ecological engineering 35 (2009) 511–520

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Spartina alterniflora invasions in the River estuary, : An overview of current status and ecosystem effects

Bo Li a,∗, Chengz-hang Liao a, Xiao-dong Zhang a, Hui-li Chen a, Qing Wang a, Zhong-yi Chen a, Xiao-jing Gan a, Ji-hua Wu a, Bin Zhao a, Zhi-jun Ma a, Xiao-li Cheng a,b, Li-fen Jiang a, Jia-kuan Chen a a Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, The Institute of Biodiversity Science, , #220 Handan Road, 200433, PR China b Wuhan Botanical Garden, CAS, Wuhan 430074, PR China article info abstract

Article history: The Yangtze River estuary is an important ecoregion. However, Spartina alterniflora, native to Received 13 November 2007 North America, was introduced to the estuary in the 1990s through both natural dispersal Received in revised form and humans and now it is a dominant species in the estuarine ecosystems, with its inva- 21 February 2008 sions leading to multiple consequences to the estuary. S. alterniflora had great competitive Accepted 12 May 2008 effects on native species, including Scirpus mariqueter and Phragmites australis, and could potentially exclude the natives locally. The presence of S. alterniflora had little influence on the total density of soil nematodes and macrobenthonic invertebrates, but significantly Keywords: altered the structure of trophic functional groups of nematode and macrobenthonic inverte- Biodiversity brate communities. The conversion of mudflats to Spartina meadows had significant effects Community structure on birds of Charadriidae and Scolopacidae, which might be attributable to the reduction Ecosystem effects of food resources and the physical alterations of habitats for shorebirds. S. alterniflora inva- Invasive species sions increased the primary productivity of the invaded ecosystems, and altered carbon Spartina alterniflora and nitrogen cycling processes. Our studies focused mainly on the effects of S. alterniflora Yangtze River estuary invasions on the structure of native ecosystems; thus further studies are clearly needed to investigate how ecosystem functioning is affected by the modification of the structure of estuarine ecosystems by S. alterniflora invasions. © 2008 Elsevier B.V. All rights reserved.

1. Introduction example, 54.7% of Shanghai’s flora is exotic (Li et al., 2001). A recently introduced plant, Spartina alterniflora, is one of the Invasive plants pose a serious threat to native ecosystems most harmful invasive exotic plants in the Yangtze River estu- and cause considerable loss to regional economy. China is a ary (Wang et al., 2006a). huge country with five climatic zones in which diverse ecosys- For the purposes of erosion control, soil amelioration and tems can receive exotic species from different biogeographic dike protection, S. alterniflora was intentionally introduced regions. In particular, southeastern China is heavily infested from three sites in North America (North Carolina, Georgia with invasive exotic plants, presumably because this part of and Florida) to China in 1979 (An et al., 2007). S. alterniflora the country has a mild climate and is more disturbed by has a number of biological traits (e.g. fast growth, well- human actitivities than other regions (Wu et al., 2006). For developed belowground structures, high salt tolerance, great

∗ Corresponding author. Tel.: +86 21 65642178; fax: +86 21 55664990. E-mail address: [email protected] (B. Li). 0925-8574/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.ecoleng.2008.05.013 512 ecological engineering 35 (2009) 511–520

Fig. 1 – Distribution of Spartina alterniflora (A) and its range expansion in Dongtan (B) and Jiuduansha (C) marshlands, the Yangtze River estuary, China.

reproductive capacity through both clonal growth and sexual species, decrease in abundance of native species, degradation reproduction), making it a good ‘ecosystem engineer’ (Chung, of native ecosystems, and considerable economic loss. 1993, 2006; Qin et al., 1998; Crooks, 2002; Chung et al., 2004; It was because of the possible negative impacts on the Zhang et al., 2005) or a suitable species for ecological restora- native ecosystems and economic consequences that S. alterni- tion (Hinkle and Mitsch, 2005). For this reason, it was widely flora was recognized as one of 16 most harmful invasive exotic introduced to the east coast of China (Chung, 2006) and is speices by the State Environmental Protection Administration widely distributed along the east coast of China, from Tian- (SEPA) of China in 2003. Nevertheless, some scientists still jin to Beihai in Guangxi (Wang et al., 2006a). S. alterniflora can insist that S. alterniflora can be a beneficial species and useful to also be used in various ways (Chung, 1993, 2006; Qin et al., ecological engineering in many different ways. They advocate 1997, 1998; An et al., 2007). The coverage of S. alterniflora was further uses of S. alterniflora in China. Therefore, S. alterniflora approximately 260 ha in six counties by 1985 (Chung, 1989) and has become a controversial species, and the debate still con- increased to more than 112 000 ha by 2000 (An et al., 2007). tinues. It should be pointed out that SEPA’s decision to include S. alterniflora was first found in 1995 in Dongtan wetlands S. alterniflora on the blacklist was made mainly on the basis of on Chongming Island in the Yangtze River estuary (Fig. 1A) and its economic consequences. To the best of our knowledge, no is believed to have arrived there though natural dispersal by formal risk assessments of S. alterniflora have been made so water flow from Qidong, Jiangsu Province. For rapid sediment far in China, which we believe is the major reason that many accretion in mudflats in the estuary, S. alterniflora was inten- scientists do not accept SEPA’s inclusion of S. alterniflora on the tionally introduced to Jiuduansha Islands in 1997 and Dongtan list. on Chongming Island in 2001 (Fig. 1A), which has led to a rapid In order to provide direct evidence for decision making, the range expansion in the estuary. It has become a dominant Shanghai government recently funded a S. alterniflora project plant species of wetland ecosystems on these islands just over that was proposed to make a comprehensive assessment of 10 years since its first occurrence in the estuary, and its impact the ecological effects of its invasions on the native ecosys- on the native ecosystems has become more and more pro- tems in the estuary, and to develop strategies for managing found (Chen, 2004; Chen et al., 2004a,b). The possible effects this invasive species. Here, we briefly review the status of S. of S. alterniflora invasions on the native ecosytems include but alterniflora invasions in the Yangtze River estuary and their are not limited to: conversion of mudflats to Spartina meadows, ecosystem effects, and their detailed descriptions have been loss of shorebirds’ foraging habitats, impact on endangered (e.g., Chen et al., 2004a,b; Cheng et al., 2006, 2007; Wang et al., ecological engineering 35 (2009) 511–520 513

2006b; Chen et al., 2007a,b; Wang et al., 2007; Liao et al., 2007, to produce viable seeds under freshwater field conditions. 2008; Wu et al., 2008) or will be published elsewhere. The ideal salinity for growth and reproduction of S. alterniflora ranges from 8 to 33‰ (USDA Natural Resources Conservation Service, 2007). 2. The Yangtze River estuary S. alterniflora has a number of superior traits such as fast growth, great productivity, high tolerance to salt and a The Yangtze River (Changjiang) is the longest river in China, well-developed belowground system that make it a typical ranking third in the world. The river originates from the ecosystem engineer (Crooks, 2002). Therefore, S. alterniflora Plateau of Tibet and empties into the East China Sea. The is widely used for erosion control along shorelines, canal Yangtze River estuary covers a large portion of Shanghai and banks, levees, and other areas of soil–water interface, and a portion of Jiangsu Province (part of it shown in Fig. 1A). The planted as a soil stabilizer on interior tidal mudflats, dredge- estuary includes a river part whose upper boundary is Datong fill sites, and other areas of loose and unconsolidated soils in the main stream of the Yangtze River (624 km upstream of associated with marsh restoration (USDA Natural Resources the estuary) and a near-shore zone (the near-shore zone of the Conservation Service, 2007). It was because of these traits that East China Sea) (Mikhailov et al., 2001). S. alterniflora was widely introduced to other coastal regions A number of islands exist in the estuary, of which Chong- out of its native range, including the west of the USA, and ming Island is the largest (the third largest in China the largest they are also the cause of the present worldwide ecological alluvial island in the world); and Jiuduansha Islands, consist- concerns (Wang et al., 2006a). ing of three islands, are the youngest, first emerging in 1954. Like other estuaries, the Yangtze River estuary provides great ecosystem services for humans and wildlife in the region; thus 4. History and status of Spartina alterniflora it is an important ecoregion. invasions in the Yangtze River estuary The estuary has a diversity of wetland ecosystems, such as shallow open waters, mudflats, salt marshes and brackish The invasions of S. alterniflora in the Yangtze River estuary have ecosystems, which make an important habitat for shore- been a recent event and the result of both natural dispersal birds, in which the key native plant species include Scirpus and intentional introductions. S. alterniflora was initially intro- mariqueter and Phragmites australis. Thus, it serves as an duced to Jiangsu Province in 1983, and then used for ecological important stopover site for migratory birds on the East Asian- engineering in Yancheng, and subsequently spread to coastal Australasian Flyway (Ma et al., 2004), which receives millions areas in the province, e.g. Qidong in the Yangtze River estu- of birds each year. In fact, the Dongtan wetland on Chongming ary. Small patches of S. alterniflora were first found in Dongtan Island was recognized as a Wetland of International Impor- marshlands on Chongming Island in the estuary in 1995, and tance by the Ramsar Convention on Wetlands in 2002. The is believed to have invaded the mudflats through seed disper- estuary also functions as an important sanctuary for a number sal from Qidong by water flow (Chen, 2004). More important, of endangered species or as a spawning site for economically S. alterniflora was transplanted into the mudflats and marsh- important aquatic species. For these reasons, two national lands dominated by S. mariqueter for rapid sediment accretion reserves were established in 2005 in the estuary, one on Chong- in April 2001, as Dongtan marshlands have been regularly ming Island and the other on Jiuduansha Islands (Fig. 1A). reclaimed. The planted area was 337 hm2, outside the dike Therefore, maintaining the integrity of the native ecosys- built in 1998 where S. mariqueter grew very well by the time tems and conserving biodiversity in the estuary are of both S. alterniflora was planted. The planting strip of S. alterniflora regional and international importance. However, the mudflats was 4500 m long and 750 m wide. Since then, S. alterniflora and salt marshes in the estuary are now heavily infested with has rapidly spread to the unplanted mudflats and vegetated introduced S. alterniflora, which may threaten the estuarine marshlands (Fig. 1A), as it can produce a large number of fertile ecosystems and their biodiversity. Our studies were carried seeds by which it can expand by long-distance seed dispersal. out mainly on Chongming and Jiuduansha Islands (Fig. 1A), S. alterniflora monocultures accounted for 49.4% of the vege- to which S. alterniflora was intentionally introduced singly or tated area in Dongtan marshlands in 2005 (Wang, 2007)(Fig. 2). repeatedly. Jiuduansha, consisting of three newly formed islands that are uninhabited, has also been invaded by S. alterniflora, which was purely the result of intentional introductions. Construc- 3. The species: Spartina alterniflora tion of International Airport was completed in 1999 at the Yangtze River mouth. For the safety of flights, S. alterni- S. alterniflora Loisel. (common name: smooth cordgrass) is a flora was introduced to part of Jiuduansha outside Pudong perennial rhizomatous C4 grass of Poaceace, native to the Airport in 1997 for rapid sediment accretion and growth of Atlantic and Gulf coasts of North America. Plant height varies marshlands so that shorebirds could find their habitats out- considerably, depending on growing conditions, but seems to side the airport (He et al., 2007). S. alterniflora subsequently higher in non-native range, up to 250 cm (e.g., in China). S. spread to most of Jiuduansha rapidly (Fig. 1C) (also see Huang alterniflora spreads through clonal propagation by rhizome and and Zhang, 2007), and locally excluded native plants—S. mari- sexual reproduction by seed, and hence is a rapidly spreading queter and P.australis, forming dense monocultures. Our recent plant. data obtained through remote sensing show that S. alterniflora S. alterniflora is an intertidal brackish plant species. monocultures accounted for 37.0% of the vegetated area in Although it can be established in freshwater, it seems unable Jiuduansha marshlands in 2005 (Wang, 2007)(Fig. 2). 514 ecological engineering 35 (2009) 511–520

Table 1 – Summary of competitive balance between Spartina alterniflora and Phragmites australis based on the values of RNE, as affected by the growing conditions (modified from Wang et al., 2006b) Factors Treatments Competitive manipulated used outcome

Salinity 0‰ Phragmites > Spartina, 15‰ Phragmites = Spartina, 30‰ Phragmites < Spartina

Sediment type Sand Phragmites < Spartina Clay Phragmites = Spartina Mix Phragmites = Spartina

Waterlogging Non-immersion Phragmites > Spartina Half-immersion Phragmites = Spartina Full-immersion Phragmites < Spartina Fig. 2 – Contribution of Spartina alterniflora community to vegetation of Dongtan on Chongming Island () and S. mariqueter serves as food of migratory birds and its commu- Jiuduansha (᭹) marshlands of the Yangtze River estuary, nities as habitats for the birds (see below). expressed as the percentage of the vegetated area. The data The competitive effects of S. alterniflora on native P. aus- are fitted to the logistic model. tralis were also evaluated under varying growing conditions in polytunnels (Wang et al., 2006b). We grew both species either in monocultures or in their mixture in large plastic Similarly, S. alterniflora also invaded other mudflats and pots. We manipulated the growing conditions to simulate marshlands in the Yangtze River estuary mainly through nat- the environmental variations in the Yangtze River estuary, ural seed dispersal (Fig. 1A). Fortunately, recently proposed including salinity (0, 15 or 30 ppt), sediment type (sand, clay intentional introductions were stopped. Our field observations and mix of sand and clay) and waterlogging (no immersion, have shown that S. alterniflora is still expanding in the estuary. half-immersion and full-immersion). In order to compare the Eradication of the populations of S. alterniflora in the Yangtze relative competitive ability of the two species, both interspe- River estuary seems difficult, as it has spread to all the habitats cific and intraspecific interactions were quantified using an that are suitable for S. alterniflora. index of the Relative Neighbor Effect (RNE) (Markham and Chanway, 1996):

P− − P RNE = N +N 5. Competitive effects on native plants x where P is a measure of plant performance in the presence One of the threats of invasive plants to native ecosystems is (+N) and absence (−N) of neighbors, and x is the measure for their competitive effects on native plants, which may result in the species with the greatest performance. the decrease in abundance and even local extinction of native Our results obtained from this experiment show that the plants. competitive balance between S. alterniflora and P. australis var- In April 2001, S. alterniflora was intentionally introduced ied among the growing conditions (Table 1). The competitive to marshlands dominated by S. mariqueter at Dongtan on dominance of S. alterniflora was shown in the conditions with Chongming Island for rapid sediment accretion and growth the highest salinity, sand and full immersion, whereas P. aus- of marshlands, a dike was built for reclamation in 1998. tralis showed competitive dominance under the conditions Beginning in March 2002, we monitored the dynamics of with the lowest salinity and non-immersion. The two species both native S. mariqueter and exotic S. alterniflora in the could co-exist under other conditions (Wang et al., 2006b). As planted area for 2 years, during which various population Daehler (2003) has commented, the exotic invaders are not parameters were recorded on Scirpus (i.e. monoculture) and statistically more likely to have greater competitive ability Spartina–Scirpus (their mixture) transects, including popula- than their co-occurring natives, but the relative performance tion density, biomass, seed and corm production. of invaders and natives often depends on their growing con- Our field studies have shown that the difference in abun- ditions. Overall, our results suggest that S. alterniflora might dance of S. mariqueter between Scirpus and Spartina–Scirpus outcompete P. australis under the conditions present in early transects becomes more and more profound with increasing succession. time of Spartina’s introduction to the S. mariqueter commu- Our recent field observations have shown that S. alterni- nities (Chen et al., 2004b). The reduction in abundance of S. flora locally replaced P. australis in the brackish marshes in mariqueter due to S. alterniflora’s competition resulted in the the Yangtze River estuary, which seems surprising because the reduced seed production and corm pool size of S. mariqueter. two species have similar growth forms and may be competi- Our further field observations conducted in 2004 have shown tively equal under certain conditions. There are two important that S. mariqueter in the Spartina–Scirpus transects were actu- points here. First, the two species have different phenolo- ally replaced by S. alterniflora. The replacement of S. mariqueter gies. P. australis emerges only in spring whereas S. alterniflora may have serious consequences for shorebird populations, as produces overwintering ramets in autumn/winter, so this ecological engineering 35 (2009) 511–520 515

phenological difference offers a competitive advantage for S. Numerical analysis of these trophic functional groups alterniflora as relative time of shoot emergence is an important further demonstrates that the relative abundance of bacteria- determinant of competitive ability. Second, the marshlands feeding nematodes (bacterivores) significantly increased, are reclaimed regularly at Dongtan on Chongming Island, whereas that of plant feeders and algal feeders declined in which forces P. australis to move towards the marshlands, S. alterniflora communities, compared with that in P. australis where S. alterniflora has a competitive advantage over P. aus- and S. mariqueter communities (Chen et al., 2007b). Our fur- tralis,asS. alterniflora is more tolerant of high salinity. ther experimental study has demonstrated that the changes It should be pointed out that S. alterniflora invasion in in nematode communities were the result of altered litter the Yangtze River estuary may also drive a new pattern of quality caused by invasive S. alterniflora (Chen et al., 2007a). plant zonation in the estuarine wetlands. There is a simple The changes in trophic functional goups, as affected by S. pattern of plant zonation in the intertidal zone in the Yangtze alterniflora invasions, may have important consequences to River estuary as common plants are very few. At the same the invaded ecosystems. In particular, the presence of S. time, frequent reclamations in the estuarine area make alterniflora is likely to alter the decomposition processes, rates the ecosystems unstable and plant community succession and pathways, as nematodes are one of the most impor- incomplete. Therefore, S. mariqueter occupies the low tide tant decomposers in ecosystems (Chapin et al., 2002), which zone and P. australis the high tide zone in naturally occurring undoubtedly modifies belowground nutrient cycling, which intertidal zone in the Yangtze River estuary, both of which will in turn influence the structure and ecosystem functioning form their respective monocultures. S. alterniflora invasion of the coastal wetlands. interrupts natural succession of plant communities through excluding S. mariqueter in the low tide zone and facilitating P. australis colonization in the high tide zone (Fig. 1B and C). A 7. Effects on macrobenthonic invertebrates new pattern might emerge in the near future if S. alterniflora is not effectively controlled in the Yangtze River estuary, which S. alterniflora very often forms dense monocultures with well- would be disastrous to birds that heavily rely on S. mariqueter developed belowground structures in the invaded ecosystems communities. on Chongming and Jiuduansha Islands in the Yangtze River estuary, which may alter the physical and chemical proper- ties of soils. Moreover, S. alterniflora marshlands have much greater pimary productivity than S. mariqueter marshlands, 6. Effects on nematode communities which produce more litter. Here an important question is: do these changes lead to alterations of benthonic invertebrate Nematodes are important components of the soil ecosys- communities? A few studies have investigated the effects of tems and play important roles in ecosystem functioning. The Spartina spp. invasions on invertebrates (e.g. Lana and Guiss, changes in composition of plant communities are believed 1991; Daehler and Strong, 1996; Luiting et al., 1997; Netto and to affect the structure of nematode communities (Yeates, Lana, 1999; Hedge and Kriwoken, 2000), but no consistent con- 1999). However, the effects of Spartina spp. on the invaded clusions seem to be reached. ecosystems have rarely been investigated, although they may In order to examine the effects of S. alterniflora invasions have important implications for soil ecosystem processes. In on macrobenthonic invertebrates, we compared the struc- order to examine the effects of S. alterniflora invasions on ture of macrobenthonic invertebrate communities between S. soil nematode communities, we compared the structure of mariqueter and S. alterniflora communities at Dongtan, Chong- soil nematode communities among native (S. mariqueter and ming Island (Chen et al., 2005). A total of 25 species of P. australis) and S. alterniflora communities on Chongming, macrobenthonic invertebrated were recorded in the two com- Jiuduansha Islands and Nanhui (Chen et al., 2007b). We esti- munities. The mean total density (±S.E.) in S. mariqueter mated richness and abundance of nematodes through taking and S. alterniflora communities was 3459 (±311) and 3119 soil cores in March 2004, and identified them to the level of (±246) individuals m−2, respectively, which was not signifi- genera. The nematodes were then divided into six trophic cantly different between the two communities. However, the functional groups: plant feeders, omnivores, fungal feeders, presence of S. alterniflora did change the abundance of 5 of predators, algal feeders, and bacterivores. We also calcu- 25 species. The abundance of Assiminea violacea was higher, lated Shannon diversity index for taxa and trophic functional and that of the four other species was lower in S. alterniflora groups. communities than in S. mariqueter communities (Table 2). A total of 48 genera of nematodes, belonging to 8 orders, Another significant aspect arising from S. alterniflora inva- were identified in our study. However, neither total density of sions is that the distribution of trophic functional groups was nematodes (individuals/g soil), number of genera or diversity also altered (Fig. 3). These macrobenthonic invertebrates were index was significantly different among the three plant com- dominated by suspensivores in both S. mariqueter and S. alterni- munities. It seems that the increase of a primary productivity flora communities. The presence of S. alterniflora led to an caused by S. alterniflora invasions did not increase benthic increase in the proportion of suspensivores, but a decrease meiofaunal abundance. Interestingly, the trophic diversity in that of herbivores and detritivores, compared with that in index in S. alterniflora communities was significantly lower the S. mariqueter communities (Chen et al., 2005). Therefore, S. than that in both the P. australis and S. mariqueter communi- alterniflora invasions may have effects on the ecosystem pro- ties, implying that S. alterniflora invasions altered the trophic cesses in the soil that are associated with macrobenthonic structure of nematode communities in soil (Chen et al., 2007b). invertebrates. 516 ecological engineering 35 (2009) 511–520

our previous study has also shown that the presence of S. Table2–Fivespecies of macrobenthonic invertebrates that were significantly affected by Spartina alterniflora alterniflora affects the distribution of the hooded crane (Grus invasions, and their mean density in native (Scirpus monacha) in the Dongtan wetlands in the estuary (Ma et al., mariqueter) and invaded communities 2003). Taxa Mean density (individuals m−2) The effects of Spartina spp. invasions on shorebirds may be direct or indirect. As discussed above, S. mariqueter is a Scirpus Spartina dominant native plant whose seeds and corms are impor- Gastopodia tant food sources for a number of bird species (including Assiminea violacea 1351 ± 181 2086 ± 225 the geese, ducks and cranes). Its replacement by S. alterni- Assiminea lutea 249 ± 57 108 ± 36 flora reduces food for birds, and hence decreases the habitats’ Cerithidea sinensis 211 ± 41 81 ± 21 carrying capacity for bird populations. S. alterniflora inva- ± ± Stenothyra glabra 332 83 54 16 sions also altered the physical characteristics of wetlands, Lamellibranchia notably converting the mudflats to S. alterniflora meadows. Glaucomya chinensis 163 ± 45 49 ± 12 However, Table 3 demonstrates that most of shorebirds pre- ferred mudflats and Scirpus communities to S. alterniflora All the differences between two plant communities are significant at P = 5% level (data extracted from Chen et al., 2005). marshlands, presumably because the previous mudflats and S. mariqueter communities invaded by S. alterniflora become unusable by shorebirds. In fact, it is almost impossible for birds to forage for food in dense S. alterniflora communities 8. Effects on birds with the mean height of 2.5 m, even though food may be abundant. Moreover, S. alterniflora may indirectly affect bird The Yangtze River estuary provides important stopover sites communities through changing the abundance of other taxa for migratory birds on the East Asian-Australiasian Flyway. For such as macrobenthonic invertebrates and fishes (Jing et al., this reason, two national nature reserves were recently set up 2007). in the Yangtze River estuary for migratory birds, thus a big It should also be pointed out that the effects of Spartina concern here is whether S. alterniflora invasions affect shore- spp. on birds may be long-term. A study carried out by Goss- birds. In fact, similar concern has also arisen from Spartina spp. Custard and Moser (1990) has shown that the number of invasions in other coastal regions of the world, for example, wading birds such as dunlin has not increased in those estu- British estuaries (e.g. Goss-Custard and Moser, 1990; Goss- aries where Spartina anglica has declined through natural Custard et al., 1995), San Francisco Bay (Callaway and Josselyn, dieback. However, long-term studies have been scarce, thus 1992), Washington (Foss, 1992) and New Zealand (Hubbard and monitoring the long-term responses of shorebirds to S. alterni- Partridge, 1981). flora invasions is desperately needed in the future as most of Although thorough studies are still being carried out to estuarine wetlands S. alterniflora invaded are associated with investigate the effects of S. alterniflora on shorebirds in the conservation of bird biodiversity. Yangtze River estuary, the prelimilary results from recent surveys show that the conversion of mudflats to meadows resulting from S. alterniflora invasions had significant impact 9. Effects on carbon and nitrogen cycling on shorebirds (Chen, 2004) (see Table 3). Table 3 shows that only Tringa nebularia selected the three habitats equally, and Although S. alterniflora has invaded the wetlands in the most of other shorebirds preferred to select mudflats or Scirpus Yangtze River estuary for just over 10 years, it has become communities rather than S. alterniflora meadows. Moreover, a dominant species here and is rapidly replacing the native plants S. mariqueter and P. australis, which are only two dominant higher vascular plants. Our survey conducted on Jiuduansha Islands in autumn 2002 showed that 13.2% of the island’s area was occupied by S. alterniflora, while S. alterniflora monocultures contributed 25.3% to the total plant biomass production of the islands (Chen et al., 2003). Obvi- ously, this is the result of increased primary productivity per unit area. In order to understand the impact of S. alterniflora on the temporal patterns of biomass production in the wetlands, we examined the seasonal variation in primary productivity among the three plant communities (i.e. their monocultures) on Jiuduansha Islands (Liao et al., 2007)(Fig. 4A). The results show that S. alterniflora had a much greater primary produc- tivity than S. mariqueter and P. australis (Fig. 4). Notably, the Fig. 3 – Distribution of three dominant trophic functional aboveground biomass of S. alterniflora was much greater than groups of macrobenthos as affected by Spartina alterniflora that of both S. mariqueter and P. australis (Fig. 4A). At the same invasions. Different letters show significant difference time, S. alterniflora is a salt marsh plant and may mainly replace between plant communities (from Chen et al., 2005). S. mariqueter and invade the mudflats in the Yangtze River ecological engineering 35 (2009) 511–520 517

Table 3 – Comparison of occurrences of plovers and snipes in three habitat typesa Species Habitat types

Mudflats Scirpus community Spartina community

Charadriidae Charadrius alexandrinus ++++ +b C. mongolus + Pluvialis squatarola +

Scolopacidae Calidris alpina ++++ C. ferruginea + C. ruficollis ++ C. sunbminuta + C. tenuirostris ++ Limicola falcinellus + Limosa limosa ++ Numenius arquata ++ Tringa nebularia ++++ ++++ ++++ T. stagnatilis + Xenus cinereus +++ ++

Glareolidae Glareola maldivarum ++

a The results presented here are based on four surveys made in Dongtan wetlands, Chongming Island, during autumn 2003 (Chen, 2004). b The number of plus signs (+) indicates the frequency of occurrence. estuary and eventually dominate the marshlands. There- fore, S. alterniflora invasions would significantly increase the productivity of the ecosystems that S. mariqueter currently dominates. The plant’s increased structure (both aboveground and belowground) and primary productivity have potentially far-reaching impacts on the rest of the ecosystems (Dethier and Hacker, 2004). Great primary productivity may imply a great ability to sequester carbon and may also contribute in other positive ways to the near-shore ecosystems. We further investigated the changes of carbon and nitro- gen stocks in response to S. alterniflora invasions at Jiuduansha (Liao et al., 2007). The results showed that the ecosystems dominated by S. alterniflora had significantly larger sizes of carbon (Fig. 5A) and nitrogen (Fig. 5B) stocks than those by S.

Fig. 5 – Sizes of total carbon and nitrogen stocks of four ecosystems in Jiuduansha wetlands, the Yangtze River estuary, as affected by S. alterniflora invasion. The total stock is the sum of plant and soil stocks, whose data were collected in September 2004 (data from Liao et al., 2007).

Fig. 4 – Seasonal variation in aboveground (A) and belowground (B) primary productivity of three mariqueter and P. australis (Fig. 5). The stable isotope analysis monocultures in Jiuduansha wetlands. The estimates were has also confirmed that the replacement of S. mariqueter by S. made in 2004. () Spartina alterniflora;(᭹) Phragmites alterniflora increased soil organic carbon and total soil nitrogen australis;() Scirpus mariqueter (data from Liao, 2007). (Cheng et al., 2006). The alterations of ecosystem productivity 518 ecological engineering 35 (2009) 511–520

and carbon/nitrogen stocks caused by S. alterniflora invasions ecological functions. The alterations of the ecosystem struc- could be explained partially by the shifts of dominant traits ture will undoubtedly affect the ecosystem functioning in the that determine carbon and nitrogen cycling processes. S. Yangtze River estuary. Therefore, further studies are clearly alterniflora had a longer growing season, higher leaf area index, needed to investigate how ecosystem functioning is affected higher net photosynthetic rate, and greater root biomass than by the modification of the structure of estuarine ecosystems S. mariqueter and P. australis, which gave a greater NPP in that is caused by S. alterniflora invasions, and how the change S. alterniflora ecosystems than in native ecosystems (Liao et of an ecosystem’s component affects or is affected by those al., 2007). Decomposition rates of S. alterniflora litters, par- of other components, as done by Levin et al. (2006) in San ticularly the belowground litter, were lower than those of S. Francisco Bay (USA). mariqueter and P. australis litters due to the lower litter qual- ity of S. alterniflora (Liao et al., 2008). In addition, epiphytic N fixation occurred in the ecosystems dominated by S. alterni- Acknowledgements flora when its stem and sheath litter decomposed. However, this epiphytic N fixation was not observed in the ecosystems We thank the students in Ecology Lab of Biological Inva- dominated by S. mariqueter and P. australis. Therefore, S. alterni- sions at Fudan University who offered assistance in the flora invasions altered ecophysiological processes, resulted in field, and Ruthmarie Mitsch for making numerous improve- changes in NPP and litter decomposition, and ultimately led ments to the early version of this manuscript. This study to enhanced ecosystem C and N stocks in invaded ecosystems was financially supported by National Basic Research Pro- in comparison to the ecosystems with native species. gram of China (Grant no. 2006CB403305), National Science The effects of S. alterniflora invasions on carbon and nitro- Foundation of China (Grant Nos. 30670330 and 30370235) and gen cycling might be of limited importance to the globe in Science & Technology Department of Shanghai (Grant No. relation to its range in the Yangtze River estuary, but might 04DZ19304) and the Ministry of Education of China (Grant no. accrue at the edges of marshes, as Dethier and Hacker (2004) 105063). have addressed. In fact, S. alterniflora as a primary producer in the estuarine ecosystems functioned as energy source for references certain nektons in the marshlands in the Yangtze River estu- ary (Quan et al., 2007). 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