 soil) (P < 0.05). Total sulfur in S. alterniflora marsh (1145.92 ± 109.22 ␮gS g−1 soil) was significantly higher than that in bare mudflat (787.06 ± 15.41 ␮gS g−1 soil) and S. salsa marsh (811.16 ± 6.97 ␮gS g−1 soil) (P < 0.05). S. salsa marsh had relatively higher contents of water-soluble, adsorbed and carbonate-occluded sulfur among the three native marshes (P < 0.05). P. australis marsh and bare mudflat were similarly lower in water-soluble, adsorbed and carbonate-occluded sulfur. No significant differences were found for total sulfur among the three native salt marshes.

3.2. Spatial variations of sulfur contents in sediments within the same marsh Sulfur contents in sediments within the five locations in the S. alterniflora marsh also varied greatly (Figs. 2 and 3), as all detected sulfur compounds were relatively higher in the center of the marsh but lower at both edges. Water-soluble and adsorbed sulfur exhibit no statistically significant difference

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Table 1 – Average sulfur compounds in sediments from exotic Spartina alterniflora and adjacent native salt marshes (␮gS g−1 soil) Water-soluble sulfur Bare mudflat S. alterniflora marsh Suaeda salsa marsh Phragmites australis marsh

15.08 24.06 23.60 13.10

± ± ± ±

1.31 a 2.64 b 1.16 b 0.88 a

Adsorbed sulfur 20.59 28.43 24.49 22.37

± 1.27 a ± 1.39 b ± 0.97 ab ± 0.71 a

Carbonate-occluded sulfur 294.13 358.48 344.89 330.11

± ± ± ±

20.42 a 16.90 b 6.66 b 9.97 ab

Total sulfur 787.06 1145.92 811.16 815.29

± ± ± ±

15.41 a 109.22 b 6.97 a 14.90 ab

Mean ± S.E. For bare mudflat, n = 3; for vegetation covered salt marshes, n = 15. Data marked by the same letter indicated no significant difference between one another at the level of 0.05 tested by one-way ANOVAs.

among locations S2 (28.01 ± 5.10 and 30.72 ± 1.24 ␮gS g−1 soil), S3 (35.04 ± 3.61 and 32.84 ± 1.90 ␮gS g−1 soil) and S4 (26.06 ± 6.90 and 32.72 ± 1.98 ␮gS g−1 soil) (P > 0.05), but were significantly lower in locations S1 (15.06 ± 2.41 and 22.63 ± 1.78 ␮gS g−1 soil) and S5 (16.10 ± 2.90 and 23.23 ± 1.88 ␮gS g−1 soil) (P < 0.05). S3 in the center of the marsh

Fig. 3 – Total sulfur levels in sediment of each location. Shown is mean ± S.E., n = 3. Statistics were only performed for locations within the same marsh, and bars marked by the same letter indicate no significant difference from one another at the 0.05 level as determined by one-way ANOVAs. Location 0, from bare mudflat, locations 1–5, from S. alterniflora marsh, locations 6–10, from S. salsa marsh, locations 11–15, from P. australis marsh.

Fig. 2 – Water-soluble, adsorbed and carbon-occluded sulfur levels in sediment of each location. Shown is mean ± S.E., n = 3. Statistics were only performed for locations within the same marsh, and bars marked by the same letter indicate no significant difference from one another at the 0.05 level as determined by one-way ANOVAs. Location 0, from bare mudflat, locations 1–5, from Spartina alterniflora marsh, locations 6–10, from Suaeda salsa marsh, locations 11–15, from Phragmites australis marsh.

occupied significantly higher amount of carbonate-occluded and total sulfur (453.93 ± 32.70 and 1902.69 ± 67.97 ␮gS g−1 soil, respectively) over the rest of locations (P < 0.05). Carbonate-occluded sulfur in S2 (367.80 ± 10.30 ␮gS g−1 soil) and S4 (375.33 ± 3.67 ␮gS g−1 soil) were also significantly higher than those in S1 (289.53 ± 8.91 ␮gS g−1 soil) and S5 (305.80 ± 14.82 ␮gS g−1 soil) (P < 0.05). The amount of total sulfur was also relatively higher in S2 (1102.84 ± 138.48 ␮gS g−1 soil) and S4 (999.72 ± 110.65 ␮gS g−1 soil) than in S1 (838.19 ± 45.44 ␮gS g−1 soil) and S5 (886.16 ± 19.85 ␮gS g−1 soil), but with no significant difference (P > 0.05). Condition of sulfur contents within locations of S. salsa or P. australis marsh was greatly different from that in the S. alterniflora marsh (Figs. 2 and 3). Small fluctuations in contents of water-soluble and adsorbed sulfur appeared among the five locations in S. salsa marsh, but no significant difference was found. Carbonate-occluded and total sulfur were also statistically homogenous in the S. salsa marsh (P > 0.05). P. australis marsh exhibited similar trends with S. salsa marsh, as small changes in contents of water-soluble and adsorbed sulfur also appeared among the five locations in P. australis marsh and without significant difference, and the contents of carbonateoccluded and total sulfur compounds all seemed statistically homogenous (P > 0.05).

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3.3. Plant sulfur storage differences among the three vegetation-covered marshes S. alterniflora marsh produced the highest biomass among the three vegetation-covered marshes (Table 2). The underground biomass production of S. alterniflora was on average 104.8 or 3.9 times that of S. salsa or P. australis (P < 0.05), and the aboveground biomass of the exotic species was on average 5.8 or 1.6 times that of S. salsa or P. australis (P < 0.05). Underground tissue of S. alterniflora, including roots and rhizomes, contained the highest level of sulfur concentration (4.54 ± 0.33 mgS g−1 tissue) among the three species (P < 0.05), while the same tissues of the two native species contained similarly lower sulfur concentrations (P > 0.05). Sulfur concentration in aboveground tissue of S. alterniflora was a little lower than that in S. salsa (2.98 ± 0.44 vs. 3.54 ± 0.32 mgS g−1 tissue, P > 0.05), but was significantly higher than that in P. australis (1.57 ± 0.09 mgS g−1 tissue, P < 0.05). Plant sulfur storage (sulfur concentration timed biomass) of S. alterniflora vegetation was 19.3 or 4.9 times that of S. salsa or P. australis vegetation (P < 0.05). Limited in biomass production, the S. salsa marsh contained the lowest plant sulfur storage (P < 0.05).

3.4. Spatial variations of plant sulfur storage within the same marsh Plant sulfur storage among the five locations of S. alterniflora marsh was also heterogeneous (Fig. 4). With both outstanding sulfur concentration and high biomass production (Table 2, Fig. 4), the underground part of S. alterniflora dominated the trends of sulfur storage in plants, as locations S2 and S3 in the center of the marsh had significantly higher underground and total sulfur storage (25.91 ± 0.29 and 32.18 ± 0.99 gS m−2 for S2 , 24.96 ± 0.26 and 30.34 ± 0.95 gS m−2 for S3 ), followed by S1 (17.87 ± 0.55 and 26.36 ± 0.80 gS m−2 ) and S4 (20.70 ± 0.73 and 26.84 ± 2.26 gS m−2 ) (P < 0.05), with S5 (12.53 ± 0.68 and 17.23 ± 1.29 gS m−2 ) being the least (P < 0.05). Sulfur storage in aboveground parts of S. alterniflora in the seaside location S1 was a little higher than those in the other locations; however, significant difference was only found between S1 and S5 (8.49 ± 0.32 gS m−2 vs. 4.69 ± 0.71 gS m−2 ) (P < 0.05). Unlike S. alterniflora marsh, no significant differences in plant sulfur storage among the five locations within S. salsa marsh were found (Fig. 4). Containing lower sulfur concentration and limited underground biomass (Table 2), sulfur storage in underground part of the vegetation contributed little to the total storage. Fluctuations on sulfur storage in aboveground part of the vegetation existed among the five locations within S. salsa marsh; however, they did not lead to the significant changes in total plant sulfur storage (P > 0.05). P. australis vegetation was characteristic with a similar proportion of under- and aboveground biomass production, but sulfur concentration in underground tissue of P. australis was 82.5% more than that in aboveground tissue (P < 0.05, Table 2). So it was the underground part that presented the most plant sulfur storage of the vegetation (Fig. 4). Similar to S. alterniflora vegetation, locations S2 and S3 in the middle of P. australis marsh were relatively higher in underground and total sulfur storage (4.04 ± 0.44 and 6.26 ± 0.33 gS m−2 for S2 , 4.06 ± 0.64

Fig. 4 – Plant sulfur storage in S. alterniflora, S. salsa and P. australis marshes. Shown is mean ± S.E., n = 3.

and 6.72 ± 0.57 gS m−2 for S3 ), followed by S4 (3.32 ± 0.42 and 5.11 ± 0.66 gS m−2 ) and S5 (3.31 ± 0.52 and 5.14 ± 0.61 gS m−2 ), but with no significant difference (P > 0.05). Location S1 in the seaside edge contained the lowest underground and total sulfur storage (2.19 ± 0.19 and 3.96 ± 0.63 gS m−2 , P < 0.05). Sulfur storage in aboveground part of the vegetation was a little higher in the center location S3 , but with no significant difference among the five locations (P > 0.05).

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Table 2 – Plant sulfur storage in different vegetations Sulfur concentrations (mgS g−1 tissue)

S. alterniflora S. salsa P. australis

Biomass (g m−2 )

Underground tissue

Aboveground tissue

Underground tissue

Aboveground tissue

4.54 ± 0.33 a 2.52 ± 0.37 b 2.95 ± 0.17 b

2.98 ± 0.44 a 3.54 ± 0.32 a 1.57 ± 0.09 b

4497.0 ± 291.6 a 42.9 ± 3.9 b 1147.0 ± 86.1 c

2081.0 ± 175.5 a 359.5 ± 25.3 b 1265.3 ± 95.1 c

Sulfur storage (gS m−2 )

26.587 ± 1.472 a 1.381 ± 0.094 b 5.379 ± 0.354 c

Mean ± S.E., n = 15. Data marked by different letters indicated significantly different at the level of 0.05 tested by one-way ANOVAs.

3.5. Correlations between plant sulfur storage and sediment total sulfur storage Plant sulfur storage was found positively correlated with sediment total sulfur storage (r = 0.623, P < 0.001), when all 45 locations in the three marshes were compared. However, no significant correlations were found between the two storage components (above- and underground) within any of the marshes (r = 0.103, 0.281 and 0.082, respectively, for S. alterniflora, S. salsa or P. australis marsh).

4.

Discussion

The marsh dominated by exotic S. alterniflora in the study site contained significantly higher levels of sulfur than the three adjacent native marshes. The total sulfur in sediment of S. alterniflora marsh was 1.5 times that of bare mudflat and 1.4 times that of S. salsa or P. australis marsh. Meanwhile, sulfur storage in plant tissue of S. alterniflora vegetation was 19.3 or 4.9 times that of S. salsa or P. australis vegetation, compared within same vegetation area. Similar to what Tyler and Grosholz (2003) found, that S. alterniflora changed carbon and nitrogen cycling in the Pacific Estuaries, this study implies that S. alterniflora increases the levels of sulfur and changes the sulfur cycling in Chinese coastal marshes. Ways that S. alterniflora vegetation stimulates the precipitation of sulfur from seawater into marsh sediments have been proposed. After chloride, sulfate is the most abundant anion in seawater (Derry and Murray, 2004), so the seawater should be an important sulfur source for coastal marshes. It is agreed that stems and leaves of S. alterniflora may act as a buffering structure that decreases water current velocity, thereby increasing sedimentation rate (Netto and Lana, 1997; Bruno and Kennedy, 2000; Morris et al., 2002). The sedimentation function of S. alterniflora has been reported to be significant in our research area (Chung et al., 2004). We suggest that, while current velocity is decreased to certain level, sulfate may be either adsorbed and precipitated with metals like Ca in the sediment or just dissolved in sediment pore water. On the other hand, the sulfate, when entering the marsh, can be reduced in the anaerobic environment, and then react with Fe and Mn to form insoluble metal sulfides, including eventually pyrite. Only the sulfide is not considered in this research. Nevertheless, the grass may directly absorb sulfur from seawater as a complement of necessary nutrition. On the other hand, S. salsa dominates to the landward side of the S. alterniflora vegetation. Daily tides can only wet the marsh creeks, but seldom inundate the entire habitat. Being in

upper intertidal zone, P. australis has an even smaller chance of receiving sea tides. So we can suggest that compared with the S. alterniflora marsh, both the S. salsa marsh and the P. australis marshes have fewer opportunities to supplement sulfur from sea tides. The high biomass production of S. alterniflora also contributes to the sulfur storage in the marsh, as biomass production per unit area together with sulfur concentration in the tissue contributes to the highest plant sulfur storage in S. alterniflora marsh. The biomaterial, after degrading in the marsh, helps with the accumulation of organic matter in the sediment (Li et al., 2001; Zhou et al., 2005). Previous research in the Yancheng Nature Reserve proved that the S. alterniflora marsh contains much higher organic matter than the adjacent bare mudflat and S. salsa and P. australis marshes (Shen et al., 2003; Gao et al., 2005). ␦13 C analysis also indicates that most of the organic matter in the S. alternifora marsh comes from decomposition of Spartina plants (Gao et al., 2005). Sulfur in biomaterial is released eventually with the decomposition of organic matter. It may be transferred into the sediment, mineralized, and reused by the plants again (Shan et al., 1992; Itanna, 2005). The degradation of biomaterial temporarily decreases the sulfur storage in plant tissue. However, the organic sulfur and total sulfur in the sediment can be enhanced. The influence of plants on seasonal cycling of sulfur in wetlands has been described by Gauci et al. (2004). The case that high-content sulfur in the environment helps with the competition of S. alterniflora over other halophytes has been proved by both lab and field experiments (Stribling, 1997; Chambers et al., 1998; Seliskar et al., 2004). With much higher levels of sulfur compounds in S. alterniflora marsh being detected in coastal China compared to other marsh types, we can imagine that the condition is favorable for the expansion of S. alterniflora over native S. salsa and P. australis. Meanwhile, sulfur, together with carbon and nitrogen, is a key component of greenhouse gas. With the hypothesis of Charlson, Lovelock, Andreae and Warren (the CLAW hypothesis), changes in biogeochemistry of sulfur may influence the process of global warming (Andreae and Crutzen, 1997). With the results showing that S. alterniflora promoted sulfur storage in Chinese coastal marshes, the ecological effects of this species in areas where it is exotic should be reconsidered. Detailed research is still needed on this topic.

5.

Conclusion

It is a fact that the S. alterniflora marsh in coastal China contains significantly higher levels of sulfur compounds than the

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adjacent bare mudflat and native S. salsa marsh and P. australis marsh. The changes in biogeochemistry of the sulfur caused by the expansion of S. alterniflora, on the other hand, may inhibit the establishment of relatively sensitive species like S. salsa and P. australis, and thus facilitate the expansion of the monospecific S. alterniflora vegetation in the intertidal zone.

Acknowledgements This research was supported by the National Natural Science Foundation of China (30400054, 30770358), Jiangsu Natural Science Foundation (BK2007152), Open Research Foundation of the State Key Laboratory of Nuclear Resource and Environment in Donghua Science and Technology University (060602) and Nanjing University Talent Development Foundation. Great thanks go to Prof. Donald R. Strong from University of California who gave instructive suggestions and helped with the language of the manuscript and to Prof. William J. Mitsch from Ohio State University who also helped with the language of the manuscript. The authors thank Prof. Chung-Hsin Chung, Pei Qin and Rongzong Zhuo from Nanjing University for their long-term help with the study. The authors thank Xiao-Quan Shan from the Chinese Academy of Sciences for helping with ¨ the methods of sulfur analysis, Guoyong Sun, Shicheng Lu, Jinjin Du, Hui Wang and all the other members in Yancheng Nature Reserve for helping with field investigation and Liwen Qiu, Hongguang Zhu, Yuhong Liu, Jue Feng and Baohua Guan from Nanjing University for helping with field and lab experiments. The authors also thank Prof. Irv Mendelssohn from Louisiana State University and another anonymous reviewer for their help in improving the manuscript.

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