Four cruise surveys were carried out in summer, winter, spring, and autumn from 2006 to 2007 to evaluate the seasonal distribution of macrobenthos in the Yangtze River estuary and its adjacent waters. A total of 59 sites were sampled and divided into three areas (estuary, inshore, and offshore areas). In all, 335 taxa were collected with polychaetes and mollusks being the dominant groups. Two-way ANOVA revealed significant differences among the numbers of species, densities, and biomasses in the areas. However, several differences were found among seasons. SIMPER analysis showed that the dominant species of macrobenthos varied in different areas, and the inshore area was the most complex of the three. The abundance/biomass comparison (ABC) curve of macrobenthos in the inshore area showed apparent rises and falls, which are characteristic of disturbance to macrobenthos. Canonical correspondence analysis showed that echinoids were closely related to the presence of silicates and temperature, whereas polychaetes were closely related to depth and temperature.

Introduction

Estuaries are generally recognized as areas that export biomass and energy to the sea. They are a transition zone between marine and freshwater domains (Gaudéncio and Cabral, 2007). Macrozoobenthic communities are key components in the functioning of estuarine systems. Benthic organisms produce considerable physical and chemical changes in sediments, especially at the water-sediment interface. They also promote the decomposition of organic matter, nutrient recycling, and energy transfer to other links of food webs (Rhoads and Young, 1970). The relationships between the distribution of soft-bottom macrofauna and sediment characteristics have been studied for decades (Gray, 1974; Rhoads, 1974; Etter and Grassle, 1992; Snelgrove and Butman, 1994). The Yangtze River, the longest river in China, has a large annual runoff and transports large amounts of material. Its influence on its estuary and on nearby marine areas is strong. Runoff from the Yangtze River is the main source of input of materials to the east sea of China. The annual amount of nutrients transported by the Yangtze River to the sea is about 3.5 million tons (Shen et al., 2001). The nutrient transport process is greatly influenced by weather changes and human activity.

The ways in which macrobenthos respond to environmental changes remains unclear. Previous studies on the topic have primarily focused on the intertidal zone and on wetlands, rather than on the seas (Yuan et al., 2002; Zhu and Lu, 2003; Zhou et al., 2006). Studies on the coupling of the environment with macrobenthos are not sufficient to resolve these issues (Liu, Meng et al., 2008; Liu, Xian et al., 2008). The current article seeks to address the response of macrobenthos to environmental changes by studying the distribution of the macrobenthic community in different areas and seasons in the Yangtze River estuary and adjacent marine areas. The aims are to analyze changes in the dominant species, reveal the influences of such changes on the macrobenthic community, and provide a scientific basis for evaluating health-related conditions in the Yangtze River estuary. The evaluation of environmental health will help sustain social, economic, and environmental development in the region.

Materials and Methods

Study area

The Yangtze River is the third longest river in the world; it ranks fourth globally in runoff and sand discharge and its annual average runoff is 9.24 × 1011 m3. The Yangtze River estuary, the largest one in China, is exceptional, owing to its very favorable geographic location and natural conditions. The Yangtze River estuary and its adjacent area are sites at which saltwater and freshwater mix. Its environment is complex and varied because of strong tides and riverbed landforms.

Sampling design

The current study is part of a large project involving a comprehensive investigation and evaluation of coastal areas in China. To understand the relationship between macrobenthos in the Yangtze River estuary and the environment, samples were collected from July 18th to August 15th in 2006 (summer), December 25th in 2006 to January 19th in 2007 (winter), April 8th to 26th in 2007 (spring), and October 11th to November 22nd in 2007 (autumn). A total of 59 sampling sites (Figure 1) were established and divided into three sections. These three sections are the estuary, inshore, and offshore areas. The biological productivity front in the Yangtze River estuary is generally located at 123°, which was the basis of dividing the inshore and offshore areas. The natural shape of the Yangtze River was the basis of dividing estuary and inshore areas. Benthic samples were collected with a weighted, manually deployed 0.1 m2 HNM grab. Only samples having a penetration of more than 10 cm were kept for faunal analysis. The material was processed through a sieve with a mesh size of 0.5 mm. The retained fraction was fixed in 5% neutral formalin. Temperature (T), salinity (S), dissolved oxygen (DO), phosphate (PO4-P), dissolved inorganic nitrogen (DIN; including nitrate, nitrite, and ammonium), silicate, total organic carbon (TOC), and pH were measured from the bottom water using a Valeport CTD meter, and the depth was recorded. In the laboratory, samples were first sorted under a binocular dissecting microscope. They were then identified to the lowest possible taxonomic level, counted, and weighed.

Data analysis

CANOCO 4.5 software was used to perform canonical correspondence analysis (CCA) to identify relationships between environmental and biological data. Two-way ANOVA and the Tukey HSD ( p < 0.05) multiple comparison test were applied to identify differences among the benthic parameters of the various areas and seasons using STATISTICA 6.0 software. All data were tested for normality (Kolmogorov–Smirnov test) and homogeneity of variances (Bartlett test) before performing the two-way ANOVA. SIMPER analysis was used to compare the dominant species among the areas and the seasons. An ABC curve was used to detect possible environmental disturbance. SIMPER analysis was employed to determine the contribution of each species to the average Bray-Curtis dissimilarity between habitats and sites. This method of analysis elucidates which species are responsible for any differences that occur (Zhou and Zhang, 2003). The ABC curve is an adaption of the k-dominance curve where two measures of abundance are plotted, namely, the number of individuals and biomass data. This plot is useful to explore the level of disturbance affecting assemblage. Community disturbance was indicated by the inversion and intersection of the ABC curve (Warwick, 1986).

Results

Composition and distribution of species

A total of 335 taxa were collected (Figure 2). The composition of macrobenthos in the estuary was found to be comparatively simple; only 42 species, including 16 annelids, 11 mollusks, 11 arthropods, 1 echinoderm, and 3 other taxonomic groups, were found. SIMPER analysis showed 26 dominant species of macrobenthos in different areas (Table 1). The apparent dominant species varied by season.

The composition of macrobenthos in inshore areas was comparatively complex (Figure 2). In total, 289 taxa, including 111 annelids, 96 mollusks, 42 arthropods, 22 echinoderms, and 18 other taxa, were found in the inshore area (Figure 2). SIMPER analysis revealed that no single species was dominant overall, but several dominant species appeared to occur in different seasons (e.g. Capitella capitata).

In offshore areas, 136 species, including 63 annelids, 41 mollusks, 19 arthropods, 11 echinoderms, and 2 other taxa, were observed (Figure 2). SIMPER analysis revealed the dominant species of macrobenthos in offshore areas were relatively obvious and differed among seasons.

The numbers of macrobenthos taxa found in different seasons and regions are shown in Figure 3. The average numbers of macrobenthic species per station were 1 in the estuary, 8 in inshore areas, and 8 in offshore areas. Two-way ANOVA revealed a significant difference among the numbers of species in the areas (F2, 232 = 40.82, P < 0.01). Very few differences were found among seasons (F3, 232 = 0.69, P = 0.56).

Distribution of density and biomass

The densities of macrobenthos in different seasons and regions are shown in Figure 4. The average densities of macrobenthos in estuary, inshore, and offshore areas were (9, 118 and 61) m−2, respectively. Two-way ANOVA analysis showed that densities varied minimally among seasons (F3,238 = 1.19, P = 0.31). However, densities differed among regions (F2,238 = 12.47, P < 0.01). The densities in the estuary and offshore areas were quite different ( P = 0.01) but they differed minimally between the inshore and offshore areas ( P = 0.12), as well as between the inshore and estuary areas ( P = 0.21).

Figure 5 shows the biomass of macrobenthos in different seasons and areas. The average biomasses in the estuary, inshore, and offshore areas were (2.32, 20.46 and 8.98) g m−2, respectively. Two-way ANOVA revealed no significant difference in the biomass among seasons (F3,238 = 0.64, P = 0.59). However, the biomass differed among areas (F2,238 = 8.07, P < 0.01). The biomass differed between the estuary and inshore areas ( P < 0.01). However, no difference was found between the offshore and estuary areas ( P = 0.56), as well as between inshore and offshore areas ( P = 0.13).

ABC Curve of macrobenthos

Spring is the biological breeding season; thus, it was chosen as the typical season for ABC analysis. Figure 6 shows the ABC curve for macrobenthos in different areas during spring. In the inshore area, the ABC curve of macrobenthos exhibited apparent rises and falls. This pattern indicates disturbance to the macrobenthos in the bio-environment in the inshore areas (Figure 6b). No apparent rise and fall were found in the ABC curve for macrobenthos in the estuary and offshore areas. The curve thus indicates no apparent disturbance in the bio-environment in those areas (Figures 6a and c)

Relationship between macrobenthos and environmental factors

Macrobenthos were divided into five groups (arthropods, echinoids, polychaetes, mollusks, and others) according to their characteristics. A CCA analysis was performed to identify possible relationships between these five groups of macrobenthos and environmental factors. In the estuary, the densities of polychaetes and echinoids were closely related to temperature, water depth, and silicate. Mollusks and others were closely related to salinity, DO, and pH. Crustacea were closely related to inorganic nitrogen and phosphate (Figure 7a). In inshore areas, the density of polychaetes was closely related to water depth and salinity; mollusk density to DO and pH; and the densities of crustaceans, echinoids and others to temperature, phosphate, silicate, and inorganic nitrogen (Figure 7b). In offshore areas, mollusk densities were closely related to DO and pH, polychaetes and others were closely related to salinity, water depth, and phosphate, and echinoids were closely related to temperature, silicate, and inorganic nitrogen (Figure 7c).

Discussion

Seasonal and spatial distributions in the macrobenthos

The estuarine delta of the Yangtze River is the most active area in China. The past 20 years have witnessed a new stage of development of the coastal cities in the Yangtze River Delta and associated changes in the environment of the sea near the estuary. Many previous surveys have studied macrobenthos in the estuary of the Yangtze River. In the 1990s, Dai (1991), Sun et al. (1992), and Xu et al. (1999) studied benthos in the Yangtze River estuary. The results of their study offered an overall outline of the Yangtze River estuary and nearby areas. In the beginning of the current century, Wu and Li (2003), Li et al. (2007), as well as Wang et al. (2009), studied the marine area of the Yangtze River estuary. The quantity of macrobenthos was shown to vary by season and area over the past 20 years. The present study shows that the macrobenthic community in the Yangtze River estuary markedly changes along the estuarine gradient. Macrobenthos in the estuary is small in quantity, not varied, simple in composition, and has apparent dominant species, with different dominant species in different seasons. Zhuang (2006) showed that in 1996, the dominant species in the Yangtze River estuary and its adjacent area were Nucula izushotoensis, Sternaspis scutata, Xenophthalmus pinnotheroides, Amphiura vadicola, and others. The current article shows that the dominant species are Nephtys polybranchia, Aglaophamus dibranchis, and Corbicula fluminea, among others. The change in the benthic community structure shows that the amount of benthos in the estuary area has decreased, and that the community structure of benthos is becoming increasingly simple. A possible reason for these changes may be the great influence of the Yangtze River on the estuary, as well as the accompanying violent disturbances resulting from waterway dredging, riverbed deposition, and erosion. The effects produced by these factors strongly suggest that the benthic environment of Yangtze estuary has become increasingly hostile to sediment communities.

A comparison of the estuary and inshore areas shows that the inshore area is influenced by the mutual action of Yangtze River diluted fresh water, northern Jiangsu seashore currents, the Yellow Sea cold water mass, Taiwan warm currents, and the Kuroshio tributaries. A freshwater runoff of 9.24 × 1011 m3 enters the sea each year. Frequent runoff brings a broad range of dilute water inputs to the Yangtze River in the estuarine sea area. The resulting area of influence extends eastward as far as Jizhou Island east of 126°E and provides rich salt and bait resources to the inshore area of the Yangtze River. Liu, Meng et al. (2008) suggested that in the last half century, the quantity of macrobenthos has not significantly changed in the inshore area of the Yangtze River, except for apparent changes in the dominant species. Small polychaetes with short life cycles replaced larger echinoids with longer life cycles and became the dominant species in the inshore area of the Yangtze River. The present study confirms the correctness of the proposal of Liu, Meng et al. (2008). According to the authors, dominant species, like S. scutata, Heteromas tusfilifo, Nassarius festivus and Mediomastus californiensis, are gradually being replaced by polychaetes, like C. capitata and Cossurella dimorpha. C. capitata, a pollution-indicating species, appears to be a dominant species in all four seasons. This change demonstrates that the fauna in the inshore area is dominated by small species with short life cycles. ABC analysis shows that the benthos in the inshore area of the Yangtze River is experiencing disturbance. Long-life species with high competitive ability are gradually being replaced by short-life species with high adaptability and high competitiveness, characteristics that enable them to adapt to the increasingly unstable environment. Macrobenthos in the inshore area can be predicted to become smaller and have shorter life cycles as a result of increasing human activities and complex natural environment.

Species in the offshore bio-environment offer the greatest stability and the best biological characteristics relative to those in the estuarine and inshore areas. Among the macrobenthos in the offshore areas, large echinoids with long life cycles account for 8.1% of all species, a higher proportion than that found in the inshore areas (7.6%) and estuary (2.4%). Only nine stations were located in the offshore areas, but the present study found 136 species of macrobenthos, far more than the number found in the estuary (42 species in 19 stations).Variations between different areas may result from the different influences of water flow in these areas. The estuary is mainly controlled by the runoff from the Yangtze River runoff. This runoff favors freshwater and euryhaline species. Therefore, the benthos composition in the estuary is simple. The macrobenthos of the inshore area are of a complex composition, and their habitat is influenced by disturbance and is located in the zone of mixing of diluted Yangtze River water, northern Jiangsu seashore currents, and warm currents from Taiwan. However, the offshore areas are only slightly influenced by the Yangtze River runoff. As a result, the bio-environment of this area is quite stable for some macrobenthos, particularly for large-bodied organisms.

Overall, the current study shows that human activities have greatly influenced the estuary of the Yangtze River. Less human influence is evident in inshore areas, and offshore areas show the least human influence.

Relationship between macrobenthos distribution and environmental factors

The relationship between the distribution of macrobenthos and environmental factors in the Yangtze River estuary showed that in each of three areas, echinoderms were closely related to silicate and temperature. This result may be connected to the change in the saline structure of the Yangtze River estuary in recent years. The increase in nitrogen and decrease in silicon may lead to the decrease in diatoms in phytoplankton (Chen, 2009). The decrease in echinoids in macrobenthos in the past decades is consistent with the temporal change in phytoplankton structure. The availability of food to echinoids may be closely associated with the abundance of diatoms. More studies are needed to demonstrate the relationship between echinoids and diatoms. A Portuguese estuarine study (Chainho et al., 2006) found that the benthos structure is altered following changes in fresh- and saltwater inputs. Thus, salt is a main factor that influences the estuarine macrobenthos structure. Teske and Wooldridge (2003) studied 13 estuaries in the Eastern Cape of South Africa and found that the type of sediment, not salt, was found to represent the decisive factor for estuarine benthos structure. Muniz and Pries (2000) as well as Teske and Wooldridge (2003) agreed that the type of sediment is the main factor influencing polychaete structure in São Sebastião Strait in Brazil. Kröncke et al. (2003) proposed that the TOC in sediment is the main factor influencing macrobenthos structure in the eastern Mediterranean Sea area. The findings of the current study regarding the dominant polychaetes and mollusks in the Yangtze River estuary suggest that polychaetes in the estuary are mainly affected by water depth and temperature, whereas those in inshore and offshore areas are mainly affected by water depth and salt. However, mollusks are affected by DO and pH in the three areas. These results indicate that the Yangtze River estuary has a complex environment and that the factors affecting benthos are also very complex. A deeper understanding of the key factors influencing macrobenthos will require further studies involving data collection and appropriate analyses.

Conclusions

A total of 335 species were recorded in the Yangtze River estuary and the adjacent area during four cruise surveys. Two-way ANOVA revealed no significant differences among seasons in all the community parameters (number of species, biomass, and density). However, differences among areas in the number of species, density, and biomass were significant. SIMPER analysis and ABC curve results indicated disturbance in the inshore area. Diluted Yangtze River water appeared to have a relatively great effect on the macrobenthic community in the Yangtze River estuary and adjacent area. Human activities could also be concluded to greatly influence the estuary of the Yangtze River; inshore areas show less human influence and offshore areas show minimal influence. More research should be conducted to study the functional aspects of macrobenthic ecology, given that few reports are available regarding the relationship between macrobenthos and the environment in the Yangtze River estuary and adjacent area.

Acknowledgements

The authors gratefully acknowledge Hu Yue-Mei, Chen Jian-Fang, Li Hong-Liang, and Wang Kui for their assistance in the laboratory and field, as well as the two anonymous reviewers for their valuable comments on the manuscript. The present work was financially supported by the National Basic Research Program of China (973 Program No. 2010CB428903) and the National Special Fund of Chinese Offshore Investigation and Assessment (Nos. 908-01-BC06, 908-ZC-I-02 and 908-01-ST04), and Zhejiang Provincial Natural Science Foundation of China (Y5100401).

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