Marine Pollution Bulletin 89 (2014) 259–266

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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul

Macrobenthic diversity in protected, disturbed, and newly formed intertidal wetlands of a subtropical estuary in China Weiwei Lv 1, Chang-an Ma 1, Youhui Huang, Yang Yang, Ji Yu, Mingqing Zhang, Yunlong Zhao ⇑,1 School of Life Science, East China Normal University, Shanghai 200241, China

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Article history: Available online 13 October 2014 Keywords: Macrobenthic diversity Intertidal zone Protected wetland Disturbed wetland Newly formed wetland Yangtze estuary

a b s t r a c t In this study, intertidal macrobenthic diversity in protected, disturbed, and newly formed wetlands of Yangtze estuary was assessed using PRIMER 5.2 based on species diversity and species relatedness. We observed high diversity in nature reserves and low diversity in adjacent disturbed and newly formed wetlands. These diversity data were then integrated with historical data to detect the variation in macrobenthic diversity over the past two decades. The integrated data indicated that the intertidal macrobenthic diversity sharply decreased in heavy reclamation tidal flats whereas markedly increased in non-disturbed nature reserve and newly formed wetland. Benthic health was observed with the departure degree of average taxonomic distinctness (D+) and variation in taxonomic distinctness (K+) from the simulated 95% confidence funnel. All the habitats were subjected to different levels of human interference, except Jiuduansha and Beigangbeisha. The degradation of intertidal wetland in Yangtze estuary was mainly attributed to land reclamation, overgrazing, and overfishing. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction The Yangtze estuary is the largest estuary in the Pacific Rim area and located in the northern subtropical monsoon climate zone (Vriend et al., 2011). Complex interactions occur between the Yangtze River and the East China Sea in this region (Chen et al., 2012; Hu et al., 2014). Each year, approximately 9.24  1011 m3 of freshwater and 1.45  108 t of sediment enter the estuary because of river runoff (Kuang et al., 2013; Shou et al., 2013). These vast quantities of sediments provide abundant material foundation to support the formation and evolution of intertidal wetland in this estuary. The intertidal wetland is mainly distributed over the continental coast, mature islands, and newly formed sandbars. The coastal intertidal wetlands range over the north and south banks of the estuary. The island wetlands, consisting of Chongming Island, Hengsha Island, Changxing Island, and Jiuduansha, are separated by forked channels and several new sandbars, such as Beigangbeisha and Zhongyangsha. The region of the Yangtze estuary is of great ecological importance as one of the major spawning and reproduction grounds for many commercial and protected species, such as

⇑ Corresponding author at: School of Life Science, East China Normal University, 500 Dongchuan Road, Shanghai 200241, China. Tel.: +86 021 54341035; fax: +86 021 54341006. E-mail address: [email protected] (Y. Zhao). 1 Weiwei Lv, Chang-an Ma, and Yunlong Zhao contributed equally to the paper. http://dx.doi.org/10.1016/j.marpolbul.2014.09.051 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.

Eriocheir sinensis and Acipenser sinensis (Luo et al., 2011; Sui et al., 2011). This estuarine wetland offers a winter home for thousands of migrating birds (Ma et al., 2002). As a core area of bird migration route in the Asia Pacific, the east shoal of Chongming Island was included in the Ramsar Convention as a wetland of international importance, especially for waterfowl habitat, in 2001 (Gao and Zhang, 2006; Xu and Zhao, 2005). To protect these vital wetlands, Jiuduansha and the east shoal of Chongming Island were established as state-level natural reserves in 2005 (Chen et al., 2009). The Yangtze estuary backs on to Shanghai, which is the most developed and populous city in China. The economic growth of this city has recently been conditioned by a highly strained relationship between an ever-increasing population and dwindling land resources (Gorenc et al., 2004). The vast estuarine wetlands are considered the main backup land in Shanghai. The constructed wetlands increased rapidly in the Yangtze estuary because of largescale reclamation projects since the 1990s. According to correlative report, the land expansion speed within 0 m depth contour increased by approximately 5.4 times in the main intertidal wetlands of the estuary from 1994 to 2011. However, the expansion speed had risen seventeenfold and twenty-one-fold in the east shoal of Hengsha Island and in the south bank of the estuary, both of which were heavily reclaimed areas (Du et al., 2013). Although considerable economic profit can be acquired from reclamation, the widespread devastation of intertidal wetlands will cause serious ecological degradation, including biodiversity loss, coastal water degradation, and aquatic resource depletion (Wang et al., 2014).

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Macrobenthos are the main providers of ecological service value in intertidal wetlands (Simone and Rui, 2010). Macrobenthic diversity indices are regarded as an ideal method for monitoring ecological status because of the sedentary life cycle and sensitivity to benthic environmental variation of macrobenthos (Dauer et al., 2000; Lavesque et al., 2009). The investigation of macrobenthos in the Yangtze estuary originated in the middle of the 20th century. Recent correlative studies mainly investigated the effects of invasive species and environmental indicators on macrobenthic communities in the intertidal or subtidal zones (Chao et al., 2012; Quan et al., 2011; Wang et al., 2010). However, such targeted research was usually confined to a limited scope of work that could not be mirrored in the distribution characteristics of macrobenthic diversity in the whole estuary. A marked absence of comprehensive investigations on macrobenthos living in protected, disturbed, and newly formed habitats is observed. In this study, we comprehensively and systematically investigated the macrobenthos in the intertidal zone of Yangtze estuary. We integrated our species data with the historical results of other research to determine the variation of macrobenthic diversity over the past 20 years. The primary purposes are (1) to study the protective effects on intertidal habitats and macrobenthic diversity with construction of natural reserves, (2) to explain the influence of human disturbance on macrobenthic diversity and wetland ecosystem, and (3) to analyze the status and development prospects of the newly formed wetland. 2. Materials and methods 2.1. Study sites Five habitats were investigated, namely, Jiuduansha where almost no human activity occurs; east shoal of Chongming Island with minimal human interference; east shoal of Hengsha Island, which is outside the natural reserve and considered exploited; south bank of Yangtze River estuary, which is an excessively exploited wetland on the edge of the continent; and Beigangbeisha, a newly formed wetland. Jiuduansha is composed of three sand islands, the sedimentary deposits of which are mainly composed of silt and sand. The habitat types include Phragmites australis, Spartina alterniflora, Scirpus mariqueter, Scirpus triqueter, and mudflat zones. Jiuduansha has been seldom influenced by human activities, except for scientific efforts, because of its remoteness from urban districts. Therefore, ecological succession occurs constantly with the expansion of the original wetland in this region. The east shoal of Chongming Island is the most comprehensive wetland in the estuary. A significant difference in habitation environment exists among the high, middle, and low intertidal zones in this island. Within the salt marshes, monoculture stands of vegetation presented an obvious zonal distribution. Artificial channels have recently been connected in series with the natural tidal creeks. These creeks have divided the contiguous tidal flat into several ‘‘small islands.’’ Individual grazing and harvesting activities often occur at the middle and south of this island. The east shoal of Hengsha Island is located between Chongming Island and Jiuduansha. The reclamation project has enclosed the central part of the whole tidal flat, which covers an area of 124.2 km2. The reserved wetland in natural tidal flat is only 3 km wide at its maximum. Stretches of Scirpus mariqueter cover the eastern and southern tidal flat, but the northern part has no salt marsh vegetation. The sediments are mainly composed of fine sand and silt. The south bank of Yangtze estuary, located on the edge of the continent, is far more likely to be influenced by human activities than islands. The reclamation region is larger in the south bank than in the east shoal of Hengsha Island. At present, the project

has enclosed the whole tidal flat above the 0 m depth contour, thus creating an enclosure of approximately 171.9 km2. The entire salt marsh vegetation has been enclosed into the reclamation zone. The reserved tidal flat is less than 1 km wide at its maximum. The sediments are largely clayey silt. Beigangbeisha is a newly formed sandbar in the central part of Yangtze estuary. Only when the tide is low could this region rise above the water surface. The tidal flat is not covered by salt marsh vegetation. The elevation of intertidal zone has not exhibited significant difference, and the sediment is mainly silt. Although no human interference was observed in Beigangbeisha, the low-lying area in the tidal flat remains unstable because of strong hydrodynamic force. 2.2. Field sampling and sample processing Five different sampling habitats based on the characteristics of wetlands were set in the Yangtze estuary: South bank of Yangtze River estuary (SYRE), East shoal of Chongming Island (CM), East shoal of Hengsha Island (HS), Jiuduansha (JDS), and Beigangbeisha (BGBS). Each investigation was conducted at low tide during spring tides in spring and fall from 2011 to 2013 (SYRE and BGBS in April and October in 2011; CM and HS in April and November in 2012; JDS in April and October in 2013). A total of 24 sampling sites were distributed into the five habitats (Fig. 1). At each sampling site, the macrobenthos were sampled at the high, middle, and low tide zones. The tide levels were defined based on the distribution of elevation and salt marsh vegetation. In CM and JDS, the high intertidal zone was located in the marshes of P. australis and S. alterniflora. The middle tide zone was in the marshes of S. mariqueter and S. triqueter. The low tide zone was in the mudflat. In HS and SYRE, the three sampling levels were defined at the elevation level along the direction perpendicular to the shoreline. The distances between the intertidal levels were appropriately adjusted to fit the width of the marshes. In BGBS, the three intertidal levels were located in the direction perpendicular to the depth contour. Each sampling site was accurately determined by a handheld GPS. Four replicate 0.25 m  0.25 m  0.30 m quadrat samples were collected at each sampling level. The qualitative samples were collected around the sampling cores. The macrobenthos were collected with a quantitative mesh of 1.0 mm aperture and then fixed in 75% alcohol solution. Each specimen was identified to the lowest classification level and enumerated. Water environment factors, such as the water temperature, salinity, pH, and dissolved oxygen (DO), were determined in every 31.8 Jiangsu Province

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Fig. 1. Sampling stations in the tidal flats of Yangtze estuary.

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sampling point by using Multi 350i water analyzer. The concentrations of nitrate (NO3-N), phosphate (PO4-P), and silicate (SiO3-Si) were measured and converted by using the standard methods from APHA (APHA et al., 1998). 2.3. Diversity measures The different measures of macrobenthic diversity, including species, taxonomic, and phylogenetic diversity, were tested by PRIMER 5.2 (Clarke and Warwick, 2001). The estimation of species diversity indices was based on the richness and evenness of species distribution. The species richness was examined using the number of species (S) and Margalef’s index (d), whereas species evenness was calculated with Pielou’s index (J0 ), Simpson’s index (1  k0 ), and Hill’s number (N1). The two attributes of species diversity were considered jointly with the Shannon–Wiener’s index (H0 log2), which represented the diverse degree of species composition. The taxonomic diversity was calculated from a species checklist of macrobenthos in the Yangtze estuary. All species obtained from the surveys were divided into six taxonomic levels (species, genus, family, order, class, and phylum) that represent the taxonomic distances of individual species before calculation. Several taxonomic measures based on presence or absence of the species were calculated, including the average taxonomic distinctness (AvTD, denoted by D+), the total taxonomic distinctness (TTD, denoted by SD+), and the variation in taxonomic distinctness (VarTD, denoted by K+). Meanwhile, the phylogenetic diversity defined by Faith (1992) was estimated based on the minimum total branch length in the phylogenetic tree. Two phylogenetic indices, the average phylogenetic diversity (AvPD, denoted by U+) and total phylogenetic diversity (PD, denoted by SU+), were used to analyze the phylogenetic patterns among macrobenthic taxa. 2.4. Interannual variation of diversity To observe the variation in macrobenthic diversity over the past 20 years, the D+ values tested from the species data of Yuan and Lu (2002) from 1998 to 2000, Liu (2007) from 2004 to 2006, as well as of this study from 2011 to 2013 were added to the simulated funnel plots constructed by a checklist of 215 species recorded from 1998 to 2013. In Yuan and Lu’s investigation, twenty sampling sites in total were sampled in four habitats (SYRE, CM, HS, and JDS) during 3 years (Fig. 2A). At each site, the tidal flat was subdivided into three tidal strata: high, middle, and low intertidal zones. Six replicate 0.50 m  0.50 m  0.20 m quadrats were randomly collected at each tidal level. 31.8

In Liu’s research, nine sampling sites scattered across all five habitats (SYRE, CM, HS, JDS, and BGBS) were investigated from September 2004 to October 2006 (Fig. 2B). The macrobenthic data were collected in high, middle, and low tidal flat, respectively. At each tidal level, six random replicates were taken with the quadrats of 0.25 m  0.25 m  0.20 m. 2.5. Assessment of benthic health A total list of 126 macrobenthic species recorded during this survey (2011–2013) were sampled randomly to construct the funnel plots of D+ and K+ as the theoretical intervals in estimating ecological health. The departure of real D+ and K+ values from the limited range was considered as the main characteristic of a disturbed benthic environment. 2.6. Statistical analysis The differences in variation of diversity measures were tested with a one-way ANOVA using SPSS16.0. Cluster and non-metric multidimensional scaling (NMDS) analyses were used to observe the differences in macrobenthic community among the five habitats by using SPSS 16.0. Redundancy analysis (RDA) examined the influences of environmental indicators on macrobenthic diversity with CANOCO 4.5. All the measures of diversity and environmental indicators were transformed as a log10(X + 1) style before analysis. 3. Results 3.1. Environmental indicators The estuary showed strong seasonal fluctuations in environmental factors. Water temperature and nutrient concentration in spring were significantly higher than those in autumn (p < 0.05). By contrast, water salinity and DO were lower in spring than those in autumn (p < 0.05). The pH did not typically vary with seasons (Table 1). All the environmental factors were not significantly different at the spatial scale (p > 0.05). The wetland in SYRE obtained a high value of water salinity but a low value of DO. Water temperature, salinity, and nutrient concentration among habitats did not indicate any obvious trends (Table 1). 3.2. Temporal and spatial variation of diversity indices All the measures of macrobenthic diversity exhibited no significant differences between the two seasons (p > 0.05), but were significantly different among the habitats (p < 0.05). 31.8

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Fig. 2. Sampling stations of Yuan and Lu’s (A) and Liu’s (B) investigation in Yangtze estuary.

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Table 1 Average values of environmental indicators at the five habitats. Environmental indicators

Salinity (‰) Temperature (°C) pH DO (mg L1) NO3-N (mg L1) SiO3-Si (mg L1) PO4-P (mg L1)

South bank of Yangtze River estuary (n = 3)

East shoal of Chongming Island (n = 5)

East shoal of Hengsha Island (n = 5)

Jiuduansha (n = 7)

Beigangbeisha (n = 4)

Spring

Autumn

Spring

Autumn

Spring

Autumn

Spring

Autumn

Spring

Autumn

6.0 21.7 7.90 7.07 1.34 1.65 0.06

10.5 15.8 7.93 7.53 1.25 1.56 0.03

4.8 21.2 8.02 7.36 1.40 1.77 0.04

6.7 15.3 8.06 8.07 1.22 1.62 0.02

3.7 21.9 8.06 7.22 1.41 1.85 0.08

4.5 15.0 8.03 8.18 1.31 1.81 0.05

3.8 20.7 8.08 8.08 1.45 2.12 0.08

4.81 15.4 7.81 9.44 1.25 1.74 0.06

2.7 20.0 8.04 7.50 1.46 2.13 0.07

3.5 15.53 8.02 7.96 1.35 1.93 0.05

The abbreviations represent the environmental variables: DO, dissolved oxygen; NO3-N, nitrate; PO4-P, phosphate; and SiO3-Si, silicate.

Among the measures of species diversity, the number of species (S) and Margalef’s richness index (d) decreased slightly between the seasons, indicating that the richness of species was considerably high in spring. By contrast, an inverse trend was observed in Shannon–Wiener’s index (H0 ), Pielou’s index (J0 ), Simpson’s index (1  k0 ), and Hill’s number (N1), which characterize the diversity and evenness of species. The spatial distribution of species richness followed a similar high-value track in JDS and a low-value track in BGBS. However, the measures of species evenness were generally high in CM and low in SYRE. Shannon–Wiener’s index was highest in CM because of high species evenness but was the lowest in BGBS because of low species richness (Table 2). From the taxonomic and phylogenetic diversity, the five indices were relatively consistent between seasons, but typically varied with samplings sites. A similar trajectory was observed in the spatial distribution of total taxonomic distinctness (SD+) and total phylogenetic diversity (SU+) with species richness. The average taxonomic distinctness (D+) and average phylogenetic diversity (U+) reached a high value in JDS and BGBS. These two indices were relatively low in SYRE. The variation of taxonomic distinctness showed a variation of being high in CM and low in JDS (Table 2). 3.3. Analysis on community structure Cluster and NMDS analysis revealed that the five habitats can be divided into three groups (Fig. 3A). Two heavily disturbed habitats, SYRE and HS, were gathered. Two protected wetlands in the natural reserve, CM and JDS, were clustered together. The newly formed wetland, BGBS, was in a separate group. The NMDS further proved the cluster result of macrobenthic diversity measures (Fig. 3B).

of variable data relative to macrobenthic diversity. Monte Carlo tests indicated no significance for the first canonical axe and for all canonical axes (p = 0.08). The relationship between diversity measures and environmental indicators was observed in the RDA ordination diagram (Fig. 5). The measures of richness (S, d, SD+, and SU+) and diversity (H0 , D+) were positively correlated with DO and salinity but negatively correlated with nutrient concentrations. However, evenness (J0 , 1  k0 , N1) and U+ were positively correlated with DO and nutrient concentrations but negatively correlated with salinity. 3.6. Ecological health status of benthic environment The health status of all habitats was observed in a funnel plot with 95% confidence intervals (Fig. 6A1, A2 and B1, B2). During this period, the D+ value in SYRE was significantly lower than expected, indicating that the relatedness of species was relatively concentrative in macrobenthic community. The K+ values in CM and HS were located above the 95% expected range, suggesting that the relatedness of species was more uneven than that in the other three sampling sites. The D+ and K+ values in BGBS and JDS fell within the 95% limit, showing that the taxonomic diversity was relatively close to the average level of Yangtze estuary. Bivariate analysis was performed to combine the observed results of D+ and K+ into an ellipse plot (Fig. 6A3 and B3). The area within the elliptical contour represented the expected range of this investigation, which further confirmed the results of the funnel plot. 4. Discussion

3.4. Decadal changes in taxonomic measure 4.1. ‘‘Reserve effect’’ in nature reserve and the interference within it The average taxonomic distinctness (D+) was tested to observe the variation in macrobenthic diversity from 1998 to 2013. The funnel plot with the three investigation results showed that the trends in macrobenthic diversity were noticeably different among habitats. During this period, the measure of taxonomic diversity in BGBS showed an evident rising trend (Fig. 4E). However, the taxonomic measure in SYRE and JDS increased markedly after a sharp decrease (Fig. 4A and D). The average taxonomic distinctness in CM and HS fluctuated within a narrow range (Fig. 4B and C). 3.5. Relationship between diversity measures and environmental indicators Detrended correspondence analysis suggested that the length of gradient of the first axe was 0.241, thus the need for a linear mode. Therefore, RDA was applied to analyze the relationship between macrobenthic diversity and environmental factors. The first and second axes respectively accounted for 41.9% and 2.1% of total variance in macrobenthic diversity. All canonical axes explained 45.7%

The features of a habitat directly determine the distribution of the macrobenthos in a wetland ecosystem (Blanchard and Feder, 2014). Nature reserves may maintain original wetland environments and develop macrobenthic communities during the course of succession (Lester et al., 2009; Linares et al., 2012; Pauly et al., 2002). Several studies showed that the species composition and diversity of macrobenthos presented better quality in nature reserves than in adjacent areas (Villamor and Becerro, 2012). In our investigation, although protected JDS and non-protected HS both belonged to island wetlands of the estuary with a similar distribution of environmental factors and salt marsh vegetation, the number of species in JDS was twice that in HS. Moreover, more complex taxonomic relationships among species existed in the former than in the later. The above results indicated that the establishment of a nature reserve caused a ‘‘reserve-effect’’ in the survival and development of macrobenthos. In the intertidal wetland, the macrobenthic diversity may be subject to the width of the tidal flat and to the coverage of salt marsh vegetation. The

45 2.36 ± 0.38 0.57 ± 0.08 0.61 ± 0.06 2.14 ± 0.31 2.62 ± 0.59 90.34 ± 2.26 1602.54 ± 342.39 312.01 ± 41.20 66.99 ± 3.43 1188.10 ± 254.54

Autumn Spring

49 2.21 ± 0.24 0.53 ± 0.10 0.59 ± 0.09 2.35 ± 0.62 2.42 ± 0.50 90.19 ± 1.70 1624.37 ± 302.41 332.65 ± 72.21 66.84 ± 2.92 1202.38 ± 218.46

Spring

U+ SU+

S H0 J0 1  k0 d N1 D+ SD+ K+

30 2.71 ± 0.52 0.67 ± 0.13 0.70 ± 0.07 1.89 ± 0.60 3.26 ± 0.96 83.83 ± 3.60 1402.62 ± 546.31 551.08 ± 70.84 57.43 ± 2.92 943.33 ± 321.15 18 1.37 ± 0.39 0.36 ± 0.06 0.38 ± 0.07 1.32 ± 0.02 1.51 ± 0.24 73.62 ± 4.81 1058.07 ± 142.67 376.82 ± 78.29 54.99 ± 1.49 788.89 ± 78.76 15 1.46 ± 0.25 0.41 ± 0.05 0.36 ± 0.07 1.05 ± 0.11 1.82 ± 0.28 73.40 ± 4.67 859.26 ± 134.89 386.16 ± 51.74 56.95 ± 3.65 666.67 ± 104.08

32 2.70 ± 0.44 0.67 ± 0.19 0.70 ± 0.09 1.94 ± 0.56 3.17 ± 0.99 84.26 ± 3.44 1392.30 ± 443.79 551.36 ± 107.29 56.58 ± 1.88 923.33 ± 250.72

23 2.22 ± 0.19 0.69 ± 0.08 0.70 ± 0.04 1.43 ± 0.17 2.03 ± 0.15 74.60 ± 8.83 747.19 ± 280.59 506.82 ± 83.96 59.43 ± 4.25 586.67 ± 181.96

26 2.16 ± 0.40 0.63 ± 0.14 0.65 ± 0.10 1.49 ± 0.34 1.91 ± 0.33 79.73 ± 2.12 959.29 ± 386.27 565.77 ± 100.05 59.95 ± 4.32 710.00 ± 251.27

8 1.05 ± 0.60 0.47 ± 0.29 0.43 ± 0.26 0.98 ± 0.19 2.11 ± 0.20 79.17 ± 3.56 378.06 ± 92.25 328.70 ± 103.06 75.28 ± 1.84 358.33 ± 78.76

Beigangbeisha (n = 4)

Autumn Jiuduansha (n = 7)

Autumn Spring

East shoal of Hengsha Island (n = 5)

Spring Autumn Spring

Autumn

East shoal of Chongming Island (n = 5) South bank of Yangtze River estuary (n = 3)

Table 2 Mean and standard deviation of diversity indices at the five habitats.

263

11 0.91 ± 0.33 0.47 ± 0.14 0.41 ± 0.04 1.05 ± 0.20 1.79 ± 0.26 79.03 ± 9.69 364.58 ± 156.11 362.42 ± 327.22 74.44 ± 10.89 325.00 ± 109.29

W. Lv et al. / Marine Pollution Bulletin 89 (2014) 259–266

Fig. 3. Cluster (A) and NMDS (B) analysis using the fourth root of diversity data. The abbreviations represent the five habitats: SYRE, south bank of Yangtze estuary; HS, east shoal of Hengsha Island; CM, east shoal of Chongming Island; JDS, Jiuduansha; and BGBS, Beigangbeisha.

original wetland in JDS stretched for miles and was markedly heterogeneous in each tidal flat, which could provide more living space and niches for macrobenthos. By contrast, the wetland in HS was characterized by widespread reclamation, and the reserved tidal flat was approximately 3 km at its widest part. The reclamation reduced the tidal flat to only the S. mariqueter and mudflat zones, thus shrinking habitats and decreasing heterogeneity, which could ultimately result in biodiversity loss. Intertidal wetlands are usually located in the ecological area of vulnerability and sensitivity, and the aim of establishing a nature reserve is to protect ecological security and diversity of animals and plants in the wetland (Sukumaran et al., 2013; Webb et al., 2013). In our research, however, the monitoring results in CM were not ideal despite the fact that CM is a national reserve. The departure of D+ and K+ values in the funnel plots showed a relative concentration and an uneven interval in taxonomic relationship, which revealed a remarkable difference from the results generated in the undisturbed JDS. Therefore, the habitats in CM were affected by human interference. In agreement with the investigation of Zhao et al. (2007), overgrazing negatively affected macrobenthic diversity in CM. The number of Moerella iridescens rapidly decreased because of overfishing, according to the research by Xu and Zhao (2005). Trophic cascade effects extensively exist in wetland ecosystems (Sangil et al., 2013). As important secondary producers, macrobenthos have an extensive ecological connection with other trophic levels. The variation in macrobenthic diversity would affect the distribution of high trophic levels in the food chain, such as birds and fishes. The east shoal of Chongming Island is approximately halfway along the bird migration itinerary from East Asia to Australia. The loss of macrobenthic diversity is bound to affect bird migration in the Asia-Pacific region because of benthic habitat degradation. 4.2. Influence of reclamation on macrobenthic diversity and wetland ecosystem With large-scale human interference, the community structure and diversity of macrobenthos will change accordingly in tidal flat

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B

100 95

100 95

95

90

90

90 98-00

Delta+

Delta+

C

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85 11-13

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Delta+

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04-06 98-00 11-13

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11-13

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75 70

70

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20

30

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0

60

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60

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0

10

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Number of species

D

40

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100

95 90 11-13

11-13

Delta+

Delta+

90 98-00

85 04-06

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80 70 75 04-06

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60 0

10

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Number of species

50

60

0

5

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20

Number of species

Axis2

Λ+

pH WT Sal

S SΔ+ SΦ+

NO3-N H' J' PO4-P

1-λ'

-1.0

Δ+

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N∞ Φ+

DO

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wetland ecosystems (Lee et al., 2006). Both SYRE and HS were affected by reclamation projects. However, these two habitats exhibited a significant difference in terms of the ecological health of the benthic environment despite the similar community structure of macrobenthos tested by cluster analysis. Our results revealed that the observed D+ value in SYRE remarkably diverged from the theoretical expectations, indicating that macrobenthos were heavily disturbed by land engineering. Instead, the D+ value in HS fell within the 95% limit, which indicated that a moderate degree of interference occurred in this region, although the taxonomic distances among species were heavily asymmetrical. The above results might be attributed to different reclamation approaches. Our findings confirm that all tidal flats above the 0 m depth contour have been enclosed and that the enclosure rate has exceeded the deposition rate. With no vegetation left on the bald mudflat, the vast majority of remaining macrobenthos in SYRE were infauna clams, such as Corbicula fluminea, Potamocorbula amurensis, and Sinonovacula constrzcta. By contrast, the tidal flat attracted more species with different lifestyles in HS because of the reservation of vast quantities of vegetation. The abundant S. mariqueter not only promoted the development of tidal flats, but also provided a food source for phytophagous and detritivorous macrobenthos. These factors result in a more reasonable richness and evenness as well as taxonomic distance of macrobenthos in HS than in SYRE. Biodiversity loss may cause substantive changes in all functional aspects of the ecosystem, such as complexity, stability, resilience features, material recycling, and energy efficiency (Weijerman et al., 2013). The Yangtze estuary did not experience any sudden or devastating natural disasters over the past 20 years. However, the number of species in SYRE has decreased

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Fig. 4. Variation in average taxonomic distinctness (D+) in the five geographical locations (A, south bank of Yangtze estuary; B, east shoal of Chongming Island; C, east shoal of Hengsha Island; D, Jiuduansha; E, Beigangbeisha) from 1998 to 2013 (98–00, 1998–2000; 04–06, 2004–2006; and 11–13, 2011–2013). The 95% confidence intervals are also shown with the expectation tested from 215 species.

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Fig. 5. RDA ordination diagram of diversity measures and environmental values ( , south bank of Yangtze estuary; , east shoal of Chongming Island; , east shoal of Hengsha Island; , Jiuduansha; and , Beigangbeisha). The abbreviations represent the environmental indicators (WT, water temperature; Sal, water salinity; DO, dissolved oxygen; NO3-N, nitrate; PO4-P, phosphate; and SiO3-Si, silicate).

by over 60%, and the taxonomic measure has experienced an evident drop during this period. This result indicates that structure simplification and habitat fragmentation are caused by

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retrogressive succession under long-term reclamation activities. Nevertheless, macrobenthic diversity in HS was maintained at a similar level over the past 20 years despite considerable variation of the species composition of macrobenthos. This result shows that the changes in community structure might be caused by horizontal evolution among the species with similar taxonomic levels. The survey reflects an upward trend in the number of species and in the diversity of macrobenthos in JDS, which indicates that the habitat function in this region has evolved over the past two decades. Therefore, an effective approach to avoid irreversible variation in wetland ecosystem is to prevent excessive reclamation and to maintain a certain density of salt marsh vegetation. However, the normal development of wetland ecosystems requires the establishment of nature reserves to protect intertidal habitat. 4.3. Ecological status in newly formed sandbar and advice on wetland exploitation In the intertidal zone, the different distribution patterns of macrobenthic community may be observed with the variation of habitats at different succession stages (Nishijima et al., 2014). The intertidal area in BGBS was only at an early stage of succession, but JDS has developed into a mature island, which undergoes different stages of intertidal succession. Although the results of the funnel plots showed that neither of the habitats was disturbed by human activities, the acute species shortage illustrates that the community structure of macrobenthos in BGBS remained simple and unstable. Such a state could be attributed to the sensitivity of BGBS habitats to the effects of frequent and powerful tides, and the development of the macrobenthic community could inevitably be limited by complicated hydrologic and substrate conditions in

this bald sandbar. However, JDS had evolved into a mature island for decades, and a remarkable differentiation of monoculture vegetation can be observed from high- to low-tide zones. This habitat has great diversification, stability, as well as species diversity and richness. The growth rate of the macrobenthic community possibly reflects the evolution speed of the wetland ecosystem. In our investigation, the increase in the number of species was threefold higher in JDS than in BGBS over the past 20 years. This result indicates that the expansion of the tidal flat in JDS is significantly faster than that in BGBS. As the largest estuary in the Western Pacific, the wetland of Yangtze estuary contributed to the modulation of global climate and preservation of the resource of animals and plants. However, large-scale reclamation is diminishing the intertidal wetland area in this estuary, and newly formed sandbar is not in the position to compete for ecological services with the mature wetland. Therefore, appropriate measures should be considered in wetland expansion. Salt marsh vegetation should be planted on the new sandbar to accelerate deposition, and more adaptable species should be released artificially for further diversity. Doing so would establish this region as a nature reserve to sustain the development of its eco-environment. Given the analyses, the nature reserve has a protective effect on macrobenthic diversity and wetland health in the intertidal zone. The wetland in the non-protected region has been extensively disturbed by human activities in the Yangtze estuary. The newly formed wetland is undergoing a long and difficult evolution process under natural conditions, such that human intervention is needed to accelerate intertidal growth and to realize its ecological value. However, studying methods by which to balance the exploitation of wetlands with the sustainable development of ecological environments is a long-term issue.

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