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Abstract. Benthic infaunal communities at Mai Po Inner Deep Bay mudflat, Hong Kong were investigated between August 2002 and August 2003. A total of 55 ...
Water, Air, and Soil Pollution: Focus (2006) 6: 575–581 DOI: 10.1007/s11267-006-9042-5 © Springer Science + Business Media B.V. 2006

BENTHIC INFAUNAL COMPOSITION AND DISTRIBUTION AT AN INTERTIDAL WETLAND MUDFLAT PING-PING SHEN1, HONG ZHOU2, HO-YAN LAI1 and JI-DONG GU1,3,* Laboratory of Environmental Toxicology, Department of Ecology and Biodiversity, The University of Hong Kong, Pokfulam Road, Hong Kong, SAR, China 2 College of Life Science, Ocean University of China, Qingdao, People’s Republic of China 3 The Swire Institute of Marine Science, The University of Hong Kong, Shek O, Cape d’Aguilar, Hong Kong, SAR, China ( *author for correspondence, e-mail: [email protected]; phone: +852-2299-0605; fax: +852-2517-6082) 1

Abstract. Benthic infaunal communities at Mai Po Inner Deep Bay mudflat, Hong Kong were investigated between August 2002 and August 2003. A total of 55 species belonging to 8 Phyla from more than 99,074 specimens were recorded. The species richness varied between 13 at Station B in August 2002 and 28 at Station D in August 2003 with an average of 21 across the mudflat and the species diversity was low [H′(log2) = 0.7–3.5 with an average H′ = 2.4]. Seasonal variations were also observed through abundance and biomass across the mudflat among the seasons. The abundance density was between 8,977 individuals m−2 at Station D in February 2003 and 77,256 individuals m−2 at Station B in November 2002 and the overall average density was 25,274 individuals m−2 for the four stations. The benthic infauna were dominated by pollution tolerant species at this wetland mudflat. Keywords: benthic infauna, composition, distribution, Mai Po mudflat, seasonal variation

1. Introduction Mai Po Inner Deep Bay Ramsar Site of Hong Kong is located at the northwestern part of the New Territories. It comprises of inter-tidal mudflats, sub-tropical mangroves, as well as man-made fishponds and drainage channels. The inter-tidal mudflat, known as part of the Mai Po Nature Reserve, is an important natural feeding habitat for migratory waterfowl passing through Hong Kong along the East Asian/Australasian flyway and for wintering birds (Young & Melville, 1993). Between 49,000 and 68,000 individuals of waterfowl have been recorded utilizing different parts of the Nature Reserve in winter and more than 100,000 during the entire year (Tsim & Lock, 2002). Due to the high number and diversity of migratory birds, the wetland was officially listed as a Wetland of International Importance under the Ramsar Convention in September 1995 reflecting its high ecological and conservation values. As a food source for the shorebirds, benthic infauna is a key structural and functional component of the ecosystem within Mai Po mudflat. Dynamics of their

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abundance and biomass could have significantly effects on the value of the site as a refueling station for the migratory birds. Furthermore, benthos can also be used as an important indicator for the ecological health of the ecosystem (Gray, 2000; Gray & Pearson, 1982). Pollution can cause significant adverse effects on benthos populations (Pearson & Rosenberg, 1978) and, thus structure of populations or communities can be used to deduce the unfavorable changes in the physical and chemical characteristics of habitat. Therefore, the objectives of the present study were to establish reliable information about local benthos communities, and investigate the changes of composition and distribution across the mudflat and along the seasons. 2. Materials and Methods 2.1. STUDY AREA AND FIELD SAMPLING The Mai Po mudflat lies within the Mai Po Nature Reserve Ramsar Site (22°30′N, 114°02′E) and is bounded by the Shenzhen River to the north and the Shan Pui River to the southwest. Detailed information about the site and sampling procedures are available (Hyder, 1998; Laboratory of Environmental Toxicology, 2003). 2.2. DATA ANALYSIS Software PRIMER v5 (Plymouth Routines In Multivariate Ecological Research, Clarke & Warwick, 1994) was used for benthic data analysis. Biological properties included the following: total abundance and biomass, number of species (S), total number of individuals, Shannon–Wiener diversity index (H′). Faunal groups not properly sampled by the methods used, such as nematodes, bryozoans and fishes as well as juveniles, were not included in the data analyses. Multivariate techniques included ordination of benthos samples by non-multidimensional scaling (nMDS) (Kruskal & Wish, 1978) and their classification by clustering using the hierarchical agglomerative method employing group average linking of Bray–Curtis similarities after square root transformation. Following clusters analysis, the species having the greatest contribution to the division of sites into cluster were determined using the similarity percentage program (SIMPER) (Clarke & Warwick, 1994). 3. Results and Discussion 3.1. SPECIES COMPOSITION A total of 55 species belonging to 8 phyla and more than 99,074 specimens (a total biomass of 492.4 g wet weight of all specimens) were recorded during the study

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period. These samples included Annelida (11 polychaetes and oligochaete), Mollusca (6 bivalves and 19 gastropods), Arthropoda (8 crustaceans, 4 insects and 1 mite), Sarcomastigophora (1 foraminiferan), Nematoda, Nemertea, Playhelminthes (1 turbellaria) and Chordata (1 fish). Gastropods and polychaetes constituted the most dominant groups in term of abundance and number of species. Total species and abundance were 35 and 37% for gastropods, and 20 and 24% for polychaetes, respectively. Other important groups included oligochaetes, crustaceans and bivalves and each of them contributed to 23, 10 and 6% of the total abundance, respectively (Table I). The species richness (SRS) varied between 13 at Station B in August 2002 and 28 at Station D in August 2003 with an average of 21 across the mudflat. The abundance density was between 8,977 individuals m−2 at Station D in February 2003 and 77,256 individuals m−2 at Station B in November 2002 (Figure 1) and the overall average density was 25,274 individuals m−2 for the four stations. The species diversity index [H′ (log2)] ranged between 0.7 and 3.5 (average H′ = 2.4) and was higher than 2 on most sampling occasions (Figure 2). The highest diversity (H′ > 3) was generally recorded at station with highest species number, e.g., Stations C and D. Both the lowest diversity and species number and the highest number of individuals occurred at Station B that was distinguished from other stations due to closer to the mangrove forest implying available high concentration of organic carbon. In this investigation, α diversity (Gray, 2000) of Mai Po intertidal mudflat was low and varied from 13 to 28 species with an average SRS =21. It is much lower than that of a recent study by Shin and Ellingsen (2004) in sub-tidal Hong Kong waters. In spite of the sample scale, TABLE I The most common species found in the Mai Po mudflat Mean density (individuals m−2) Species Polychaeta Neanthes glandicincta Tharyx sp. Capitella capitata Potamilla acuminata Oligochaeta Mollusca Pseudopythina maipoensis Sermyla riquetii Stenothyra devalis Crustacea Discapseudes mackei Harpacticoida

Group I

Group II

Group III

347 0 270 38 7,893

116 2,464 0 1,155 770

539 192 39 539 539

116 11,281 193

116 7,199 1,348

270 731 154

38 39

1,425 1,771

192 77

Mean densities were calculated for the main groups from cluster analysis.

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Figure 1. Mean abundance and biomass density of benthic infauna at Mai Po Inner Deep Bay mudflat between August 2002 and August 2003 (vertical lines show the standard deviation).

results of this study illustrated another example showing that the pattern of species richness increased from shallow water to deep sea (Gray, 2000). 3.2. SEASONAL CHANGES Seasonal variation of benthic infauna in terms of abundance and biomass showed a clear pattern that samples were much more dissimilar to each others in August 2002 (most dissimilar in February or May 2003) and then became more similar to the starting time in August 2003 (Figure 3). Variations of the infauna abundance

Figure 2. Species number and diversity of benthic infauna at Mai Po Inner Deep Bay mudflat between August 2002 and August 2003. Station codes are given with month and an extension for the year of sampling.

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Figure 3. Multidimensional Scaling (MDS) ordination plot of the four stations at different seasons of sampling at Mai Po Inner Deep Bay (stress 0.14).

at Station B was much higher than those of the other three stations during the five seasons while the biomass changed very little except for Station A where substantial increase was evident in winter (Figure 3). During the five sampling events, two opposite trends of fluctuation were detected within the mudflat. At Stations B and D, both abundance and biomass of infauna decreased to the lowest level in winter of 2003, while at Stations A and C, both parameters reached the highest level except for the abundance of infauna at Station A. 3.3. COMMUNITY STRUCTURE ANALYSIS Cluster analysis grouped the four stations of different sampling seasons into three main clusters. Group I consisted of all samplings from B mostly; Group II included various samples from stations excluding B; while Group III consisted of all samples from A, C and D. Similarly, distinctive assemblages could be identified from multi-dimensional scaling ordination plots for each infauna sample (Figure 3). It is apparent that the samples from Station B were more closely related to each other than those from the other stations indicated by the clustering of the sampling from the sites. The organisms mainly responsible for the seasonal and spatial differences (SIMPER analysis, cut-off of 70%) were Oligochaeta, Gastropoda (Sermyla riquetii, Stenothyra devalis) and Polychaeta (Neanthes glandicincta, Tharyx sp., Capitella capitata and Potamilla acuminata). Most species were found at majority of the stations at different sampling times, but the mean densities of the three main clusters differed remarkably (Table I). Another feature of the benthic community of the Mai Po mudflat was composed of high densities of small short-lived pollution-tolerant opportunistic species, a typical feature of impacted community by organic pollution and/or other disturbance (Pearson & Rosenberg, 1978). The global opportunist C. capitata and

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Oligochaeta, for instance, may respond both to physical disturbance and organic pollution (Lai, 2004). C. capitata reached a highest density of 2,301 individuals m−2 at Station B in May 2003 and peak of Oligochaeta density was 28,484 individuals m−2, indicating a severely polluted site compared to the others on the mudflat. A major factor contributing to the seasonal changes in benthic infauna at Inner Deep Bay can be attributed to the freshwater discharge from Shenzhen River as well as freshwater outflow from the Pearl River delta, especially in summer. Unfortunately, no significant relationship could be detected between the salinity gradient and abundance and biomass of macrofauna on the mudflat during this monitoring period (Laboratory of Environmental Toxicology, 2003). The lowest number of species may be due to more widespread predation in this area as this site is in the vicinity of the bird feeding locations on Mai Po mudflat in particular during the winter–spring period (Hyder, 1998). However, the predation by birds is not likely to cause a reduction on the number of species, on the contrary the abundance of infauna increased at the same time in recent monitoring (Laboratory of Environmental Toxicology, 2003). The community changes can therefore hardly be explained by the predation by birds. On the contrary, the feeding behavior of over-wintering birds on Mai Po mudflat might contribute to the lowest abundance during the winter period at both Stations B and D.

4. Conclusions The present investigation suggested that the Mai Po mudflat generally supported a poor benthic infauna community. The abundance and biomass of infauna at Mai Po mudflat showed seasonal changes, which involved shifts in the relative abundance of species and taxonomic group, but the changes were not large enough to alter the species composition of the fauna of the mudflat. Another feature of the community was that it was composed of high densities of a few pollution-tolerant opportunistic species: C. capitata and Oligochaeta, a typical feature of impacted community by organic pollution and/or other disturbance. Both low species diversity and high abundance of a few infaunal species as shown in the present study reflected the polluted condition at the Deep Bay and to protect the habitat of waterfowls. Acknowledgement This study is part of the Baseline Ecological Monitoring Programme for the Mai Po and Inner Deep Bay Ramsar Site supported by Agriculture, Fisheries and Conservation Department (AFCD) of the Hong Kong SAR Government. We would like to thank the team members in our Laboratory of Environmental

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Toxicology at The University of Hong Kong and the field-working group of AFCD at Mai Po for logistic support on sampling transport and assistance. Any opinions, findings, conclusions or recommendations expressed in this publication do not reflect the view of the Government of Hong Kong Special Administrative Region.

References Clarke, K. R., & Warwick, R. M. (1994). Change in marine communities: An approach to statistical analysis and interpretation (2nd ed.). Plymouth, UK: Plymouth Marine Laboratory. Gray, J. S. (2000). The measurement of marine species diversity, with an application to the benthic fauna of the Norwegian continental shelf. Journal of Experimental Marine Biology and Ecology, 250, 23–49. Gray, J. S., & Pearson, T. H. (1982). Objective selection on sensitive species indicative of pollutioninduced change in benthic communities. I. Comparative methodology. Marine Ecology Progress Series, 9, 111–119. Hyder (1998). Agreement no. CE 17/95—Deep Bay water quality regional control strategy study: Final Report. Environmental protection department water policy and planning group. Hyder Consulting, CES (Asia) Ltd. and Delft Hydraulics, Hong Kong. Kruskal, J. B., & Wish, M. (1978). Multidimensional scaling. Beverley Hills, CA: Sage. Laboratory of Environmental Toxicology (2003). Tender reference no. AFCD/SQ/28/01 ecological monitoring program for the Mai Po and Inner Deep Bay Ramsar Site (Oct. 2001–Sept. 2002). Final Report submitted to Agriculture, Fisheries and Conservation Department. Laboratory of Environmental Toxicology, The University of Hong Kong, Hong Kong SAR. Lai, M. Y. (2004). Fractionation, mobilization and bioaccumulation of heavy metals and mineralogical characteristics of the Mai Po inner deep bay mudflat. M.Phil. Thesis. University of Hong Kong, Hong Kong SAR. Pearson, T. H., & Rosenberg, R. (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology: Annual Review, 16, 229–311. Shin, P. K. S., & Ellingsen, K. E. (2004). Spatial patterns of soft-sediment benthic diversity in subtropical Hong Kong waters. Marine Ecology. Progress Series, 276, 25–35. Tsim, S. T., & Lock, F. N. Y. (2002). Knowing Ramsar wetland. Hong Kong: Cosmos Books. Young, L., & Melville, D. S. (1993). Conservation of the deep bay environment. In B. Morton (ed.), The marine biology of the South China Sea, Proceedings of the first international conference on the marine Biology of Hong Kong and South China Sea, Hong Kong, 1990 (pp. 211–231). Hong Kong: Hong Kong University Press.