J. Ocean Univ. China (Oceanic and Coastal Sea Research)https://doi.org/10.1007/s11802-018-3313-4
ISSN 1672-5182, 2018 17 (2): 437-444
http://www.ouc.edu.cn/xbywb/
E-mail:xbywb@ouc.edu.cn

Seasonal and Spatial Variations of Macro Benthos
in the Intertidal Mudflat of Southern Yellow River
Delta, China in 2007/2008
ZOU Li1), 2), *, YAO Xiao3), YAMAGUCHI Hitomi4), GUO Xinyu5), GAO Huiwang1), 2),
WANG Kai2), and SUN Mingyi6)1) Key Laboratory of Marine Environmental Science and Ecology, Ministry of Education, Ocean University of China,
Qingdao 266100, China
2) College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
3) Dongying Environmental Protection Bureau, Dongying 257091, China
4) Faculty of Agriculture, Kagawa University, 2393 Ikenobe, Kita, Miki 7610795, Japan5) Affiliation & Position National University Corporation Ehime University, Ehime 79085775, Japan
6) Department of Marine Sciences, University of Georgia, Athens 30602-3636, USA(Received September 20, 2016; revised March 20, 2017; accepted May 29, 2017)© Ocean University of China, Science Press and Springer-Verlag GmbH Germany 2018
Abstract In order to examine the seasonal and spatial distributions of benthic animals in the intertidal mudflat of the southern
Yellow River Delta, field investigations were carried out in 2007 and 2008 and multiple methods were applied. Results showed that,the biomass of macro benthos ranged at 0.751151.00 g wet m−2 and averaged at 156.31 g wet m−2, in which Mactra veneriformis
accounted for 75.6%93.4% of the total macro benthic biomass. More than 90% of macro benthos inhabited in the middle and low
tide lines, and higher biomass occurred in early summer and lower in winter. Statistical analysis showed that: 1) M. veneriformis
growth was primarily favored at higher temperature and lower salinity; 2) after long time interaction, benthic bivalve grazers led topatching distributions of Chlorophyll a (Chl a); 3) macro benthic biomass positively related with Chl a when the concentration of
Chl a was low, but they were negatively related when Chl a concentration was high; and 4) furthermore, the biomass of benthic bivalves peaked in the sediment with median grain size about 0.55 mm, but decreased gradually in coarse or fine sediments. The secondary productivity ranged at 0.37283.68 g m−2yr−1 and averaged at 47.88 g m−2 yr −1, in which 69.7% was contributed by M. veneriformis It was estimated that primary production was transformed to secondary production at a rate of 6.87% approximately, which
implies that there is a local sustainability of high bivalve production.
Key words macro benthos; Mactra veneriformis; distribution; intertidal mudflat; southern Yellow River Delta

1 Introduction
The temperate intertidal mudflats were characterizedby 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 foodwebs (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 etal., 2011; Benoit-Bird and McManus, 2012; Benoit-Bird
et al., 2013 a, b; Rameshkumar and Rajaram, 2017), and* Corresponding author. Tel: 0086-532-66782260
E-mail: zouli@ouc.edu.cn

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 ofbenthic 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 iscomparatively 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

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macro benthos in middle and low intertidal mudflats inNorth China (Han et al., 2014; Zhang et al., 2016), thesouthern intertidal mudflat of YRD is abundant in Mactra
veneriformis, but it has been unclear how the temporaland spatial distributions of M. veneriformis vary in theintertidal YRD.
In 2007 and 2008, field investigation was carried out inorder to examine: 1) temporal and spatial variations ofbenthic 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.

2 Materials and Methods
2.1 Study Area and Sampling Sites
The intertidal mudflat of the southern YRD, which lo-

cates 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 thecoastline (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.
Three cruises were carried out in spring tide period, inorder to cover the intertidal region as wide as possible in
September, 2007, and April and July, 2008. The timeseries 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.

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

2.2 Sampling Methods
Muds were first collected with an Eckmane Birge grab
sampler (24 by 24 cm area to a depth of 30 cm), and thenflushed 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 andgrain size analyses.
2.3 Biomass Analysis of Macro Benthos andMactra veneriformis
Macrobenthic animals were sorted, counted, andweighted (excess waters were removed with blotting paper) into three groups, which were bivalve  M. veneriformis, shellfish (shells except M. veneriformis) and theothers (non shells), using a magnifying glass.
2.4 Chl a Analysis
Chl a samples were thawed in room temperature,
extracted with 90% acetone at 4℃ in dark overnight, andmeasured 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).

2.5 Statistical Analysis
Pearson’s correlation analysis (PCA) was used toevaluate the relationships between benthic biomass andenvironmental 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 exceptM.v.) and non-shells. 15 species of macro benthos wereidentified: polychaetes (5 species), mollusca (6 species)
and Crustacea (3 species). The total biomass (Fig.2) ofmacro 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%

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91.3%, 79.5%93.4% and 81.2%91.1% of the total biomass of macro benthos, correspondingly.
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 reachedhigh levels as 500 gww m−2, followed by those in April at439

about 450 g wet m−2, and decreased below 50 g wet m−2 inMarch and December at last. A difference of 16 times
was observed between the higher biomass in August andlower 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.

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 bythat in July (50.0% of the density in August), and thenlower 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 andJune, 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, themacro 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-

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tion from study area. The macro benthic biomass variedamong 22.10 and 257.30 g m−2 in the intertidal flats
southward from YRD along the coastal line of NorthWest 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 biomassmight 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 biomassstood 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, twoquestions are arisen: who supported the higher benthic
biomass, and would this higher benthic biomass be sustained?

similar level from high to middle and then to low tideareas, except several episodic sites in low and high tideareas.

3.2 Factors Affecting the Macro Benthic Biomass
Multiple factors influence the growth and distributionof macro benthos and bivalves. Based on the spontaneously monitoring parameters, the relationship between themacro 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 themost positively related with macro benthic biomass (r =0.8159). Salinity followed and negatively influenced themacro benthic biomass (r = −0.6152), suggesting thatmacro benthic animals preferred higher temperature but
lower salinity in a certain range.

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

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

Similar patterns on the biomass distribution of macro
benthos in September, 2007, April and July, 2008 wereobserved: 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 tidearea, 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 thesand flat of Midori River Estuary, Japan (Yamaguchi etal., 2004). The total density of macro benthos kept at a

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 foodsource 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 andmacro benthic and bivalve biomasses existed when Chl aconcentration 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 thebenthic bivalves when Chl a was limited, showing anegative relationship. The long time interaction led to thepatching distribution of benthic animals and algae (van deKoppel et al., 2008).

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441

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

As shown in Figs.5b and 5d, the median grain size primarily was at 0.0270.081 mm, and the most was in thesize smaller than 0.050 mm. It was also observed that,higher macro benthic biomass presented in the sedimentswith median grain size closing to 0.055 mm, and macro
benthic biomass decreased gradually in the sedimentswith median grain size apart from 0.055 mm. The sediments in smaller grain size generally enriched in organiccarbon, which might provide more organic carbon to bivalves. However, oxygen is usually depleted in sedimentwith smaller grain size and higher organic carbon, whichmight limit the growth and reproduce of bivalves. It wasalso observed that the sediments quickly changed fromoxic 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, andthen 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.

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).
LgP = 0.27LgA + 0.737LgB − 0.4,

(1)

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 ofsouthern 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.

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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 becaused by the aquaculture activity in the intertidal mudflat, which was comparable with other similar aquacultureareas, 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 at116.072779.8 g m−2yr−1 (average 696.48 g m−2yr−1) in thebenthic 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 tooffshore area. Water dynamics, both tiding and current in
the intertidal zone was quite active, by which the surface
sediment was disturbed heavily. The heavy disturbancenot only re-suspended and removed the microphytobenthos into the overlying water, but also transported microphytobenthos from shallow to deep waters (Colijn and deJonge, 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

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showed that, the biomass of macro benthos varied widely
at 0.751151.00 g wet m−2, in which higher biomass andproductivity 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 andbiomass of M. veneriformis, including both sediment
background (temperature, salinity and grain size) andpotential food source of microphytobenthos. 75.6%
93.4% of the total macro benthic biomass was contributedby M. veneriformis. However, it was suggested that thehigh 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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(Edited by Ji Dechun)