Environmentally associated spatial changes of a macrozoobenthic community in the Saemangeum tidal flat, Korea

Journal of Sea Research 65 (2011) 390–400

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Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s

Environmentally associated spatial changes of a macrozoobenthic community in the Saemangeum tidal flat, Korea Jongseong Ryu a, Jong Seong Khim b,⁎, Jin-Woo Choi c, Hyun Chool Shin d, Soonmo An e, Jinsoon Park f, Daeseok Kang g, Chang-Hee Lee h,⁎⁎, Chul-Hwan Koh f a

Office of Policy Research, Korea Ocean Research & Development Institute (KORDI), P.O. Box 29, Ansan 425-600, Republic of Korea Division of Environmental Science and Ecological Engineering, Korea University, Seoul 136-713, Republic of Korea South Sea Research Institute, KORDI, Jangmok, Geoje 656-830, Republic of Korea d Faculty of Marine Technology, Chonnam National University, Yeosu 550-749, Republic of Korea e Coastal Environmental System School, Pusan National University, 30 Jangjeon-dong, Geumjeong-gu, Busan 609-735, Republic of Korea f School of Earth and Environmental Sciences, Seoul National University, Seoul 151-742, Republic of Korea g Department of Ecological Engineering, Pukyong National University, Busan 608-737, Republic of Korea h Department of Environmental Engineering and Biotechnology, Myongji University, Yongin, Gyeonggi-do 449-728, Republic of Korea b c

a r t i c l e

i n f o

Article history: Received 2 November 2010 Received in revised form 15 March 2011 Accepted 15 March 2011 Available online 26 March 2011 Keywords: Zoobenthos Community Composition Multivariate Analysis Ecological Zonation

a b s t r a c t Estuarine tidal flats are both ecologically and economically important, hence developing methods to reliably measure ecosystem health is essential. Because benthic fauna play a central role in the food web of tidal flats, in this study we set out to quantitatively describe the intertidal zonation of macro-invertebrates and their associations with specific environmental parameters along three transects in the Saemangeum tidal flat, Korea. The abundance and biomass of intertidal fauna with respect to five environmental parameters (i.e., shore level, mud content, coarse sand content, water content, and organic content) were measured, to identify environmental factors that influence macrofaunal distribution in intertidal soft bottom habitats. A total of 75 species were identified, with dominant species showing distinct zones of distribution along all transects. The number of species recorded in each transect was found to be dependent on sediment characteristics and salinity. Cluster analysis classified the entire study area into three faunal assemblages (i.e., location groups), which were delineated by characteristic species, including (A) ‘Periserrula–Macrophthalmus’, (B) ‘Umbonium– Meretrix’, and (C) ‘Prionospio–Potamocorbula’. Four environmental variables (i.e., shore level, water content, mud content, and organic content) appeared to determine factors that distinguished the three faunal assemblages, based on the discriminant analysis. The faunal assemblage types of the sampled locations were accurately predicted from environmental variables in two discriminant functions, with a prediction accuracy of 98%. It should be noted that the zonation of benthos in the lower section (C) of Sandong had been affected by the construction of a nearby dike, while this parameter had remained essentially unchanged at the other two location groups (A–B). Overall, the zonation of benthos from the Saemangeum tidal flat was explained adequately by the measured environmental variables, implying that faunal assemblages are closely associated with certain combinations of abiotic factors. The identification of such reliable associations may facilitate the development of statistical models to predict faunal distributions based on environmental variables at both local and regional scales. The entire study area was embanked in 2006 (one year after this study), and an integrated plan was set into force to develop claimed land into industrial, residential and agricultural districts, which also included a partial restoration program of the tidal flats located near to the study area. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Estuaries provide valuable ecosystem services in terms of nutrient recycling, biodiversity, and recreational activities (Costanza et al.,

⁎ Corresponding author. Tel.: + 82 2 3290 3041; fax: + 82 2 953 0737. ⁎⁎ Corresponding author. Tel.: + 82 31 330 6698; fax: + 82 31 601 3156. E-mail addresses: [email protected] (J.S. Khim), [email protected] (C.-H. Lee). 1385-1101/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2011.03.003

1997). This is because estuaries form important transition zones, with ecological processes that functionally link terrestrial, freshwater, and marine ecosystems (Gray, 2002). Tidal flats in this critical transition zone are known to be one of the principal energy links between primary producers and high-level consumers, such as fish, birds, and humans (Levin et al., 2001; Wall et al., 2001). Benthic fauna play a central role in the food web of tidal flats as significant primary consumers and/or as prey. In fact, the importance of tidal flats for migratory birds, which are at the top of the food chain, has also been clearly acknowledged.

J. Ryu et al. / Journal of Sea Research 65 (2011) 390–400

The zonal distribution of benthic fauna in intertidal flats has been well documented (Dittmann, 2000; Peterson, 1991). The spatial distribution of benthos is generally explained by the combined influence of the physical environment, animal-sediment associations, and species interactions (Snelgrove and Butman, 1994). Based on these factors, zonation patterns result from the ability of different species to function in different environmental gradients, including changes in salinity, sediment particle size, exposure duration and shore level (Dittmann, 2000; Koh and Shin, 1988; Ysebaert et al., 1998). The identification of relationships between faunal distribution and environmental variables is of great benefit for developing scientific knowledge and the coastal management of benthic ecosystems for a number of reasons. First, the assessment of biological diversity would serve as the baseline for future monitoring and restoration work. Second, data on environment-fauna relationships are necessary for scientific modeling research, from which biodiversity hotspots could be identified for management purposes through the screening and tracking of habitat diversity, with respect to selected key environmental variables that are available (Mumby, 2001). Third, the provision of scientific data would support the designation of coastal and marine reserves. The present study was performed in the Mangyeong–Dongjin estuary of the Saemangeum tidal flat. The Mangyeong–Dongjin estuary is considered to be one of the most important coastal wetlands in Korea for many reasons, including fisheries, biodiversity, seascape, and as intermediate resting sites for migratory birds (Koh et al., 2010). Ecologically, this tidal flat was recognized as an important feeding area, maintaining large populations of migratory birds that use East Asian/ Australasian pathways (Rogers et al., 2006). Economically, this tidal flat was highlighted as an important ground for artisanal fisheries of indigenous communities. Despite the recognized importance and active use of the Saemangeum ecosystems, there has been a paucity of scientific studies over the last decade (Koo et al., 2008). To encourage the ecosystem approach within environmental management, it is essential to obtain detailed information about the spatial distribution of benthic invertebrates and clarify associations with relevant environmental factors. This study aims to delineate the structural assemblage and spatial distribution of intertidal macrobenthic invertebrates in the Saemangeum tidal flat, focusing on faunal zonation along environmental gradients and associations with several environmental parameters. The relative importance of environmental parameters was determined, and predictions of faunal assemblages were tested in relation to these environmental parameters using multivariate analyses. In brief, the objectives of the present study were to, (1) establish a baseline database on the distribution of benthic macrofauna for future monitoring and/or possible restoration practices in the proximate area, (2) identify the relative importance of environmental variables that explain faunal zonation, and (3) develop a statistical model to predict the type of faunal assemblages for each location based on environmental variables. Finally, we discuss the potential application of the current findings to conduct regional scale assessments for an ecosystem approach to tidal flat management. 2. Materials and methods 2.1. Study area The study was conducted in the macrotidal regime (tidal range =1.2– 7.2 m) of the Saemangeum estuarine intertidal flats (35° 30′ N to 35° 50′ N and 125° 40′ E to 126° 00′ E), situated on the west coast of Korea. The Saemangeum tidal flat covers an area of 233 km2, with a width of 5 km in many places, extending to a maximum of 15 km at the mouth of the estuary. Two rivers (the Mangyeong and Dongjin rivers) flow into the tidal flat area, forming two main channels that subsequently flow out to the Yellow Sea through two artificial openings (~1.5 km wide each) in the middle of the dike (Fig. 1). Two small dams were built ~15 km upstream from the estuary in the Mangyeong river and ~5 km upstream in the Dongjin river. The year-round freshwater input is approximately

391

6.4 billion tons, 60% of which occurs during the short summer monsoon season (July–September). While most of the sampling sites in the current study were strongly influenced by seawater, a strong year-round salinity gradient (from ~10 to ~24) was observed in the study area due to intermittent discharges from the river dams and possible submarine groundwater discharges in the estuary (Kim et al., 2010; Waska and Kim, 2011). In the main channel, the current velocity of the flood tide reaches 1.0 m s−1 and the current velocity of the ebb tide reaches 0.8 m s−1, respectively. The Saemangeum tidal flat sediment bottom is muddominated in the upper intertidal areas, and sand-dominated in lower intertidal areas. The Saemangeum reclamation project has been in development at the study area since the early 1990s. The project aimed to build a 33-km long dike and convert ~400 km2 of tidal flats into farmland within the dike (Fig. 1). Dike construction was ~90% complete during the study period (2004–2005) and was completed in April 2006, at which point the tidal current was completely blocked. As a result of the dike construction across the last decade, significant changes in sedimentation and topography of the tidal flats in the Saemangeum area have been reported (Lee and Ryu, 2007, 2008). Three transects were delineated, the locations of which were identical to that of An and Koh (1992) to allow comparative analysis. The three transects represented diverse intertidal zones and were named after nearby towns: (1) Gyehwa, the outer area, (2) Gwanghwal, the inner area, and (3) Sandong, the disturbed area (Fig. 1). The Sandong area had been significantly disturbed by a relatively large accumulation of muddy sediments, due to reduced tidal currents since the completion of the nearby dike section in 2003 (viz., Sector IV). The distance between transects was ~10 km. 2.2. Sampling design Twenty six sampling locations were surveyed along the 5 km Gyehwa transect (TG) at intervals of 200 m in September 2004. The 3.7 km long Gwanghwal transect (TW) had 20 sampling locations at 200 m intervals, and was sampled in March 2005. Seven sampling locations were examined along the 3.4 km Sandong transect (TS) at intervals of 500 m in April 2005. The use of different sampling periods was not considered to impact the study, based on the results of an unpublished year-round study (2004–2005) conducted in the Gyehwa area, in which a low degree of seasonal variation in dominant species composition of macroinvertebrates was found. However, there remains uncertainty about whether comparisons of the entire species compositions are valid between transects. At each location, random sediment samples were taken (by throwing a quadrat) in triplicate from the top 10 cm using a rectangular stainless steel can-corer (13 cm× 22 cm= 286 cm2) for macrofaunal analysis. At locations adjacent to faunal can-core spots, surface sediments were also sampled to a depth of 10 cm using a hand-corer for analyses of sediment parameters. A total of 159 cores were taken from the sampling locations at the three transects (78 cores from TG, 60 cores from TW, and 21 cores from TS). A sampling depth of 10 cm was selected based on the preliminary survey conducted at Gyehwa transect (TG), where it was found that the top 10 cm of sediment contained the majority of species (92%), macrofaunal abundance (85%), and biomass (77% in wet weight (WW), 60% in dry weight (DW), 60% in ash-free dry weight (AFDW)) across a 30 cm sediment depth range. All data of the preliminary survey on vertical distribution of macrofauna across sediment depths are provided in Supplementary Data (see Table S1 and Fig. S1). The results were not appreciably different at various depths and thus a 10 cm sampling depth was selected with the deeper layers being disregarded in the subsequent study at TW and TS, for the purpose of efficiency and sampling speed. In addition, visual observation of biosedimentary features of the sediment surface was documented by counting the number of burrows and observed epifauna within a quadrat (three repeats of 1 × 1 m) at 100 m intervals along all transects to complement the faunal data obtained from core samples.

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Fig. 1. Map showing the sampling area and locations along the three transects of Gyehwa (TG), Gwanghwal (TW), and Sandong (TS) in the Saemangeum tidal flat, Korea. The line showing the dike represents the status during the study period as of September of 2004.

2.3. Macrofauna analyses Sediment samples from the cores were sieved through a 1 mm pore size mesh on site. Because live animals are relatively easy to catch and separate from the sediments, macrofauna were sorted on the sampling day, to minimize the loss of animals. This process also reduces the amount of formalin solution being used on site. The sorted animals were fixed in a 4% buffered formalin solution, and then preserved in 70% ethanol for laboratory based species identification, counting and biomass measurements. Taxa were identified to the species level in the laboratory, using a dissecting microscope or optical microscope where necessary. In certain cases, juveniles or certain taxa (e.g., Phylum Nematoda, Phylum Sipuncula, Class Turbellaria, and Family Lineidae) were identified to the lowest possible taxonomic level, and treated as species to calculate the number of species, abundance, and biomass. After identification and counting, the biomass of each species was measured and expressed as AFDW. Wet (WW) and dry weights (DW) were also measured during the weighing process and the conversion factors between WW, DW, and AFDW for certain taxa are provided in Table S2. The AFDW was measured by incineration in an oven at 500 °C for 2 h according to previously reported methods (Ricciardi and Bourget, 1998). The shells of mollusks and barnacles were removed before measuring their biomass. The respective abundances of four species (Bullacta exarata, Macrophthalmus japonicus, Macrophthalmus dilatatus, and Periserrula leucophryna) were recorded by counting the number of burrows or observed individuals within triplicate 1 m2 quadrat areas at each sampling location. The biomass of these four species was estimated by using the mean individual weight of corresponding species, based on the biomass measured from the can-core data. 2.4. Environmental parameters The five environmental parameters that were measured included (1) shore level, (2) mud content, (3) coarse sand content, (4) water

content, and (5) organic content. Shore level was determined either by a direct level measurement (TW and TS) on site, or by estimation (TG) from the tide table of nearby Gunsan Harbor, which was based on the time of waterline arrival to the sampling location. For sediment parameters, sediment samples were mixed well and stored in airtight plastic bags to prevent evaporation, and subsequently transferred to the laboratory for further analyses. The mud content (% of particles b62.5 μm) and coarse sand content (% of particles N1 mm) were both determined from rapid partial analysis by wet-sieving (Buchanan, 1984). Water content was obtained by measuring weight loss after drying the sediments at 70 °C for 72 h until a constant weight was attained. Organic content was obtained by burning sediments to ashes at 550 °C for 4 h (Heiri et al., 2001), to measure weight loss after combustion. 2.5. Data analyses To provide a representation of the zonation of macrofauna and its relationship with environmental parameters, cluster analysis (CA) and discriminant analysis (DA) were used. Abundance and biomass data of macrofauna were expressed as individuals per square meter (indiv. m−2) and g AFDW m−2, respectively. The zonation of macrofauna was further analyzed by clustering locations based on the similarity of abundance data. The similarity matrix for CA was calculated using the Bray–Curtis index based on the fourth root transformed abundance data (Field et al., 1982), which was inclusive for all recorded species. Group average linking was adopted to delineate the dendrogram of CA and to cluster location groups. Non-metric multidimensional scaling (MDS) was also utilizes to place sampling locations in two-dimensional space based on the same similarity matrix used for CA. To select characteristic species in location groups, four criteria delineated by Salzwedel et al. (1985) were used: (1) the ratio of species abundance in each group over the total species abundance in the corresponding group (dominance, DOM), (2) the ratio in the number of locations at which the species occurs in each group over the entire

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(relatively consistent) in surface sediment conditions along the transect lines from high to low tidal level (Fig. 2). However, the third transect, which was situated in a disturbed region (TS), showed a different pattern of mud, organic, and water content compared to the TG and TW transects. For example, sediment parameters tended to decrease on approach to the lower intertidal zone along TG and TW, while those of TS increased until the middle of the transect line and subsequently decreased on approaching the shoreline (Fig. 2). However, it should be noted that on average mud content was the lowest at TG when compared to that of TW and TS, which was consistent with the sanddominant sediment facies observed at most sampling locations along TG. Evaluation of the distribution of organic content, which was measured by loss on ignition, indicated a similar spatial trend to that of mud content along all three transects. This finding demonstrates that the two parameters were closely associated in all transect lines; TG (r2 = 0.80), TW (r2 = 0.80), and TS (r2 = 0.72), respectively. While the mud content at TW (69%) and TS (64%) was relatively similar, higher mean organic content was recorded at TS (2.4%) than TW (1.9%). Water content remained relatively consistent along the TG (mean= 21.2%) and TW (mean= 22.1%) transects, with standard deviations of less than 10% (Fig. 2). However, water content level increased to over 30% in the mid and lower intertidal zones of TS (mean= 27.2%). Overall, considering the distribution pattern of sediment parameters, TG and TW closely reflected the typical features of temperate intertidal flats, while TS showed distinct variation in sediment patterns along the transect.

number of locations for the corresponding group (constancy, CON), (3) the ratio of species abundance in each group over the total abundance of corresponding species in the entire area (degree of association regarding individuals, DAI), and (4) the ratio in the number of locations at which the species occurs in each group over the total number of locations at which the corresponding species occurs in the entire area (degree of association regarding stations, DAS). After identifying the location groups by using CA, DA was used to extract significant discriminant functions and to identify the major environmental parameters that discriminate across the location groups. Each sampling location was consecutively placed in the two-dimensional space of discriminant functions to calculate the prediction accuracy of the functions. The prediction accuracy was defined as the probability that the predicted type of faunal assemblage is matched to the real type of faunal assemblage. The use of DA had not been popular in benthic studies (Weston, 1988), but has been increasingly applied in recent years for developing benthic indicators to assess marine environmental quality (Muxika et al., 2007; Paul et al., 2001). For more information, the concept, objective and applicability of DA in benthic ecological studies are clearly described in Muxika et al. (2007). Data on environmental parameters pffiffiffi were transformed with arcsine ( x) for mud content and with ln (x+ 1) for other variables for the normality (Zar, 1984). The CA and MDS were performed using PRIMER software (Clarke and Gorley, 2006), and DA was examined using SPSS 12.0. The data previously obtained at the same sites in 1988 (An and Koh, 1992) were compared with the data of the present study to provide new insights about the long-term changes in benthic community structure following the placement of dikes. In the 1988 survey, benthic animals were collected by hand-picking to a depth of 30 cm from the top sediment layer by using a quadrat (1× 0.5 m = 0.5 m2) with two repeats. Given the different sampling methods and sizes, comparative analysis was limited to just the dominant species and zonation patterns, and not applied to species numbers and density.

3.2. Macrofauna assemblages Collectively, a total of 75 species, comprising 1961 individuals, were recorded at the 53 sampling locations that were examined in the study; TG (n= 26 sampling stations), TW (n= 20), and TS (n= 7). The entire list of macrofaunal species is provided in Table S3. The numbers of macrofaunal species found along TG (51 species) and TS (50 species) were more than double that of TW (24 species). While the sampling size of TS was approximately a third of TG, the number of species found along TS was comparable to that of TG. The five most dominant species of macrofauna, which were calculated based on density and biomass, are presented in Table 1. While the total density of macrofauna was similar in each area, the composition of dominant species was subject to variation. For example, TG and TW shared two species of the five dominant species (Sinocorophium japonicum and

3. Results 3.1. Environmental parameters Two of the transects, located in the outer (TG) and inner region (TW) of the Saemangeum tidal flat, showed a similar spatial pattern of mud content (decreasing), organic content (decreasing), and water content

Shore level (cm)

Water content (%)

Organic content (%)

Mud content (%)

Gyehwa (TG)

Environment

393

Gwanghwal (Tw)

Sandong (Ts)

100 50 0 4 2 0 40 20 0 300 0 -300 G1

G11

G21

G31

G41 G51 W1

W11 W21 W31 W39 S3

S13

S23

S33

Locations Fig. 2. Data of the environmental parameters; mud content (%), organic content (%), water content (%), and shore level (cm) along the three transects of Gyehwa (TG), Gwanghwal (TW), and Sandong (TS) in the Saemangeum tidal flat, Korea.

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Table 1 Dominant species by density (indiv. m−2) and biomass (g AFDW m−2) in the Saemangeum tidal flat, Korea (relative proportion given in parenthesis). Density dominant Species name Gyehwa (TG) Umbonium thomasi Ilyoplax pingi Moerella rutila Sinocorophium japonicum Glycera subaenea Others Total Gwanghwal (TW) Sinocorophium japonicum Ilyoplax pingi Mediomastus californiensis Perinereis aibuhitensis Nephtys polybranchia Others Total Sandong (TS) Heteromastus filiformis Potamocorbula amurensis Prionospio japonica Balanus albicostatus Batillaria cumingi Others Total

Biomass dominant Class

Density (%)

Species name

Class

Biomass (%)

G D B A P

125 (29) 56 (13) 37 (9) 25 (6) 24 (6) 159 (37) 426 (100)

Lingula unguis Meretrix petechialis Umbonium thomasi Mactra veneriformis Cyclina sinensis Others Total

I B G B B

0.9 0.8 0.4 0.3 0.2 1.3 4.0

(24) (20) (9) (9) (6) (32) (100)

A D P P P

335 (78) 27 (6) 12 (3) 9 (2) 6 (1) 39 (9) 428 (100)

Cyclina sinensis Perinereis aibuhitensis Lingula unguis Macrophthalmus japonicus Ilyoplax pingi Others Total

B P I D D

0.4 0.2 0.2 0.2 0.1 0.3 1.4

(27) (16) (15) (14) (7) (21) (100)

P B P M G

152 (30) 67 (13) 58 (11) 38 (8) 22 (4) 174 (34) 510 (100)

Mactra veneriformis Potamocorbula amurensis Lingula unguis Heteromastus filiformis Batillaria cumingi Others Total

B B I P G

6.2 5.6 1.9 0.4 0.4 1.7 16.2

(38) (35) (11) (3) (3) (10) (100)

Acronyms: A = amphipod, B = Bivalvia, D = Decapoda, G = Gastropoda, I = Inarticulata, M = Maxillopoda, and P = Polychaeta.

Ilyoplax pingi) based on density. Moreover, the total biomass and biomass-based dominant species in each area was subject to large variation. Two bivalves (Mactra veneriformis and Potamocorbula amurensis) accounted for 73% of the total biomass of TS (16.2 g AFDW m−2). Interestingly, the absence of these two bivalve species resulted in the total biomass of TS being comparable to that of TG. The total biomass found at TW was the lowest of the three transects, due to the absence of sand-inhabiting bivalves and gastropods. The brachiopod Lingula unguis was the most biomass-dominant and widespread species across all three transects in the Saemangeum tidal flat. In general, the density distributions of the major macrofaunal species along the three transects reflected the horizontal zonation, following the gradual slope of the tidal flat (Fig. 3). Three species characterized the uppermost intertidal zone of all three transects: including the two nereids Periserrula leucophryna and Perinereis aibuhitensis and the decapod M. japonicus. The habitats of the small decapod I. pingi, the brachiopod L. unguis and the carnivore polychaete Glycera subaenea overlapped with the habitats of the species closest to the highest intertidal zone, but extended further toward the lower intertidal zone. The amphipod S. japonicum, which was an abundant species of TG and TW, showed high densities in the upper intertidal zone. Four species (the gastropod Umbonium thomasi, the decapod Scopimera globosa longidactyla, the polychaete Heteromastus filiformis, and the bivalve Moerella rutila) co-occurred in the mid-lower intertidal zone of TG. However, H. filiformis and M. rutila did not have overlapping distributions at TS. Three densely populated species in TS (the amphipod Melita setiflagella, the polychaete Prionospio japonica and the bivalve P. amurensis) did not share common habitats. Three distinct groups were identified from the dendrogram derived from CA (Fig. 4a). The dimensions of the matrix used for CA was comprised of 53 locations (rows) by 75 species (columns), which included all recorded species. Collectively, those groups were located in relation to the shore level (Fig. 4b). Location groups formed by cluster analysis are superimposed on the two-dimensional MDS obtained from the same similarities (Bray–Curtis similarity index) used in CA. The MDS ordination showed that the location groups

matched well with the result of CA, except for locations G17 and S13 (Fig. 4c). Each group was named after its representative characteristic species (see Graphical abstract), which represented typical macrofauna assemblages in the Saemangeum tidal flat (Table 2). Five characteristic species belonged to the Periserrula–Macrophthalmus assemblage (Group A) that occupied the upper most intertidal zone. Eight species comprised characteristic species of the Umbonium– Meretrix assemblage (Group B), with species being distributed in the lower intertidal zones of TG and TW, and in the mid intertidal zone of TS. The Prionospio–Potamocorbula assemblage (Group C) was only present in the mid-lower intertidal zone of TS, with five characteristic species. The distribution of three species in Group C (P. japonica, P. amurensis, and M. setiflagella) did not overlap along this transect. In the 1988 survey (An and Koh, 1992), three faunal assemblages were also recorded in the study area (Perineries, Macrophthalmus, and Bullacta–Mactra–Umbonium zones). The Perinereis and Macrophthalmus zones that were observed in 1988 are identical to the Periserrula– Macrophthalmus assemblage recorded along all three transects in the current study (Fig. 5: D vs. A). The dominant species of the Bullacta– Mactra–Umbonium assemblage that were recorded in 1988 have been slightly changed to comprise the current Umbonium–Meretrix assemblage at the mid intertidal area (Fig. 5: E vs. B). However, U. thomasi remained the dominant species in both studies. Of additional note, the mid and lower TS area showed a complete change in the structure of benthic assemblages between 1988 and 2005 (Fig. 5: F vs. C). 3.3. Environment–macrofauna relationship DA was performed to identify the environmental variables that would best discriminate the location groups (i.e., faunal assemblages), which were previously determined by CA. The five environmental variables that were used in the analysis included shore level, mud content, coarse sand content, water content, and organic content. The DA resulted in the formulation of the discriminant function (1):

DF = a⋅SL + b⋅MC + c⋅OC + d⋅WC + e⋅CSC

ð1Þ

J. Ryu et al. / Journal of Sea Research 65 (2011) 390–400

Gyehwa (TG)

Gwanghwal (Tw)

395

Sandong (Ts)

40

Periserrula leucophryna 0 100

Perinereis aibuhitensis

0 20

Macrophthalmus japonicus

0 400

Ilyoplx pingi

0 100

Lingula unguis

0 80

Abundance (indiv. m-2)

0 5000 0 2000 0 200

Glycera subaenea Sinocorophium japonicum Umbonium thomasi Scopimera globosa longidactyla

0 400

Heteromastus filiformis

0 200

Moerella rutila

0 60

Nephtys polybranchia

0 50

Meretrix petechialis

0 50

Mactra veneriformis

0 60

Melita setiflagella

0 300

Prionospio japonica

0 500

Potamocorbula amurensis

0 G1

G51 W1

W39 S3

S33

Locations Fig. 3. Abundance (indiv. m−2) of major macrofauna from the upper to lower intertidal locations along the three transects of Gyehwa (TG), Gwanghwal (TW), and Sandong (TS) in the Saemangeum tidal flat, Korea.

where a, b, c, d and e should be replaced by the standardized canonical discriminant coefficients presented in Table 3 (acronyms: DF (discriminant function), SL (shore level), MC (mud content), OC (organic content), WC (water content), and CSC (coarse sand content)). Two DFs seemed to be significant in differentiating three location groups based on the χ2 test. The first and second DFs accounted for 69.6% and 30.4% of total separation between the groups, respectively. Standardized DF coefficients refer to the relative contribution of the variables in calculating the discriminant scores for each function. Thus, the coefficients may be used as a measure of the relative importance of the variables between groups (Weston, 1988). Organic (−1.58) and mud content (1.43) were found to be the most significant discriminating variables on DF I, followed by shore level (0.66). Mud content also had the highest standardized coefficient (1.28) in DF II. The Pearson product-moment correlations between DFs and environmental variables (total structure coefficient) provided evidence

towards determining environmental factors that discriminate groups (Weston, 1988). These variables may be represented graphically as vectors in two-factor discriminant space (Fig. 6). The DF I appeared to be representative of shore level (0.47) and water content (−0.56), and clearly separated Group C (low shore level and high water content) from Groups A and B (high shore level and low water content). Meanwhile, the DF II, which had about half the discriminating power of the first function, was strongly correlated with mud (0.98) and organic content (0.83). Next, water content (0.51) also showed a good correlation with the DF II. The DF II served to differentiate Group A (high mud and high organic content) from Group B (low mud and low organic content). The two DFs also accurately predicted the faunal assemblage type of each location based on the environmental variables that were present in each location. The functions presented a prediction accuracy of 97.7%, indicating that the predicted type of faunal assemblage in 51 of 53 locations was consistent with the real assemblage classified by CA (Table 3).

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Fig. 4. Cluster analysis and non-metric MDS ordination of 53 locations (G#: Gyehwa, W#: Gwanghwal, and S#: Sandong) in terms of species composition and abundance: a) groupaveraged clustering from Bray–Curtis similarities based on √√-transformed macrofaunal data; b) shore level of location groups (Groups A, B, and C) on the three transects in the Saemangeum tidal flat, Korea; and c) location groups formed by cluster analysis are superimposed on the two-dimensional MDS obtained from the same similarities (blue: Group A, red: Group B, and black: Group C).

4. Discussion 4.1. Species diversity Diverse species assemblages are often associated with habitat heterogeneity (Attrill et al., 2001; Compton et al., 2008). This hypothesis was supported by the results of the comparison of species richness across the three transects in this study. The number of species in TG (n = 51) and TS (n = 49) were more than double that recorded in TW (n = 24), the results of which agreed with the habitat characteristics in terms of salinity and sediment type. For example, TW was situated close to the mouth of the Dongjin River, and showed lower and broader salinity fluctuations (12–24) than TG and TS (24– 27), based on data collected in July 2004 from an independent survey (KORDI, 2005). The lower salinity recorded in TW is likely to result from freshwater discharge by the intermittent opening of the river dams, and/or from possible submarine groundwater (Kim et al., 2010; Waska and Kim, 2011). TW also showed low variation in sediment type, being primarily dominated by muddy sediment, except for a couple of locations at the lower intertidal zone. While the number of sampling locations surveyed at TS (n = 7) was approximately 3–4 times less than that of TW (n = 20) and TG (n = 26), the number of species at TS (50 species) was comparable to that of TG (51 species). This finding indicates that the benthic habitats of TS are probably more diverse for macrofaunal species, which

supported the theory that geographical locations and/or habitat characteristics may be more important when species diversity is determined. Overall, TS seemed to provide the most optimal benthic habitats for macrofaunal species in terms of species diversity. A total of 75 species were recorded in the Saemangeum tidal flat in the present study, which was comparable the 64 species recorded in the same area during the earlier study (An and Koh, 1992). The numbers obtained in the current study also fell within the range of 24–106 species (median = 44) that have been reported to be present in 16 other temperate tidal flats worldwide (Rodrigues et al., 2006). 4.2. Species distribution The mud-dominated transect of TW had a species composition similar to the upper mud zones in TG and TS, which was shown by the high proportion of co-occurring species. Of the 24 species found along TW, a total of 19 and 20 species were common to the upper intertidal zones of TS and TG, respectively (Table S3). While the total abundance of the upper mud zone differed across transects, it was obvious that similar sedimentary habitats resulted in common benthic faunal assemblages. The results of CA also indicates that the mud-dominated upper zones of the three transects are well sorted into Group A. Overall, species richness and distribution across the three transects of the Saemangeum tidal flat reflected “habitat-dependent” zonal distribution. In fact, Moerella rutila was the only species that showed

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Table 2 Characteristics of three location groups by cluster analysis in Saemangeum tidal flat. All values are given as mean for all locations within the corresponding group.

Environmental characteristics (Mean ± SD) Shore level (cm + MSL) Mud content (%) Organic matter content (%) Water content (%) Community structure indices Total number of species Species density (858 cm−2) Mean density (indiv. m−2) Mean biomass (g AFDW m−2) Ecological indices Diversity (H′) Evenness (J) Richness (R) Dominance (D) Density (indiv. m−2) Macroinvertebrate speciesa Sinocorophium japonicum (A) Ilyoplax pingi (D) Lingula unguis (Br) Perinereis aibuhitensis (P) Periserrula leucophryna (P) Macrophthalmus japonicus (D) Umbonium thomasi (G) Moerella rutila (B) Glycera subaenea (P) Scopimera globosa longidactyla (D) Nephtys polybranchia (P) Mactra veneriformis (B) Meretrix petechialis (B) Cyclina sinensis (B) Macrophthalmus dilatatus (D) Heteromastus filiformis (P) Potamocorbula amurensis (B) Prionospio japonica (P) Balanus albicostatus (Ci) Melita setiflagella (A) Mactra chinensis (B) Feeding type Deposit feeder Filter feeder

Group A

Group B

Group C

235 ± 36 71 ± 14 1.9 ± 0.4 22 ± 2

82 ± 105 37 ± 9 1.4 ± 0.1 21 ± 1

−90 ± 119 74 ± 7 2.7 ± 0.4 29 ± 2

29 6.3 414 2.5

42 9.7 427 3.9

37 12.8 613 19.1

1.5 0.4 4.6 0.8

2.4 0.7 6.8 0.5

2.4 0.7 5.6 0.5

Biomass (g AFDW m−2)

Density (indiv. m−2)

Biomass (g AFDW m−2)

Density (indiv. m−2)

Biomass (g AFDW m−2)

–

–

– – –

–

0.53 0.21 0.18 0.12 N0.01 0.97 1.03 0.19 N0.01 N0.01 – – – – –

– –

0.2 212.1 93.2 81.6 53.6 18.6 2.3

– N 0.01 2.36 – N 0.01 0.25 – – 0.01 – N 0.01 6.54 – – N 0.01 0.63 7.88 0.05 0.08 N 0.01 0.46

0.49 3.17

298.5 291.4

1.15 17.96

262.7 55.8 16.7 16.7 14.8 5.3 – 1.2 3.7 0.8 3.7 – 0.8 0.8 – 2.5 – – – 0.4 –

– N0.01 N0.01 0.04 N0.01 – N0.01 0.39 – N0.01 – – – N0.01 –

– 21.0 5.2 – – – 163.2 54.8 30.3 24.5 17.5 12.8 8.2 1.7 0.7 22.7 – – – – –

383.1 22.1

1.12 1.39

130.1 260.5

0.07 0.21 0.97 0.32 0.05 0.37

0.05 0.15

0.7 9.3 0.3 3.5

7.0 – 11.7 14.0 – –

a Species in bold indicate characteristic species selected, in case of meeting criteria more than three of DOM N 0.05, CON N 0.5, DAI N 0.6 and DAS N 0.6. Acronyms in parenthesis: (A) amphipod, (D) decapod, (Br) brachiopod, (G) gastropod, (B) bivalve, and (Ci) cirriped.

site-specific distribution, whereby it was present in the mid-lower sand flat of TG and in the mid-upper sand flat of TS. Based on the spatial distribution of the major groups of species shown in Fig. 3, four types of species distributions may be delineated in the study area: (1) upper mud, (2) lower sand, (3) lower mud, and (4) wide range zone. In the upper mud zone, P. leucophryna, P. aibuhitensis, and M. japonicus were found to be highly abundant across all three transects. The lower sand zone was dominated by several species, including U. thomasi, S. globosa longidactyla, H. filiformis, M. rutila, N. polybranchia, M. petechialis, and M. veneriformis. Species that were only present in the lower mud zone of TS included P. japonica, H. filiformis, and P. amurensis, all of which were opportunistic and capable of exploiting organic-enriched environments (Pearson and Rosenberg, 1978; Roper et al., 1989). Interestingly, H. filiformis was recorded in high abundance in the lower sand zone of TG as well as the lower mud zone of TS, the cause of which is not clearly understood in this study. Species that were distributed across a wide range included L. unguis, G. subaenea, and M. setiflagella. Peak densities of the capitellid polychaete (H. filiformis) were consistently found in the lower mudflat of TS, which was probably due to its ability to quickly colonize the disturbed region of the TS area. Overall, the spatial distribution and abundance of co-occurring macrofaunal species that were observed along the three transects closely reflected the features of intertidal zonation, although some species expressed unique habitat characteristics.

The sand-dwelling bivalve M. petechialis is renowned as the best tasting bivalve in Korea and is an the iconic species of the Saemangeum tidal flat, resulting in high exports to Japan, and is a typical clam found on the sand-bottom of tidal flats around western coasts of Korean Peninsula (Koh, 1997). This species was previously recorded to inhabit the lower intertidal of the Sandong area with 2 individuals m–2 (An and Koh, 1992), but was not found in this study. This change may have been caused by the environmental shift towards the accumulation of finer sediment near to the TS area, as a result of Sector-IV dike construction (see Lee and Ryu, 2008). 4.3. Zonation characteristics The present study identified three distinct faunal assemblages along the transect lines that were comparable to three zonation patterns found in former studies on several Korean tidal flats. For example, Frey et al. (1987) described three zone assemblages (Brachyuran, Molluscan, and Holothurian zones) along a transect in the Songdo tidal flat (now land-filled and converted to the Songdo International Business District in Incheon of South Korea, 37°23′49″ N, 126°39′16″ E). The Brachyuran and the Molluscan zones from the study by Frey et al. (1987) are comparable to the Periserrula–Macrophthalmus and the Umbonium– Meretrix assemblages of the current study, respectively. However, the Holothurian zone was not found in the present study. Three faunal zones

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Fig. 5. Comparison of benthic assemblages along the three identical transects between 1988 (An and Koh, 1992) and 2004–2005 in the present study in the Saemangeum tidal flat, Korea. Assemblages of two studies were separately classified by cluster analysis.

(Helice, Macrophthalmus, and Laonome–Potamocorbula zones) were also characterized by Koh and Shin (1988) for three intertidal transects of the Banweol mudflat (now land-filled within the artificial lake Sihwa, 37°16′37″ N, 126°50′07″ E). The boundary between the Periserrula–Macrophthalmus and the Umbonium–Meretrix zones may be easily distinguished by two indicators; comprising surface sediment characteristics (by measurement) and biogenic structure (by observation). First, the location that exhibited a sharp change in mud and organic content in sediments effectively indicates the boundary between the two faunal assemblages. The DA analysis also supported this finding. Second, the burrows of M. japonicus and the mounds of P. leucophryna are prominent biogenic structures that are indicative of the Periserrula–Macrophthalmus zone, with these two surface structures abruptly disappearing at the beginning of the Umbonium–Meretrix zone. The Prionospio–Potamocorbula assemblage was only observed in the lower mud zone of TS, and seemed to receive a temporary beneficial effect during the dike construction process. This assemblage showed relatively high levels of diversity, abundance, and biomass when compared to the other two assemblages. Biomass was found to be approximately one order of magnitude greater than that recorded in the other assemblages. Previous research has reported that a moderately nutrient-enriched environment might result in an increase in the

number of species, individuals, and biomass above the level of normal environmental conditions (Dauer and Conner, 1980). As a result of the dike (Sector IV) construction being completed in close proximity to TS in 2003, which was a year before the samples were collected, there was a reduction in the speed of flow of tidal currents, which led to the accumulation of finer sediments and a shift towards higher organic content in the substratum near to the Sandong area (Lee and Ryu, 2008). Thus, favorable conditions of food availability might have promoted greater species numbers and biomass at the low intertidal zone of TS. This assemblage was not observed in 1988, implying the current faunal assemblage in the mid-lower TS might also be caused by the dike construction. However, after the completion of the 33-km dike in April 2006, the majority of the Saemangeum tidal flats were dried out and the benthic community of the study area completely collapsed as a result of desiccation. Based on the DA, shore level and water content are strongly correlated with DF I, which separated Group A and Group B from Group C (Fig. 6), in terms of the total structure coefficient. In addition, the DA and BIOENV results were consistent. However, the standardized DF coefficients in the present study suggest a different interpretation, whereby mud and organic content were considerably more influential than other variables in DF I. Even though the standardized DF coefficients of the mud and organic content in DF I are greater than

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been used successfully as alternative measures to determine the importance of a variable (Flint and Rabalais, 1980). Specifically, when highly variable co-linearity exists (i.e., strong positive/negative correlation), the use of total structure coefficients seems to be more appropriate than the use of standardized DF coefficients (Klecka, 1980). Coarse sand content showed little or no explanatory power for the benthic community pattern. 4.4. Management perspectives

DF1

Fig. 6. Ordination of location groups (Groups A, B, and C) in two-factor discriminant space (■: centroid of the location group). Vectors indicating the relative orientation of the environmental variables are also shown, which were determined from the correlation coefficients between the discriminant functions and the environmental variables (CS: coarse sand content, MC: mud content, OC: organic content, SL: shore level, and WC: water content).

other coefficients, the sum of their contributions in calculating discriminant scores might become zero in most locations because of the strong positive correlation between mud and organic content (note coefficients of 1.43 and −1.58, respectively). Thus, the resulting discriminant scores of DF I are unaffected by the combination of mud and organic content. In this regard, the total structure coefficients have

Table 3 Discriminant analysis of environmental variables among the three location groups in the Saemangeum tidal flat, Korea. Discriminant function (DF) Details

DF I

% of discriminating power 69.6 Eigen value 4.77 Canonical correlation 0.91 Test of significance Chi-squared value 138.25 Significance level p b 0.001 Degree of freedom 10 Standardized canonical discriminant function coefficients Shore level (SL) 0.66 Mud content (MC) 1.43 Organic content (OC) −1.58 Water content (WC) −0.44 Coarse sand content (CSC) 0.40 Total structure coefficient (correlations between DFs and variables) Shore level (SL) 0.47 Mud content (MC) −0.03 Organic content (OC) −0.32 Water content (WC) −0.56 Coarse sand content (CSC) −0.02

DF II 30.4 2.09 0.82 54.12 p b 0.001 4 0.02 1.28 −0.33 0.12 0.24 0.30 0.98 0.83 0.51 −0.17

Classification matrix (n = 53) Original group

No. of locations

Predicted groups (%-accuracy) A

B

C

A B C

27 21 5

26 (96%) 1 0

1 20 (95%) 0

0 0 5 (100%)

Estuarine tidal flats are ecological hotspots, but are often degraded through anthropogenic activities, including land claims, drainage of wastes, shipping and dredging. Such activities are directly and indirectly responsible for the loss of healthy estuarine ecosystems (Gray, 1997). For example, during recent decades in Korea, all estuarine areas have been blocked by dikes to secure water resources for agriculture, with the exception of one estuary, which is impossible to access due to military contentions (Han River). In the past, Korean estuary management strategies have valued ecosystem functions less than economic interests and needs (Koh et al., 2010). However, a recent increase in public awareness about the values and wise uses of wetlands has shifted the environmental management paradigm from development to conservation. The management sector has begun to take ecosystem functions into consideration, through the introduction of sustainable development of these valuable estuarine environments and coastal zones. Furthermore, since 1999 Korea has also designated nine coastal wetlands as protected areas, in an effort to conserve these valuable natural assets (Nam et al., 2010). Thus, it is important to improve our current understanding of marine community structures, functional processes, and food webs in estuarine tidal flats, to promote sustainable use and achievable ecosystem approaches to management practices. In general, the distribution patterns of the major invertebrate species in the Saemangeum tidal flat closely corresponded with the zonation patterns of macrofauna in a typical Korean tidal flat. Of note, the distribution of benthic fauna may be attributed primarily to sediment variables, rather than geographic locality at a scale of tens of kilometers (Kay and Knights, 1975). Assuming that seasonal changes of zoned distribution are minimal and that intertidal soft-bottom benthic assemblages within tens of kilometers from the study area are characterized by the three types of zonation presently reported, DFs might provide a practical tool to predict benthic faunal assemblages based on environmental variables (shore level, mud content, organic content and water content). Such information could potentially be used to produce an ecological map of zoned distribution for the local tidal flat management. For application to a regional scale, existing benthic data and additional studies should be further developed and expanded to identify benthic assemblages of other tidal flats, which may subsequently be extracted from a remote-sensing database. 5. Conclusions Identification of the type and extent of benthic habitats in Korean tidal flats is of growing importance, due to increasing demands for tidal flat management, such as the designation of coastal wetland protected areas. Furthermore, many tidal flats are under significant threat of habitat change as a result of human activities (such as land claims and pollution), and thus benthic habitats require monitoring and science-based management for the selection of appropriate conservation efforts. Despite considerable environmental variability in the Saemangeum tidal flat, ecologically reliable macrofauna-sediment associations were identified. Salinity and sediment characteristics were the major factors that contributed to determining species diversity in the estuarine tidal flat. The results of the present study conclusively suggested the presence of three representative faunal assemblages, which were reliably explained by environmental variables that are relatively easily measured. The comparison of faunal composition across a 17 year period indicated

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the consistent adjustment of fauna over time, and provided indications of the impact of certain environmental changes. Given the strong and consistent association between environmental parameters and benthic faunal distribution over the years, further modeling studies are required to predict and estimate intertidal macrozoobenthic assemblages across broad regional scales, both qualitatively and quantitatively, by using the known environmental parameters. The assimilation of such information could potentially lead to the establishment of a robust scientific database for the ecosystem approach to tidal flat management in partnership with China, Japan and Korea within the Yellow Sea Large Marine Ecosystem. Supplementary materials related to this article can be found online at doi:10.1016/j.seares.2011.03.003.

Acknowledgments This study was supported by a grant (Project # PM55600) from “Support for research and applications of Geostationary Ocean Color Satellite (GOCI)” funded by the Ministry of Land, Transportation and Maritime Affairs, Republic of Korea, given to JSK. This work was also supported, in part, by the project entitled “Development of Integrated Estuarine Management System” funded by the Ministry of Land, Transport and Maritime Affairs (No. 41873-01), given to JSK & CHL. We kindly appreciate the valuable comments and suggestions of the reviewers during the review process.

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