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A study on seed characteristics and seed bank of Spartina alterniflora at saltmarshes in the Yangtze Estuary, China
Estuarine, Coastal and Shelf Science 83 (2009) 105–110
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A study on seed characteristics and seed bank of Spartina alterniflora at saltmarshes in the Yangtze Estuary, China Derong Xiao a, Liquan Zhang a, b, *, Zhenchang Zhu a a b
State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, China Shanghai Key Laboratory of Urbanization and Ecological Restoration, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 5 January 2009 Accepted 19 March 2009 Available online 5 April 2009
Since Spartina alterniflora was introduced into the Chongming Dongtan Nature Reserve in 1995, there has been a rapid expansion of this species, seriously threatening the overall biodiversity. In this study, the seed production, germination characteristics and soil seed bank of S. aterniflora were studied at the nature reserve along an intertidal gradient where this invasive species distributed and spread. The results showed that the middle intertidal zone (MIT) had the largest seed production and higher viability than those of lower (LIT) and higher (HIT) intertidal zones. The differences in seed production among these sites were largely dependent on the higher percentage of fruiting culms, longer spike and higher seed number per spike. The differences in seed viability among these sampling sites seemed largely dependent on the higher seed weight at the site MIT. The chilling treatment (at low temperature and in moist conditions) could significantly enhance the germinability of S. alterniflora seeds and shorten the time of onset seed germination. The seeds from the site MIT had much higher germinability than the sites LIT and HIT. The highest density of soil seed bank was recorded at the site of MIT, where had the highest seed production. By July, before there was any replenishment with fresh seeds from the current year, the soil seed bank was completely exhausted and the persistent time of soil seed bank for S. alterniflora was less than 9 months, which is in agreement with that of the transient seed bank. The results from this study indicated that the seed propagation could have an important attribution to the spreading of this invasive plant and the implications in terms of controlling and managing the invasion of S. alterniflora at the nature reserve were discussed. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: Spartina alterniflora invasive species seed biology soil seed bank Chongming Dongtan wetland
1. Introduction Biological invasion has received considerable attention recently and is now recognized as one of the six most serious environmental problems which may influence future economical and social development (Gewin, 2005; Mooney et al., 2005). Spartina alterniflora (smooth cordgrass), native to the Atlantic and Gulf coasts of North American, is a perennial and deep-rooted salt marsh grass, which plays important ecological functions in its native ecosystems (Simenstad and Thom, 1995). With its great capacity of reducing tidal wave energy, mitigating erosion and trapping sediments, S. alterniflora had been widely introduced to many coastal and estuarine regions of the world as a species for ecological engineering (Callaway and Josselyn, 1992; Chung, 1993; Chung et al.,
* Corresponding author:Shanghai Key Laboratory of Urbanization and Ecological Restoration, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, China. E-mail address: [email protected] (L. Zhang). 0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.03.024
2004). This exotic species was introduced to the eastern coasts of China for the purpose of land reclamation in 1970s and 1980s (Chung, 1993, 2004; Zhang et al., 2004) and to the Yangtze Estuary in 1990s. Since then it has expanded rapidly and the mono-dominant community of S. alterniflora accounted for almost one fourth of the total intertidal saltmarsh vegetation in Shanghai region by 2005 (Li et al., 2006; Huang et al., 2007). Moreover, some reports suggested that this exotic species may out-compete native plants, threaten the native ecosystems and coastal aquaculture, and cause a decline in native species richness (Callaway and Josselyn, 1992; Daehler and Strong, 1994; Tian et al., 2008). Both the sexual reproduction by seeds and asexual propagation by tillering and rhizoming are the two main approaches by which Spartina aterniflora can keep fast rate of geographic spread (Daehler and Strong, 1994; Davis et al., 2004; Huang et al., 2008). The seeds of S. aterniflora could be dispersed long-distance by floating wracks at Willapa Bay, USA, germinate as new individuals at suitable habitats, form patches by asexual propagation, and finally merge into dense continuous meadows (Davis et al., 2004). Recruitment by seed has also been reported as the most important means for the
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fast rate of geographic spread of S. aterniflora at San Francisco Bay (Daehler and Strong, 1996; Daehler, 1999). Previous studies on the saltmarshes at the Yangtze Estuary reported that S. aterniflora had a great capability of asexual propagation (Zhang et al., 2006) and the range expansion rate was three to five times faster than that of native species Phragmites australis (Huang et al., 2008). However, the sexual reproduction and its role played on the spreading of S. aterniflora at the Yangtze Estuary were still unclear. In this study, the seed production, germination characteristics and seed bank of Spartina aterniflora were studied at the Chongming Dongtan Nature Reserve along an intertidal gradient where S. aterniflora distributed and spread. The objectives were: (1) to investigate the seed characteristics of S. alterniflora including seed production and viability, seed germination characteristics; (2) to detect the spatial-temporal dynamics of seed bank of S. alterniflora; and (3) to understand seed dispersal and its role played on the spreading of S. aterniflora at the Yangtze Estuary. The results of this study were intended to obtain useful insights into the population ecology as well as the control of this invasive plant at the nature reserve.
with 60% of rainfall occurring during May–September, and average humidity is 82% (Gao and Zhang, 2006). The total area of the nature reserve (to the east of the 1998 reclamation dyke) covers 24,600 ha, including 10,000 ha and 14,000 ha of tidal flats above and below the elevation of 0 m, respectively. Three distinct zones of salt marsh vegetation, related to elevation, can be identified, stretching from the 1998 inland dyke and moving eastwards towards the low tide (Huang et al., 2007). The tidal flats with an elevation of less than 2 m are characterized by mud flats without any vascular plants. The tidal flats between 2.0 m and 2.9 m elevation are dominated by a Scirpus mariqueter community, with some local areas dominated by Scirpus triqueter. Above 2.9 m, plant communities are dominated by Phragmites australis. An additional species is Spartina alterniflora, which was introduced to Dongtan in 1995. With its great capacity of reducing tidal wave energy, trapping sediment and mitigating erosion, S. alterniflora had been planted in the upper zone along the northern and eastern parts of the 1998 reclamation dyke. Over the last 10 years, the area of S. alterniflora increased to 1284 ha by 2005, amounted to more than one fourth of the total saltmarsh vegetation and formed a large area of mono-dominant community (Huang et al., 2007).
2. Materials and methods 2.2. Seed production and viability 2.1. Study area The Chongming Dongtan Nature Reserve, one of the largest nature reserves for migratory birds in East Asia, is located on Chongming Island at the mouth of the Yangtze River, between 31250 w31380 N, 121500 w122 050 E (Fig. 1). The Dongtan wetlands were listed in the Chinese Protected Wetlands (1992), and were designated as internationally important under the Ramsar Wetlands Convention (2001) and as a national nature reserve in 2005. The island has a northern sub-tropical monsoon climate, with an average annual temperature 15.3 C, summer temperatures average 26 C while winters are cold with an average temperature of 3 C. Average annual precipitation is approximately 1022 mm,
Four sampling sites were set along an intertidal gradient at the northern part of the nature reserve, stretching from the 1998 inland dyke and moving towards the low tide (Fig. 1). The site characters of at the bare mud flats (BMF), lower intertidal zone (LIT), middle intertidal zone (MIT) and higher intertidal zone (HIT) were recorded (Table 1). Counting of fruiting culms with seeded spikes and number of seeds per spike could give an estimation of seed production in the population as a whole. During November 2007, the total number of Spartina alterniflora culms and fruiting culms were recorded at each of the five 2 2 m plots set randomly at the sampling sites of LIT, MIT and HIT. The spike length and spikelets per spike were
Fig. 1. The location of Chongming Dongtan Nature Reserve as well as the sampling sites along an intertidal gradient.
D. Xiao et al. / Estuarine, Coastal and Shelf Science 83 (2009) 105–110 Table 1 Site characters of the sampling sites along an intertidal gradient at the Chongming Dongtan Nature Reserve. BMT ¼ bare mud flat, LIT ¼ lower intertidal zone, MIT ¼ middle intertidal zone and HIT ¼ higher intertidal zone. Site characters
Sampling sites BMF
LIT
MIT
HIT
Elevation (m) Culm density (no./m2) Vegetation height (cm) Soil pH
2.0–2.4 – – 6.72 0.01
2.4–2.9 211 21 192 7 6.68 0.18
2.9–3.5 228 25 197 8 6.82 0.02
3.5–3.9 223 42 175 5 7.00 0.08
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placed in trays. The trays were then kept in a climate chamber at a temperature of 25 C, 12 h light/dark and humidity of 75% to test the germinability. The germinated seeds were counted and removed whenever necessary until no seeds germinated for two continuous weeks. The soil seed bank samples collected from the field in April and July of 2008 were directly brought to test the germinability. The results were expressed as mean percentage of germinable seeds. 2.5. Data analysis
measured for five culms selected randomly from each plot. The spikes sampled were brought into the laboratory and air-dried. The seed number per spike was counted and the seeds were weighted. The seed production from each sampling sites was expressed as mean number of seeds/m2. A sample of 200 Spartina aterniflora seeds with five replicates freshly-collected during November 2007 from the LIT, MIT and HIT sampling sites were taken back to laboratory and tested for viability using the tetrazolium staining method (Leist and Kr amer, 2003; Jessie and Moore, 2008). The seed coats were removed, the embryos were then placed in 9 cm glass Petri dish on filter paper soaked in a 1% tetrazolium chloride solution and kept in the climate chamber at a temperature of 30 C for 24 h. The viability was examined under a dissecting scope. When more than 50% of the embryo was stained red, the embryo was accounted for the positive test (living) and otherwise the negative test (dead). 2.3. Germination tests in the laboratory The seeds collected during November 2007 from the sampling sites were taken to laboratory for chilling treatments. The capacity of the freshly-collected seeds of Spartina aterniflora for immediate germination was tested. A sample of 200 seeds with five replicates from each sampling site were placed in 9 cm glass Petri dishes on filter paper moistened with distilled water and kept in a climate chamber at a temperature of 25 C for 12 h light/20 C for 12 h dark and humidity of 75% until no seeds germinated for two continuous weeks. Another group of seeds were placed in a growth chamber at a temperature of 4 C, 12 h light/dark and kept moistened with distilled water. After 3 months (March of 2008) of chilling treatment, a sample of 200 seeds with five replicates from each sampling site were placed in 9 cm glass Petri dishes on filter paper moistened with distilled water and kept in a climate chamber at a temperature of 25 C for 12 h light/20 C for 12 h dark and humidity of 75%. The date of onset germination was recorded and the germinated seeds were counted and removed whenever necessary until no seeds germinated for two continuous weeks. The results were expressed as mean percentage of germinable seeds.
The data collected from field measurements and laboratory experiments were analyzed using one-way ANOVA to test for significant differences among the sampling sites as well as among different treatments. When necessary, the data were log(x þ 1) transformed to satisfy the assumption of homogeneous variances (Iva, 2008). The one-way ANOVA was implemented using SPSS13.0 and OriginLabÔ 7.5 packages. 3. Results 3.1. Seed production and viability The seed production and seed viability of Spartina alterniflora from the lower intertidal zone (LIT), middle intertidal zone (MIT) and higher intertidal zone (HIT) along an intertidal gradient at the Chongming Dongtan Nature Reserve are presented in Table 2. Although there were no significant differences in culm density of Spartina alterniflora among these sites, which were 211/m2, 228/ m2 and 223/m2 for the sites of LIT, MIT and HIT, respectively. The first remarkable point in these figures was the much higher seed production of S. alterniflora at the site MIT in 2007. The seed production at the site MIT amounted to 53,581/m2 and was significantly higher (P < 0.05) than 27,514/m2 at the site LIT and 31,300/m2 at the site HIT. The differences in seed production among these sites were largely dependent on the higher percentage of fruiting culms, longer spike and higher seed number per spike at the site MIT (Table 2). Another remarkable point in these figures was the much higher seed viability at the site MIT, which reached to 35.7% and was significantly higher (P < 0.05) than 4.2% at the site LIT and 6.7% at the site HIT. The seed weight/1000 seeds were 5.3 g, 3.3 g and 3.3 g for the sites MIT, LIT and HIT, respectively. The differences in seed viability among these sampling sites seemed largely dependent on the higher seed weight at the site MIT (R ¼ 0.99; P < 0.05) (Table 2). 3.2. Seed germination response to chilling The freshly-collected seeds of S. alterniflora during November 2007 had a lower germination percentage at the initial germination
2.4. Seasonal dynamics of soil seed bank The seasonal changes of seed population in the soil were assessed by collecting a series of soil samples from the sampling sites. Ten soil samples, each 25 25 cm and 6 cm in depth, were collected: (1) November of 2007; (2) April of 2008; and (3) July of 2008 at random points from each of the sampling sites, respectively. The seeds of Spartina aterniflora were large enough to be separated from the soil by hand-sorting and the size of soil seed bank was expressed as mean number of seeds/m2. The soil seed bank samples collected in November 2007 were brought to the laboratory and stored in a growth chamber at temperature of 4 C for chilling treatment. After 3 months of chilling treatment (March of 2008), the samples were taken out and
Table 2 The seed production and seed viability (mean SE) of Spartina aterniflora in 2007 from the sampling sites LIT, MIT and HIT along an intertidal gradient. The differences among the sampling sites were tested by one-way ANOVA and significant differences (d.f. ¼ 2, P < 0.05) were indicated by the different letters. Sexual production parameters Seed sampling sites LIT Fruiting culm (%) Mean spike length (cm) Seeds per spike (no) Seed production (no./m2) Seed weight (g/1000 seeds) Seed viability (%)
MIT
HIT
41 7 ab 52 6 a 40 3 b 25.7 0.5 a 37.4 2.6 b 29.9 1.2 c 351 24 a 609 81 b 451 71 c 27514 7795 a 53581 10033 b 31300 3577 a 3.3 0.2 a 5.3 0.3 b 3.3 0.3 a 4.2 0.3 a 35.7 1.8 b 6.7 0.3 c
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test at a temperature of 25 C for 12 h light/20 C for 12 h dark. The germination percentages were 0.1%, 3.2% and 0.5% for the seeds collected from the sites LIT, MIT and HIT, respectively (Fig. 2a). There was no any germination for the seeds kept in the growth chamber at a temperature of 4 C, 12 h light/dark and kept moistened with distilled water. After 3 months, theses seeds were transferred to a climate chamber at a temperature of 25 C for 12 h light/20 C for 12 h dark. The results showed that the chilling treatment (at low temperature and in moist conditions) could significantly increase the germinability of the Spartina alterniflora seeds (P < 0.05), which reached 0.7%, 9.9% and 1.2% for the sites of LIT, MIT and HIT, respectively (Fig. 2a). The much higher seed germinability at the site MIT seemed also largely dependent on the higher seed quality at the site MIT (R ¼ 0.99; P < 0.05). The chilling treatment had also a positive effect on the days of onset seed germination. The onset time for the initial germination test was 32 days, 25 days and 33 days for the seeds collected from the sites of LIT, MIT and HIT, while after chilling treatment 28 days, 22 days and 29 days, respectively (Fig. 2b). 3.3. Spatial-temporal dynamics of soil seed bank The seasonal changes of soil seed bank of Spartina alterniflora at the sites of bare mud flats (BMF), lower intertidal zone (LIT), middle
Fig. 2. Effect of chilling treatment on seed germination percentage (mean SE) of Spartina aterniflora for the seeds collected from the sampling sites LIT, MIT and HIT along an intertidal gradient. NC ¼ freshly-collected seeds without chilling treatment, C ¼ after 3 months chilling treatment. (a) Germination percentages; and (b) DOG ¼ days from start of experiment to the onset of germination. The differences between treatments were tested by one-way ANOVA and significant differences (d.f. ¼ 1, P < 0.05) were indicated by the different letters.
intertidal zone (MIT) and higher intertidal zone (HIT) along an intertidal gradient at the Chongming Dongtan Nature Reserve are presented in Fig. 3. Most seeds of Spartina alterniflora were released after ripening and the highest density of seeds in the soil were, therefore, recorded in the samples sampled in November 2007, which reached 0/ m2, 4127/m2, 10,716/m2 and 6260/m2 for the sites of BMF, LIT, MIT and HIT, respectively. Out of the seeds which had reached soil seed bank in November 2007, more than 98.5% of seeds were lost at the beginning of field germination. The amount of seeds subsequently decreased as a result of field germination, tidal movement or possible predation, fungal attack and decay. The seeds in soil seed bank in the samples collected from the sites of BMF, LIT, MIT and HIT were only 0/m2, 28/m2, 161/m2 and 63/m2 in April 2008 and 0/ m2, 0/m2, 11/m2 and 7/m2 in July 2008, respectively (Fig. 3a). It was noticeable that no soil seed bank was found at the bare mud flats for all seasons. The germinable percentages for the seeds in the soil seed bank for all the sites are presented in Fig. 3b. The highest germinable percentage of 13.0% was recorded for the seeds in soil seed bank collected in November 2007 from the site of MIT, subsequently decreased to 4.1% in April 2008 until no viable seeds were recorded in July 2008. The germinable percentages for the seeds in the soil seed bank for the sites of LIT and HIT were 1.6% and 1.2% in November 2007, 0.5% and 0.7% in April 2008 and both 0% in July 2008, respectively. The combined results presented above indicated that the highest density of soil seed bank was recorded at the site of MIT,
Fig. 3. The spatio-temporal dynamics of soil seed bank of Spartina aterniflora during 2007–2008 along an intertidal gradient at the Chongming Dongtan Nature Reserve. (a) Size of the soil seed bank; and (b) germinable percentage of the soil seed bank. The differences among the sampling sites were tested by one-way ANOVA and significant differences (d.f. ¼ 3, P < 0.05) were indicated by the different letters.
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where had the highest seed production. By July, before there was any replenishment with fresh seeds from the current year, the soil seed bank was completely exhausted and the persistent time of soil seed bank for Spartina alterniflora at the Chongming Dongtan Nature Reserve was less than 9 months. 4. Discussions 4.1. Seed biology of Spartina alterniflora The results from this study indicated that the variation in seed production and viability of Spartina alterniflora at the Chongming Dongtan Nature Reserve was strongly correlated with the intertidal gradient. The middle intertidal zone at an elevation of 2.9–3.5 m was the favorite habitat for S. alterniflora where it had the higher number and better quality of seeds. While the ebb and flow at the lower intertidal zone and the intense competition with other species such as Phragmites australis at the high intertidal zone could be responsible for the reduction in seed production and seed quality. The results from a study at Willapa Bay, western coast of USA indicated that the nucleus community of S. alterniflora at the middle intertidal zone had the higher number and better quality of seeds (Davis et al., 2004). Trnka and Zedler (2000) also showed a similar result that the seed production of S. alterniflora at saltmarshes in the East and Gulf Coasts was strongly correlated with the suitable habitats. Mature seeds of many species can germinate immediately after release from the parent plants, whilst others require a period of after ripening (Baskin et al., 2003). Our results of the laboratory experiment showed that the seeds of Spartina aterniflora could germinate immediately after ripe with a relative low percentage given optimum conditions. While chilling treatment could greatly enhance the percentage and speed of seed germination. The seeds after released from the parent plants and entered into the soil seed bank in the field could be under an innate or enforced dormancy due to low temperature during the winter. As soon as the soil surface temperature reached above 10 C in March, many of the seeds began to germinate. The combination of these dormancy mechanisms of S. aterniflora and the field conditions is of great importance in causing a spring flush of germination in the field, thus preventing premature germination in winter (Greenwood and DuBowy, 2005). 4.2. Soil seed bank of Spartina alterniflora Seed bank formation plays an important role in plant population dynamics (Wagner and Mitschunas, 2008), which can be used to predict the initial composition of post-recruitment vegetation and yield information on the species composition of previous and new vegetation (Onaindia and Amezaga, 2000). The big discrepancy between the seed production and the soil seed bank (Table 2 and Fig. 3) suggested that numerous agents could profoundly affect the number of seeds that could reach the soil. Once the seeds had entered the soil seed bank, ebb and flow, predation and pathogens might become important in reducing the seed population as the relatively large seeds of Spartina alterniflora on the soil could be subject to a high rate of these agents. On the other hand, the fact that no seed bank was found at the bare mud flat suggested that the possibility of seeds movement by ebb and flow could be little, which was consistent with the phenomenon at Willapa Bay, USA (Davis et al., 2004). Rand (2000) also reported that the spatial distribution of seeds across saltmarshes strongly paralleled the patterns of adult plant abundance across the marsh. The physical mechanisms that reduced hydrological flow and increased sedimentation within saltmarshes could likely increase seed deposition
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and retention (Goodson et al., 2003; Lambrinos and Bando, 2008). However, further study is needed to verify these assumptions at the Chongming Dongtan Nature Reserve. Thompson and Grime (1979) have discussed the distinction between a transient seed bank and a persistent seed bank. A transient seed bank is defined as one without any accumulation of seeds produced in different years and the seed bank is replaced annually, while a persistent seed bank as one with an accumulation of seeds produced in different years and some component seeds can keep their viable state for more than 1 year. The characteristics of seed bank and seed germination behavior of Spartina alterniflora at the Chongming Dongtan Nature Reserve had a pattern of innate and enforced dormancy in winter, followed by a flush germination in spring and thereafter complete exhaustion before there was any replenishment with fresh seeds from the current year. This is in agreement with that of the transient seed bank described by Thompson and Grime (1979). 4.3. Implications for invasion capacity and its management Studies on seed biology and seed bank of invasive species may provide opportunities to better understand aspects of plant population dynamics and are crucial for applications in restoration ecology (Daehler and Strong, 1994). Spartina alterniflora is a clonal and perennial salt marsh grass and both the sexual reproduction by seeds and asexual propagation by tillers and rhizomes are the two major means to keep a fast rate of geographic spread. Spartina alterniflora can produce a large amount of seeds, even if a low fraction of these seeds is viable, and it is likely that some of them could deposited in suitable locations and invade into new regions (Davis et al., 2004; Zhang et al., 2004; Jessie and Moore, 2008). Recruitment by seed had been reported as an important means for invasion of S. alterniflora across the open mudflats in San Francisco Bay (Daehler and Strong, 1996; Daehler, 1999). It had also been showed that each recruit germinated from a single seed could grow clonally into a circular patch and finally merge to form dense continuous meadows on previously bare intertidal mudflats in Willapa Bay (Davis et al., 2004). Further work is needed to understand how the seed production and seedbank patterns reported in this study can be related to seedling recruitment patterns in the nature reserve, as these patterns will ultimately translate into seedling recruitment pattern which is critical to understanding the spread dynamics (Lambrinos and Bando, 2008). To control and eradicate the invasive plant Spartina alterniflora at the Chongming Dongtan Nature Reserve is important and necessary for biodiversity conservation. The results from this study on seed biology and seed bank of this invasive species could provide valuable insights on which strategic control efforts can be designed and applied. The physical or mechanical measures such as cutting, burning, pruning, excavating and waterlogging have been suggested and tested to control S. alterniflora at the nature reserve (Li and Zhang, 2008; Yuan et al., 2008). The most successful and fast measure to eradicate S. alterniflora at a demonstration site in the nature reserve has been proved by adopting an integrated technique of cutting at the florescent period (July) combined thereafter with waterlogging for about 3 months. Based on the evidence drawn from this study, this integrated technique of control could effectively prevent S. alterniflora from seed setting and forming a soil seed bank in the current year, thus minimizing the risk of reinvasion as it has a transient seed bank. Acknowledgements The authors would like to thank members of the Ecological Section of the State Key Laboratory of Estuarine and Coastal
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Research, East China Normal University, for their assistance with the collection of field data. The editor and two anonymous reviewers provided valuable comments and suggestions on an earlier draft of this paper were also appreciated. The research was funded by the National Key Fundamental Research and Development Program (2008DFB90240 and 2006BAC01A14) and Project 908-ZC-II-03. References Baskin, C.C., Baskin, J.M., Chester, E.W., 2003. Ecological aspects of seed dormancybreak and germination in Heteranthera limosa (Pontederiaceae), a summer annual weed of rice fields. Weed Research 43, 103–107. Callaway, J.C., Josselyn, M.N., 1992. The introduction and spread of smooth cordgrass (Spartina alterniflora) in South San Francisco Bay. Estuaries 15, 218–226. Chung, C.H., 1993. Thirty years of ecological engineering with Spartina plantations in China. Ecological Engineering 2, 261–289. Chung, C.H., Zhuo, R.Z., Xu, G.W., 2004. Creation of Spartina plantations for reclaiming Dongtai, China, tidal flats and offshore sands. Ecological Engineering 23, 135–150. Daehler, C.C., 1999. Inbreeding depressing in smooth cordgrass (Spartina aterniflora, Poaceae) invading San Francisco Bay. American Journal of Botany 86, 131–139. Daehler, C.C., Strong, D.R., 1994. Variable reproductive output among clones of Spartina alterniflora (Poaceae) invading San Francisco Bay, California: the influence of herbivory, pollination, and establishment site. American Journal of Botany 81, 307–313. Daehler, C.C., Strong, D.R., 1996. Status, prediction and prevention of introduced cordgrass Spartina spp. Invasions in Pacific estuaries, USA. Biological Conservation 78, 51–58. Davis, H.G., Taylor, C.M., Civille, J.C., 2004. An Allee effect at the front of a plant invasion: Spartina in a Pacific estuary. Journal of Ecology 92, 321–327. Gao, Z.G., Zhang, L.Q., 2006. Multi-seasonal spectral characteristics analysis of coastal salt marsh vegetation in Shanghai. China. Estuarine. Coastal and Shelf Science 69, 217–224. Gewin, V., 2005. Industry lured by the gains of going green. Nature 436, 173. Goodson, J.M., Gurnell, A.M., Angold, P.G., Morrissey, I.P., 2003. Evidence for hydrochory and the deposition of viable seeds within winter flow-deposited sediments: the River Dove, Derbyshire, UK. River Research and Application 19, 317–334. Greenwood, M.E., DuBowy, P.J., 2005. Germination characteristics of Zannichellia palustris from New South Wales, Australia. Aquatic Botany 82, 1–11. Huang, H.M., Zhang, L.Q., Yuan, L., 2007. The spatio-temporal dynamics of salt marsh vegetation for Chongming Dongtan National Nature Reserve, Shanghai. Acta Ecologica Sinica 27, 4166–4172 (in Chinese with English Abstract). Huang, H.M., Zhang, L.Q., Guan Y.J., Wang D.H., 2008. A cellular automata model for population expansion of Spartina alterniflora at Jiuduansha Shoals, Shanghai, China. Estuarine, Coastal and Shelf Science 77, 47-55.
Iva, W., 2008. Seasonal and spatial variance of seed bank species composition in an oligotrophic wet meadow. Flora 203, 204–214. Jessie, J.C., Moore, K.A., 2008. Influence of environmental factors on Vallisneria americana seed germination. Aquatic Botany 88, 283–294. Lambrinos, J.G., Bando, K.J., 2008. Habitat modification inhibits conspecific seedling recruitment in populations of an invasive ecosystem engineer. Biological Invasions 10, 729–741. mer, S., 2003. ISTA Working Sheets on Tetrazolium Testing, vol. I: Leist, N., Kra Agricultural, Vegetable and Horticultural Species. International Seed Testing Association. Li, H.P., Zhang, L.Q., 2008. An experimental study on physical controls of an exotic plant Spartina alterniflora in Shanghai, China. Ecological Engineering 32, 11–21. Li, H.P., Zhang, L.Q., Wang, D.H., 2006. Distribution of an exotic plant Spartina alterniflora in Shanghai. Biodiversity Science 14, 114–120 (in Chinese with English Abstract). Mooney, H., Cropper, A., Reid, A., 2005. Confronting the human dilemma. Nature 434, 561–562. Onaindia, M., Amezaga, I., 2000. Seasonal variation in the seed banks of native woodland and coniferous plantations in Northern Spain. Forest Ecology and Management 126, 163–172. Rand, T.A., 2000. Seed dispersal, habitat suitability, and the distribution of halophytes across a salt marsh tidal gradient. Journal of Ecology 88, 608–621. Simenstad, C.A., Thom, R.M., 1995. Spartina alterniflora (smooth cordgrass) as an invasive halophyte in Pacific Northwest estuaries. Hortus Northwest. A Pacific Northwest Native Plant Directory and Journal 6, 9–13. Thompson, K., Grime, J.P., 1979. Seasonal variation in the seed banks of herbaceous species in ten contrasting habitats. Journal of Ecology 67, 893–921. Tian, B., Zhou, Y.X., Zhang, L.Q., Yuan, L., 2008. Analyzing the habitat suitability for migratory birds at the Chongming Dongtan Nature Reserve in Shanghai, China. Estuarine. Coastal and Shelf Science 80, 296–302. Trnka, S., Zedler, J.B., 2000. Site conditions, not parental phenotype, determine the height of Spartina foliosa. Estuaries 23, 572–582. Wagner, M., Mitschunas, N., 2008. Fungal effects on seed bank persistence and potential applications in weed biocontrol: a review. Basic and Applied Ecology 9, 191–203. Yuan, L., Zhang, L.Q., Xiao, D.R., Zhang, J., Wang, R.Z., Yang, L.Q., Gu, Z.Q., Chen, X., Zhou, X.X., Ping, Y., Zhu, Z.C., 2008. A demonstration study using the integrated technique of cutting plus waterlogging for the control of Spartina alterniflora. Acta Ecologica Sinica 28, 5723–5730 (in Chinese with English Abstract). Zhang, R.S., Shen, Y.M., Lu, L.Y., Yan, S.G., Wang, Y.H., Li, J.L., Zhang, Z.L., 2004. Formation of Spartina alterniflora salt marshes on the coast of Jiangsu Province, China. Ecological Engineering 23, 95–105. Zhang, D., Yang, M.M., Li, J.X., Chen, X.Y., 2006. Vegetative dispersal ability of Spartina alterniflora in eastern end of Chongming Island. Journal of East China Normal University (Natural Science) 2, 130–135 (in Chinese with English Abstract).
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A study on seed characteristics and seed bank of Spartina alterniflora at saltmarshes in the Yangtze Estuary, China Derong Xiao a, Liquan Zhang a, b, *, Zhenchang Zhu a a b
State Key Laboratory of Estuarine and Coastal Research, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, China Shanghai Key Laboratory of Urbanization and Ecological Restoration, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 5 January 2009 Accepted 19 March 2009 Available online 5 April 2009
Since Spartina alterniflora was introduced into the Chongming Dongtan Nature Reserve in 1995, there has been a rapid expansion of this species, seriously threatening the overall biodiversity. In this study, the seed production, germination characteristics and soil seed bank of S. aterniflora were studied at the nature reserve along an intertidal gradient where this invasive species distributed and spread. The results showed that the middle intertidal zone (MIT) had the largest seed production and higher viability than those of lower (LIT) and higher (HIT) intertidal zones. The differences in seed production among these sites were largely dependent on the higher percentage of fruiting culms, longer spike and higher seed number per spike. The differences in seed viability among these sampling sites seemed largely dependent on the higher seed weight at the site MIT. The chilling treatment (at low temperature and in moist conditions) could significantly enhance the germinability of S. alterniflora seeds and shorten the time of onset seed germination. The seeds from the site MIT had much higher germinability than the sites LIT and HIT. The highest density of soil seed bank was recorded at the site of MIT, where had the highest seed production. By July, before there was any replenishment with fresh seeds from the current year, the soil seed bank was completely exhausted and the persistent time of soil seed bank for S. alterniflora was less than 9 months, which is in agreement with that of the transient seed bank. The results from this study indicated that the seed propagation could have an important attribution to the spreading of this invasive plant and the implications in terms of controlling and managing the invasion of S. alterniflora at the nature reserve were discussed. Ó 2009 Elsevier Ltd. All rights reserved.
Keywords: Spartina alterniflora invasive species seed biology soil seed bank Chongming Dongtan wetland
1. Introduction Biological invasion has received considerable attention recently and is now recognized as one of the six most serious environmental problems which may influence future economical and social development (Gewin, 2005; Mooney et al., 2005). Spartina alterniflora (smooth cordgrass), native to the Atlantic and Gulf coasts of North American, is a perennial and deep-rooted salt marsh grass, which plays important ecological functions in its native ecosystems (Simenstad and Thom, 1995). With its great capacity of reducing tidal wave energy, mitigating erosion and trapping sediments, S. alterniflora had been widely introduced to many coastal and estuarine regions of the world as a species for ecological engineering (Callaway and Josselyn, 1992; Chung, 1993; Chung et al.,
* Corresponding author:Shanghai Key Laboratory of Urbanization and Ecological Restoration, East China Normal University, 3663 Zhongshan Road North, Shanghai 200062, China. E-mail address: [email protected] (L. Zhang). 0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.03.024
2004). This exotic species was introduced to the eastern coasts of China for the purpose of land reclamation in 1970s and 1980s (Chung, 1993, 2004; Zhang et al., 2004) and to the Yangtze Estuary in 1990s. Since then it has expanded rapidly and the mono-dominant community of S. alterniflora accounted for almost one fourth of the total intertidal saltmarsh vegetation in Shanghai region by 2005 (Li et al., 2006; Huang et al., 2007). Moreover, some reports suggested that this exotic species may out-compete native plants, threaten the native ecosystems and coastal aquaculture, and cause a decline in native species richness (Callaway and Josselyn, 1992; Daehler and Strong, 1994; Tian et al., 2008). Both the sexual reproduction by seeds and asexual propagation by tillering and rhizoming are the two main approaches by which Spartina aterniflora can keep fast rate of geographic spread (Daehler and Strong, 1994; Davis et al., 2004; Huang et al., 2008). The seeds of S. aterniflora could be dispersed long-distance by floating wracks at Willapa Bay, USA, germinate as new individuals at suitable habitats, form patches by asexual propagation, and finally merge into dense continuous meadows (Davis et al., 2004). Recruitment by seed has also been reported as the most important means for the
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fast rate of geographic spread of S. aterniflora at San Francisco Bay (Daehler and Strong, 1996; Daehler, 1999). Previous studies on the saltmarshes at the Yangtze Estuary reported that S. aterniflora had a great capability of asexual propagation (Zhang et al., 2006) and the range expansion rate was three to five times faster than that of native species Phragmites australis (Huang et al., 2008). However, the sexual reproduction and its role played on the spreading of S. aterniflora at the Yangtze Estuary were still unclear. In this study, the seed production, germination characteristics and seed bank of Spartina aterniflora were studied at the Chongming Dongtan Nature Reserve along an intertidal gradient where S. aterniflora distributed and spread. The objectives were: (1) to investigate the seed characteristics of S. alterniflora including seed production and viability, seed germination characteristics; (2) to detect the spatial-temporal dynamics of seed bank of S. alterniflora; and (3) to understand seed dispersal and its role played on the spreading of S. aterniflora at the Yangtze Estuary. The results of this study were intended to obtain useful insights into the population ecology as well as the control of this invasive plant at the nature reserve.
with 60% of rainfall occurring during May–September, and average humidity is 82% (Gao and Zhang, 2006). The total area of the nature reserve (to the east of the 1998 reclamation dyke) covers 24,600 ha, including 10,000 ha and 14,000 ha of tidal flats above and below the elevation of 0 m, respectively. Three distinct zones of salt marsh vegetation, related to elevation, can be identified, stretching from the 1998 inland dyke and moving eastwards towards the low tide (Huang et al., 2007). The tidal flats with an elevation of less than 2 m are characterized by mud flats without any vascular plants. The tidal flats between 2.0 m and 2.9 m elevation are dominated by a Scirpus mariqueter community, with some local areas dominated by Scirpus triqueter. Above 2.9 m, plant communities are dominated by Phragmites australis. An additional species is Spartina alterniflora, which was introduced to Dongtan in 1995. With its great capacity of reducing tidal wave energy, trapping sediment and mitigating erosion, S. alterniflora had been planted in the upper zone along the northern and eastern parts of the 1998 reclamation dyke. Over the last 10 years, the area of S. alterniflora increased to 1284 ha by 2005, amounted to more than one fourth of the total saltmarsh vegetation and formed a large area of mono-dominant community (Huang et al., 2007).
2. Materials and methods 2.2. Seed production and viability 2.1. Study area The Chongming Dongtan Nature Reserve, one of the largest nature reserves for migratory birds in East Asia, is located on Chongming Island at the mouth of the Yangtze River, between 31250 w31380 N, 121500 w122 050 E (Fig. 1). The Dongtan wetlands were listed in the Chinese Protected Wetlands (1992), and were designated as internationally important under the Ramsar Wetlands Convention (2001) and as a national nature reserve in 2005. The island has a northern sub-tropical monsoon climate, with an average annual temperature 15.3 C, summer temperatures average 26 C while winters are cold with an average temperature of 3 C. Average annual precipitation is approximately 1022 mm,
Four sampling sites were set along an intertidal gradient at the northern part of the nature reserve, stretching from the 1998 inland dyke and moving towards the low tide (Fig. 1). The site characters of at the bare mud flats (BMF), lower intertidal zone (LIT), middle intertidal zone (MIT) and higher intertidal zone (HIT) were recorded (Table 1). Counting of fruiting culms with seeded spikes and number of seeds per spike could give an estimation of seed production in the population as a whole. During November 2007, the total number of Spartina alterniflora culms and fruiting culms were recorded at each of the five 2 2 m plots set randomly at the sampling sites of LIT, MIT and HIT. The spike length and spikelets per spike were
Fig. 1. The location of Chongming Dongtan Nature Reserve as well as the sampling sites along an intertidal gradient.
D. Xiao et al. / Estuarine, Coastal and Shelf Science 83 (2009) 105–110 Table 1 Site characters of the sampling sites along an intertidal gradient at the Chongming Dongtan Nature Reserve. BMT ¼ bare mud flat, LIT ¼ lower intertidal zone, MIT ¼ middle intertidal zone and HIT ¼ higher intertidal zone. Site characters
Sampling sites BMF
LIT
MIT
HIT
Elevation (m) Culm density (no./m2) Vegetation height (cm) Soil pH
2.0–2.4 – – 6.72 0.01
2.4–2.9 211 21 192 7 6.68 0.18
2.9–3.5 228 25 197 8 6.82 0.02
3.5–3.9 223 42 175 5 7.00 0.08
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placed in trays. The trays were then kept in a climate chamber at a temperature of 25 C, 12 h light/dark and humidity of 75% to test the germinability. The germinated seeds were counted and removed whenever necessary until no seeds germinated for two continuous weeks. The soil seed bank samples collected from the field in April and July of 2008 were directly brought to test the germinability. The results were expressed as mean percentage of germinable seeds. 2.5. Data analysis
measured for five culms selected randomly from each plot. The spikes sampled were brought into the laboratory and air-dried. The seed number per spike was counted and the seeds were weighted. The seed production from each sampling sites was expressed as mean number of seeds/m2. A sample of 200 Spartina aterniflora seeds with five replicates freshly-collected during November 2007 from the LIT, MIT and HIT sampling sites were taken back to laboratory and tested for viability using the tetrazolium staining method (Leist and Kr amer, 2003; Jessie and Moore, 2008). The seed coats were removed, the embryos were then placed in 9 cm glass Petri dish on filter paper soaked in a 1% tetrazolium chloride solution and kept in the climate chamber at a temperature of 30 C for 24 h. The viability was examined under a dissecting scope. When more than 50% of the embryo was stained red, the embryo was accounted for the positive test (living) and otherwise the negative test (dead). 2.3. Germination tests in the laboratory The seeds collected during November 2007 from the sampling sites were taken to laboratory for chilling treatments. The capacity of the freshly-collected seeds of Spartina aterniflora for immediate germination was tested. A sample of 200 seeds with five replicates from each sampling site were placed in 9 cm glass Petri dishes on filter paper moistened with distilled water and kept in a climate chamber at a temperature of 25 C for 12 h light/20 C for 12 h dark and humidity of 75% until no seeds germinated for two continuous weeks. Another group of seeds were placed in a growth chamber at a temperature of 4 C, 12 h light/dark and kept moistened with distilled water. After 3 months (March of 2008) of chilling treatment, a sample of 200 seeds with five replicates from each sampling site were placed in 9 cm glass Petri dishes on filter paper moistened with distilled water and kept in a climate chamber at a temperature of 25 C for 12 h light/20 C for 12 h dark and humidity of 75%. The date of onset germination was recorded and the germinated seeds were counted and removed whenever necessary until no seeds germinated for two continuous weeks. The results were expressed as mean percentage of germinable seeds.
The data collected from field measurements and laboratory experiments were analyzed using one-way ANOVA to test for significant differences among the sampling sites as well as among different treatments. When necessary, the data were log(x þ 1) transformed to satisfy the assumption of homogeneous variances (Iva, 2008). The one-way ANOVA was implemented using SPSS13.0 and OriginLabÔ 7.5 packages. 3. Results 3.1. Seed production and viability The seed production and seed viability of Spartina alterniflora from the lower intertidal zone (LIT), middle intertidal zone (MIT) and higher intertidal zone (HIT) along an intertidal gradient at the Chongming Dongtan Nature Reserve are presented in Table 2. Although there were no significant differences in culm density of Spartina alterniflora among these sites, which were 211/m2, 228/ m2 and 223/m2 for the sites of LIT, MIT and HIT, respectively. The first remarkable point in these figures was the much higher seed production of S. alterniflora at the site MIT in 2007. The seed production at the site MIT amounted to 53,581/m2 and was significantly higher (P < 0.05) than 27,514/m2 at the site LIT and 31,300/m2 at the site HIT. The differences in seed production among these sites were largely dependent on the higher percentage of fruiting culms, longer spike and higher seed number per spike at the site MIT (Table 2). Another remarkable point in these figures was the much higher seed viability at the site MIT, which reached to 35.7% and was significantly higher (P < 0.05) than 4.2% at the site LIT and 6.7% at the site HIT. The seed weight/1000 seeds were 5.3 g, 3.3 g and 3.3 g for the sites MIT, LIT and HIT, respectively. The differences in seed viability among these sampling sites seemed largely dependent on the higher seed weight at the site MIT (R ¼ 0.99; P < 0.05) (Table 2). 3.2. Seed germination response to chilling The freshly-collected seeds of S. alterniflora during November 2007 had a lower germination percentage at the initial germination
2.4. Seasonal dynamics of soil seed bank The seasonal changes of seed population in the soil were assessed by collecting a series of soil samples from the sampling sites. Ten soil samples, each 25 25 cm and 6 cm in depth, were collected: (1) November of 2007; (2) April of 2008; and (3) July of 2008 at random points from each of the sampling sites, respectively. The seeds of Spartina aterniflora were large enough to be separated from the soil by hand-sorting and the size of soil seed bank was expressed as mean number of seeds/m2. The soil seed bank samples collected in November 2007 were brought to the laboratory and stored in a growth chamber at temperature of 4 C for chilling treatment. After 3 months of chilling treatment (March of 2008), the samples were taken out and
Table 2 The seed production and seed viability (mean SE) of Spartina aterniflora in 2007 from the sampling sites LIT, MIT and HIT along an intertidal gradient. The differences among the sampling sites were tested by one-way ANOVA and significant differences (d.f. ¼ 2, P < 0.05) were indicated by the different letters. Sexual production parameters Seed sampling sites LIT Fruiting culm (%) Mean spike length (cm) Seeds per spike (no) Seed production (no./m2) Seed weight (g/1000 seeds) Seed viability (%)
MIT
HIT
41 7 ab 52 6 a 40 3 b 25.7 0.5 a 37.4 2.6 b 29.9 1.2 c 351 24 a 609 81 b 451 71 c 27514 7795 a 53581 10033 b 31300 3577 a 3.3 0.2 a 5.3 0.3 b 3.3 0.3 a 4.2 0.3 a 35.7 1.8 b 6.7 0.3 c
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test at a temperature of 25 C for 12 h light/20 C for 12 h dark. The germination percentages were 0.1%, 3.2% and 0.5% for the seeds collected from the sites LIT, MIT and HIT, respectively (Fig. 2a). There was no any germination for the seeds kept in the growth chamber at a temperature of 4 C, 12 h light/dark and kept moistened with distilled water. After 3 months, theses seeds were transferred to a climate chamber at a temperature of 25 C for 12 h light/20 C for 12 h dark. The results showed that the chilling treatment (at low temperature and in moist conditions) could significantly increase the germinability of the Spartina alterniflora seeds (P < 0.05), which reached 0.7%, 9.9% and 1.2% for the sites of LIT, MIT and HIT, respectively (Fig. 2a). The much higher seed germinability at the site MIT seemed also largely dependent on the higher seed quality at the site MIT (R ¼ 0.99; P < 0.05). The chilling treatment had also a positive effect on the days of onset seed germination. The onset time for the initial germination test was 32 days, 25 days and 33 days for the seeds collected from the sites of LIT, MIT and HIT, while after chilling treatment 28 days, 22 days and 29 days, respectively (Fig. 2b). 3.3. Spatial-temporal dynamics of soil seed bank The seasonal changes of soil seed bank of Spartina alterniflora at the sites of bare mud flats (BMF), lower intertidal zone (LIT), middle
Fig. 2. Effect of chilling treatment on seed germination percentage (mean SE) of Spartina aterniflora for the seeds collected from the sampling sites LIT, MIT and HIT along an intertidal gradient. NC ¼ freshly-collected seeds without chilling treatment, C ¼ after 3 months chilling treatment. (a) Germination percentages; and (b) DOG ¼ days from start of experiment to the onset of germination. The differences between treatments were tested by one-way ANOVA and significant differences (d.f. ¼ 1, P < 0.05) were indicated by the different letters.
intertidal zone (MIT) and higher intertidal zone (HIT) along an intertidal gradient at the Chongming Dongtan Nature Reserve are presented in Fig. 3. Most seeds of Spartina alterniflora were released after ripening and the highest density of seeds in the soil were, therefore, recorded in the samples sampled in November 2007, which reached 0/ m2, 4127/m2, 10,716/m2 and 6260/m2 for the sites of BMF, LIT, MIT and HIT, respectively. Out of the seeds which had reached soil seed bank in November 2007, more than 98.5% of seeds were lost at the beginning of field germination. The amount of seeds subsequently decreased as a result of field germination, tidal movement or possible predation, fungal attack and decay. The seeds in soil seed bank in the samples collected from the sites of BMF, LIT, MIT and HIT were only 0/m2, 28/m2, 161/m2 and 63/m2 in April 2008 and 0/ m2, 0/m2, 11/m2 and 7/m2 in July 2008, respectively (Fig. 3a). It was noticeable that no soil seed bank was found at the bare mud flats for all seasons. The germinable percentages for the seeds in the soil seed bank for all the sites are presented in Fig. 3b. The highest germinable percentage of 13.0% was recorded for the seeds in soil seed bank collected in November 2007 from the site of MIT, subsequently decreased to 4.1% in April 2008 until no viable seeds were recorded in July 2008. The germinable percentages for the seeds in the soil seed bank for the sites of LIT and HIT were 1.6% and 1.2% in November 2007, 0.5% and 0.7% in April 2008 and both 0% in July 2008, respectively. The combined results presented above indicated that the highest density of soil seed bank was recorded at the site of MIT,
Fig. 3. The spatio-temporal dynamics of soil seed bank of Spartina aterniflora during 2007–2008 along an intertidal gradient at the Chongming Dongtan Nature Reserve. (a) Size of the soil seed bank; and (b) germinable percentage of the soil seed bank. The differences among the sampling sites were tested by one-way ANOVA and significant differences (d.f. ¼ 3, P < 0.05) were indicated by the different letters.
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where had the highest seed production. By July, before there was any replenishment with fresh seeds from the current year, the soil seed bank was completely exhausted and the persistent time of soil seed bank for Spartina alterniflora at the Chongming Dongtan Nature Reserve was less than 9 months. 4. Discussions 4.1. Seed biology of Spartina alterniflora The results from this study indicated that the variation in seed production and viability of Spartina alterniflora at the Chongming Dongtan Nature Reserve was strongly correlated with the intertidal gradient. The middle intertidal zone at an elevation of 2.9–3.5 m was the favorite habitat for S. alterniflora where it had the higher number and better quality of seeds. While the ebb and flow at the lower intertidal zone and the intense competition with other species such as Phragmites australis at the high intertidal zone could be responsible for the reduction in seed production and seed quality. The results from a study at Willapa Bay, western coast of USA indicated that the nucleus community of S. alterniflora at the middle intertidal zone had the higher number and better quality of seeds (Davis et al., 2004). Trnka and Zedler (2000) also showed a similar result that the seed production of S. alterniflora at saltmarshes in the East and Gulf Coasts was strongly correlated with the suitable habitats. Mature seeds of many species can germinate immediately after release from the parent plants, whilst others require a period of after ripening (Baskin et al., 2003). Our results of the laboratory experiment showed that the seeds of Spartina aterniflora could germinate immediately after ripe with a relative low percentage given optimum conditions. While chilling treatment could greatly enhance the percentage and speed of seed germination. The seeds after released from the parent plants and entered into the soil seed bank in the field could be under an innate or enforced dormancy due to low temperature during the winter. As soon as the soil surface temperature reached above 10 C in March, many of the seeds began to germinate. The combination of these dormancy mechanisms of S. aterniflora and the field conditions is of great importance in causing a spring flush of germination in the field, thus preventing premature germination in winter (Greenwood and DuBowy, 2005). 4.2. Soil seed bank of Spartina alterniflora Seed bank formation plays an important role in plant population dynamics (Wagner and Mitschunas, 2008), which can be used to predict the initial composition of post-recruitment vegetation and yield information on the species composition of previous and new vegetation (Onaindia and Amezaga, 2000). The big discrepancy between the seed production and the soil seed bank (Table 2 and Fig. 3) suggested that numerous agents could profoundly affect the number of seeds that could reach the soil. Once the seeds had entered the soil seed bank, ebb and flow, predation and pathogens might become important in reducing the seed population as the relatively large seeds of Spartina alterniflora on the soil could be subject to a high rate of these agents. On the other hand, the fact that no seed bank was found at the bare mud flat suggested that the possibility of seeds movement by ebb and flow could be little, which was consistent with the phenomenon at Willapa Bay, USA (Davis et al., 2004). Rand (2000) also reported that the spatial distribution of seeds across saltmarshes strongly paralleled the patterns of adult plant abundance across the marsh. The physical mechanisms that reduced hydrological flow and increased sedimentation within saltmarshes could likely increase seed deposition
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and retention (Goodson et al., 2003; Lambrinos and Bando, 2008). However, further study is needed to verify these assumptions at the Chongming Dongtan Nature Reserve. Thompson and Grime (1979) have discussed the distinction between a transient seed bank and a persistent seed bank. A transient seed bank is defined as one without any accumulation of seeds produced in different years and the seed bank is replaced annually, while a persistent seed bank as one with an accumulation of seeds produced in different years and some component seeds can keep their viable state for more than 1 year. The characteristics of seed bank and seed germination behavior of Spartina alterniflora at the Chongming Dongtan Nature Reserve had a pattern of innate and enforced dormancy in winter, followed by a flush germination in spring and thereafter complete exhaustion before there was any replenishment with fresh seeds from the current year. This is in agreement with that of the transient seed bank described by Thompson and Grime (1979). 4.3. Implications for invasion capacity and its management Studies on seed biology and seed bank of invasive species may provide opportunities to better understand aspects of plant population dynamics and are crucial for applications in restoration ecology (Daehler and Strong, 1994). Spartina alterniflora is a clonal and perennial salt marsh grass and both the sexual reproduction by seeds and asexual propagation by tillers and rhizomes are the two major means to keep a fast rate of geographic spread. Spartina alterniflora can produce a large amount of seeds, even if a low fraction of these seeds is viable, and it is likely that some of them could deposited in suitable locations and invade into new regions (Davis et al., 2004; Zhang et al., 2004; Jessie and Moore, 2008). Recruitment by seed had been reported as an important means for invasion of S. alterniflora across the open mudflats in San Francisco Bay (Daehler and Strong, 1996; Daehler, 1999). It had also been showed that each recruit germinated from a single seed could grow clonally into a circular patch and finally merge to form dense continuous meadows on previously bare intertidal mudflats in Willapa Bay (Davis et al., 2004). Further work is needed to understand how the seed production and seedbank patterns reported in this study can be related to seedling recruitment patterns in the nature reserve, as these patterns will ultimately translate into seedling recruitment pattern which is critical to understanding the spread dynamics (Lambrinos and Bando, 2008). To control and eradicate the invasive plant Spartina alterniflora at the Chongming Dongtan Nature Reserve is important and necessary for biodiversity conservation. The results from this study on seed biology and seed bank of this invasive species could provide valuable insights on which strategic control efforts can be designed and applied. The physical or mechanical measures such as cutting, burning, pruning, excavating and waterlogging have been suggested and tested to control S. alterniflora at the nature reserve (Li and Zhang, 2008; Yuan et al., 2008). The most successful and fast measure to eradicate S. alterniflora at a demonstration site in the nature reserve has been proved by adopting an integrated technique of cutting at the florescent period (July) combined thereafter with waterlogging for about 3 months. Based on the evidence drawn from this study, this integrated technique of control could effectively prevent S. alterniflora from seed setting and forming a soil seed bank in the current year, thus minimizing the risk of reinvasion as it has a transient seed bank. Acknowledgements The authors would like to thank members of the Ecological Section of the State Key Laboratory of Estuarine and Coastal
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