Five cruise surveys were carried out in May–June 2013 to evaluate the status of macrobenthic diversity and distribution in Subei Shoal, China. Twenty-four stations were sampled and divided into four groups according to depth (5–10 m, 10–20 m, 20–30 m and 30–35 m). A total of 163 species were collected with Polychaeta dominating in species composition and abundance. All of the community parameters (abundance, biomass, mean species richness, Margalef richness index, Shannon-Wiener index and Pielou's evenness) were not significantly different among the five cruises or among the four groups, except that Shannon-Wiener index at 5–10 m was significantly lower than that in other depth groups. No significant difference in community structure was detected among cruises, but when the data from the same station were pooled together, significant differences among stations were observed basically from inshore to offshore. The benthic opportunistic polychaetes amphipods index showed four stations having moderate ecological status in Subei Shoal. Canonical correspondence analysis showed that Sigambra bassi and Praxillella sp. were positively correlated with depth and salinity, and Paralacydonia paradoxa was positively correlated with dissolved oxygen.

Introduction

Macrobenthos communities are key components in the functioning of marine and coastal systems (Lu, 2005). Benthic fauna can promote nutrient cycling, organic matter decomposition, and provide direct food sources for fishes and large crustaceans of economic importance (Gaudéncio and Cabral, 2007; Zhang et al., 2013). They can also bring about considerable variations in physical and chemical elements of marine bottom sediments, especially in the water-sediment interface (Gaudéncio and Cabral, 2007; Shou et al., 2009). Most of the macrobenthic fauna live in the surface of the seabed with high organic matter and oxygen concentration (Shou et al., 2009). They can be used as biological indicators of the health of marine and coastal environments (Jayaraj et al., 2007; Hampel et al., 2009).

Subei Shoal is considered one of the largest muddy seabeds in Asia (Yi and Liu, 2007), located in southwest Yellow Sea, adjacent to Jiangsu Province in China (Figure 1). The hydrological regime of Subei Shoal is mainly influenced by the Yellow Sea coastal water, the Yangtze River diluted water and the Yellow Sea Cold Water Mass (YSCWM) (Que et al., 2012). The ecosystem of Subei Shoal has been affected by water pollution, eutrophication, and habitat fragmentation, and biodiversity is at a very low level (Zhang et al., 2009) and overall ecosystem health is poor (Yi and Liu, 2007). The Ulva prolifera blooms (green tides) occurred in Yellow Sea every summer since 2007 and Subei Shoal was considered as a primary source location because of the Porphyra aquaculture activities (Liu et al., 2013) and a critical area to study the mechanisms in the formation of green tides in Yellow Sea (Zhou et al., 2015). The macrobenthos can be used to assess the status of Subei Shoal ecosystem, as many of some of the species in degraded areas have short life cycles, mature rapidly and have higher reproductive capacities such as opportunistic species Capitella capitata (Zhang et al., 2013). The benthos are also important food resources of commercial fishes and large crustaceans that forage on Subei Shoal both temporarily and permanently, as also occurs in the Georges Bank and the Ship Shoal in the coast of USA (Thouzeau et al., 1991; Dubois et al., 2009). Some field investigations on the Subei Shoals have been carried out (Dubois et al., 2009; Fan et al., 2010; Que et al., 2012), but the knowledge of the benthic faunal composition is much less than that on other continental shelf environments (Brooks et al., 2006; Dubois et al., 2009).

The objectives of this study were to analyze the species composition, diversity and spatial distribution of macrobenthos in Subei Shoal, to compare current species composition and abundance to previous surveys, to assess the ecological status of macrobenthic community, and to examine relationships between the dominant species and environmental parameters.

Materials and methods

Study area and sampling design

Twenty-four stations (31.75 to 33.5°N in latitude and 121.25 to 122.75°E in longitude) were situated in Subei Shoal (Figure 1) to investigate macrobenthos and environmental parameters and divided into four groups according to depth (5–10 m, 10–20 m, 20–30 m and 30–35 m). Samples were taken during five cruises in May–June 2013: First (5–7 May), Second (13–15 May), Third (20–21 May), Fourth (29 May–1 June) and Fifth (5–6 June). Duplicate benthic samples were collected at each station using a modified 0.1 m2 Gray-O’ Hara box-corer. Samples were sieved on a 0.5 mm mesh sieve in the field and then preserved in 75% ethanol for subsequent sorting. Environmental parameters (temperature, salinity and dissolved oxygen) were measured about 1 m above the sea bottom using a CTD meter (Alec Electronics, AAQ1183-IF mode). In the laboratory, macrobenthic samples were identified to the lowest possible taxonomic level, counted and weighted (wet weight; shells included for Mollusca).

Data analysis

For each sample, global species richness (Global S), mean species richness (Mean S), Margalef richness index (d), Shannon-Wiener index (H’, loge), Pielou's evenness (J’), abundance (ind. m−2) and biomass (g m−2) were calculated. One-way ANOVA was applied to test the temporal and spatial trends in biotic parameters of macrobenthic community using SPSS (version 16). Kolmogorov-Smirnov test was performed for the normality and Levene's test for the homogeneity of variances. Mean species richness and biomass were loge(x+1) transformed, and d and J' were tested using the Kruskal-Wallis test for the unequal variances. Tukeys HSD for unequal number of samples were used for post hoc comparison of means.

Multivariate macrobenthic community analysis was performed through PRIMER (version 6). Differences in the macrobenthic community structure between stations were determined using cluster analysis (Clarke and Warwick, 2001) and the significantly different station groups were detected using similarity profile (SIMPROF) tests (Clarke et al., 2008). Before analysis, we constructed the Bray-Curtis similarity matrices based on fourth-root transformed abundance data (Clarke and Warwick, 2001). Species with their occurrence frequency less than 5% were eliminated to minimize effects of rare species (Almeida et al., 2008). Analysis of similarities (ANOSIM) was performed to assess the statistical significance of differences among cruises and stations (Clarke, 1993). Similarity percentage (SIMPER) routines was employed to detect the species contributing mostly to the Bray-Curtis similarity in each cruise or station group.

The benthic opportunistic polychaetes amphipods (BOPA) index was employed to detect the ecological status of macrobenthic community. The formula is:
formula

where fP is the percentage of numbers of opportunistic polychaete individuals to numbers of all individuals in the sample; fA is the percentage of numbers of amphipod individuals (except the opportunistic Jassa amphipods) to numbers of all individuals in the sample (Dauvin and Ruellet, 2007). The BOPA boundaries were used to define five ecological quality status classes (high, good, moderate, poor and bad) according to Dauvin and Ruellet (2007).

Canonical correspondence analysis (CCA) was used to analyze the correlations between environmental parameters (depth, temperature, salinity and dissolved oxygen) and the dominant species using CANOCO (version 4.5) software (Ter Braak and Šmilauer, 2002). CCA was appropriate for data analysis as in the preliminary detrended correspondence analysis (DCA) the lengths of gradient for the first axis was 3.879 SD > 3 SD.

Results

Environmental variables

No obvious change was observed among five cruises for all environmental variables. Pooling the data from different cruises together, we found that salinity increased while temperature decreased with depth (see Appendix 1 in the online supplementary files). Dissolved oxygen was similar among the 4 depth groups.

Species composition and diversity

In total, 163 macrobenthic species were identified from Subei Shoal over all five sampling cruises. Polychaeta represented 43.6% (71 species) of the Global S, followed by Mollusca (25.8%, 42 species), Crustacea (19.6%, 32 species), Echinodermata (6.7%, 11 species) and others (Nemertea, Actinia, Sipunculida etc. 4.3%, 7 species). For Mean S, diversity index (d, H' and J'), abundance, and biomass, no significant difference was detected (P > 0.05, one-way ANOVA) among cruises, so we pooled the data from different cruises together to examine the spatial trends. The Mean S and diversity index increased with depth (Table 1). However, no significant difference was detected among depth for these index (P > 0.05) except that H' in 5–10 m was significantly lower than that in other depth groups (unequal HSD, P < 0.05).

The mean abundance of macrobenthic community in 4 depth groups were 111.1, 107.8, 148.9 and 118.1 ind. m−2, respectively (Figure 2a). Polychaeta increased with depth, and accounted for 30.5, 76.0, 79.8 and 80.5% of total abundance in the 4 depth groups, respectively. The mean biomass of macrobenthos were 4.9, 5.1, 7.7 and 2.5 g m−2, respectively (Figure 2b). No significant differences were detected for abundance and biomass among depth (P > 0.05, one-way ANOVA).

Macrobenthic community classification

No significant differences among five cruises were detected through ANOSIM test (Global R = −0.015, P = 0.63), so we pooled the abundance data from the same station together (average value) for further analysis. Cluster analysis showed significant differences among stations and SIMPROF test identified four main groups basically from inshore to offshore (Figure 3). ANOSIM test revealed significant differences in macrobenthos composition among the four groups (Global R = 0.848, P = 0.001) and SIMPER analysis showed the main macrobenthic contributors within each group (see Appendix 2 in the online supplementary files). Group 1 was situated in the northwest of Subei Shoal and dominated by Mysidae. Group 2, located in the west of the Subei Shoal, was dominated by Nephtys oligobranchia, P. paradoxa, Glycera chirori and Magelona cincta. Group 3, in which N. oligobranchia and P. paradoxa were the most abundant species as in Group 2, followed by Nereis longier, Sigambra bassi and Notomastus latericeus, was situated in the middle and east of Subei Shoal. Group 4 was scattered in the northeast and south of Subei Shoal, dominated by Praxillella sp., N. latericeus, N. oligobranchia, Tharyx multifilis and Aricidea fragilis. All of the dominant species were Polychaeta except for Mysidae. The abundance of dominant species in each station (average value) were listed in Appendix 3 (see the online supplementary files).

Ecological status of macrobenthic community

The plot of BOPA index showed 4 stations (16.7% of total stations; D4, K3, Kb and I4) having moderate ecological status (Figure 4), of which 3 stations (D4, K3 and I4) were situated along 20 m bathymetric contour (Figure 1). Other stations had good (6 stations; 25%) or high ecological quality status (14 stations; 58.3%). At those moderately disturbed stations, high colonization by opportunistic polychaetes Paraprionospio pinnata (26.67 and 58.75 ind. m−2 at D4 and K3, respectively, in average during five cruises), Aonides oxycephala (37.5 ind. m−2 at I4), T. multifilis (31.25 ind. m−2 at K3) and N. latericeus (35 ind. m−2 at Kb) and low abundance of amphipods were observed (1.67 ind. m−2 of Orchomene breviceps at D4; 12.5 ind. m−2 of Sinurothoe sp. at I4; 1.25 ind. m−2 of both Ampelisca bocki and Melita longidactyla at K3, respectively; no amphipods at Kb).

Relationship between macrobenthos and environmental variables

The relationship between macrobenthos and environmental variables was detected by CCA, which explained more than 28% of the species abundance variation (see Appendix 4 in the online supplemental files). The results were interpreted in consideration of only the first two axes because they cumulatively explained 19.9% of the species data variance and 70.7% of the species-environment relation variance. Most of the species were positively correlated with the first axis, and negatively with depth and salinity (Figure 5). Mysidae, dominated only in Group 1, the shallowest part of Subei Shoal, occurred in the right of the CCA ordination diagram. S. bassi and Praxillella sp., the main contributor in Group 3 and Group 4, were positively correlated with depth and salinity, located in the left of the diagram. P. paradoxa, the main contributor in Groups 2 and 3, was positively correlated with dissolved oxygen (DO for short) and situated in the bottom of the CCA diagram.

Discussion

Community characteristics of macrobenthos in Subei Shoal

In our study in spring 2013, Polychaeta were the largest contributor for the Global S, followed by Mollusca and Crustacea. This compared to results of a study in autumn 2007 which reported 68 species of Polychaeta (46.6% of Global S), 31 Mollusca (21.5%) and 30 Crustacea (20.5%) in Subei Shoal (the geographic coordinate range of most stations was the same with ours in water depth >10 m) (Fan et al., 2010). In our study, mean S and diversity index showed an increasing trend with depth, agreeing with the result in 2007 (Fan et al., 2010). However, the composition of macrobenthos in Subei Shoal has experienced a tremendous change in the past six years. Polychaeta (71.7% of total abundance in 2013; 42.8% in 2007), especially the opportunistic species such as P. pinnata, has replaced Crustacea (8.0% in 2013; 25.1% in 2007) and Echinodermata (7.7% in 2013; 14.9% in 2007) as the important colonies in Subei Shoal (Fan et al., 2010). The shifts in the dominance of taxonomic groups may be the result of anthropogenic influences (Obolewski and Glińska-Lewczuk, 2011). For instance, Porphyra aquaculture (covering >20,000 ha) in Subei Shoal has expanded since 2006 (Liu et al., 2013), and the facilities of Porphyra aquaculture provided the substrate for the growing of U. prolifera, which caused the U. prolifera blooms (green tides) since 2007 (Shi et al., 2015). A considerable amount of untreated industrial wastewater and sewage were discharged into Subei Shoal every year, which has also threatened the ecology and environment of Subei Shoal (Zhang et al., 2009).

Cluster analysis showed significant differences among stations and four groups were identified basically from inshore to offshore. The divergence between the inshore group stations (Group 1, station A2 and I1) and the other stations was greater than the divergence among other stations (Figure 3). Station A2 and I1 were located in the west of Subei Shoal, closer to the mainland than most of the other stations, so they might be more easily influenced by human activities and tides. The sandy sediment type of A2 and I1 also made the two stations different from others, most of which having the muddy sediment type. The well sorted mobile sands were characterized by dominance of mobile polychaetes and crustaceans (Van Hoey et al., 2004), as found in station A2 and I1, which were dominated by Mysidae, followed by Glycera capitata, a kind of worldwide distributed polychaete with the large niche width. Group 2 and Group 3 were dominated by N. oligobranchia and P. paradoxa (Appendix 2), different from the investigation result in the same area in 2007, which showed the dominance of Paraprionospio sp., N. latericeus, Sternaspis scutata, Tellinidae and Terebellides stroemii (Fan et al., 2010). In our study, only six species belonging to Tellinidae were identified (Semelangulus miyatensis at station D2 and Semelangulus hungerfordi at A3 in first cruise; Moerella nishimurai and Cadella delta at K4 in second cruise; Moerella sp. at A3 and D2 in third cruise; Cadella narutoensis at D5 in fifth cruise), but most of them were in low abundance (5–10 ind. m−2 in the station which the species occurred) with low occurrence frequency.

Ecological status assessment of macrobenthic community

The BOPA index has been proven to be a useful tool in assessing the ecological quality status of the coastal and estuarine area (Dauvin and Ruellet, 2007; Zhang et al., 2013). In Subei Shoal, the BOPA index showed that four stations were moderately disturbed (moderate ecological status in Figure 4). These stations were located adjacent to the 20 m bathymetric contour (Figure 1). Perhaps because of the wave turbulence, unstable substrates, and other variables, high abundance of opportunistic polychaete species such as P. pinnata, A. oxycephala, N. latericeus and T. multifilis were detected at these four stations. These small and fast-growing r-selected polychaete species are the pioneer forms which dominated in the initial succession stages after disturbance (Giangrande et al., 2005). Like the representative opportunistic polychaete species–C. capitata (Giangrande et al., 2005), the life history traits of the polychaete species mentioned above give them ability to develop dense populations rapidly. Contrast to the high abundance of opportunistic polychaete species, low colonization by amphipods were also observed in the four stations. Amphipods are “structural” species of the macrobenthic community and can be good indicators of environment recovery (Goméz-Gesteira and Dauvin, 2000). They can live in the previously anoxic sediment within their burrows or tubes and create small oxidized cylinders which allows oxygenation and nitrification process in the sediment (Zhang et al., 2013). Other stations were in good or high ecological status, indicating slightly disturbed or undisturbed environmental condition (de-La-Ossa-Carretero et al., 2009).

Relationship between macrobenthos and environmental variables

The CCA biplot indicated that depth and dissolved oxygen were the most important environmental factors influencing the macrobenthos (Figure 5). Depth has been identified as one of important factors influencing the macrobenthic communities in many surveys worldwide (Zimmermann, 2006; Dolbeth et al., 2007; Shou et al., 2013; Peng et al., 2014). The depth gradient was often in accordance with the inshore to offshore gradient, which reflected other variations such as salinity and anthropogenic stressors. In this study, only two dominant species (S. bassi and Praxillella sp.) were positively correlated with depth (Figure 5). Both of these polychaete species have a wide distribution. S. bassi is also found in the intertidal zones of North Carolina, South Florida and California in America and Praxillella sp. in Arctic, Mediterranean and Japan (Yang and Sun, 1988). But in Yellow Sea, both of these two species lived in the area deeper than 20 m (Yang and Sun, 1988). Other species showed negative relationship with depth (Figure 5). The negative relationship between polychaetes (except S. bassi and Praxillella sp.) and depth in our study was not consistent with the result in Yangtze River estuary and adjacent area (south of the Subei Shoal), which indicated that polychaetes were positively correlated with depth both in the inshore and offshore area (Shou et al., 2013). Therefore, more studies are needed to clarify the relationship between polychaetes and depth. Dissolved oxygen was another important factor influencing macrobenthos (Lim et al., 2006). Low DO levels (i.e., DO < 2 mg l−1) have negative effects on macrobenthos. In this study, P. paradoxa, which was also collected in Mediterranean, South Africa, North America and Indonesia (Yang and Sun, 1988), was positively correlated with dissolved oxygen (Figure 5). When the DO was not the critical factor, the effects of other factors emerged. The lowest level of DO in this study was 6.62 mg l−1 at station Kb (average during five cruises), which was well above the level of hypoxia. Thus the negative relationship between DO and the main species may be due to other factors such as interspecific competition and predation which may be more intense as the DO increases and have a more negative effect on some polychaetes. However, P. paradoxa may take the lead in the competition as it was positively correlated to DO (Figure 5) and found to be dominant in this study and other studies (La Porta et al., 2009; Seo et al., 2014). Other environmental factors such as the characteristics of sediment, the nutritive concentrations in the water on the bottom, and biotic factors (the abundance of fish and other nektons which feed on the macrobenthos) need to be added in the future research.

Conclusions

A total of 163 macrobenthic species were collected in Subei Shoal during five cruises. One-way ANOVA results showed that all community parameters were not significantly different among depth groups except that H' in 5–10 m was significantly lower than that in other depth groups. Significant differences in community structure of macrobenthos among stations were detected basically from inshore to offshore. BOPA index exhibited that four stations had moderate ecological status in Subei Shoal. Depth, salinity and dissolved oxygen appeared to be the main factors influencing the pre-dominate macrobenthic species. However, more investigations should be conducted to determine whether other environmental factors and biotic factors would influence macrobenthos in Subei Shoal.

Acknowledgements

We thank Dong Dong, Gan Zhi-Bin, Kou Qi, Ma Lin, Sui Ji-Xing, Wang Jin-Bao and Wang Yue-Yun for their work in the field and laboratory. We also appreciate the valuable comments on the manuscript by the anonymous reviewers.

Funding

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA11020303), the National Natural Science Foundation of China (No. 41176133) and the National Basic Research Program of China (No. 2011CB403605).

Supplemental material

Supplemental data for this article can be accessed on the publisher's website.

The text of this article is only available as a PDF.

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