Changes in the Shelf Macrobenthic Community Over Large Temporal and Spatial Scales in the Bohai Sea, China ⁎ H

Journal of Marine Systems 67 (2007) 312–321 www.elsevier.com/locate/jmarsys

Changes in the shelf macrobenthic community over large temporal and spatial scales in the Bohai Sea, China ⁎ H. Zhou a, Z.N. Zhang a, , X.S. Liu a,b, L.H. Tu c, Z.S. Yu a

a College of Marine Life Science, Ocean University of China, 5 Yushan Road, Qingdao 266003, PR China b Department of Biology and Chemistry, City University of Hong Kong, Hong Kong SAR, PR China c Department of Life Science, Capital Normal University, Beijing, PR China Received 5 December 2005; received in revised form 30 April 2006; accepted 30 April 2006 Available online 19 October 2006

Abstract

Over the past 20 years, the Bohai Sea has been subjected to a considerable human impact through over-fishing and pollution. Together with the influence of the Yellow River cut-off, the ecosystem experienced a dramatic change. In order to integrate available information to detect any change in macrobenthic community structure and diversity over space and time, data collected during the 1980s and the 1990s from 3 regions of the Bohai Sea (Laizhou Bay, 16 stations, 37–38°N, 119–120.5°E; central Bohai Sea, 25 stations, 38–39°N, 119–121°E; eastern Bohai Bay, 12 stations, 38–39°N, 118.5–119°E) were reanalyzed in a comparative way by means of a variety of statistical techniques. A considerable change in community structure between the 1980s and the 1990s and over the geographical regions at both the species and family level were revealed. After 10 years, there was a considerable increase in abundance of small polychaetes, bivalves and crustaceans but decreased number of echinoderms. Once abundant in Laizhou Bay in the 1980s, a large echinoderm Echinocardium cordatum and a small mussel Musculista senhousia almost disappeared from the surveying area in the 1990s. Coupled with the increased abundance was the increased species richness in general whereas evenness was getting lower in central Bohai Sea and Bohai Bay but increased in Laizhou Bay. K-dominance plot showed the same trend as evenness J′. After 10 years, the macrobenthic diversity in the Bohai Sea as a whole was slightly reduced and a diversity ranking of central Bohai SeaNLaizhou BayNeastern Bohai Bay over space was also suggested. Sediment granulometry and organic content were the two major agents behind the observed changes. © 2006 Elsevier B.V. All rights reserved.

Keywords: Changes; Macrobenthos; Community composition; Diversity; Bohai Sea (37°07′–41°00′N, 117°35′–121°10′E)

1. Introduction and an average depth of 18 m, with a maximum depth of 80 m. More than one hundred rivers flow into it, with a The Bohai Sea, located between 37°07′–41°00′N and total annual run-off of 8.88×1010 m3, nearly half of 117°35′–121°10′E in north Pacific, is a marginal inland which is contributed by the Yellow River (Huanghe), the sea enclosed by the Liaodong and Shandong peninsulas second largest river in China. The Yellow River plays a and connected with northern Yellow Sea by the Bohai fundamental role in controlling the ecosystem dynamics Strait (Fig. 1). It has an extension of about 7.7×104 km2 and function. Each year, it exports large quantities of sediment of about 12×108 t, representing approximately ⁎ Corresponding author. Tel./fax: +86 532 2032716. 10–15% of the total world riverine sediment load (Zhang E-mail address: [email protected] (Z.N. Zhang). et al., 1990) and leading to a quick delta building at the

Fig. 1. Map of sampling stations in the Bohai Sea. stations sampled in the 1980s; stations sampled in the 1990s. river mouth. It also determines the nutrient flux and had drawn great concern to the Chinese government and salinity of the Bohai Sea by total runoff. Bohai Sea has an agency, which invest considerable effort in monitoring annually average salinity of 30‰,26‰ at the coastal the environment. area and 22‰ adjacent to the river mouth. Its sediments During 1997–1999, the first Chinese GLOBEC are dominated by fine particles of silt–clay, especially in project, Processes of the Bohai Sea Ecosystem Dynam- the coastal Liaodong Bay, Bohai Bay and Laizhou Bay, ics was initiated which included annual sampling for but with relatively high sand component at the middle macro- and meiobenthos from a large-scale grid of basin and strait region. There exists a strong seasonal stations (Su and Tang, 2002). The present study thermocline and the surface water temperature can be up compares macrofaunal data with historical data collect- to 28 °C in summer in the coastal area and 24 °C in the ed during the Sino-US Joint Investigation of the middle basin; in winter, surface temperature can be as Huanghe Estuary Sedimentation Dynamics during low as 0–2 °C and even below zero in the three bays. 1985–1987. The aim of the study was to (1) detect The Bohai Sea is of great commercial importance as any change in the macrobenthic system over a decadal one of the major fishing areas in China and important temporal scale and over a regional spatial scale, with spawning and feeding grounds for many species of fish, respect to species composition, community structure shellfish and shrimp such as Penaeus chinensis. Over and diversity; (2) provide evidence of a changed eco- the past 20 years, it has been subjected to a considerable logical environment from the macrobenthic view point; human impact through over-fishing and pollution and (3) Relate the observed change to measured environ- the ecological environment has changed greatly. Each mental variables and explore the underlying agents. year, some 2.8×109 t of waste-water and 7×105 tof other pollutants were brought into the sea by the river 2. Material and methods runoff. This approximates 50% of China's total mari- time discharge of pollutants. In recent years it has also 2.1. Field sampling and processing of samples been subjected to intensive offshore exploration for production of natural gas and petroleum reserves (Fan Three cruises were implemented, respectively in June and Zhang, 1988). As a result, fishery resources were 1985 (856), August 1986 (868) and October 1987 greatly reduced and eutrophication gave rise to frequent (8710) for the 1980s' investigation and in June 1997 occurrences of ‘red tide’ and uncontrollable diseases in (976), September 1998 (989) and April 1999 (994) mari-cultured species. In 1980s, fish farming prevailed during the 1990s’ survey. During the two surveys, 92 as a supporting fishery industry in northern China, but samples were collected from 53 stations among which declined rapidly in 1990s. The warning of “dead sea” 12 were located in Laizhou Bay, 25 in central Bohai Sea 314 H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321 and 16 in the eastern part of Bohai Bay (Fig. 1). The Diversity change was assessed using Shannon- stations sampled during the two investigations provided Wiener H′ (loge), evenness J′ and k-dominance plots a broad geographic coverage of the Bohai Sea. (Lambshead et al., 1983). K-dominance curves are Samples were collected from each station during cumulative ranked abundances plotted against either cruises on board the R/V Dong Fang Hong I and II. In the species rank or log species rank. Relative diversity was 1980s, either a 0.1 m2 HNM grab or a 0.1 m2 Gary- indicated by the relative elevation of the curves in a plot: O'Hara box-corer were deployed when the bottom was the more elevated, the lower diversity. Difference of the soft but a Smith-McIntyre grab was applied to hard- univariate index between any two groups of samples packed sediment. In the 1990s, all samples were collected was tested by means of student t-test. by a modified 0.1 m2 Gary-O'Hara box-corer. Triplicate sediment samples were brought on-deck, pooled and 3. Results sieved onto 0.5 mm mesh and organisms were preserved in 10% formalin. Additional samples for the later 3.1. Change in faunal group composition determination of environmental variables were also collected for each station and frozen at −20 °C. In the A total of 460 macrofaunal species has been recorded laboratory, organisms were counted under stereoscopic from the study area, 249 species from Laizhou Bay, 271 microscope, identified to species and family level (Holme species from central Bohai Sea and 168 species from and McIntyre, 1984; Kramer et al., 1994). Bohai Bay. In the Bohai Sea, Polychaeta and Crustacea were the two groups consisting of more than 60% of 2.2. Data analysis total faunal species (Fig. 2). There was a decreasing trend in relative number of Polychaeta species whereas Zhang et al. (1990a,b) based on the cluster analysis of relative number of Crustacea species tended to increase 18 environmental variables and 68 dominant and from the 1980s to the 1990s. common macrofauna species classified the Bohai Sea Overall the average macrofaunal abundance in Bohai into four fauna areas, i.e. 1) the area of submarine delta; Sea was estimated to be 1700 inds m−2, of which 2) the area of Laizhou Bay; 3) the area of central Bohai Polychaeta and Bivalvia were the most dominant groups, Sea; and 4) the area of eastern Bohai Bay. To make the together contributing more than 50% of the total data comparable between the two investigation events, abundance (Fig. 3). One exception is for the Bohai Bay stations located in the submarine delta area in the 1980s in 1980s when Echinodermata had a quite high and stations located in Bohai Strait and Liaodong Bay in dominance of up to 25%. Noteworthy is that relative the 1990s were not included in the study. The com- abundances of Echinodermata declined at all locations in munity data were then categorized into three groups according to their geographical locations, i.e. Laizhou Bay group (L), central Bohai Sea group (C) and Bohai Bay group (B) (Fig. 1). Temporal change in community structure was eval- uated using non-metric MDS (Multi-Dimensional Scaling) and ANOSIM (Analysis of Similarity) included in PRIMER version 5. These analyses were performed on mean fauna densities per sediment slice at species and family levels, respectively for each sampling date. Data were square root transformed prior to the analyses to reduce the influence of over-dominance by numerically abundant species and Bray–Curtis similarity was employed to create a similarity matrix. Stations sampled for the sampling date from the same geographic group were treated as replicates and ANOSIM was performed to test statistically any significant differences between decades and among geographic groups. SIMPER analysis was used to identify those species or families most contributing to differ- Fig. 2. Species composition of major macrofaunal groups in the Bohai ences in community structure. Sea. L, Laizhou Bay; C, central Bohai Sea; B, Bohai Bay. H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321 315

Fig. 3. Relative abundance of major macrofaunal groups in the Bohai Sea. L, Laizhou Bay; C, central Bohai Sea; B, Bohai Bay. the study area from 1980s to 1990s and t-test showed that their density was also significantly reduced in central Bohai Sea (Table 3). On the other hand, there were Fig. 4. MDS ordination based on pooled data for each geographic significant increases in abundance of Polychata and group. (A) at the species level, stress=0.10 (B) at the family level, stress=0.11. Bivalvia in both central Bohai Sea and Bohai Bay, Gastropoda in central Bohai Sea and Crustacea in Bohai Bay, respectively (Table 3). However, dominance of these ues were the same. Relatively low R-value at the family groups may have increased, decreased or remained level (R =0.289) compared with the species level unchanged (Fig. 3). (R=0.585) reflected a less changed community over decades when only family abundance data were taken 3.2. Change in community structure at the species and into account. Similarly, relative R-values obtained family level among different geographic locations suggested that the greatest dissimilarity in macrofaunal community Two-dimensional configuration plots of the MDS occurred between Bohai Bay and Laizhou Bay. ordination on the macrofaunal abundance data at the species and family level are illustrated by Fig. 4. Such a Table 1 plot is a visual representation of the dissimilarity in Results from two-way crossed ANOSIM global and pair-wise tests using macrofaunal composition between each sample. There Bray–Curtis similarity calculated on square-root transformed species and showed two distinct groups of samples from 1980s to family abundance data, showing significant differences in community structure between 1980s and 1990s and among the three geographic 1990s at the species level whereas distinctions among locations: C, central Bohai Sea; B, Bohai Bay; L, Laizhou Bay samples from the three geographic locations, i.e. Laizhou Bay, Central Bohai Sea and Bohai Bay were Between Among geographic decades locations not visually identifiable (Fig. 4A). It was even difficult to identify any sample grouping at the family level by RPR P MDS analysis (Fig. 4B). However, the results of the Global (at species level) 0. 585 0.001 0.222 0.001 ANOSIM test (Table 1) showed that at both the species Pair-wise (at species level) C/B: 0.228 0.001 ––C/L: 0.163 0.005 and family levels, there were indeed statistically sig- B/L: 0.406 0.001 nificant differences in community structure between the Global (at family level) 0. 289 0.001 0.256 0.001 two surveys in 1980s and 1990s (P=0.001) and among Pair-wise (at family level) C/B: 0.257 0.001 different geographic locations (Pb0.01). The values of ––C/L: 0.207 0.001 R statistics indicated relative dissimilarity when P val- B/L: 0.446 0.001 316 H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321

Table 2 Differences (N and b) in average abundance of species (inds m−2) contributing to Bray–Curtis dissimilarities between decade groups based on √- transformed abundance data Laizhou Bay Central Bohai Sea Bohai Bay 1980s (n=25) 1990s (n=5) 1980s (n=22) 1990s (n=22) 1980s (n=11) 1990s (n=7) Musculista senhousia 382 N 03 N 01N 0 Amphioplus japonicus 13 N 060N 44 120 N 97 Echinocardium cordatum 67 N 01 N 00=0 Ampelisca sp. 46 N 843N 216N 0 Rissoina bureri 46 N 19 39 N 31 0 b 83 Glycinde gurjanvae 45 N 31 15 b 21 11 N 9 Aricidea fragilis 28 N 811b 28 2 b 3 Alvenius ojianus 188 b 249 36 N 31 0 b 1327 Iphinoe tenera 5 b 83 18 N 17 6 b 25 Moerella jedoensis 56 b 99 54 b 203 3 b 192 Modiolus elongatus 0 b 71 b 42 1 b 452 Leptomya minuta 2 b 19 24 b 56 2 b 63 Yokoyamaia argentata 0 b 195 0 b 23 0 b 16 Sternaspis scutata 50 b 55 31 b 89 11 b 21 Paralacydonia paradoxa 9 b 27 66 b 84 28 b 50 Ancistrasyllis constricta 18 b 57 33 b 70 12 b 40 Nephtys oligobranchia 8 b 46 24 b 88 7 b 41 Total abundance (N) 1610±309 ns 1851±552 1153±236 ⁎ 1654±242 457±133 ⁎⁎ 3483±1567 Species richness (S) 44±3 ns 47±8 45±5 ns 51±2 23±4 ⁎⁎ 52±6

Shannon–Wiener H′(loge) 2.65±0.17 ns 2.89±0.14 3.07±0.01 ns 3.08±0.05 2.36±0.18 ns 2.66±0.25 Evenness J′ 0.70±0.04 ns 0.77±0.04 0.86±0.01 ⁎⁎ 0.79±0.01 0.81±0.05 ns 0.68±0.07 A cut-off at a cumulative % dissimilarity of 25% was applied. Diversity values (mean±SE) are also presented and difference between decades tested with t-test. ns, not significant; *Pb0.05; **Pb0.01.

Table 3 Differences (N and b) in average abundance of family (inds m− 2) contributing to Bray–Curtis dissimilarities between decade groups based on √- transformed abundance data Family Taxonomic Laizhou Bay Central Bohai Sea Bohai Bay group 1980s (n=25) 1990s (n=5) 1980s (n=22) 1990s (n=22) 1980s (n=11) 1990s (n=7) Sternaspidae Poly 50 b 55 31 b 83 11 b 39 Lacydoniidae Poly 9 b 27 66 b 72 28 b 89 Nephtyidae Poly 19 b 46 42 b 85 10 b 51 Pilargiidae Poly 18 b 57 34 b 58 12 b 77 Goniadidae Poly 46 b 78 17 b 32 11 b 20 Tellinidae Biva 82 b 119 78 b 223 10 b 218 Semelidae Biva 9 b 29 29 b 68 6 b 76 Philinidae Gast 28 b 195 26 N 19 4 b 29 Kelliellidae Biva 188 b 249 36 N 34 0 b 1319 Lumbrinereidae Poly 26 b 33 36 N 34 25 b 26 Ampeliscidae Crus 46 b 49 43 N 27 16 b 38 Mytilidae Biva 382 N 73 b 116 1 b 220 Amphiuridae Echi 15 N 12 62 b 65 124 b 144 Rissoidae Gast 50 N 19 51 N 26 0 b 110 Capitellidae Poly 25 N 19 51 N 42 6 b 49 Polychaeta 429±70 ns 509±163 467±95 ⁎ 674±127 160±45 ⁎ 429±129 Bivalvia 706±267 ns 520±281 240±67 ⁎⁎ 477±109 41±15 ⁎⁎⁎ 2249±1516 Gastropoda 147±45 ns 284±165 105±32 ⁎ 171±36 30±14 ns 235±135 Crustacea 210±37 ns 489±124 221±44 ns 225±43 79±33 ⁎⁎ 332±77 Echinodermata 83±48 ns 12±9 63±36 ⁎ 55±18 124±80 ns 181±53 A cut-off at a cumulative % dissimilarity of 25% was applied. Total abundance (mean±SE) for each taxonomic group was also provided and difference between decades tested with t-test. ns, not significant; ⁎Pb0.05; ⁎⁎Pb0.01; ⁎⁎⁎Pb0.001. H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321 317

3.3. Species/families contributing to the observed Bohai Bay but increased in Laizhou Bay (Fig. 5A) and change the macrobenthic diversity in the Bohai Sea as a whole was only slightly decreased (Fig. 5B). A general spatial Over a decade from 1980s to 1990s, macrofaunal pattern of diversity could also be identified if samples community structure in the Bohai Sea changed notably. were pooled for each region (Fig. 5C), i.e. a diversity Species and families most responsible (contributing to ranking of central Bohai SeaNLaizhou BayNBohai Bay. 25% of the differences) identified by SIMPER analyses were listed in Tables 2 and 3. Most of the species/ 3.5. Related changes in the benthic environment families increased in abundance consistently over the three geographic locations. These are small-sized spe- Over 10 years from 1980s to 1990s, some changes in cies including four polychaetes (Sternaspis scutata, the benthic environment could be seen as with those Paralacydonia paradoxa, Ancistrasyllis constricta, Nephtys oligobranchia), three bivalves (Moerella jedoensis, Modiolus elongates, Leptomya minuta) and one gastropod (Yokoyamaia argentata). On the other hand, only one bivalve (Musculista senhousia) and two echinoderms (Amphioplus japonicus, Echinocardium cordatum) showed consistently and notably reduced abundance after 10 years. E. cordatum, ever abundant in the Laizhou Bay nearly disappeared from the study area during the 1990s' survey although its distribution was still recorded in the Bohai Strait (Han, 2001, 2003). The rest of the species showed an inconsistent pattern over space in temporal change of abundance. The most evident increases of abundance at the family level were identified from five polychaete families (Sternaspidae, Lacydoniidae, Nephtyidae, Pilargii- dae, Goniadidae) and two families of bivalve (Tellinidae, Semelidae) (Table 3). Clearly this is a mirror of temporal pattern of the dominant species in the respective families.

3.4. Diversity

There appeared an increasing trend from the 1980s to 1990s for the diversity indices and total faunal abundance across the study area except evenness J′ which was significantly decreased in central Bohai Sea (Table 2). Nevertheless, results of t-tests showed that only few of these differences were statistically significant. These may be due to the low statistical power caused by unbalanced sample size (n=25 for 1980s but n=5 for 1990s), especially for the Laizhou Bay comparison. Species diversity can be considered as a combination of species richness and evenness. Lambshead et al. (1983) used k-dominance curves to describe “the in- trinsic diversity” which combines the two aspects of diversity. This graphical method was considered the most robust to the affection of sample size as compared Fig. 5. K-dominance curves to compare diversity between decades and among geographic locations using A, pooled samples for the two with other diversity indices. Relative elevation of k- decades (80s, 90s) within each of the three regions (C, central Bohai dominance curves clearly suggested that after 10 years, Sea; B, Bohai Bay; L, Laizhou Bay); B, pooled samples for the diversity was decreased in the central Bohai Sea and two decades; C, pooled samples for the three regions. 318 H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321 variables listed in Table 4. Sediment composition Table 5 changed with an increased proportion of silt but de- Spearman correlations between environmental variables and macrofaunal community structure using BIOENV in PRIMER, creased clay in the Bohai Sea. Accordingly changed showing the coefficient r for individual variable as well as for were the sediment granulometry parameters: both the combinations of several variables which yielded the beast match median grain size (MDφ) and sorting coefficient (QD) (maximum correlation) of biotic and abiotic similarity matrices increased, indicating that the sediment was getting finer Factor r and very poorly sorted. Skewness (Sk) decreased in % Sand −0.207 Laizhou Bay but increased in central Bohai Sea and % Silt −0.389 Bohai Bay. It seemed that the most marked change in % Clay 0.171 sediment composition occurred in Laizhou Bay where MDφ −0.146 silt proportion has increased by 7%. Coupled with the QD 0.411 change of sediment characteristics, organic content in- Sk 0.282 Chla (mg/m3) 0.307 creased nearly four fold of that in 1980s all over the Organic content (g/m3) 0.654 study area while benthic chlorophyll a decreased in Max. correlation % Clay, Sk, Organic content Laizhou Bay but increased in both central Bohai Sea and R=0.882 Bohai Bay. Linking biotic to environmental patterns was implemented by the BIOENV procedure, an exploratory tool for the maximum correlation (R=0.882) and thus best explain identifying potential agents in the shaping of community the observed change in community structure (Table 5). structure (Clarke and Warwick, 1994). Spearman correlation between the biotic and abiotic similarity matrices 4. Discussion showed that among the individual variables measured, combination of %clay, skewness and organic content gave There are ample evidences indicating that the Bohai Sea ecosystem has been experiencing a dramatic change. From 1960 to 1997, an increasing tendency Table 4 was observed in both salinity and temperature of the Average value and standard error (in parentheses) of the environmental surface sea-water (Deng et al., 1999). The increase in variables measured in the Bohai Sea temperature was coincident with global warming. The Laizhou Bay Central Bohai Bohai Bay increase in salinity was attributed to a decline of Sea freshwater discharge, especially related to the Yellow 1980s 1990s 1980s 1990s 1980s 1990s River cutoff: days of Yellow River cutoff increased from (n=9) (n=4) (n=9) (n=20) (n=4) (n=6) annual average of 18 d in the 1980s to 94 d in the 1990s. % Sand 3.85 1.43 35.62 35.76 0.56 1.63 In the meantime, terrestrial pollutants carried by the (0.62) (0.65) (9.52) (6.98) (0.16) (0.83) river runoff were increasing and organic discharge in- % Silt 66.65 73.96 32.74 38.35 46.60 50.95 creased with rapid development of shrimp pond culture. (5.11) (5.51) (5.69) (4.94) (4.19) (3.79) There were also changes in nutrient levels: in general % Clay 26.24 24.56 31.61 25.86 52.83 47.43 silica and phosphorus decreased but inorganic nitrogen, (1.95) (6.09) (5.39) (3.14) (4.20) (4.61) MDφ 2.08 6.62 6.10 6.04 7.68 8.22 especially nitrite and nitrate increase, resulting a higher (0.06) (0.45) (0.68) (0.35) (0.52) (0.47) N:P ratio of 23.15 in 1998, 8 times higher than that in QD 0.66 2.39 2.08 2.65 1.79 2.68 1982 and much higher than Redfield ratio (Yu et al., (0.10) (0.30) (0.25) (0.11) (0.08) (0.06) 2002). The Bohai Sea was considered turning from − Sk 1.22 0.48 0.50 0.55 0.10 0.31 nitrogen limited to phosphorus limited. Changes were (0.33) (0.07) (0.19) (0.05) (0.09) (0.04) Chla 6.50 2.98 2.53 4.29 1.42 3.56 also documented in the pelagic system. Primary pro- 2 (mg/m3) (1.09) (0.64) (0.50) (0.82) (0.27) (1.20) duction in June 1997 (132 mg C/m d) was much lower Organic 0.54 2.05 0.53 2.21 0.55 3.80 than that in the same month of 1983 (208 mg C/m2 d) content (0.05) (0.77) (0.05) (0.31) (0.06) (0.14) (Ning et al., 2002; Sun et al., 2003a, b). In 1998–1999, (%) fish biomass was only 4–19% of that in 1982–1983 and Surface 28.6 – 31.7 – 31.8 – salinity (0.9) (0.2) (0.4) diversity of the commercially important species was (‰) greatly reduced (Jin, 2000, 2004). Superimposed with DO (mg/l) – 0.93 – 1.47 – 0.84 over-fishing, nursery grounds of fish, shrimp and (0.06) (0.23) (0.19) shellfish in the Bohai Sea were depleted at alarming – – – – – – Depth (m) 16 17 22 38 19 24 rate. One of the examples is the rapid collapse of prawn H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321 319 fisheries and culture output from the peak of 100 thou- cribed an Amphiura-Echinocardium macrobenthic com- sand tons in late 1980s to less than one thousand tons in munity at a mud-sandy site in the southern North Sea and late 1990s (Deng et al., 1999). demonstrated an inverse relationship between the abun- Since early 1980s, several surveys were carried out to dance of the burrowing brittle star Amphiura filiformis investigate the meio- and macrobenthic communities in and bed rigidity. More recently, the reworking effect of the Bohai Sea and it was noticed that some changes had E. cordatum bioturbation on sediment was determined happened to the benthic ecosystem over the past in a laboratory experiment (Yu et al., 2000). Sedimentary 20 years (Zhang et al., 1990a,b; Sun and Liu, 1991; environment in Laizhou Bay seemed to be getting less Han, 2001). However, there was no direct comparison stable where, as a biological response to increased phy- made because of different sampling and sorting methods sical stress, large burrowing species were replaced by adopted and thus to render any evaluation of changes in small surface-dwelling opportunistic species. Satellite benthic ecosystem a matter of speculation. Although images clearly showed that since the location of the different sampling methods did introduce significant Yellow River mouth was artificially altered in 1976, the differences in nematode community structure, the de- coastline has been changing and the Yellow River delta tected differences were small and did not suggest a has been extending into the Laizhou Bay (Huang and Su, strong or ecologically meaningful explanation (Somer- 2002). The majority of the material carried by the river is field and Clarke, 1997). A comparison between grab medium to coarse silt (Shanming, 1986). The increased sampler and box-corer for collecting soft-bottom macro- silt proportion in the sediment composition in Laizhou benthos in the Bohai Sea suggested no differences in Bay (Table 4) could be related to extension of the Yellow abundance and biomass (unpublished results). Data em- River delta and was one of the factors accounting for the ployed in the present study were obtained by the same observed changes (Table 5). mesh diameter and there were great overlaps in the In the central Bohai Sea and eastern Bohai Bay, geographic coverage of the sampling stations and sea- although species replacement was not so obvious as in sons. Inconsistency in sampling gears was not likely a the Laizhou Bay, the common feature was the increase biasing factor for the apparent faunal changes observed. in abundance and dominance of small polychaetes and bivalves. Whereas diversity indices failed to indicate 4.1. Changes over time obvious patterns of change (Table 2), k-dominance curves showed a decreasing trend in diversity from the Over a decade, we observed a considerable change in 1980s to the 1990s (Fig. 5) although the decrease was the macrobenthic community structure of the Bohai Sea only observed in the central Bohai Sea and Bohai Bay shelf (Fig. 4, Table 1). However our concern is which and the decrease in diversity in the Bohai Sea as a whole direction it was changing toward. Comparisons of the was not remarkable (Fig. 5C). The increased diversity in community properties between the 1980s and 1990s Laizhou Bay (Fig. 5A) was not definitely an indication suggested that species composition and relative abun- of a decreased level of disturbance. Both theories dance changed: most of the dominant species and total (Connell, 1978; Huston, 1979) and empirical observa- fauna increased in abundance while several species dec- tions (e.g. Dauvin, 1984) suggested that diversity does reased in number such as the echinoderm Amphioplus not behave monotonically or predictably in response to japonicus and the crustacean Ampelisca sp. Total num- environmental stress; with a slightly increased level or ber of individuals of echinoderms decreased, particularly frequency of disturbance competition is relaxed, result- deposit feeding Echinocardium cordatum, an important ing in an increased diversity (Clarke and Warwick, species in terms of benthic biomass, seemed to lose its 1994). Guo et al. (2001) based on a comparison of the distribution in the Laizhou Bay (Tables 2 and 3). Echi- taxonomic distinctness (Δ+) and variation in taxonomic nodermata was the phylum most sensitive to ecological distinctness (Λ+) suggested that meiobenthos of the stress (Clarke and Warwick, 1994) and thus phenomenon Bohai Sea as a whole is not yet under major pollution of declined number or lost of some of the large species stress. Using the Abundance–Biomass comparison are possibly indicative of increased stress. Species like method, Han (2001) also demonstrated that the offshore the suspension feeder Musculista senhousia also dis- macrobenthic community was not yet under significant appeared from the Laizhou Bay, replaced by a predatory anthropogenic disturbance in the Bohai Sea. However, gastropod Yokoyamaia argentata. Zhang et al. (1990b), some of the stations did show signs of medium based on the 1980s survey, concluded that sedimentary disturbance. environment in Laizhou Bay was relatively stable with The changes observed in the Bohai Sea parallel distinct biological activity. Rowden et al. (1998) des- changes that have taken place in other parts of the world 320 H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321

(Reise, 1982). Small, opportunistic, short-lived organ- change at the decadal scale was more prominent than isms such as polychaetes are becoming more dominant at spatial difference at the regional scale (Fig. 4, Table 1). the expense of other taxa; suspension feeders are rep- In a study on macrobenthic species diversity in laced by carnivores and deposit feeders. These changes southern and central Bohai Sea, Han (2003) found no were often coupled with diminishing demersal fish spatial pattern of macrofaunal species diversity. The stocks (Rijnsdorp et al., 1996; Jin, 2000, 2004). Demer- results from the present study showed that in both the sal fishing was considered as a major agent for the above 1980s and 1990s, diversity in the central Bohai Sea was changes (Reise, 1982; Bradshaw et al., 2002; Chicaro the highest (H′=3.07–3.08, J′=0.79–0.86) among the et al., 2002; Cryer et al., 2002; Dolmer, 2002). It exerts three regions compared (Table 2). This was also greater impact on benthic system than other natural and indicated by the k-dominance plot which clearly showed anthropogenic disturbances in the marine continental a diversity ranking of central Bohai SeaNLaizhou shelf and slope by crushing, burying, and exposing BayNeastern Bohai Bay (Fig. 5C). Nematode diversity benthic organisms to predation and by altering sediment in the central part of Bohai Sea was the highest among and water column biogeochemistry (Watling and Norse, other locations in the Bohai Sea like Laizhou Bay and 1998). In the Bohai Sea, bottom trawling had been subaquatic delta (Zhang et al., 2001a). The highest increasing since the early 1960s when prawn fisheries benthic diversity in the central Bohai Sea was not un- were flourishing until it was forbidden in 1988. The expected because most of stations were not under direct, severe reduction in Echinocardium cordatum could be either natural or anthropogenic disturbance. Significant- commensurate with fishing as another explanation, be- ly changed macrobenthic community structure and de- cause its test is very fragile and would be damaged by creased diversity in this area deserves more attentions. bottom trawling whereas changes in sediment granulometry and organic content are less likely to affect it. 5. Conclusions There is always a danger of attributing cause of change in terms of those measured variables when it may be some From the 1980s to 1990s, macrobenthic community other unmeasured variable that is largely responsible (R. in the Bohai Sea changed considerably. This change was Warwick, personal communication). Nevertheless, our most remarkable in community structure whereas spe- study suggested that over 10 years from the 1980s to cies diversity was reduced slightly. There was a con- 1990s, organic content in the Bohai Sea shelf sediments siderable increase in abundance of small polychaetes, has increased by 4–7times(Table 4)andtheincreased bivalves and crustaceans but decreased number of echi- abundance of small polychaetes and bivalves, and the noderms. There were also prominent spatial variations decreased faunal diversity, could be a community res- in terms of community structure and diversity among ponse to organic enrichment as suggested by the BIO the three regions compared. The decadal changes in ENVanalysis (Table 5). This was in agreement with the benthic system in the Bohai Sea parallel a general ten- finding by Zhang et al. (2001b) who suggested that dency worldwide and were coincident with degradation nematode trophic group composition has greatly of the semi-enclosed shelf environment. changed with 1B/2A ratio nearly doubled after 10 years. Acknowledgements 4.2. Changes over space This study was financially supported by the National Although spatial variation was not the major concern Key Fundamental Study Project (No. G 1999043709) of the present study, it is not realistic to think about and National Science Foundation of China (No. temporal changes without regard to spatial differences. 497901001; 39770145) Science Foundation of China. Results of statistical analyses confirmed statistically that We are very much indebted to all the crew members of there were still significant differences in terms of macro- R/V Dong Fang Hong I, Dong Fang Hong II and benthic community structure among the three regions Science I, for their kind help in the sample collection. compared: Laizhou Bay, central Bohai Sea and eastern Bohai Bay (Table 1). This result supported the former proposition of dividing the Bohai Sea into four areas of References subaquatic delta, the Laizhou Bay, the central part of Bradshaw, C., Veale, L.O., Brand, A.R., 2002. The role of scallop Bohai and the southeast part of Bohai Bay based on the dredge disturbance in long-term changes in Irish Sea benthic biological and environmental characters (Zhang et al., communities: a re-analysis of an historical dataset. Journal of Sea 1989, 1990b). However, it is noticeable that temporal Research 47, 161–184. H. Zhou et al. / Journal of Marine Systems 67 (2007) 312–321 321

Chicaro, L., Chicharo, A., Gaspar, M., Alves, F., Regala, J., 2002. between 1906–1909 and 1990–1995. ICES Journal of Marine Ecological characterization of dredged and non-dredged bivalve Science 53, 1054–1062. fishing areas off south Portugal. Journal of the Marine Biological Rowden, A.A., Jago, C.F., Jones, S.E., 1998. Influence of benthic Association of the United Kingdom 82, 41–50. macrofauna on the geotechnical and geophysical properties of Cryer, M., Hartill, B., O'Sheab, S., 2002. Modification of marine surficial sediment, North Sea. Continental Shelf Research 18, benthos by trawling: toward a generalization for the deep ocean. 1347–1363. Ecological Applications 12, 1824–1839. Shanming, G., 1986. The effects of sediments from rivers to the Bohai Clarke, K.R., Warwick, R.M., 1994. Change in Marine Communities: Gulf on changes in coastlines. Third International Symposium an Approach to Statistical Analysis and Interpretation. Plymouth on River Sedimentation. University of Mississippi, Jackson, Marine Laboratory, Plymouth. pp. 579–587. Connell, J.H., 1978. Diversity in tropical rain forests and coral reefs. Somerfield, P.J., Clarke, K.R., 1997. A comparison of some methods Science N.Y. 199, 1302–1310. commonly used for the collection of sublittoral sediments and their Dauvin, J.C., 1984. Dynamique d'ecosystemes macrobenthiques des associated fauna. Marine Environmental Research 43, 145–156. fonds sedimentaires de la Baie de Morlaix et leur perturbation par Su, J.L., Tang, Q.S. (Eds.), 2002. Study on Ecosystem Dynamics in les hydrocarbures de l'Amoco-Cadiz. Doctoral thesis, Univ. Pierre Coastal Ocean II. Processes of the Bohai Sea Ecosystem et Marie Curie, Paris. Dynamics. Science Press, Beijing (in Chinese). Deng, J.Y., Zhuang, Z.N., Zhu, J.S., 1999. Recruitment characteristics Sun, D.Y., Liu, Y.C., 1991. Species composition and quantitative and stack dynamics of Penaeus chinensis in the Bohai Bay. distribution of biomass and density of the macrobenthic infauna in Zoological Study 20, 46–49 (in Chinese, with English Abstr.). the Bohai Sea. Journal of Oceanography of Huanghai and Bohai Dolmer, P., 2002. Mussel dredging: impact on epifauna in Limfjorden, Sea 9, 42–50 (in Chinese, with English Abstr.). Denmark. Journal of Shellfish Research 21, 529–537. Sun, J., Liu, D.Y., Zhang, C., Zhang, H., 2003a. The preliminary study Fan, Z., Zhang, Y.F., 1988. Levels and trends of oil pollution in the on size-fractionated biomass of phytoplankton in the central Bohai Bohai Sea. Marine Pollution Bulletin 19, 572–575. Sea, the Bohai Strait and its adjacent area. Acta Oceanologica Guo, Y., Somerfield, P.J., Warwick, R.M., Zhang, Z.N., 2001. Large- Sinica 25, 103–112 (in Chinese, with English Abstr.). scale patterns in the community structure and biodiversity of free- Sun, J., Liu, D.Y., Cai, X.Y., Zhang, C., 2003b. The chlorophyll a living nematodes in the Bohai Sea, China. Journal of the Marine concentration and estimation of primary productivity in the Bohai Biological Association of the United Kingdom 81, 755–763. Sea in 1998∼1999. Acta Ecologica Sinica 23, 517–526 (in Han, J., 2001. Study on Macrobenthic Ecology in Bohai Sea. PhD Chinese, with English Abstr.). Thesis. The Ocean University of China, Qingdao, PR China. (in Watling, L., Norse, E.A., 1998. Disturbance of the seabed by mobile Chinese, with English Abstr.). fishing gear: a comparison to forest clear-cutting. Conservation Han, J., 2003. Study on macrobenthic species diversity in southern and Biology 12, 1180–1197. central Bohai Sea. Biodiversity Science 11, 20–27 (in Chinese, Yu, Z.S., Zhang, Z.N., Han, J., Zhou, Y., 2000. The effect of with English Abstr.). bioturbation of Echinocardium cordatum (Pennant, 1777) on Holme, N.A., McIntyre, A.D., 1984. Methods for the Study of Marine vertical distribution of sediment particles. Chinese Science Ab- Benthos. Blackwell Scientific Publications, Oxford. stracts 6, 95–97 (in Chinese, with English Abstr.). Huang, D.J., Su, J.L., 2002. The effects of the Huanghe River Delta on Yu, Z.G., Liu, X.M., Zhang, J., 2002. The key biogeochemical the circulation and transportation of larvae. Acta Oceanologica processes influencing habitats of Chinese prawn in the Bohai Sea. Sinica 24, 104–111 (in Chinese, with English Abstr.). In: Su, J.L., Tang, Q.S. (Eds.), Study on Ecosystem Dynamics in Huston, M., 1979. A general hypothesis of species diversity. American Coastal Ocean II, Processes of the Bohai Sea Ecosystem Naturalist 113, 81–101. Dynamics. Science Press, Beijing, pp. 39–50 (in Chinese). Jin, X.S., 2000. A study of fishery resources fluctuation in the Bohai Zhang, Z.N., Li, Y.G., Tu, L.H., Yu, Z.S., 1989. Preliminary study in Sea. Chinese Fishery Sciences 5, 18–24 (in Chinese, with English the ecology of the benthic meiofauna in the Huanghe River estuary Abstr.). and its adjacent waters. Oceanologia et Limnologia Sinica 20, Jin, X.S., 2004. Long-term changes in fish community structure in the 197–208 (in Chinese, with English Abstr.). Bohai Sea, Ching Estuarine. Coastal and Shelf Science 59, Zhang, J., Huang, W.W., Shi, M.C., 1990. Huanghe (Yellow River) 163–171. and its estuary: sediment origin, transport and deposition. Journal Kramer, K.J.M., Brockmann, U.H., Warwick, R.M., 1994. Tidal of Hydrology 120, 203–223. Estuaries: Manual of Sampling and Analytical Procedures. Zhang, Z.N., Tu, L.H., Yu, Z.S., 1990a. Preliminary study on the Balkema, Rotterdam, the Netherlands. macrofauna in the Huanghe River estuary and its adjacent waters, Lambshead, P.J.D., Platt, H.M., Shaw, K.M., 1983. The detection of (I) the biomass. Journal of Ocean University of Qingdao 20, 37–45 differences among assemblages of marine benthic species based on (in Chinese, with English Abstr.). an assessment of dominance and diversity. Journal of Natural Zhang, Z.N., Tu, L.H., Yu, Z.S., 1990b. Preliminary study on the History 17, 859–874. macrofauna in the Huanghe River estuary and its adjacent waters, Ning, X.R., Liu, Z.L., Cai, Y.M., Liu, C.G., 2002. Size-fractional (II) in relation to the sedimentary environment. Journal of Ocean biomass and primary production of phytoplankton in spring– University of Qingdao 20, 45–51 (in Chinese, with English Abstr.). summer in the Bohai Sea. Studia Marina Sinica 44, 1–8 (in Zhang, Z.N., Zhou, H., Mu, F.H., 2001a. Biodiversity and neutral Chinese, with English Abstr.). model analyses on nematode community in Bohai Sea, China. Acta Reise, K., 1982. Long-term changes in the macrobenthic invertebrate Ecologica Sinica 21, 1808–1814 (in Chinese, with English Abstr.). fauna of the Wadden Sea — are polychaetes about to take over. Zhang, Z.N., Zhou, H., Guo, Y.Q., Mu, F.H., 2001b. Comparative Netherlands Journal of Sea Research 16, 29–36. study on the nematode community structure in the submarine delta Rijnsdorp, A.D., van Leeuwen, P.I., Daan, N., Heesen, H.J.L., 1996. of Huanghe River estuary and its adjacent waters. Oceanologia et Changes in abundance of demersal fish species in the North Sea Limnologia Sinica 32, 436–444 (in Chinese, with English Abstr.).