- Email: [email protected]
Invasion and ecological effects of exotic smooth cordgrass Spartina alterniflora in China
Ecological Engineering 143 (2020) 105670
Contents lists available at ScienceDirect
Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Review
Invasion and ecological effects of exotic smooth cordgrass Spartina alterniflora in China
T
⁎
Weiqing Menga,b, Rusty A. Feaginb, , Rachel A. Innocentib, Beibei Hua, Mengxuan Hea, Hongyuan Lic a
School of Geographic and Environmental Science, Tianjin Normal University, Tianjin 300387, China Dept. Ecosystem Science and Management, Dept. Ocean Engineering, Texas A&M University, College Station, TX, USA c College of Environment Science and Engineering, Nankai University, Tianjin 300350, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Smooth cordgrass Spartina alterniflora Exotic species Ecological effects China
Smooth cordgrass (Spartina alterniflora) was introduced to China in December 1979 to buffer against tides and to accelerate coastal wetland accretion. Since then, its propagation and natural dispersal have allowed this exotic plant to rapidly expand throughout coastal China with generally negative ecological effects. In 2003 S. alterniflora was labeled as an invasive plant in China, and it now covers ~50,000 ha. In this review, we first summarize the mechanisms of spread and spatial distribution of S. alterniflora, and how its physiological characteristics and strong adaptability to the available niche space in China's wetlands have enabled its spread and competition with native plants. Then we review the effects of S. alterniflora on ecosystem function in terms of habitat conversion and the alteration of biodiversity, soil carbon flux and sequestration, and various processes of nutrient regulation. We conclude that we need a long-term and context-dependent perspective, in order to maximize the benefits and minimize the costs of S. alterniflora within each of China's unique provinces.
1. Introduction Smooth cordgrass (Spartina alterniflora) is a perennial grass that is native to the Atlantic coast of the Americas, ranging from Canada to Argentina. It has been introduced to many coastal regions throughout Europe, Australia, and Asia, primarily for mitigating coastal wetland erosion, which it does by reducing tidal wave energy, trapping sediments, and promoting vertical accretion (Chung, 1993; Maricle and Lee, 2002). Coastal erosion can occur through many processes. Daily erosion occurs when waves wear away the shoreline, and it can pose a serious threat to the infrastructure and resources of coastal communities. Historically, people have built sea walls to resist erosion, but this method is expensive and can even exacerbate the problem by robbing sediment supply to beaches. More recently, people have shifted to the use of natural solutions to coastal erosion that mitigate sediment loss and foster ecosystem function. For this reason, Spartina alterniflora was introduced to China. The first successful seed germination of S. alterniflora in China was carried out in December 1979 by the botanical garden of Nanjing University, using plants from the United States' Atlantic Coast. The species was then transplanted to Luoyuan County, Fujian province onto barren mudflats to defend against storm surges. A lack of survey data ⁎
prevents us from knowing the initial degradation level of this affected habitat, but from the description in the relevant literature, the participants had not expected the forthcoming negative ecological effects (potentially due to the lack of information about an ecological invasion at the time) (Chung, 1993, 2006). Both further plantings and natural dispersal, paired with the S. alterniflora's environmental adaptability and strong reproductive capacity, allowed it to expand rapidly throughout China's coastal zone. In 1985, the area of S. alterniflora in China was ~260 ha. In 2003, S. alterniflora was included in the first list of exotic invasive plants jointly issued by the State Environment Protection Administration of China and Chinese Academy of Sciences (Wang et al., 2006a, 2006b). By 2007, it covered 34,178 ha, with the population in the coastal areas of Jiangsu accounting for more than 52% of this total (17,842 ha; Lu and Zhang, 2013). Today, S. alterniflora has expanded to around 50,000 ha of the coastal regions of China. The spread of smooth cordgrass has already altered aspects of Chinese wetlands including productivity, soil water content, hydrodynamics, sedimentary processes, soil formation, and accumulation of nutrients. The positive versus negative effects of these changes vary by location and habitat condition. For example, S. alterniflora plays an important positive role in shoreline protection in some regions, whereas in others, it has caused damage to maricultural activities (Chen et al.,
Corresponding author. E-mail address: [email protected] (R.A. Feagin).
https://doi.org/10.1016/j.ecoleng.2019.105670 Received 3 September 2018; Received in revised form 21 October 2019; Accepted 15 November 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
2.2. Expansion of S. alterniflora
2009; Gao et al., 2016; Wan et al., 2009). Many researchers have discussed its benefits and drawbacks as well as its population dynamics and control (Chen et al., 2012; Chung et al., 2004; Jiang et al., 2009; Wang et al., 2008). Here, we seek to review the progress of S. alterniflora research. We discuss the effect of this species on coastal wetland ecosystems in China, and whether it was inevitable that S. alterniflora would become ‘invasive’ as a function of the relevant aspects of its physiology. We also discuss how to best capitalize on the positive effects of Spartina alterniflora while also controlling its negative effects.
S. alterniflora grows well in China: the average aboveground biomass and belowground biomass of a mature S. alterniflora community in the Yellow River Delta in 1998 was 2657 and 3517 g/m2 respectively (Qin et al., 1998). Biological invasions often exhibit a lag time between colonization and the time that rapid population growth begins (Sakai et al., 2001). After initial colonization and establishment, S. alterniflora may increase in coverage by short distance growth via runners and rhizomes or long distance dispersal via seeds (Davis and Thompson, 2000; Huang and Zhang, 2007). One study in San Francisco Bay showed that S. alterniflora had an exponential increase in cover and a constant areal expansion rate of 18–20% (Ayres et al., 2004). At the coast of Jiangsu province, China, the initial colonization and establishment phase was completed in the period 1993–1995 with an annual expansion rate of 30%. S. alterniflora began to rapidly spread approximately in the year 2000, with annual increases of 43% between 1999 and 2001 (Zhang et al., 2004; Huang and Zhang, 2007). S. alterniflora reproduces quite easily and at a high rate of success. It also has a quite wide niche, given the stressful saltwater environment in which few other species live (Huang and Zhang, 2007). One individual of S. alterniflora in Chongming Island near Shanghai was found to produce 86–222 tillers (Zhang et al., 2006). The fast reproductive rate and rapid range expansion of S. alterniflora gives the species its competitive edge over native species and facilitates its invasion (Li and Zhang, 2008). We summarize the invasion mechanism of S. alterniflora in China as a function of both biotic factors and abiotic factors (Fig. 2). Of these, the biotic characteristics of S. alterniflora are the most important factors for its invasion success. Strong reproductive capacity and tolerance to environmental conditions such as high salinity and flooding makes S. alterniflora a successful competitor over native species (Jarvis and Moore, 2008). Of the abiotic factors linked with invasion, the purposeful introduction is the most obvious factor; it can be assumed invasion would not have happened if the species had not been introduced. Further establishment of S. alterniflora was affected by its seeds' ability to float with the tide and be carried away from the location of initial introduction (Ayres et al., 2004). Human use of coastal habitat has an indirect promoting effect on invasion success, as well. Nitrogen inputs to the environment from agricultural runoff, industry, and pollution, paired with the strong nitrogen utilization of S. alterniflora inevitably contributes to its growth and adaptability. Invasion rates differ according to ecosystem and the niche space available for S. alterniflora. For example, within systems of competitive reeds (like Phragmites communis) and mangroves, S. alterniflora invasion is relatively slow compared to invasion within Scirpus mariqueter communities: once S. alterniflora invades, it can form patches with a diameter of 1–2 m in a growing season. Patches expand and, in 2–3 years,
2. Spread mechanism and distribution of S. alterniflora 2.1. Physiognomic and physiological characteristics Spartina alterniflora has stiff, erect stems, with maximum 11 nodes each, which can reach more than 2.0 m tall and 1.2 cm in diameter. Its leaves extend approximately 50 cm long and 2 cm wide (Wan et al., 2009). The species propagates both sexually via seeds and asexually by tillers and rhizomes which gives it a fast rate of geographic spread (Huang and Zhang, 2007). Under suitable conditions, S. alterniflora can reach sexual maturity within 3–4 months, and the length of its inflorescence is related to its geographical location in China. The seed survival time is estimated to be only eight months, suggesting that there is no long-lasting seed bank in the soil. As the dominant marsh plant species in many coastal wetlands in China and at other locations, the species grows in a wide range of salinities (from about 5–32 psu); however, salt-tolerant germination tests show the germination rate of seeds decreases with increased salinity (Qin et al., 1998). Elongation of the rhizome is very fast, with one study indicating the transverse elongation of the rhizome to be 0.5–1.7 m per year on the tidal flat of Washington (Simenstad and Thom, 1995). The adaptation of S. alterniflora to its abiotic environment is mainly characterized by its high tolerance and adaptation to environmental stresses. S. alterniflora has a stronger tolerance to the stress of a salt marsh than Phragmites australis, Spartina patens, Scirpus robustus, and Scirpus mariqueter (Chen et al., 2004) as well as to flooding on the lower elevations of tidal flats, which is an important factor for its successful invasion (Fig. 1). It has aerenchyma, making it suitably adapted to the anoxic environment. Although excessive inundation inhibits the growth of S. alterniflora, some flooding has been shown to promote its growth, with research showing the fastest leaf growth rate of S. alterniflora under flooding of 30 days duration (Levine, 1998). S. alterniflora can also absorb different forms of nitrogen such as ammonium nitrogen and nitrate nitrogen, and the biomass of S. alterniflora is positively correlated with nitrogen concentration.
Fig. 1. The niche of S. alterniflora location in China's coastal wetland. 2
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
Fig. 2. Invasion mechanism of S. alterniflora in China.
3. Ecological effects of Spartina alterniflora invasion
connect with other S. alterniflora patches to form the dominant community. Some studies showed that the change of ecological factors can change the competitive situation between the reed and S. alterniflora, and further affect the distribution of S. alterniflora and reed on the coastal wetlands. With higher salinity (1%–2%), S. alterniflora has competitive ability, while at lower salinity (less than 0.5%), reeds have superior competitive ability (Wang et al., 2006a, 2006b). On the southern coast of China, woody mangroves, shrubs and trees are present; however, very few native salt marsh macrophytes can persist on China's northern coast (Wan et al., 2009). Suaeda is the dominant native intertidal vegetation in China's northern coastal wetlands, but its smaller height and biomass compared to S. alterniflora results in weak competitiveness for light. The long-distance dispersal capability of S. alterniflora and the absence of a similar species occupying its niche in the north played a strong role. Only then was the rapid expansion of S. alterniflora facilitated by its suitability to abiotic factors such as climate, substrate, and geomorphic context (Huang and Zhang, 2007).
3.1. Soil carbon The soil organic carbon (SOC) content of China's wetlands decreases with an increase in latitude (Table 2; see also Meng et al., 2019). This pattern is most evident in the Minjiang estuary wetlands. Moreover, SOC in these wetlands decreases rapidly with increasing depth within the 0–10 cm, but past this range, there is no obvious change (Gao et al., 2007). This pattern results in the SOC concentration in bottom layer being nearly 7 times less than that of the surface in Minjiang river estuary (Cheng et al., 2006; Pan et al., 2015), possibly due to the strong hydrodynamic processes of the estuary, which can have significant effects on the soil organic carbon content. Invasion of S. alterniflora in coastal regions alters ecosystem structure and nutrient cycling processes, thereby affecting these soil C pools (Windham and Ehrenfeld, 2003; Zhang et al., 2010). One study in the coastal wetland of Jiangsu province showed that after an 8 to 14-year invasion time-frame of S. alterniflora, the SOC increased by 27.0–69.6% and N content by 21.8–55.2% in the upper 0–10 cm soil layer, as compared to the native Sueda salsa (Zhang et al., 2010). The ability of S. alterniflora to sequester carbon is mainly a function of two features: its high biomass and deposition rate. According to photosynthesis reaction equations, the annual carbon sequestration capacity of S. alterniflora is 2274 g·m−2·yr−1, which is 4.6 times of the average value of Chinese vegetation (494 g·m−2·yr−1) (He et al., 2005). The SOC concentration in Eastern Chinese coastal wetlands increased remarkably at the 0–10 cm depth during the period of plant invasion and varied from 3.67 to 4.90 g SOC / kg of soil (Zhang et al., 2010). Unique ecosystem properties cause the soil organic carbon content to vary spatially and temporally, in some cases even within the same area. Standing native plants, latitude, hydrological conditions, time since invasion, and sampling depth are thought to be major contributors to differences in SOC distribution of S. alterniflora wetlands. When the plants invaded bare flat and native C3 plant communities such as Sueda salsa and Cyperus malaccensis, SOC was significantly increased in the upper 0–30 cm soil layer (Yang et al., 2013). However,
2.3. Current spatial distribution of S. alterniflora in China The spatial distribution of S. alterniflora in China's coastal zones was qualitatively mapped based on information from existing literature, particularly a large governmental effort as described in Meng et al. (2017) (Fig. 3). Almost 40 years after being introduced to the country, S. alterniflora has spread to all Chinese coastal areas, covering a total area of 35,889 ha (Table 1, Fig. 3). The species is most prominent in Jiangsu, Shanghai, Fujian and Zhejiang with growth patterns mainly shaped by temperature, with some influence from precipitation (Zhao et al., 2015). The area of S. alterniflora in the four provinces makes up 92.81% of the distribution. In the Jiangsu coastal zone, the area of S. alterniflora was 18,711 ha, constituting 52.14% of the S. alterniflora coverage in China. Our conservative estimate of the area of S. alterniflora distribution in Chinese coastal zones at present is greater than 5 × 104 ha; however, the area of S. alterniflora is sure to increase due to the species' rapid spread rate.
3
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
Fig. 3. Spatial distribution S. alterniflora in china's coastal zones.
and type of habitat involved. The biotic characteristics and strong adaptability of S. alterniflora cause it to spread and out-compete native plants for growth space. In the MinJiang estuary wetland of Fujian province, the expansion speed of S. alterniflora was rapid; within three years, S. alterniflora seized the habitats of native plants and became the dominant species, resulting in a great loss of vegetative biodiversity (Zhang et al., 2011). S. alterniflora also alters benthic animal communities. Benthic fauna is easily influenced by changes of vegetation and soil characteristics, and the community structure of benthic fauna needs a long time to restore after being destroyed (Quan et al., 2016). S. alterniflora can improve physical and chemical properties of sediment for benthic animals, and its roots, stems and leaves can provide food for mollusks,
invasion in mangrove ecosystems produced the opposite effect (Jing et al., 2017). Another investigation of S. alterniflora along the Chinese coast showed significant differences in individual and population traits among twenty-six populations were closely related to latitude. Plant height, inter-node length, basal stem diameter, and plant biomass increased initially and then decreased with increasing latitude and the productivity of S. alterniflora gradually decreased as the latitude increased (Zhang et al., 2010; Zhao et al., 2015).
3.2. Biodiversity The invasive nature of S. alterniflora in China's coastal wetlands can have different effects on biodiversity depending on the location, age, 4
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
alterniflora communities and they offer shelter against predation (Zhu et al., 2004). These birds have adapted to the transformation of natural habitats by S. alterniflora invasion, such as the marsh grassbird (Locustella pryeri) for which S. alterniflora communities are important habitats (Ma et al., 2014). As a pioneer plant, S. alterniflora can grow in mudflats where other vegetation cannot and facilitate the succession of plants such as mangroves, which provide nesting areas for birds. For these reasons, the invasion of S. alterniflora and its potential impacts on biodiversity throughout the trophic levels is a topic that warrants further research.
Table 1 The area and proportion of S. alterniflora in Chinese provinces (ha). Province
Area (ha)
Proportion (%)
Liaoning Hebei Tianjin Shandong Jiangsu Shanghai Zhejiang Fujian Guangdong Guangxi Total
57 474 570 686 18,711 5336 5092 4166 546 251 35,889
0.16 1.32 1.59 1.91 52.14 14.87 14.19 11.61 1.52 0.70 100.00
3.3. Habitats
Data source: (Wang et al., 2008; Wan et al., 2009; Zuo et al., 2012; Lu and Zhang, 2013).
One way S. alterniflora alters China's wetland habitats is by competitive exclusion. With the introduction of the species to the Yangtze estuary in 1990, S. alterniflora out-competed native Scirpus mariqueter and Phragmites communis, resulting in the original pioneer species of Scirpus mariqueter being replaced at ChongMing Island (Bo et al., 2009; Zhu et al., 2012). However, S. alterniflora also impacts China's wetlands by creating radically different habitats and elevations from previously unvegetated mudflats. On the coast of Jiangsu province, the ecological niche of S. alterniflora is the upper part of the tidal estuarine beach, historically unoccupied by plants; S. alterniflora quickly populates these areas void of competition (Zhang et al., 2005). The growth of S. alterniflora into unvegetated areas causes the addition of highly productive habitat for tidal animals; however, if the intertidal zone is too narrow, this expansion can further threaten the survival of the local ecosystem. In their native range in the Americas, S. alterniflora salt marshes are one of the most productive ecosystems. The species is dominant in the coastal intertidal zone because of its ability to adapt to various types of soil, salinity, and hydrology (Gallagher et al., 1980). It is important directly and indirectly to food sources such as benthic animals and insects, and provides a place for waterfowl to inhabit and forage (Silliman and Zieman, 2001). For China, S. alterniflora is an exotic species, and its introduction came as an individual species, rather than as an entire ecosystem. As a result, the structure and function of a S. alterniflora communities in China's coastal areas are vastly different than in the native range in North America. Chen et al. (2005) found a decrease in the density of benthic animals in S. alterniflora mudflats compared to Scirpus mariqueter mudflats. Furthermore, the invasion of S. alterniflora changed the nutrient structure of the ecosystem by affecting the number of detritivores and herbivores compared to the
crustaceans, etc. (Chung, 1993). However, S. alterniflora can also alter illumination and temperature of the soil surface, which can negatively affect the survival of native benthic animals (Jiang et al., 2016). The impact of S. alterniflora invasion on local benthic fauna is influenced by invasion time (Neira et al., 2007). In Jiangsu province coastal wetland, Spartina-vegetated sediments were found to have lower densities of surface-feeding amphipods, bivalves, cirratulid and spionid polychaetes than that of an adjacent unvegetated tidal flat (Quan et al., 2016). Other studies found that impacts on the benthic community were more complicated at the primary stage of S. alterniflora invasion, with an initial increase in species richness and biomass, followed by a downward trend 5 and 20 years post-invasion (Ge et al., 2012). Spartina alterniflora invasion has the potential to impact higher trophic level animals, as well. In the Chongming wetland of Shanghai, the species and number of birds in the S. alterniflora-vegetated community were much lower than in native reed communities. A highdensity S. alterniflora population can act as an “isolation belt” between birds and their food resources, and also threaten the survival of these resources, such as bivalve species, for birds and fishes (Ma et al., 2017; Lee and Khim, 2016; Cui et al., 2011). Moreover, a S. alterniflora population can competitively exclude native vegetation such as Scirpus mariqueter, which the seeds and underground bulb provide food sources for some waterbirds (Chen et al., 2004). However, S. alterniflora can also provide conditions beneficial to birds. In spring, there are few plants in low tidal flats which can provide habitat for birds. During spring migration, some birds will forage in S. Table 2 Soil organic carbon contents in S. alterniflora salt marshes in China. ID
Location
Latitude
Longitude
Core depth (cm)
Invasion time (year)
Soil carbon concentration (g C kg−1)
Reference
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Yancheng nature reserve Xiaoyang estuary Xinyang wetland1 Xinyang wetland2 Xinyang wetland3 Xinyang wetland4 Wanggang estuary1 Wanggang estuary2 Wanggang estuary3 Yancheng coastal area1 Yancheng coastal area2 Yancheng coastal area3 Yancheng coastal area4 Jiuduansha wetland Dongtan wetland1 Dongtan wetland2 Dongtan wetland3 Hangzhou bay Minjiang estuary1 Minjiang estuary2 Minjiang estuary3
33°34′54”N 33° 3′34”N 33°33′0.97”N 33°32′44”N 33°32′21”N 33°31′42”N 33°10′2.36”N 33°10′12”N 33°10′6”N 33°35′24”N 33°34′42”N 33°35′3”N 33°35′31”N 31°18′44”N 31°31′52”N 31°31′51”N 31°31′51”N 30°18′2”N 26°10′38”N 26°13′54”N 26°12′59”N
120°38′13″E 120°54′26″E 120°41′7″E 120°40′20″E 120°39′3″E 120°36′50″E 120°49′38″E 120°49′5″E 120°49′48″E 120°34′9″E 120°33′39″E 120°32′40″E 120°31′27″E 121°54′25″E 121°59′19″E 121°58′18″E 121°57′30″E 121°22′19″E 119°37′58″E 119°42′45″E 119°46′47″E
0–20 0–20 0–20 0–20 0–20 0–20 0–10 0–10 0–10 0–30 0–30 0–30 0–30 0–40 0–50 0–50 0–50 0–30 0–60 0–60 0–60
10 5 1 3 5 12 8 12 14 3 5 9 12 7 4 6 10 6 4 8 12
6.08 4.79 0.82 ± 0.13 1.55 ± 0.24 7.60 ± 0.22 6.35 ± 0.30 3.67 ± 0.60 4.52 ± 0.51 4.90 ± 0.33 6.2 6.8 7.8 10.2 5.6 10.2–11.5 10.3–15.5 15.6–20.8 6.50 14.3–16.9 16.9–20.2 17.3–23.5
Gao et al., 2007 (Liu et al., 2007) Wang et al., 2013 Wang et al., 2013 Wang et al., 2013 Wang et al., 2013 (Zhang et al., 2010) (Zhang et al., 2010) (Zhang et al., 2010) (Yang et al., 2013) (Yang et al., 2013) (Yang et al., 2013) (Yang et al., 2013) (Cheng et al., 2006) Wang et al., 2015 Wang et al., 2015 Wang et al., 2015 Zhang et al., 2010 Jin et al., 2016 Jin et al., 2016 Jin et al., 2016
5
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
Scirpus mariqueter community (Chen et al., 2005). Xie et al. (2008) found that the time that has elapsed since S. alterniflora invaded can affect the metrics of different biological indicators. In a salt marsh that S. alterniflora invaded ten years prior, the quantity, density, biomass and biodiversity of macrobenthos were higher than in an existing reed community. Currently, the production and habitat provided by S. alterniflora as a species in China is still in its initial stages; the formation of stable S. alterniflora ecosystems and the potential for increased productivity may take much longer.
(Chung et al., 2004). The accretion in salt marshes with S. alterniflora coverage in Jiangsu coastal areas were more than mudflats, and more than 1000 ha land was created each year (Shen, 2001). Given that China has a population of 1.4 billion people, more than 60% of which live in coastal areas, China has altered vast lands through reclamation to meet the needs of urban construction and industrial development. These lands can be protected by S. alterniflora wetlands.
3.4. Processes of nutrient cycling
4.1. Long-term trajectory of S. alterniflora ecosystems in China
Carbon and nitrogen cycling are two basic processes that are regulated by wetland ecosystems. S. alterniflora's longer growth period, greater leaf area index, higher net photosynthesis rate, and greater volume of fine root biomass, as compared to China's native wetland plants (Scirpus mariqueter and Phragmites communis), should increase the carbon loading into the soil, as well as the overall flux across atmospheric and aquatic boundaries (Liao et al., 2010). In Jiangsu province, since the establishment of the S. alterniflora community (a C4 grass), the primary organic carbon source to the soil has been C4 based, rather than C3 based as might be expected from the local native Suaeda glauca (Gao et al., 2012a, 2012b). S. alterniflora dominance could also result in an increase of the nitrogen in the standing biomass stock of China's coastal ecosystems. The roots of S. alterniflora are plentiful and can absorb nitrogen quickly, whereas most native species are not as efficient. Furthermore, the decomposition of stems and leaf sheaths is accompanied by nitrogen fixation, which is also not observed in Scirpus mariqueter and Phragmites communis communities. Further experiments from greenhouse work has shown that processes of microbial epiphytic nitrogen fixation can increase the nitrogen content in S. alterniflora in its aboveground portions (Luo et al., 2006). This presence of N inputs previously absent from the system would affect the existing N content and potential pool size of local coastal wetlands. S. alterniflora can also affect the presence of heavy metals in wetlands, through absorption. However, the leaves of S. alterniflora can also re-release heavy metal ions, making it a source. In general, it is a sink, as shown by a study in Luoyuan Bay of Fujian where there was a higher heavy metal content in sediments surrounding S. alterniflora, as compared with that of background quantity in un-invaded sediments (Gao et al., 2012a, 2012b).
S. alterniflora was first introduced to China to reduce erosion along shorelines. The species became invasive due to its biotic adaptability and the nature of local abiotic conditions. In North America, the species is a keystone species within an integral ecosystem. However, in China, it has broken apart the structure and function of tidal mudflat ecosystems, and the stability of the new ecosystem has not yet been assessed in time or across a broader ecological context. Recently, policy-makers have begun to recognize the harm it has caused, especially in Fujian, Shanghai and Jiangsu provinces. Many measures have been taken to control S. alterniflora, including its removal by fire, mechanical, chemical, or biological methods. In an effort to control it on Chongming Island near Shanghai, the S. alterniflora was surrounded by cofferdams, cut to the ground, and flooded to more than 40 cm. After this procedure, native reeds were added, and salinity and water levels were adjusted to become suitable for them. This project took place in 2010, lasted 3 years, and cost over $160 million USD. Although this removal effort was successful, the cost of this investment was huge, and the immediate impact on the soil structure, benthic animals, and other plants was strongly negative. In general, it is difficult to eradicate an exotic species, after it has successfully established across a broad geographic region. For S. alterniflora, we should begin to consider the future trajectory of coastal ecosystems in China across longer time and spatial scales. Today, scientists and policymakers generally perceive S. alterniflora invasion as negative. Although the first introduction of S. alterniflora was over 50 years ago, this is still quite brief within the context of the evolution of its surrounding ecosystem structure and function. Could a longer period of evaluation eventually show S. alterniflora co-existing with native species and forming a new stable ecosystem? We need work that assesses the effects of S. alterniflora from different perspectives, and across larger spatio-temporal scales, in order to better predict the longterm value of S. alterniflora to China's wetlands. Otherwise, without reconciling the science that was used to justify bringing this species to China, together with the science that says it has been exclusively negative, we are simply like a yo-yo, swinging going back and forth with the newest scientific trend, and without the wisdom of time and context.
4. Discussion
3.5. Flood protection and land creation Plants can dissipate waves, and the wider the width of the plants crossed, the more noticeable the attenuation of wave height (Barbier et al., 2008). S. alterniflora communities have a high density of plants and strong wave damping ability. Knutson et al. (1982) found that the wave energy loss was about 26% for every 1 m of wave entering S. alterniflora, and that the 40 m wide S. alterniflora belt was equivalent to a 2 m high dam. Tests in Zhejiang Province show that the wave damping ability is 97% when the wave of 5 m high passes through the 100 m wide S. alterniflora belt. The wave damping ability of S. alterniflora was 10 times that of the mangrove (Qin et al., 1998). Due to the protection provided by 200 m wide Spartina alterniflora, a 15 km long seawall was well preserved whereas a seawall without S. alterniflora distribution was destroyed (Wan et al., 2009). S. alterniflora reduces erosion and promotes accretion; this was the reason it was originally introduced to China. Stems retard the velocity of the tidal waters that flow past them, causing sediments to drop out of suspention and deposit onto the surface of the wetland (Wan et al., 2009). They also deposit plant materials and organic detritus onto the surface, as well as build subsurface elevation by the production of root biomass. According to a field record taken over 3.4 years, 48.5–52.1 cm of deposition was obtained in the mudflat with S. alterniflora cover whereas only 10.5–16.9 cm was found in areas without S. alterniflora
4.2. Balancing the positive and the negative Overall, we need a more expansive and context-dependent strategy to deal with S. alternilfora, based on targeted opportunities in specific regions of China. For example, in coastal China north of Hangzhou Bay, S. alterniflora marshes have given us a new kind of salt marsh wetland, occupying only a portion of the intertidal zone. However to its south, S. alterniflora marsh is replacing the original salt marsh (Li et al., 2009). Alternately, one could argue that in Zhejiang province and Fujian province, S. alterniflora is necessary to buffer against flooding from rain and waves during typhoon events, whereas this function is less critical in other provinces. For some mariculture farms north of Jiangsu province, we could actively protect and possibly expand S. alterniflora in an effort to purify water and boost food production. The control of S. alterniflora itself can be negative to ecosystem function (particularly with herbicide application), take a long time to complete, and cost a great 6
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
deal, with successes often uncertain (Daehler et al., 1996). We need to better tailor management to the specific needs of each province, and test new biological methods of control (Wang et al., 2008).
Zhao, B., Ma, Z.J., 2009. Spartina alterniflora invasions in the Yangtze River estuary, China: an overview of current status and ecosystem effects. Ecol. Eng. 35, 511–520. Chen, Z., Bo, L., Yang, Z., Chen, J., 2004. Local competitive effects of introduced Spartina alterniflora on Scirpus mariqueter at Dongtan of Chongming Island, the Yangtze River estuary and their potential ecological consequences. Hydrobiologia 528, 99–106. Chen, Z., Fu, C., Wang, H., 2005. Effects of Spartina alterniflora invasions on the benthic macro-onvertebrates community at dongtan of chongming salt marsh, the Yangtze River estuary. Wetland. Sci. 3 (1), 1–7 in Chinese. Chen, Z., Guo, L., Jin, B., Wu, J., Zheng, G., 2009. Effect of the exotic plant Spartina alterniflora on macrobenthos communities in salt marshes of the Yangtze River estuary, China. Estuar. Coast. Shelf Sci. 82, 265–272. Chen, J., Wang, L., Li, Y., Zhang, W., Fu, X., Le, Y., 2012. Effect of Spartina alterniflora invasion and its controlling technologies on soil microbial respiration of a tidal wetland in Chongming Dongtan, China. Ecol. Eng. 41, 52–59. Cheng, X., Luo, Y., Chen, J., Lin, G., Chen, J., Li, B., 2006. Short-term C4 plant Spartina alterniflora invasions change the soil carbon in C3 plant-dominated tidal wetlands on a growing estuarine Island. Soil Biol. Biochem. 38 (12), 3380–3386. Chung, C.-H., 1993. Thirty years of ecological engineering with Spartina plantations in China. Ecol. Eng. 2, 261–289. Chung, C.-H., 2006. Forty years of ecological engineering with Spartina plantations in China. Ecol. Eng. 27, 49–57. Chung, C.H., Zhuo, R.Z., Xu, G.W., 2004. Creation of Spartina plantations for reclaiming Dongtai, China, tidal flats and offshore sands. Ecol. Eng. 23, 135–150. Cui, B.S., He, Q., An, Y., 2011. Spartina alterniflora invasions and effects on crab communities in a western Pacific estuary. Ecol. Eng. 37, 1920–1924. Daehler, C.C., Strong, D.R., Carey, J.R., Moyle, P., Rejmánek, M., Vermeij, G.J., 1996. Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol. Conserv. 78, 51–58. Davis, M., Thompson, K., 2000. Eight ways to be a Colonizer; two ways to be an invader: a Pro- posed nomenclature scheme for invasion ecology. ESA Bull. 81, 226–230. Gallagher, J.L., Reimold, R.J., Linthurst, R.A., Pfeiffer, W.J., 1980. Aerial production, mortality, and mineral accumulation-export dynamics in Spartina alterniflora and Juncus roemerianus plant stands in a Georgia Salt Marsh. Ecology 61, 303–312. Gao, J., Yang, G., Ou, W., 2007. The influence after introduction of Spartina alterniflora on the distribution of TOC, TN and TP in the national Yancheng rare birds nature reserve, Jiangsu Province, China. Geogr. Res. 26 (4), 799–808 (in Chinese). Gao, J., Bai, F., Yang, Y., Gao, S., Liu, Z., Li, J., 2012a. Influence of Spartina Colonization on the supply and accumulation of organic carbon in Tidal Salt Marshes of Northern Jiangsu Province, China. J. Coast. Res. 28, 486–498. Gao, W., Du, Y., Wang, D., Gao, S., 2012b. Distribution patterns of heavy metals in surficial sediment and their influence on the environment quality of the intertidal flat of Luoyuan Bay, Fujian coast. Environ. Sci. 33 (9), 3097–3103 (in Chinese). Gao, J.H., Feng, Z.X., Chen, L., Wang, Y.P., Bai, F., Li, J., 2016. The effect of biomass variations of Spartina alterniflora on the organic carbon content and composition of a salt marsh in northern Jiangsu Province, China. Ecol. Eng. 95, 160–170. Ge, B.M., Bao, Y.X., Cheng, H.Y., Zhang, D.Z., Hu, Z.Y., 2012. Influence of Spartina alterniflora invasion stages on macrobenthic communities on a tidal flat in Wenzhou Bay, China. Braz. J. Oceanogr. 60, 441–448. He, H., Pan, Y., Zhu, W., Liu, X., Zhang, Q., Zhu, X., 2005. Measurement of terrestrial ecosystem service value in China. Chin. J. Appl. Ecol. 16 (6), 1122–1127 (in Chinese). Huang, H., Zhang, L., 2007. A study of the population dynamics of Spartina alterniflora at Jiuduansha shoals, Shanghai, China. Ecol. Eng. 29, 164–172. Jarvis, J.C., Moore, K.A., 2008. Influence of environmental factors on Vallisneria americana seed germination. Aquat. Bot. 88, 283–294. Jiang, L.-F., Luo, Y.-Q., Chen, J.-K., Li, B., 2009. Ecophysiological characteristics of invasive Spartina alterniflora and native species in salt marshes of Yangtze River estuary, China. Estuar. Coast. Shelf Sci. 81, 74–82. Jiang, K., Chen, X., Bao, Y., Haihong, L.I., Shi, W., Wang, H., 2016. Effect of Spartina alterniflora invasion on the vertical structure of macrobenthic community. Acta Ecol. Sin. 36 (2), 535–544 (in Chinese). Jin, B., Gao, D., Yang, P., Wang, W., Zeng, C., 2016. Change of soil organic carbon with different years of Spartina alterniflora invasion in wetlands of Minjiang River estuary. J. Nat. Res. 31 (4), 608–619 (in Chinese). Jing, B., Yan, J.Y., Dong-Jin, H.E., Cai, J.B., Ren, W., You, W.B., 2017. Effects of Spartina alterniflora invasion in eastern Fujian coastal wetland on the physicochemical properties and enzyme activities of mangrove soil. J. Beijing For. Univ. 39 (1), 70–77 (in Chinese). Josselyn, M., Larsson, B., Fiorillo, A., 1993. An Ecological Comparison of an Introduced Marsh Plant, Spartina alterniflora, with its Native Congener, Spartina foliosa, in San Francisco Bay. San Francisco Bay Estuary Project Report, Romberg Tiburon Centers, Tiburon, CA. Francisco Bay. San. Knutson, P.L., Brochu, R.A., Seelig, W.N., Inskeep, M., 1982. Wave damping in Spartina alterniflora, marshes. Wetlands 2 (1), 87–104. Lee, S.Y., Khim, J.S., 2016. Hard science is essential to restoring soft-sediment intertidal habitats in burgeoning East Asia. Chemosphere 168, 765. Levine, J.M., Brewer, J. Stephen, Bertness, Mark D., 1998. Nutrients, competition and plant zonation in a New England salt marsh. J. Ecol. 86, 285–292. Li, H., Zhang, L., 2008. An experimental study on physical controls of an exotic plant Spartina alterniflora in Shanghai, China. Ecol. Eng. 32, 11–21. Li, B., Liao, C., Zhang, X., Chen, H., Wang, Q., Chen, Z., Gan, X., Wu, J., Zhao, B., Ma, Z., Cheng, X., Jiang, L., Chen, J., 2009. Spartina alterniflora invasions in the Yangtze River estuary, China: An overview of current status and ecosystem effects. Ecol. Eng. 35, 511–520. Liao, C., Tang, X., Cheng, X., 2010. Nitrogen dynamics of aerial litter of exotic Spartina alterniflora and native Phragmites australis. Biodivers. Sci. 18 (6), 631–637 (in Chinese).
4.3. Comparison with other invasions Invasion and the domestication of plants have been critical to the evolution of organisms and modern-day ecosystems across the globe. Many studies have focused on invasive species that have caused serious damage in recent years or decades, such as Eichhornia crassipes, Ageratina adenophora, and Chromolaena odorata. In many cases, human activities have encouraged or instigated these invasions (Sang et al., 2008). In the March 2010 Report of the United Nations Convention on Biological Diversity, the United States, Australia, the United Kingdom, South Africa, and China combined were estimated to be losing more than 100 billion dollars a year because of invasive species. However, invasion is the preferred term when the costs exceed the benefits, from a human perspective, and we may instead refer to the same facts as ‘introduction’ when the connotation is more positive. In China, S. alterniflora generally increases carbon deposition, nutrient filtration and cycling processes, vertical accretion, and storm protection. It can reduce habitat value and biodiversity, depending on the invaded ecosystem, but in some cases it can provide forage and benefit some species. We can generally assume that the loss of unvegetated tidal flats is negative for birds, while the gain of vegetated surfaces and detritus enhances fisheries production. In some cases, there may be no great effect; for example, Josselyn et al. (1993) found that S. alterniflora has not significantly changed the structure of benthic fauna in salt marsh in the past 40 years. Still, the jury is out: the long-term of these relatively new ecosystems in China has not been decided. We propose that efforts to eradicate and suppress S. alterniflora in China's coastal wetlands are fighting uphill against a dominant, natural process. Instead, we contend that we should spend more effort to identify the best way to beneficially use these new ecosystems. 5. Conclusion In summary, the introduction of S. alterniflora to China has greatly altered the structure and function of coastal wetlands. Our approach to controlling, promoting, or eradicating S. alterniflora should be conducted with a long-term and context-dependent perspective in order to maximize the ecological cost-benefit calculus for each of China's provinces. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This study was supported by the Grand Science and Technology Special Project of Tianjin (No. 18ZXSZSF00200). The authors would like to thank the editors and anonymous reviewers for their insightful comments and suggestions. References Ayres, D., Smith, D., Zaremba, K., Klohr, S., Strong, D., 2004. Spread of Exotic Cordgrasses And Hybrids (Spartina spp.) in the Tidal Marshes of San Francisco Bay. 6. Biological Invasions, California, USA, pp. 221–231. Barbier, E.B., Koch, E.W., Silliman, B.R., Hacker, S.D., Wolanski, E., Primavera, J., et al., 2008. Coastal ecosystem-based management with nonlinear ecological functions and values. Science 319 (5861), 321–323. Bo, L., Liao, C.H., Zhang, X.D., Chen, H.L., Wang, Q., Chen, Z.Y., Gan, X.J., Wu, J.H.,
7
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
biology, ecology and management. Acta. Phytotax. Sin. 44, 559–588. Wang, Q., Wang, C., Zhao, B., Ma, Z., Luo, Y., Chen, J., et al., 2006b. Effects of growing conditions on the growth of and interactions between salt marsh plants: implications for invasibility of habitats. Biol. Invasions 8 (7), 1547–1560. Wang, G., Qin, P., Wan, S., Zhou, W., Zai, X., Yan, D., 2008. Ecological control and integral utilization of Spartina alterniflora. Ecol. Eng. 32, 249–255. Wang, G., Yang, W., Wang, G., Liu, J., Hang, Z., 2013. The effects of Spartina alterniflora seaward invasion on soil organic carbon fractions, sources and distribution. Acta Ecol. Sin. 33 (8), 2474–2483 (in Chinese). Wang, D., Zhang, R., Xiong, J., Guo, H., Zhao, B., 2015. Contribution of invasive species Spartina alterniflora to soil organic carbon pool in coastal wetland: Stable isotope approach. Chin. J. Plant. Ecol. 39 (10), 941–949 (in Chinese). Windham, L., Ehrenfeld, J.G., 2003. Net Impact of a Plant Invasion on Nitrogen-Cycling Processes within a Brackish Tidal Marsh. Ecol. Appl. 13, 883–896. Xie, Z., He, W., Liu, W., Lu, J., 2008. Influence of Spartina alterniflora salt marsh at its different development stages on bacrobenthos. Chin. J. Plant. Ecol. 27 (1), 63–67 (in Chinese). Yang, W., Zhao, H., Chen, X., Yin, S., Cheng, X., An, S., 2013. Consequences of short-term C4 plant Spartina alterniflora invasions for soil organic carbon dynamics in a coastal wetland of Eastern China. Ecol. Eng. 61, 50–57 Part A. 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. Ecol. Eng. 23, 95–105. Zhang, R., Shen, Y., Lu, L., 2005. Formation of Spartina alterniflora salt marsh on Jiangsu coast of China. Oceanologia et Limnologia Sinica 36, 358–366 (in Chinese). Zhang, D., Yang, M.M., Li, J.X., Chen, X.Y., 2006. Vegetative dispersal ability of Spartina alterniflora in Eastern end of Chongming Island. J. East China Normal Univ. (Nat. Sci.) 2, 130–135 (in Chinese with English abstract). Zhang, Y., Ding, W., Luo, J., Donnison, A., 2010. Changes in soil organic carbon dynamics in an Eastern Chinese coastal wetland following invasion by a C4 plant Spartina alterniflora. Soil Biol. Biochem. 42, 1712–1720. Zhang, W., Zeng, C., Tong, C., Zhang, Z., Huang, J., 2011. Analysis of the Expanding Process of the Spartina alterniflora Salt Marsh in Shanyutan Wetland, Minjiang River Estuary by Remote Sensing. Procedia Environ. Sci. 10, 2472–2477. Zhao, X., Zhao, C., Liu, X., Gong, L., Deng, Z., Li, J., 2015. Growth characteristics and adaptability of Spartina alterniflora in different latitude areas along China coast. Ecol. Sci. 34 (1), 119–128 (in Chinese). Zhu, H., Qin, P., Wang, H., 2004. Functional group classification and target species selection for Yancheng nature reserve, China. Biodivers. Conserv. 13 (7), 1335–1353. Zhu, Z., Zhang, L., Wang, N., Schwarz, C., Ysebaert, T., 2012. Interactions between the range expansion of saltmarsh vegetation and hydrodynamic regimes in the Yangtze Estuary, China. Estuar. Coast. Shelf Sci. 96, 273–279. Zuo, P., Zhao, S., Liu, C., Wang, C., Liang, Y., 2012. Distribution of Spartina spp. along China’s coast. Ecol. Eng. 40, 160–166.
Liu, J., Zhou, H., Qin, P., Zhou, J., 2007. Effects of Spartina alterniflora salt marshes on organic carbon acquisition in intertidal zones of Jiangsu Province, China. Ecol. Eng. 30, 240–249. Lu, J., Zhang, Y., 2013. Spatial distribution of an invasive plant Spartina alterniflora and its potential as biofuels in China. Ecol. Eng. 52, 175–181. Luo, Y., Hui, D., Zhang, D., 2006. Elevated CO₂ stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87, 53–63. Ma, Z., Gan, X., Choi, C., 2014. Effects of invasive cordgrass on presence of Marsh Grassbird in an area where it is not native. Conserv. Biol. 28 (1), 150–158. Ma, Qiang, Wu, Wei, Tang, C., Niu, D., Wu, Jihua, Ma, Zhijun, 2017. Effects of habitat restoration on the diversity of bird and marcobenthos in the Chongming wetland. J. Nanjing For. Univ. 41 (1), 9–14 (in Chinese). Maricle, B.R., Lee, R.W., 2002. Aerenchyma development and oxygen transport in the estuarine cordgrasses Spartina alterniflora and S. anglica. Aquat. Bot. 74, 109–120. Meng, W., He, M., Hu, B., Mo, X., Li, H., Liu, B., et al., 2017. Status of wetlands in China: a review of extent, degradation, issues and recommendations for improvement. Ocean Coast. Manag. 146, 50–59. Meng, W., Feagin, R.A., Hu, B., Wang, Z., Li, H., 2019. The spatial distribution of blue carbon in the coastal wetlands of China. Estuar. Coast. Shelf Sci. 222, 13–20. Neira, C., Levin, L.A., Grosholz, E.D., Mendoza, G., 2007. Influence of invasive Spartina growth stages on associated macrofaunal communities. Biol. Invasions 9, 975–993. Pan, T., Zeng, L., Zeng, C., Wang, W., 2015. Effects of Spartina alterniflora invasion on soil organic carbon in the bare tidal flat wetland of Minjiang River estuary. Sci. Soil. Water. Conserv. 13 (1), 84–90 (in Chinese). Qin, P., Xie, M., Jiang, Y., 1998. Spartina green food ecological engineering1. Ecol. Eng. 11, 147–156. Quan, W., Zhang, H., Wu, Z., Jin, S., Tang, F., Dong, J., 2016. Does invasion of Spartina alterniflora alter microhabitats and benthic communities of salt marshes in Yangtze River estuary? Ecol. Eng. 88, 153–164. Sakai, A., Allendorf, W.F., Holt, J., Lodge, D., Molofsky, J., With, K., Baughman, S., Cabin, J.R., Cohen, J., Ellstrand, C.N., McCauley, E.D., O’Neil, P., Parker, I.N., Thompson, J.G., Weller, S., 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32, 305–332. Sang, W., Feng, J., Xue, D., 2008. Human, ethnical and social insights of biological invasion. J. Cent. Univ. Nation. 17 (4), 17–23 in Chinese. Shen, Y., 2001. The study of the function of the wetlands of Spartina alternifloura manpower salt marsh in Jiangsu. Ecol. Econ. 9, 72–73 (in Chinese). Silliman, B.R., Zieman, J.C., 2001. Top-down control of Spartina alterniflora, production by periwinkle grazing in a Virginia salt marsh. Ecology 82 (10), 2830–2845. Simenstad, C., Thom, R., 1995. Spartina alterniflora(smooth cordgrass) as an invasive halophyte in Pacific northwest estuaries. Hortus Northwest: a Pacific Northwest native plant directory. Journal 6, 9–13. Wan, S., Qin, P., Liu, J., Zhou, H., 2009. The positive and negative effects of exotic Spartina alterniflora in China. Ecol. Eng. 35, 444–452. Wang, Q., An, S., Ma, Z., Zhao, B., Chen, J., Li, B., 2006a. Invasive Spartina alterniflora:
8
Contents lists available at ScienceDirect
Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Review
Invasion and ecological effects of exotic smooth cordgrass Spartina alterniflora in China
T
⁎
Weiqing Menga,b, Rusty A. Feaginb, , Rachel A. Innocentib, Beibei Hua, Mengxuan Hea, Hongyuan Lic a
School of Geographic and Environmental Science, Tianjin Normal University, Tianjin 300387, China Dept. Ecosystem Science and Management, Dept. Ocean Engineering, Texas A&M University, College Station, TX, USA c College of Environment Science and Engineering, Nankai University, Tianjin 300350, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Smooth cordgrass Spartina alterniflora Exotic species Ecological effects China
Smooth cordgrass (Spartina alterniflora) was introduced to China in December 1979 to buffer against tides and to accelerate coastal wetland accretion. Since then, its propagation and natural dispersal have allowed this exotic plant to rapidly expand throughout coastal China with generally negative ecological effects. In 2003 S. alterniflora was labeled as an invasive plant in China, and it now covers ~50,000 ha. In this review, we first summarize the mechanisms of spread and spatial distribution of S. alterniflora, and how its physiological characteristics and strong adaptability to the available niche space in China's wetlands have enabled its spread and competition with native plants. Then we review the effects of S. alterniflora on ecosystem function in terms of habitat conversion and the alteration of biodiversity, soil carbon flux and sequestration, and various processes of nutrient regulation. We conclude that we need a long-term and context-dependent perspective, in order to maximize the benefits and minimize the costs of S. alterniflora within each of China's unique provinces.
1. Introduction Smooth cordgrass (Spartina alterniflora) is a perennial grass that is native to the Atlantic coast of the Americas, ranging from Canada to Argentina. It has been introduced to many coastal regions throughout Europe, Australia, and Asia, primarily for mitigating coastal wetland erosion, which it does by reducing tidal wave energy, trapping sediments, and promoting vertical accretion (Chung, 1993; Maricle and Lee, 2002). Coastal erosion can occur through many processes. Daily erosion occurs when waves wear away the shoreline, and it can pose a serious threat to the infrastructure and resources of coastal communities. Historically, people have built sea walls to resist erosion, but this method is expensive and can even exacerbate the problem by robbing sediment supply to beaches. More recently, people have shifted to the use of natural solutions to coastal erosion that mitigate sediment loss and foster ecosystem function. For this reason, Spartina alterniflora was introduced to China. The first successful seed germination of S. alterniflora in China was carried out in December 1979 by the botanical garden of Nanjing University, using plants from the United States' Atlantic Coast. The species was then transplanted to Luoyuan County, Fujian province onto barren mudflats to defend against storm surges. A lack of survey data ⁎
prevents us from knowing the initial degradation level of this affected habitat, but from the description in the relevant literature, the participants had not expected the forthcoming negative ecological effects (potentially due to the lack of information about an ecological invasion at the time) (Chung, 1993, 2006). Both further plantings and natural dispersal, paired with the S. alterniflora's environmental adaptability and strong reproductive capacity, allowed it to expand rapidly throughout China's coastal zone. In 1985, the area of S. alterniflora in China was ~260 ha. In 2003, S. alterniflora was included in the first list of exotic invasive plants jointly issued by the State Environment Protection Administration of China and Chinese Academy of Sciences (Wang et al., 2006a, 2006b). By 2007, it covered 34,178 ha, with the population in the coastal areas of Jiangsu accounting for more than 52% of this total (17,842 ha; Lu and Zhang, 2013). Today, S. alterniflora has expanded to around 50,000 ha of the coastal regions of China. The spread of smooth cordgrass has already altered aspects of Chinese wetlands including productivity, soil water content, hydrodynamics, sedimentary processes, soil formation, and accumulation of nutrients. The positive versus negative effects of these changes vary by location and habitat condition. For example, S. alterniflora plays an important positive role in shoreline protection in some regions, whereas in others, it has caused damage to maricultural activities (Chen et al.,
Corresponding author. E-mail address: [email protected] (R.A. Feagin).
https://doi.org/10.1016/j.ecoleng.2019.105670 Received 3 September 2018; Received in revised form 21 October 2019; Accepted 15 November 2019 0925-8574/ © 2019 Elsevier B.V. All rights reserved.
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
2.2. Expansion of S. alterniflora
2009; Gao et al., 2016; Wan et al., 2009). Many researchers have discussed its benefits and drawbacks as well as its population dynamics and control (Chen et al., 2012; Chung et al., 2004; Jiang et al., 2009; Wang et al., 2008). Here, we seek to review the progress of S. alterniflora research. We discuss the effect of this species on coastal wetland ecosystems in China, and whether it was inevitable that S. alterniflora would become ‘invasive’ as a function of the relevant aspects of its physiology. We also discuss how to best capitalize on the positive effects of Spartina alterniflora while also controlling its negative effects.
S. alterniflora grows well in China: the average aboveground biomass and belowground biomass of a mature S. alterniflora community in the Yellow River Delta in 1998 was 2657 and 3517 g/m2 respectively (Qin et al., 1998). Biological invasions often exhibit a lag time between colonization and the time that rapid population growth begins (Sakai et al., 2001). After initial colonization and establishment, S. alterniflora may increase in coverage by short distance growth via runners and rhizomes or long distance dispersal via seeds (Davis and Thompson, 2000; Huang and Zhang, 2007). One study in San Francisco Bay showed that S. alterniflora had an exponential increase in cover and a constant areal expansion rate of 18–20% (Ayres et al., 2004). At the coast of Jiangsu province, China, the initial colonization and establishment phase was completed in the period 1993–1995 with an annual expansion rate of 30%. S. alterniflora began to rapidly spread approximately in the year 2000, with annual increases of 43% between 1999 and 2001 (Zhang et al., 2004; Huang and Zhang, 2007). S. alterniflora reproduces quite easily and at a high rate of success. It also has a quite wide niche, given the stressful saltwater environment in which few other species live (Huang and Zhang, 2007). One individual of S. alterniflora in Chongming Island near Shanghai was found to produce 86–222 tillers (Zhang et al., 2006). The fast reproductive rate and rapid range expansion of S. alterniflora gives the species its competitive edge over native species and facilitates its invasion (Li and Zhang, 2008). We summarize the invasion mechanism of S. alterniflora in China as a function of both biotic factors and abiotic factors (Fig. 2). Of these, the biotic characteristics of S. alterniflora are the most important factors for its invasion success. Strong reproductive capacity and tolerance to environmental conditions such as high salinity and flooding makes S. alterniflora a successful competitor over native species (Jarvis and Moore, 2008). Of the abiotic factors linked with invasion, the purposeful introduction is the most obvious factor; it can be assumed invasion would not have happened if the species had not been introduced. Further establishment of S. alterniflora was affected by its seeds' ability to float with the tide and be carried away from the location of initial introduction (Ayres et al., 2004). Human use of coastal habitat has an indirect promoting effect on invasion success, as well. Nitrogen inputs to the environment from agricultural runoff, industry, and pollution, paired with the strong nitrogen utilization of S. alterniflora inevitably contributes to its growth and adaptability. Invasion rates differ according to ecosystem and the niche space available for S. alterniflora. For example, within systems of competitive reeds (like Phragmites communis) and mangroves, S. alterniflora invasion is relatively slow compared to invasion within Scirpus mariqueter communities: once S. alterniflora invades, it can form patches with a diameter of 1–2 m in a growing season. Patches expand and, in 2–3 years,
2. Spread mechanism and distribution of S. alterniflora 2.1. Physiognomic and physiological characteristics Spartina alterniflora has stiff, erect stems, with maximum 11 nodes each, which can reach more than 2.0 m tall and 1.2 cm in diameter. Its leaves extend approximately 50 cm long and 2 cm wide (Wan et al., 2009). The species propagates both sexually via seeds and asexually by tillers and rhizomes which gives it a fast rate of geographic spread (Huang and Zhang, 2007). Under suitable conditions, S. alterniflora can reach sexual maturity within 3–4 months, and the length of its inflorescence is related to its geographical location in China. The seed survival time is estimated to be only eight months, suggesting that there is no long-lasting seed bank in the soil. As the dominant marsh plant species in many coastal wetlands in China and at other locations, the species grows in a wide range of salinities (from about 5–32 psu); however, salt-tolerant germination tests show the germination rate of seeds decreases with increased salinity (Qin et al., 1998). Elongation of the rhizome is very fast, with one study indicating the transverse elongation of the rhizome to be 0.5–1.7 m per year on the tidal flat of Washington (Simenstad and Thom, 1995). The adaptation of S. alterniflora to its abiotic environment is mainly characterized by its high tolerance and adaptation to environmental stresses. S. alterniflora has a stronger tolerance to the stress of a salt marsh than Phragmites australis, Spartina patens, Scirpus robustus, and Scirpus mariqueter (Chen et al., 2004) as well as to flooding on the lower elevations of tidal flats, which is an important factor for its successful invasion (Fig. 1). It has aerenchyma, making it suitably adapted to the anoxic environment. Although excessive inundation inhibits the growth of S. alterniflora, some flooding has been shown to promote its growth, with research showing the fastest leaf growth rate of S. alterniflora under flooding of 30 days duration (Levine, 1998). S. alterniflora can also absorb different forms of nitrogen such as ammonium nitrogen and nitrate nitrogen, and the biomass of S. alterniflora is positively correlated with nitrogen concentration.
Fig. 1. The niche of S. alterniflora location in China's coastal wetland. 2
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
Fig. 2. Invasion mechanism of S. alterniflora in China.
3. Ecological effects of Spartina alterniflora invasion
connect with other S. alterniflora patches to form the dominant community. Some studies showed that the change of ecological factors can change the competitive situation between the reed and S. alterniflora, and further affect the distribution of S. alterniflora and reed on the coastal wetlands. With higher salinity (1%–2%), S. alterniflora has competitive ability, while at lower salinity (less than 0.5%), reeds have superior competitive ability (Wang et al., 2006a, 2006b). On the southern coast of China, woody mangroves, shrubs and trees are present; however, very few native salt marsh macrophytes can persist on China's northern coast (Wan et al., 2009). Suaeda is the dominant native intertidal vegetation in China's northern coastal wetlands, but its smaller height and biomass compared to S. alterniflora results in weak competitiveness for light. The long-distance dispersal capability of S. alterniflora and the absence of a similar species occupying its niche in the north played a strong role. Only then was the rapid expansion of S. alterniflora facilitated by its suitability to abiotic factors such as climate, substrate, and geomorphic context (Huang and Zhang, 2007).
3.1. Soil carbon The soil organic carbon (SOC) content of China's wetlands decreases with an increase in latitude (Table 2; see also Meng et al., 2019). This pattern is most evident in the Minjiang estuary wetlands. Moreover, SOC in these wetlands decreases rapidly with increasing depth within the 0–10 cm, but past this range, there is no obvious change (Gao et al., 2007). This pattern results in the SOC concentration in bottom layer being nearly 7 times less than that of the surface in Minjiang river estuary (Cheng et al., 2006; Pan et al., 2015), possibly due to the strong hydrodynamic processes of the estuary, which can have significant effects on the soil organic carbon content. Invasion of S. alterniflora in coastal regions alters ecosystem structure and nutrient cycling processes, thereby affecting these soil C pools (Windham and Ehrenfeld, 2003; Zhang et al., 2010). One study in the coastal wetland of Jiangsu province showed that after an 8 to 14-year invasion time-frame of S. alterniflora, the SOC increased by 27.0–69.6% and N content by 21.8–55.2% in the upper 0–10 cm soil layer, as compared to the native Sueda salsa (Zhang et al., 2010). The ability of S. alterniflora to sequester carbon is mainly a function of two features: its high biomass and deposition rate. According to photosynthesis reaction equations, the annual carbon sequestration capacity of S. alterniflora is 2274 g·m−2·yr−1, which is 4.6 times of the average value of Chinese vegetation (494 g·m−2·yr−1) (He et al., 2005). The SOC concentration in Eastern Chinese coastal wetlands increased remarkably at the 0–10 cm depth during the period of plant invasion and varied from 3.67 to 4.90 g SOC / kg of soil (Zhang et al., 2010). Unique ecosystem properties cause the soil organic carbon content to vary spatially and temporally, in some cases even within the same area. Standing native plants, latitude, hydrological conditions, time since invasion, and sampling depth are thought to be major contributors to differences in SOC distribution of S. alterniflora wetlands. When the plants invaded bare flat and native C3 plant communities such as Sueda salsa and Cyperus malaccensis, SOC was significantly increased in the upper 0–30 cm soil layer (Yang et al., 2013). However,
2.3. Current spatial distribution of S. alterniflora in China The spatial distribution of S. alterniflora in China's coastal zones was qualitatively mapped based on information from existing literature, particularly a large governmental effort as described in Meng et al. (2017) (Fig. 3). Almost 40 years after being introduced to the country, S. alterniflora has spread to all Chinese coastal areas, covering a total area of 35,889 ha (Table 1, Fig. 3). The species is most prominent in Jiangsu, Shanghai, Fujian and Zhejiang with growth patterns mainly shaped by temperature, with some influence from precipitation (Zhao et al., 2015). The area of S. alterniflora in the four provinces makes up 92.81% of the distribution. In the Jiangsu coastal zone, the area of S. alterniflora was 18,711 ha, constituting 52.14% of the S. alterniflora coverage in China. Our conservative estimate of the area of S. alterniflora distribution in Chinese coastal zones at present is greater than 5 × 104 ha; however, the area of S. alterniflora is sure to increase due to the species' rapid spread rate.
3
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
Fig. 3. Spatial distribution S. alterniflora in china's coastal zones.
and type of habitat involved. The biotic characteristics and strong adaptability of S. alterniflora cause it to spread and out-compete native plants for growth space. In the MinJiang estuary wetland of Fujian province, the expansion speed of S. alterniflora was rapid; within three years, S. alterniflora seized the habitats of native plants and became the dominant species, resulting in a great loss of vegetative biodiversity (Zhang et al., 2011). S. alterniflora also alters benthic animal communities. Benthic fauna is easily influenced by changes of vegetation and soil characteristics, and the community structure of benthic fauna needs a long time to restore after being destroyed (Quan et al., 2016). S. alterniflora can improve physical and chemical properties of sediment for benthic animals, and its roots, stems and leaves can provide food for mollusks,
invasion in mangrove ecosystems produced the opposite effect (Jing et al., 2017). Another investigation of S. alterniflora along the Chinese coast showed significant differences in individual and population traits among twenty-six populations were closely related to latitude. Plant height, inter-node length, basal stem diameter, and plant biomass increased initially and then decreased with increasing latitude and the productivity of S. alterniflora gradually decreased as the latitude increased (Zhang et al., 2010; Zhao et al., 2015).
3.2. Biodiversity The invasive nature of S. alterniflora in China's coastal wetlands can have different effects on biodiversity depending on the location, age, 4
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
alterniflora communities and they offer shelter against predation (Zhu et al., 2004). These birds have adapted to the transformation of natural habitats by S. alterniflora invasion, such as the marsh grassbird (Locustella pryeri) for which S. alterniflora communities are important habitats (Ma et al., 2014). As a pioneer plant, S. alterniflora can grow in mudflats where other vegetation cannot and facilitate the succession of plants such as mangroves, which provide nesting areas for birds. For these reasons, the invasion of S. alterniflora and its potential impacts on biodiversity throughout the trophic levels is a topic that warrants further research.
Table 1 The area and proportion of S. alterniflora in Chinese provinces (ha). Province
Area (ha)
Proportion (%)
Liaoning Hebei Tianjin Shandong Jiangsu Shanghai Zhejiang Fujian Guangdong Guangxi Total
57 474 570 686 18,711 5336 5092 4166 546 251 35,889
0.16 1.32 1.59 1.91 52.14 14.87 14.19 11.61 1.52 0.70 100.00
3.3. Habitats
Data source: (Wang et al., 2008; Wan et al., 2009; Zuo et al., 2012; Lu and Zhang, 2013).
One way S. alterniflora alters China's wetland habitats is by competitive exclusion. With the introduction of the species to the Yangtze estuary in 1990, S. alterniflora out-competed native Scirpus mariqueter and Phragmites communis, resulting in the original pioneer species of Scirpus mariqueter being replaced at ChongMing Island (Bo et al., 2009; Zhu et al., 2012). However, S. alterniflora also impacts China's wetlands by creating radically different habitats and elevations from previously unvegetated mudflats. On the coast of Jiangsu province, the ecological niche of S. alterniflora is the upper part of the tidal estuarine beach, historically unoccupied by plants; S. alterniflora quickly populates these areas void of competition (Zhang et al., 2005). The growth of S. alterniflora into unvegetated areas causes the addition of highly productive habitat for tidal animals; however, if the intertidal zone is too narrow, this expansion can further threaten the survival of the local ecosystem. In their native range in the Americas, S. alterniflora salt marshes are one of the most productive ecosystems. The species is dominant in the coastal intertidal zone because of its ability to adapt to various types of soil, salinity, and hydrology (Gallagher et al., 1980). It is important directly and indirectly to food sources such as benthic animals and insects, and provides a place for waterfowl to inhabit and forage (Silliman and Zieman, 2001). For China, S. alterniflora is an exotic species, and its introduction came as an individual species, rather than as an entire ecosystem. As a result, the structure and function of a S. alterniflora communities in China's coastal areas are vastly different than in the native range in North America. Chen et al. (2005) found a decrease in the density of benthic animals in S. alterniflora mudflats compared to Scirpus mariqueter mudflats. Furthermore, the invasion of S. alterniflora changed the nutrient structure of the ecosystem by affecting the number of detritivores and herbivores compared to the
crustaceans, etc. (Chung, 1993). However, S. alterniflora can also alter illumination and temperature of the soil surface, which can negatively affect the survival of native benthic animals (Jiang et al., 2016). The impact of S. alterniflora invasion on local benthic fauna is influenced by invasion time (Neira et al., 2007). In Jiangsu province coastal wetland, Spartina-vegetated sediments were found to have lower densities of surface-feeding amphipods, bivalves, cirratulid and spionid polychaetes than that of an adjacent unvegetated tidal flat (Quan et al., 2016). Other studies found that impacts on the benthic community were more complicated at the primary stage of S. alterniflora invasion, with an initial increase in species richness and biomass, followed by a downward trend 5 and 20 years post-invasion (Ge et al., 2012). Spartina alterniflora invasion has the potential to impact higher trophic level animals, as well. In the Chongming wetland of Shanghai, the species and number of birds in the S. alterniflora-vegetated community were much lower than in native reed communities. A highdensity S. alterniflora population can act as an “isolation belt” between birds and their food resources, and also threaten the survival of these resources, such as bivalve species, for birds and fishes (Ma et al., 2017; Lee and Khim, 2016; Cui et al., 2011). Moreover, a S. alterniflora population can competitively exclude native vegetation such as Scirpus mariqueter, which the seeds and underground bulb provide food sources for some waterbirds (Chen et al., 2004). However, S. alterniflora can also provide conditions beneficial to birds. In spring, there are few plants in low tidal flats which can provide habitat for birds. During spring migration, some birds will forage in S. Table 2 Soil organic carbon contents in S. alterniflora salt marshes in China. ID
Location
Latitude
Longitude
Core depth (cm)
Invasion time (year)
Soil carbon concentration (g C kg−1)
Reference
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
Yancheng nature reserve Xiaoyang estuary Xinyang wetland1 Xinyang wetland2 Xinyang wetland3 Xinyang wetland4 Wanggang estuary1 Wanggang estuary2 Wanggang estuary3 Yancheng coastal area1 Yancheng coastal area2 Yancheng coastal area3 Yancheng coastal area4 Jiuduansha wetland Dongtan wetland1 Dongtan wetland2 Dongtan wetland3 Hangzhou bay Minjiang estuary1 Minjiang estuary2 Minjiang estuary3
33°34′54”N 33° 3′34”N 33°33′0.97”N 33°32′44”N 33°32′21”N 33°31′42”N 33°10′2.36”N 33°10′12”N 33°10′6”N 33°35′24”N 33°34′42”N 33°35′3”N 33°35′31”N 31°18′44”N 31°31′52”N 31°31′51”N 31°31′51”N 30°18′2”N 26°10′38”N 26°13′54”N 26°12′59”N
120°38′13″E 120°54′26″E 120°41′7″E 120°40′20″E 120°39′3″E 120°36′50″E 120°49′38″E 120°49′5″E 120°49′48″E 120°34′9″E 120°33′39″E 120°32′40″E 120°31′27″E 121°54′25″E 121°59′19″E 121°58′18″E 121°57′30″E 121°22′19″E 119°37′58″E 119°42′45″E 119°46′47″E
0–20 0–20 0–20 0–20 0–20 0–20 0–10 0–10 0–10 0–30 0–30 0–30 0–30 0–40 0–50 0–50 0–50 0–30 0–60 0–60 0–60
10 5 1 3 5 12 8 12 14 3 5 9 12 7 4 6 10 6 4 8 12
6.08 4.79 0.82 ± 0.13 1.55 ± 0.24 7.60 ± 0.22 6.35 ± 0.30 3.67 ± 0.60 4.52 ± 0.51 4.90 ± 0.33 6.2 6.8 7.8 10.2 5.6 10.2–11.5 10.3–15.5 15.6–20.8 6.50 14.3–16.9 16.9–20.2 17.3–23.5
Gao et al., 2007 (Liu et al., 2007) Wang et al., 2013 Wang et al., 2013 Wang et al., 2013 Wang et al., 2013 (Zhang et al., 2010) (Zhang et al., 2010) (Zhang et al., 2010) (Yang et al., 2013) (Yang et al., 2013) (Yang et al., 2013) (Yang et al., 2013) (Cheng et al., 2006) Wang et al., 2015 Wang et al., 2015 Wang et al., 2015 Zhang et al., 2010 Jin et al., 2016 Jin et al., 2016 Jin et al., 2016
5
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
Scirpus mariqueter community (Chen et al., 2005). Xie et al. (2008) found that the time that has elapsed since S. alterniflora invaded can affect the metrics of different biological indicators. In a salt marsh that S. alterniflora invaded ten years prior, the quantity, density, biomass and biodiversity of macrobenthos were higher than in an existing reed community. Currently, the production and habitat provided by S. alterniflora as a species in China is still in its initial stages; the formation of stable S. alterniflora ecosystems and the potential for increased productivity may take much longer.
(Chung et al., 2004). The accretion in salt marshes with S. alterniflora coverage in Jiangsu coastal areas were more than mudflats, and more than 1000 ha land was created each year (Shen, 2001). Given that China has a population of 1.4 billion people, more than 60% of which live in coastal areas, China has altered vast lands through reclamation to meet the needs of urban construction and industrial development. These lands can be protected by S. alterniflora wetlands.
3.4. Processes of nutrient cycling
4.1. Long-term trajectory of S. alterniflora ecosystems in China
Carbon and nitrogen cycling are two basic processes that are regulated by wetland ecosystems. S. alterniflora's longer growth period, greater leaf area index, higher net photosynthesis rate, and greater volume of fine root biomass, as compared to China's native wetland plants (Scirpus mariqueter and Phragmites communis), should increase the carbon loading into the soil, as well as the overall flux across atmospheric and aquatic boundaries (Liao et al., 2010). In Jiangsu province, since the establishment of the S. alterniflora community (a C4 grass), the primary organic carbon source to the soil has been C4 based, rather than C3 based as might be expected from the local native Suaeda glauca (Gao et al., 2012a, 2012b). S. alterniflora dominance could also result in an increase of the nitrogen in the standing biomass stock of China's coastal ecosystems. The roots of S. alterniflora are plentiful and can absorb nitrogen quickly, whereas most native species are not as efficient. Furthermore, the decomposition of stems and leaf sheaths is accompanied by nitrogen fixation, which is also not observed in Scirpus mariqueter and Phragmites communis communities. Further experiments from greenhouse work has shown that processes of microbial epiphytic nitrogen fixation can increase the nitrogen content in S. alterniflora in its aboveground portions (Luo et al., 2006). This presence of N inputs previously absent from the system would affect the existing N content and potential pool size of local coastal wetlands. S. alterniflora can also affect the presence of heavy metals in wetlands, through absorption. However, the leaves of S. alterniflora can also re-release heavy metal ions, making it a source. In general, it is a sink, as shown by a study in Luoyuan Bay of Fujian where there was a higher heavy metal content in sediments surrounding S. alterniflora, as compared with that of background quantity in un-invaded sediments (Gao et al., 2012a, 2012b).
S. alterniflora was first introduced to China to reduce erosion along shorelines. The species became invasive due to its biotic adaptability and the nature of local abiotic conditions. In North America, the species is a keystone species within an integral ecosystem. However, in China, it has broken apart the structure and function of tidal mudflat ecosystems, and the stability of the new ecosystem has not yet been assessed in time or across a broader ecological context. Recently, policy-makers have begun to recognize the harm it has caused, especially in Fujian, Shanghai and Jiangsu provinces. Many measures have been taken to control S. alterniflora, including its removal by fire, mechanical, chemical, or biological methods. In an effort to control it on Chongming Island near Shanghai, the S. alterniflora was surrounded by cofferdams, cut to the ground, and flooded to more than 40 cm. After this procedure, native reeds were added, and salinity and water levels were adjusted to become suitable for them. This project took place in 2010, lasted 3 years, and cost over $160 million USD. Although this removal effort was successful, the cost of this investment was huge, and the immediate impact on the soil structure, benthic animals, and other plants was strongly negative. In general, it is difficult to eradicate an exotic species, after it has successfully established across a broad geographic region. For S. alterniflora, we should begin to consider the future trajectory of coastal ecosystems in China across longer time and spatial scales. Today, scientists and policymakers generally perceive S. alterniflora invasion as negative. Although the first introduction of S. alterniflora was over 50 years ago, this is still quite brief within the context of the evolution of its surrounding ecosystem structure and function. Could a longer period of evaluation eventually show S. alterniflora co-existing with native species and forming a new stable ecosystem? We need work that assesses the effects of S. alterniflora from different perspectives, and across larger spatio-temporal scales, in order to better predict the longterm value of S. alterniflora to China's wetlands. Otherwise, without reconciling the science that was used to justify bringing this species to China, together with the science that says it has been exclusively negative, we are simply like a yo-yo, swinging going back and forth with the newest scientific trend, and without the wisdom of time and context.
4. Discussion
3.5. Flood protection and land creation Plants can dissipate waves, and the wider the width of the plants crossed, the more noticeable the attenuation of wave height (Barbier et al., 2008). S. alterniflora communities have a high density of plants and strong wave damping ability. Knutson et al. (1982) found that the wave energy loss was about 26% for every 1 m of wave entering S. alterniflora, and that the 40 m wide S. alterniflora belt was equivalent to a 2 m high dam. Tests in Zhejiang Province show that the wave damping ability is 97% when the wave of 5 m high passes through the 100 m wide S. alterniflora belt. The wave damping ability of S. alterniflora was 10 times that of the mangrove (Qin et al., 1998). Due to the protection provided by 200 m wide Spartina alterniflora, a 15 km long seawall was well preserved whereas a seawall without S. alterniflora distribution was destroyed (Wan et al., 2009). S. alterniflora reduces erosion and promotes accretion; this was the reason it was originally introduced to China. Stems retard the velocity of the tidal waters that flow past them, causing sediments to drop out of suspention and deposit onto the surface of the wetland (Wan et al., 2009). They also deposit plant materials and organic detritus onto the surface, as well as build subsurface elevation by the production of root biomass. According to a field record taken over 3.4 years, 48.5–52.1 cm of deposition was obtained in the mudflat with S. alterniflora cover whereas only 10.5–16.9 cm was found in areas without S. alterniflora
4.2. Balancing the positive and the negative Overall, we need a more expansive and context-dependent strategy to deal with S. alternilfora, based on targeted opportunities in specific regions of China. For example, in coastal China north of Hangzhou Bay, S. alterniflora marshes have given us a new kind of salt marsh wetland, occupying only a portion of the intertidal zone. However to its south, S. alterniflora marsh is replacing the original salt marsh (Li et al., 2009). Alternately, one could argue that in Zhejiang province and Fujian province, S. alterniflora is necessary to buffer against flooding from rain and waves during typhoon events, whereas this function is less critical in other provinces. For some mariculture farms north of Jiangsu province, we could actively protect and possibly expand S. alterniflora in an effort to purify water and boost food production. The control of S. alterniflora itself can be negative to ecosystem function (particularly with herbicide application), take a long time to complete, and cost a great 6
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
deal, with successes often uncertain (Daehler et al., 1996). We need to better tailor management to the specific needs of each province, and test new biological methods of control (Wang et al., 2008).
Zhao, B., Ma, Z.J., 2009. Spartina alterniflora invasions in the Yangtze River estuary, China: an overview of current status and ecosystem effects. Ecol. Eng. 35, 511–520. Chen, Z., Bo, L., Yang, Z., Chen, J., 2004. Local competitive effects of introduced Spartina alterniflora on Scirpus mariqueter at Dongtan of Chongming Island, the Yangtze River estuary and their potential ecological consequences. Hydrobiologia 528, 99–106. Chen, Z., Fu, C., Wang, H., 2005. Effects of Spartina alterniflora invasions on the benthic macro-onvertebrates community at dongtan of chongming salt marsh, the Yangtze River estuary. Wetland. Sci. 3 (1), 1–7 in Chinese. Chen, Z., Guo, L., Jin, B., Wu, J., Zheng, G., 2009. Effect of the exotic plant Spartina alterniflora on macrobenthos communities in salt marshes of the Yangtze River estuary, China. Estuar. Coast. Shelf Sci. 82, 265–272. Chen, J., Wang, L., Li, Y., Zhang, W., Fu, X., Le, Y., 2012. Effect of Spartina alterniflora invasion and its controlling technologies on soil microbial respiration of a tidal wetland in Chongming Dongtan, China. Ecol. Eng. 41, 52–59. Cheng, X., Luo, Y., Chen, J., Lin, G., Chen, J., Li, B., 2006. Short-term C4 plant Spartina alterniflora invasions change the soil carbon in C3 plant-dominated tidal wetlands on a growing estuarine Island. Soil Biol. Biochem. 38 (12), 3380–3386. Chung, C.-H., 1993. Thirty years of ecological engineering with Spartina plantations in China. Ecol. Eng. 2, 261–289. Chung, C.-H., 2006. Forty years of ecological engineering with Spartina plantations in China. Ecol. Eng. 27, 49–57. Chung, C.H., Zhuo, R.Z., Xu, G.W., 2004. Creation of Spartina plantations for reclaiming Dongtai, China, tidal flats and offshore sands. Ecol. Eng. 23, 135–150. Cui, B.S., He, Q., An, Y., 2011. Spartina alterniflora invasions and effects on crab communities in a western Pacific estuary. Ecol. Eng. 37, 1920–1924. Daehler, C.C., Strong, D.R., Carey, J.R., Moyle, P., Rejmánek, M., Vermeij, G.J., 1996. Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol. Conserv. 78, 51–58. Davis, M., Thompson, K., 2000. Eight ways to be a Colonizer; two ways to be an invader: a Pro- posed nomenclature scheme for invasion ecology. ESA Bull. 81, 226–230. Gallagher, J.L., Reimold, R.J., Linthurst, R.A., Pfeiffer, W.J., 1980. Aerial production, mortality, and mineral accumulation-export dynamics in Spartina alterniflora and Juncus roemerianus plant stands in a Georgia Salt Marsh. Ecology 61, 303–312. Gao, J., Yang, G., Ou, W., 2007. The influence after introduction of Spartina alterniflora on the distribution of TOC, TN and TP in the national Yancheng rare birds nature reserve, Jiangsu Province, China. Geogr. Res. 26 (4), 799–808 (in Chinese). Gao, J., Bai, F., Yang, Y., Gao, S., Liu, Z., Li, J., 2012a. Influence of Spartina Colonization on the supply and accumulation of organic carbon in Tidal Salt Marshes of Northern Jiangsu Province, China. J. Coast. Res. 28, 486–498. Gao, W., Du, Y., Wang, D., Gao, S., 2012b. Distribution patterns of heavy metals in surficial sediment and their influence on the environment quality of the intertidal flat of Luoyuan Bay, Fujian coast. Environ. Sci. 33 (9), 3097–3103 (in Chinese). Gao, J.H., Feng, Z.X., Chen, L., Wang, Y.P., Bai, F., Li, J., 2016. The effect of biomass variations of Spartina alterniflora on the organic carbon content and composition of a salt marsh in northern Jiangsu Province, China. Ecol. Eng. 95, 160–170. Ge, B.M., Bao, Y.X., Cheng, H.Y., Zhang, D.Z., Hu, Z.Y., 2012. Influence of Spartina alterniflora invasion stages on macrobenthic communities on a tidal flat in Wenzhou Bay, China. Braz. J. Oceanogr. 60, 441–448. He, H., Pan, Y., Zhu, W., Liu, X., Zhang, Q., Zhu, X., 2005. Measurement of terrestrial ecosystem service value in China. Chin. J. Appl. Ecol. 16 (6), 1122–1127 (in Chinese). Huang, H., Zhang, L., 2007. A study of the population dynamics of Spartina alterniflora at Jiuduansha shoals, Shanghai, China. Ecol. Eng. 29, 164–172. Jarvis, J.C., Moore, K.A., 2008. Influence of environmental factors on Vallisneria americana seed germination. Aquat. Bot. 88, 283–294. Jiang, L.-F., Luo, Y.-Q., Chen, J.-K., Li, B., 2009. Ecophysiological characteristics of invasive Spartina alterniflora and native species in salt marshes of Yangtze River estuary, China. Estuar. Coast. Shelf Sci. 81, 74–82. Jiang, K., Chen, X., Bao, Y., Haihong, L.I., Shi, W., Wang, H., 2016. Effect of Spartina alterniflora invasion on the vertical structure of macrobenthic community. Acta Ecol. Sin. 36 (2), 535–544 (in Chinese). Jin, B., Gao, D., Yang, P., Wang, W., Zeng, C., 2016. Change of soil organic carbon with different years of Spartina alterniflora invasion in wetlands of Minjiang River estuary. J. Nat. Res. 31 (4), 608–619 (in Chinese). Jing, B., Yan, J.Y., Dong-Jin, H.E., Cai, J.B., Ren, W., You, W.B., 2017. Effects of Spartina alterniflora invasion in eastern Fujian coastal wetland on the physicochemical properties and enzyme activities of mangrove soil. J. Beijing For. Univ. 39 (1), 70–77 (in Chinese). Josselyn, M., Larsson, B., Fiorillo, A., 1993. An Ecological Comparison of an Introduced Marsh Plant, Spartina alterniflora, with its Native Congener, Spartina foliosa, in San Francisco Bay. San Francisco Bay Estuary Project Report, Romberg Tiburon Centers, Tiburon, CA. Francisco Bay. San. Knutson, P.L., Brochu, R.A., Seelig, W.N., Inskeep, M., 1982. Wave damping in Spartina alterniflora, marshes. Wetlands 2 (1), 87–104. Lee, S.Y., Khim, J.S., 2016. Hard science is essential to restoring soft-sediment intertidal habitats in burgeoning East Asia. Chemosphere 168, 765. Levine, J.M., Brewer, J. Stephen, Bertness, Mark D., 1998. Nutrients, competition and plant zonation in a New England salt marsh. J. Ecol. 86, 285–292. Li, H., Zhang, L., 2008. An experimental study on physical controls of an exotic plant Spartina alterniflora in Shanghai, China. Ecol. Eng. 32, 11–21. Li, B., Liao, C., Zhang, X., Chen, H., Wang, Q., Chen, Z., Gan, X., Wu, J., Zhao, B., Ma, Z., Cheng, X., Jiang, L., Chen, J., 2009. Spartina alterniflora invasions in the Yangtze River estuary, China: An overview of current status and ecosystem effects. Ecol. Eng. 35, 511–520. Liao, C., Tang, X., Cheng, X., 2010. Nitrogen dynamics of aerial litter of exotic Spartina alterniflora and native Phragmites australis. Biodivers. Sci. 18 (6), 631–637 (in Chinese).
4.3. Comparison with other invasions Invasion and the domestication of plants have been critical to the evolution of organisms and modern-day ecosystems across the globe. Many studies have focused on invasive species that have caused serious damage in recent years or decades, such as Eichhornia crassipes, Ageratina adenophora, and Chromolaena odorata. In many cases, human activities have encouraged or instigated these invasions (Sang et al., 2008). In the March 2010 Report of the United Nations Convention on Biological Diversity, the United States, Australia, the United Kingdom, South Africa, and China combined were estimated to be losing more than 100 billion dollars a year because of invasive species. However, invasion is the preferred term when the costs exceed the benefits, from a human perspective, and we may instead refer to the same facts as ‘introduction’ when the connotation is more positive. In China, S. alterniflora generally increases carbon deposition, nutrient filtration and cycling processes, vertical accretion, and storm protection. It can reduce habitat value and biodiversity, depending on the invaded ecosystem, but in some cases it can provide forage and benefit some species. We can generally assume that the loss of unvegetated tidal flats is negative for birds, while the gain of vegetated surfaces and detritus enhances fisheries production. In some cases, there may be no great effect; for example, Josselyn et al. (1993) found that S. alterniflora has not significantly changed the structure of benthic fauna in salt marsh in the past 40 years. Still, the jury is out: the long-term of these relatively new ecosystems in China has not been decided. We propose that efforts to eradicate and suppress S. alterniflora in China's coastal wetlands are fighting uphill against a dominant, natural process. Instead, we contend that we should spend more effort to identify the best way to beneficially use these new ecosystems. 5. Conclusion In summary, the introduction of S. alterniflora to China has greatly altered the structure and function of coastal wetlands. Our approach to controlling, promoting, or eradicating S. alterniflora should be conducted with a long-term and context-dependent perspective in order to maximize the ecological cost-benefit calculus for each of China's provinces. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments This study was supported by the Grand Science and Technology Special Project of Tianjin (No. 18ZXSZSF00200). The authors would like to thank the editors and anonymous reviewers for their insightful comments and suggestions. References Ayres, D., Smith, D., Zaremba, K., Klohr, S., Strong, D., 2004. Spread of Exotic Cordgrasses And Hybrids (Spartina spp.) in the Tidal Marshes of San Francisco Bay. 6. Biological Invasions, California, USA, pp. 221–231. Barbier, E.B., Koch, E.W., Silliman, B.R., Hacker, S.D., Wolanski, E., Primavera, J., et al., 2008. Coastal ecosystem-based management with nonlinear ecological functions and values. Science 319 (5861), 321–323. Bo, L., Liao, C.H., Zhang, X.D., Chen, H.L., Wang, Q., Chen, Z.Y., Gan, X.J., Wu, J.H.,
7
Ecological Engineering 143 (2020) 105670
W. Meng, et al.
biology, ecology and management. Acta. Phytotax. Sin. 44, 559–588. Wang, Q., Wang, C., Zhao, B., Ma, Z., Luo, Y., Chen, J., et al., 2006b. Effects of growing conditions on the growth of and interactions between salt marsh plants: implications for invasibility of habitats. Biol. Invasions 8 (7), 1547–1560. Wang, G., Qin, P., Wan, S., Zhou, W., Zai, X., Yan, D., 2008. Ecological control and integral utilization of Spartina alterniflora. Ecol. Eng. 32, 249–255. Wang, G., Yang, W., Wang, G., Liu, J., Hang, Z., 2013. The effects of Spartina alterniflora seaward invasion on soil organic carbon fractions, sources and distribution. Acta Ecol. Sin. 33 (8), 2474–2483 (in Chinese). Wang, D., Zhang, R., Xiong, J., Guo, H., Zhao, B., 2015. Contribution of invasive species Spartina alterniflora to soil organic carbon pool in coastal wetland: Stable isotope approach. Chin. J. Plant. Ecol. 39 (10), 941–949 (in Chinese). Windham, L., Ehrenfeld, J.G., 2003. Net Impact of a Plant Invasion on Nitrogen-Cycling Processes within a Brackish Tidal Marsh. Ecol. Appl. 13, 883–896. Xie, Z., He, W., Liu, W., Lu, J., 2008. Influence of Spartina alterniflora salt marsh at its different development stages on bacrobenthos. Chin. J. Plant. Ecol. 27 (1), 63–67 (in Chinese). Yang, W., Zhao, H., Chen, X., Yin, S., Cheng, X., An, S., 2013. Consequences of short-term C4 plant Spartina alterniflora invasions for soil organic carbon dynamics in a coastal wetland of Eastern China. Ecol. Eng. 61, 50–57 Part A. 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. Ecol. Eng. 23, 95–105. Zhang, R., Shen, Y., Lu, L., 2005. Formation of Spartina alterniflora salt marsh on Jiangsu coast of China. Oceanologia et Limnologia Sinica 36, 358–366 (in Chinese). Zhang, D., Yang, M.M., Li, J.X., Chen, X.Y., 2006. Vegetative dispersal ability of Spartina alterniflora in Eastern end of Chongming Island. J. East China Normal Univ. (Nat. Sci.) 2, 130–135 (in Chinese with English abstract). Zhang, Y., Ding, W., Luo, J., Donnison, A., 2010. Changes in soil organic carbon dynamics in an Eastern Chinese coastal wetland following invasion by a C4 plant Spartina alterniflora. Soil Biol. Biochem. 42, 1712–1720. Zhang, W., Zeng, C., Tong, C., Zhang, Z., Huang, J., 2011. Analysis of the Expanding Process of the Spartina alterniflora Salt Marsh in Shanyutan Wetland, Minjiang River Estuary by Remote Sensing. Procedia Environ. Sci. 10, 2472–2477. Zhao, X., Zhao, C., Liu, X., Gong, L., Deng, Z., Li, J., 2015. Growth characteristics and adaptability of Spartina alterniflora in different latitude areas along China coast. Ecol. Sci. 34 (1), 119–128 (in Chinese). Zhu, H., Qin, P., Wang, H., 2004. Functional group classification and target species selection for Yancheng nature reserve, China. Biodivers. Conserv. 13 (7), 1335–1353. Zhu, Z., Zhang, L., Wang, N., Schwarz, C., Ysebaert, T., 2012. Interactions between the range expansion of saltmarsh vegetation and hydrodynamic regimes in the Yangtze Estuary, China. Estuar. Coast. Shelf Sci. 96, 273–279. Zuo, P., Zhao, S., Liu, C., Wang, C., Liang, Y., 2012. Distribution of Spartina spp. along China’s coast. Ecol. Eng. 40, 160–166.
Liu, J., Zhou, H., Qin, P., Zhou, J., 2007. Effects of Spartina alterniflora salt marshes on organic carbon acquisition in intertidal zones of Jiangsu Province, China. Ecol. Eng. 30, 240–249. Lu, J., Zhang, Y., 2013. Spatial distribution of an invasive plant Spartina alterniflora and its potential as biofuels in China. Ecol. Eng. 52, 175–181. Luo, Y., Hui, D., Zhang, D., 2006. Elevated CO₂ stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87, 53–63. Ma, Z., Gan, X., Choi, C., 2014. Effects of invasive cordgrass on presence of Marsh Grassbird in an area where it is not native. Conserv. Biol. 28 (1), 150–158. Ma, Qiang, Wu, Wei, Tang, C., Niu, D., Wu, Jihua, Ma, Zhijun, 2017. Effects of habitat restoration on the diversity of bird and marcobenthos in the Chongming wetland. J. Nanjing For. Univ. 41 (1), 9–14 (in Chinese). Maricle, B.R., Lee, R.W., 2002. Aerenchyma development and oxygen transport in the estuarine cordgrasses Spartina alterniflora and S. anglica. Aquat. Bot. 74, 109–120. Meng, W., He, M., Hu, B., Mo, X., Li, H., Liu, B., et al., 2017. Status of wetlands in China: a review of extent, degradation, issues and recommendations for improvement. Ocean Coast. Manag. 146, 50–59. Meng, W., Feagin, R.A., Hu, B., Wang, Z., Li, H., 2019. The spatial distribution of blue carbon in the coastal wetlands of China. Estuar. Coast. Shelf Sci. 222, 13–20. Neira, C., Levin, L.A., Grosholz, E.D., Mendoza, G., 2007. Influence of invasive Spartina growth stages on associated macrofaunal communities. Biol. Invasions 9, 975–993. Pan, T., Zeng, L., Zeng, C., Wang, W., 2015. Effects of Spartina alterniflora invasion on soil organic carbon in the bare tidal flat wetland of Minjiang River estuary. Sci. Soil. Water. Conserv. 13 (1), 84–90 (in Chinese). Qin, P., Xie, M., Jiang, Y., 1998. Spartina green food ecological engineering1. Ecol. Eng. 11, 147–156. Quan, W., Zhang, H., Wu, Z., Jin, S., Tang, F., Dong, J., 2016. Does invasion of Spartina alterniflora alter microhabitats and benthic communities of salt marshes in Yangtze River estuary? Ecol. Eng. 88, 153–164. Sakai, A., Allendorf, W.F., Holt, J., Lodge, D., Molofsky, J., With, K., Baughman, S., Cabin, J.R., Cohen, J., Ellstrand, C.N., McCauley, E.D., O’Neil, P., Parker, I.N., Thompson, J.G., Weller, S., 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32, 305–332. Sang, W., Feng, J., Xue, D., 2008. Human, ethnical and social insights of biological invasion. J. Cent. Univ. Nation. 17 (4), 17–23 in Chinese. Shen, Y., 2001. The study of the function of the wetlands of Spartina alternifloura manpower salt marsh in Jiangsu. Ecol. Econ. 9, 72–73 (in Chinese). Silliman, B.R., Zieman, J.C., 2001. Top-down control of Spartina alterniflora, production by periwinkle grazing in a Virginia salt marsh. Ecology 82 (10), 2830–2845. Simenstad, C., Thom, R., 1995. Spartina alterniflora(smooth cordgrass) as an invasive halophyte in Pacific northwest estuaries. Hortus Northwest: a Pacific Northwest native plant directory. Journal 6, 9–13. Wan, S., Qin, P., Liu, J., Zhou, H., 2009. The positive and negative effects of exotic Spartina alterniflora in China. Ecol. Eng. 35, 444–452. Wang, Q., An, S., Ma, Z., Zhao, B., Chen, J., Li, B., 2006a. Invasive Spartina alterniflora:
8