1 Introduction

The temperate intertidal mudflats were characterized by high productivity and dominated by invertebrate(Pinckney and Zingmark, 1993; McLusky and Elliott,2004). Bivalves play a key role as the primary consumer in these areas and control vital balance between organic matters and predators, as well as benthic and aquatic food webs (Heip et al., 1995). Therefore, many researches have examined the compositions and distributions (Fortin et al., 2002; Legendre and Legendre, 2012), dynamics(Blanchard 1990; Guarini et al., 1998; Kostylev and Erlandsson, 2001; Seuront and Spilmont, 2002; Weerman et al., 2011; Benoit-Bird and McManus, 2012; Benoit-Bird et al., 2013 a, b; Rameshkumar and Rajaram, 2017), and feeding-predating relationship (Sims et al., 2008; Reynolds and Rhodes, 2009; Benoit-Bird and McManus,2012; Beninger and Boldina, 2014) of intertidal benthos.Meanwhile, abiotic factors were also investigated as associated with abundance, composition, and structure of benthic animals (Miller et al., 1996).

The Yellow River, originating from the Loess Plateau and discharging into the Bohai Sea, ranks at the top 6th of the world’s largest river in length, the 20th in water discharge (McKee et al., 2004), and the 1st in particle discharge (1.05×107tons yr −1) (Cui et al., 2009). Thus, a Yellow River Delta (YRD) as well as a broad intertidal mudflat, has been developed at the rates of 0.08-0.30 km yr −1 (Qiao and Shi, 2010). The mud in the intertidal flat is comparatively course with a median grain size of 0.025- 0.081 mm and low content of organic carbon(0.1%- 0.5%), while the nutrients are abundant and higher primary productivity have been discovered spontaneously (Yao et al., 2010; Zhang et al., 2011). As a key species of macro benthos in middle and low intertidal mudflats in North China (Han et al., 2014; Zhang et al.,2016), the southern intertidal mudflat of YRD is abundant in Mactra veneriformis, but it has been unclear how the temporal and spatial distributions of M. veneriformis vary in the intertidal YRD.

一是发展政府领导位置。各级政府起到主导作用，有目的地实施扶贫政策，为培育工作创造良好环境。二是注重市场的作用。在资源配置过程中，市场所起作用是无法忽视的，这也是提高培育质量的基础。三是加强农业主导地位。为了发展新型农业，需要将农业作为主导产业，并结合实际状况，发展特色、优势产业［2］。

In 2007 and 2008, field investigation was carried out in order to examine: 1) temporal and spatial variations of benthic biomasses in the intertidal mudflat of southern YRD, 2) factors affecting the benthic biomasses, and 3)the secondary production and appropriate transformation efficiency from primary production to macro benthos.

东南亚目前没有核电装机容量。该地区核电容量在2040年和2050年的高值情景预测值分别为4 GWe和9 GWe，低值情景预测值分别为1 GWe和3 GWe。

2 Materials and Methods

2.1 Study Area and Sampling Sites

The intertidal mudflat of the southern YRD, which locates at the South-East Bohai, North China, is greatly impacted by the Yellow River. In this study, three sections were selected in the middle of the southern YRD, which covers an area about 6 km long and 3-5 km wide off the coastline (Fig.1). Samples were collected from 11, 10 and 7 sites along Sections A, B and C, depending on the distance between high and low water lines. One time series station (L) was close to the middle water line at Section B.

分离到的20株酵母菌用结晶紫染色后进行镜检，在显微镜下可以看到分离菌株的细胞形态：存在杆状，球状，椭圆形，见图2。

Muds were first collected with an Eckmane Birge grab sampler (24 by 24 cm area to a depth of 30 cm), and then flushed through a 1 mm mesh sieve. Benthic macro fauna,including M. veneriformis, on the sieve were fixed with 10% formalin. The sampling was duplicated at every station. Bivalve M. veneriformis for isotope analysis was kept frozen until laboratory analysis. Surface sediments(0-1 cm) were collected and kept frozen for Chl a and grain size analyses.

Fig.1 Study area and sampling sites in the intertidal area of the southern Yellow River Delta.

2.2 Sampling Methods

Three cruises were carried out in spring tide period, in order to cover the intertidal region as wide as possible in September, 2007, and April and July, 2008. The time series station was monitored every month from July 2007 to July 2008 except January and February 2008 due to ice coverage. Samples were collected from near shore to off shore areas by following the tide cycle and surface sediment exposure time. The furthest sample was collected on the low water line in low tidal region.

2.3 Biomass Analysis of Macro Benthos and Mactra veneriformis

Macrobenthic animals were sorted, counted, and weighted (excess waters were removed with blotting paper) into three groups, which were bivalve - M. veneriformis, shellfish (shells except M. veneriformis) and the others (non shells), using a magnifying glass.

Grain size stands for the benthic background and its distribution may be influenced by current and tide dynamics, accumulation of organic carbon and nutrients,and even redox conditions. Chl a represents for the standing stock and productivity of primary producer,which may serve as an indicator of the potential food source to in situ bivalves. Relationships between Chl a,median grain size, macro benthic biomass, and M. veneriformis biomass were different (Fig.5). The relationships between Chl a and macro benthic and bivalve biomasses were generally segmented into two parts, except several episodic points. A positive relationship between Chl a and macro benthic and bivalve biomasses existed when Chl a concentration was lower than 25 mg m−2, while a negative relationship occurred when Chl a concentration was higher than 25 mg m−2. The feeding interaction may be responsible for these different relationships because microphytobenthos proliferated with Chl a increase corresponding to a positive relationship, while the food supplication by microphytobenthic biomass controlled the benthic bivalves when Chl a was limited, showing a negative relationship. The long time interaction led to the patching distribution of benthic animals and algae (van de Koppel et al., 2008).

2.4 Chl a Analysis

As shown in Figs.5b and 5d, the median grain size primarily was at 0.027-0.081 mm, and the most was in the size smaller than 0.050 mm. It was also observed that,higher macro benthic biomass presented in the sediments with median grain size closing to 0.055 mm, and macro benthic biomass decreased gradually in the sediments with median grain size apart from 0.055 mm. The sediments in smaller grain size generally enriched in organic carbon, which might provide more organic carbon to bivalves. However, oxygen is usually depleted in sediment with smaller grain size and higher organic carbon, which might limit the growth and reproduce of bivalves. It was also observed that the sediments quickly changed from oxic to anoxic conditions from surface to subsurface(0.5-1 cm) in most sampling stations. Meanwhile, low Chl a and organic carbon may be responsible for the low macro benthic biomass in sediment with larger grain size.That is to say, the sediment grain size controlled the Redox conditions and accumulation of organic carbon, and then influenced the macro benthic and bivalve biomasses.For the case in YRD, macro benthos and bivalves tended to reside in the sediment with median grain size of 0.055 mm, due to the food availability and dwelling conditions.

Similar patterns on the biomass distribution of macro benthos in September, 2007, April and July, 2008 were observed: the biomass increased from high tide line to middle tide line and then decreased to the low tide line gradually. About 100 times difference was seen between the high and low total biomass, especially to M. veneriformis. M. veneriformis was hard to be found in high tide area, but it was abundant in middle and low tide areas,accounting for over 90% of the total biomass. This distribution pattern of M. veneriformis was consistent with its habitat of coastal mudflat in middle and low tide areas(Yuan et al., 2006). But it was a little seaward shift compared with those fitted in middle to high tide areas in the sand flat of Midori River Estuary, Japan (Yamaguchi et al., 2004). The total density of macro benthos kept at a similar level from high to middle and then to low tide areas, except several episodic sites in low and high tide areas.

2.5 Statistical Analysis

Pearson’s correlation analysis (PCA) was used to evaluate the relationships between benthic biomass and environmental factors with SPSS software (version 18.0,SPSS Inc.).

3 Results and Discussion

3.1 Distribution of Macro Benthic and M. veneriformis Biomasses

Macro benthos were sorted as three groups: M. veneriformis (M.v.), shells except M. veneriformis (shells except M.v.) and non-shells. 15 species of macro benthos were identified: polychaetes (5 species), mollusca (6 species)and Crustacea (3 species). The total biomass (Fig.2) of macro benthos in September, 2007, April and July, 2008 were 0.72-574.44, 1.28-814.08 and 15.14-1151.00 g wet m−2 and averaged at 87.88, 164.56 and 261.80 g wet m−2.The biomass of M. veneriformis accounted for 75.6%-91.3%, 79.5%-93.4% and 81.2%-91.1% of the total biomass of macro benthos, correspondingly.

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Fig.2 Biomass and density of macro benthos in the intertidal mudflat of the southern Yellow River Delta.

Macro benthic density ranged at 12-868 ind m−2 (Fig.3).The highest density was observed in August, followed by that in July (50.0% of the density in August), and then lower in the other months. M. veneriformis accounted for 17.6%-100.0% of the total density, in which higher percentages in March and November, followed by April and June, and then as low as 17.6%-34.0% from July to September. Although the relative density of M. veneriformis decreased, M. veneriformis biomass increased and kept as the dominant in July and August.

Macro benthic biomass varied largely with locations and sedimentary conditions. It was reported that, the macro benthic biomass averaged at 35.28 g m−2 in the estuarine sediment of YRD (Zhang et al., 1990), which located in the north of study area, and 7.96 g m−2 in the Bohai Sea (Yu et al., 2001), which was at eastward loca-tion from study area. The macro benthic biomass varied among 22.10 and 257.30 g m−2 in the intertidal flats southward from YRD along the coastal line of North-West Pacific Ocean (Gao et al., 2009; Cai et al., 1980;Shao et al., 1980), in which the largest estuarine intertidal flat of Yangtze River was included (44.54 g m−2, Gao et al.,2009). However, the maximum macro benthic biomass might reach 782.5 g m−2 in Shuangtaizi River estuary(Zhang et al., 2016). Meanwhile, in Sato Sea, Japan, located in similar latitude, the macro benthic biomass ranged at 0.4-78.8 g m−2 in coastal area (Yamaguchi et al.,2007). Mostly dominated in the sand flat of Midori River Estuary, Kyushu, Japan, M. veneriformis accounted for 15.2%-28.4% of total numerical composition (Yamaguchi et al., 2004). It appears that macro benthic biomass stood at a higher level in the intertidal mudflat of YRD,compared with other locations. This higher benthic biomass was likely related to and attributed by the aquaculture of M. veneriformis in the southern mudflat of YRD,sowing every spring and growing naturally. Then, two questions are arisen: who supported the higher benthic biomass, and would this higher benthic biomass be sustained?

Fig.3 Monthly density and biomass of macro benthos in the intertidal mudflat of southern Yellow River Delta.

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Monthly biomass of macro benthos at time series station from August 2007 to July 2008 varied among 36.96-655.57 g wet m−2, with an average of 301.37 g wet m−2(Fig.3). The biomass in June, July and August reached high levels as 500 gww m−2, followed by those in April at about 450 g wet m−2, and decreased below 50 g wet m−2 in March and December at last. A difference of 16 times was observed between the higher biomass in August and lower in December. Same as the seasonal biomass pattern,monthly benthic biomass was primarily contributed by M.veneriformis which was more than 50%, and even close to 100% in March and November.

3.2 Factors Affecting the Macro Benthic Biomass

Multiple factors influence the growth and distribution of macro benthos and bivalves. Based on the spontaneously monitoring parameters, the relationship between the macro benthic biomass and temperature, salinity, sediment grain size, pH and Chl a were analyzed by PCA method (Fig.4). It was revealed that, temperature was the most positively related with macro benthic biomass (r =0.8159). Salinity followed and negatively influenced the macro benthic biomass (r = −0.6152), suggesting that macro benthic animals preferred higher temperature but lower salinity in a certain range.

Fig.4 Relationship between macro benthic biomass and environmental factors in study area by PCA analysis.

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Fig.5 Distributions of macro benthic and M. veneriformis biomasses, Chl a content and median grain size in sediment of the southern Yellow River Delta.

Chl a samples were thawed in room temperature,extracted with 90% acetone at 4℃ in dark overnight, and measured by fluoresce spectrometry. Pure Chl a (Sigma)were quantified by spectrometry (Jeffery and Humphrey,1975) and then diluted as standard for fluorescence spectrometry (Hitachi F-4500, Germany).

3.3 Estimation on the Local Secondary Production

According to the density and biomass of macro benthos,secondary production was estimated by the following equation in the intertidal mudflat of YRD (Yu et al.,2001).

in which, P (g m−2yr−1) represents the secondary production, A (ind m−2yr −1) and B (g m−2yr −1) represent the density and biomass of macro benthos, separately. The estimations on spatial and monthly secondary production(Figs.6 and 7) showed that in the intertidal mudflat of southern YRD, the spatial distributions of secondary production followed a quite similar pattern with those of macro benthic biomass and density, but the higher values concentrated in the middle and low tide lines. The variations of secondary production showed that, macro benthos reproduced more in early summer and the highest in August, while M. v. reproduced the highest in July.

Fig.6 Spatial secondary production of macro benthos in the intertidal mudflat of southern Yellow River Delta.

Fig.7 Monthly secondary production of macro benthos in the intertidal mudflat of southern Yellow River Delta.

Secondary productions ranged at 0.37-44.75 g m−2yr−1(average 9.69 g m−2yr−1), 0.64-230.62 g m−2a−1 (average 50.08 g m−2yr−1) and 6.64-283.68 g m−2yr−1 (average 79.43 g m−2yr−1) in September 2007, April and July 2008. The monthly secondary production averaged at 47.88 g m−2yr−1,in which 69.7% of the production was contributed by M.veneriformis. This higher secondary production, corresponding to higher macro benthic biomass, might be caused by the aquaculture activity in the intertidal mudflat, which was comparable with other similar aquaculture areas, such as the higher benthic secondary production of 47.34 g m−2yr−1 in Jiaozhou Bay, north China (Yuan et al.,2007). Simultaneously, the primary production ranged at 116.07-2779.8 g m−2yr−1 (average 696.48 g m−2yr−1) in the benthic environment (Yao et al., 2010). Thus, a transformation rate of about 6.87% was calculated from primary to secondary productions. Considering the general 10%transformation efficiency from primary to secondary productions, it was implied that the in situ primary production sufficiently supported the sustainability of macro benthos in the intertidal mudflat of southern YRD.

In addition, a 3.13% of primary production was remained in the intertidal sediment and/or transported to offshore area. Water dynamics, both tiding and current in the intertidal zone was quite active, by which the surface sediment was disturbed heavily. The heavy disturbance not only re-suspended and removed the microphytobenthos into the overlying water, but also transported microphytobenthos from shallow to deep waters (Colijn and de Jonge, 1984; Varela and Penas, 1985; Sullivan and Moncreiff, 1988; Cahoon and Cooke, 1992). Due to the presence of the coarse sediment and low OC content of 0.1%-0.5% (Yao et al., 2010), it was suggested that majority of the 3.13% primary production was likely transported to offshore area in study area.

4 Conclusions

Shellfish ranching was highly developed in the mudflat of southern Yellow River Delta, in which M. veneriformis was one of the key species. One year investigations showed that, the biomass of macro benthos varied widely at 0.75-1151.00 g wet m−2, in which higher biomass and productivity occurred in early summer, and more than 90% macro benthos was located in the middle and low tide lines. Multiple factors affected on the growth and biomass of M. veneriformis, including both sediment background (temperature, salinity and grain size) and potential food source of microphytobenthos. 75.6%-93.4% of the total macro benthic biomass was contributed by M. veneriformis. However, it was suggested that the high production of M. veneriformis would be sustainable in the mudflat of southern Yellow River Delta, based on the ratio of secondary production to primary production(6.87%).

Acknowledgements

The study is supported by the National Natural Science Foundation of China (No. 41176064), and NSFC-Shandong Joint Fund for Marine Science Research Centers(No. U1406403).

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