Decadal change in sublittoral macrofaunal biodiversity in the Bohai Sea, China
Highlights
► Change of biodiversity in the Bohai Sea, China was assessed from 1980s to 2000s. ► Assessment of biodiversity was based on species diversity and species relatedness. ► No deleterious change of sublittoral macrofaunal biodiversity was observed. ► About one fifth stations in the Bohai Sea were subjected to environmental stress.
Introduction
The Bohai Sea, located between 37°07′–41°00′N and 117°35′–121°10′E in the North Pacific, is a marginal inland sea enclosed by the Liaodong and Shandong peninsulas and connected with the northern Yellow Sea by the Bohai Strait (average depth 18 m, maximum depth 80 m) (Fig. 1). The Bohai Sea is of great commercial importance as one of the major fishing areas in China and contains important spawning and feeding grounds for many species of fish, shellfish and shrimp, such as Penaeus chinensis. The Bohai economic circle is the most rapidly developing area in northern China. Over the past 30 years, the Bohai Sea has been subjected to considerable human impacts through overfishing, pollution and eutrophication (Zhang et al., 2006). Each year, approximately 2.8 × 109 t of wastewater and 7 × 105 t of other pollutants enter the sea in river runoff. This amount represents approximately 50% of China’s total maritime discharge of pollutants. In recent years, intensive offshore petroleum exploration also caused frequent oil spills. Bohai Bay, Laizhou Bay and Liaodong Bay, in the Bohai Sea, were among the most polluted waters in China. The warning of a “dead sea” attracted considerable attention from the Chinese government and its administrative agency, and substantial effort has been invested in monitoring and restoring the environment.
Change and degradation in estuarine and coastal marine ecosystems is a general phenomenon worldwide as a result of human activities and climate change. Successful management of marine ecosystems needs to be based on a scientifically robust approach to the monitoring of ecological status (Leonard et al., 2006). The search for appropriate indicators of ecosystem health has become an important subject of research. Biodiversity is suggested as the ultimate measure of ecosystem health (Leonard et al., 2006).
Conventional measures of species diversity such as Margalef species richness and Shannon-Wiener diversity are the most widely used ecological indicators for monitoring purposes. Most of these measures are strongly affected by sample size, sampling effort and natural environmental variability and do not show monotonic responses to anthropogenic disturbances (Leonard et al., 2006, Rogers et al., 1999). For this reason, comparisons between data sets are difficult. Moreover, efforts to distinguish different levels of anthropogenic disturbance are confounded by different degrees of sampling effort and by natural environmental conditions, such as salinity and water depth. To address these problems, new diversity indices based on taxonomic relatedness were proposed (Clarke and Warwick, 1998, Clarke and Warwick, 2001a, Warwick and Clarke, 1995, Warwick and Clarke, 1998, Warwick and Clarke, 2001). Two of the taxonomic distinctness measures, average taxonomic distinctness Δ+ and variation in taxonomic distinctness Λ+, were claimed to represent good ecological indicators. They may play promising roles in biodiversity assessment relative to global change and on global scales because of their ecological relevance (i.e., a genuine reflection of biodiversity), robustness (i.e., sampling-effort and habitat-type independent and meaningful comparisons of regional/global studies and/or historic data sets) and cost-effectiveness (i.e., based only on data on the presence or absence of species). The importance and robustness of taxonomic distinctness for marine biodiversity assessment have been demonstrated indifferent taxonomic groups (Hall and Greenstreet, 1998, Leonard et al., 2006, Mouillot et al., 2005, Price et al., 1999, Rogers et al., 1999), although the sensitivity of these ecological indicators has been questioned relative to different scenarios of anthropogenic disturbance (Heino et al., 2005, Salas et al., 2006, Somerfield et al., 1997).
An accurate and objective assessment of the biodiversity and ecological status of the Bohai Sea is imperative for ecosystem management. However, biodiversity is not easy to measure. No single index can reflect all the diversity attributes of a community. Most studies on marine and terrestrial systems examine patterns of biodiversity in terms of a number of indices based on species richness and evenness. However, the number and relative abundance of species express only one facet of biodiversity. Biodiversity assessment needs to recognize the relatedness of the species included in the assemblages in a community. In this study, sublittoral macrofaunal community data collected during the 2000s were integrated with data from historical collections from the 1980s to 1990s. The aims of the study were as follows: (1) to detect any change of biodiversity over decades in terms of different diversity measures, (2) to compare the spatial pattern of different diversity measures, (3) to show the relationships between different diversity measures, and (4) to assess the ecological status of the Bohai Sea benthic environment with taxonomic distinctness and other measures.
Section snippets
Sampling scheme
Three cruises were conducted during each decade. The cruises occurred in June 1985 (6/85), August 1986 (8/86) and October 1987 (10/87) during the 1980s, in June 1997 (6/97), September 1998 (9/98) and April 1999 (4/99) during the 1990s and in November 2006 (11/06), August 2008 (8/08) and June 2009 (6/09) during the 2000s. During the three decadal surveys, 150 stations were sampled. The stations were situated in four general geographic locations (54 stations in Laizhou Bay, 25 stations in Bohai
The Bohai Sea benthic environment
Fundamental changes in the environmental parameters were observed over the three study decades in the Bohai Sea (Table 1). In the central Bohai Sea, the bottom salinity increased from 31.8 in the 1980s to 33.0 in the 1990s and returned to 31.3 in the 2000s. The sediment chlorophyll a and phaeopigment concentrations were 7- to 9-fold lower in the 2000s than in the 1980s and 1990s. However, the organic content increased by 3- to 4-fold in the 1990s. Accordingly, both the meiofaunal and
Discussion
During the past 30 years, China experienced extremely rapid economic development. Ample evidence of degradation is available for both the benthic and the pelagic ecosystems in the Bohai Sea (Jin, 2004; Zhou et al., 2010). Fundamental changes in macrofaunal community structure and species composition between the 1980s and the 1990s have also been demonstrated (Zhou et al., 2007). However, our data, which cover the past three decades and represent locations throughout the Bohai Sea, suggest no
Conclusions
Our study suggested that no deleterious change in sublittoral macrofaunal biodiversity occurred over the past three decades in the Bohai Sea but that a considerable portion of the macrofaunal community was subjected to environmental stress and perturbation. The impacted stations were not confined to any particular decade or geographic location. This result implies that even if the Bohai Sea sublittoral benthic environment is generally not showing major impacts of anthropogenic disturbance,
Acknowledgments
This study was funded by Grants to Z.N.Z. (No. 40730847), H.Z. (No.41076090) and E.H. (No. 40906063) from the Natural Science Foundation of China. We are grateful to Zishan Yu for providing historical data. Special thanks go to the two anonymous reviewers for their invaluable comments on the manuscript.
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