Structural Changes in Macrozoobenthic Communities ... - Springer Link

Ocean Sci. J. (2012) 47(1):27-40 http://dx.doi.org/10.1007/s12601-012-0003-9

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Article

Structural Changes in Macrozoobenthic Communities due to Summer Hypoxia in Gamak Bay, Korea Jin-Young Seo1, So-Hyun Park1, Jung-Ho Lee2, and Jin-Woo Choi1* 1

South Sea Environment Research Department, South Sea Branch, KORDI, Geoje 656-830, Korea Division of Marine Technology, College of Fisheries and Ocean Sciences, Chonnam National University, Yeosu 550-749, Korea

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Received 27 October 2011; Revised 30 January 2012; Accepted 14 March 2012 © KSO, KORDI and Springer 2012

Abstract − The purpose of this study was to examine the structural changes that macrozoobenthic communities underwent as a result of the annual summer hypoxia at the northern part of Gamak Bay, Korea. During this study period, summer hypoxia occurred at the northern part of Gamak Bay in July. Under hypoxic conditions, both the number of species and population density decreased rapidly. Species diversity also manifested lower values during this hypoxic period. Faunal composition changed seasonally with Capitella capitata dominant at the hypoxic sites in spring but disappearing in summer. The health condition of the benthic faunal community assessed by the composition of functional groups within community also changed due to the summer hypoxia from a slightly polluted condition to a highly polluted condition. From these results it has been shown that the recent macrozoobenthic community structure in Gamak Bay has returned to a state similar to what it was before dredging works commenced. Key words − hypoxia, macrozoobenthos, structural change, functional group, Gamak Bay

1. Introduction Hypoxia is defined as a concentration of dissolved oxygen that is less than 2.8 mg L-1 (Diaz and Rosenberg 1995). The formation of hypoxic conditions is thought to begin when both the DO consumption by decomposing bacteria is high and the input of particulate organic matters produced in nutrient enrichment conditions is increasing and when there is a restriction of DO supply to bottom layers as a result of physical stratification. Hypoxia is a worldwide problem, and is deemed responsible for many *Corresponding author. E-mail: [email protected]

environmental issues such as periodic fish kills, reduced abundance and distribution of fish and reduced catches (Breitberget et al. 2003; Wu 2002). Furthermore, from evidence in recent decades, the frequency and severity of hypoxic events has increased (Diaz and Rosenberg 1995; Wu 2002; Diaz et al. 2004), and ‘dead zones’ have been recorded in over 140 locations from enclosed bays and estuaries to open seas (Diaz and Rosenberg 2008). The biological effects of hypoxia on biota are numerous and varied and are related to different levels of residence and tolerance. Such responses include predator avoidance and changed feeding behaviors (Lefrancoiset et al. 2005; McNeil and Closs 2007; Wannamaker and Rice 2000; Wu et al. 2002), some negative effects on early life stages (Ciuhanduet et al. 2005; Czerkieset et al. 2001; Hassell et al. 2008), changes in physiological functions (Cerezoet et al. 2006; Cooper et al. 2002; Taylor and Miller 2001), and most importantly, decreased reproductive activity (Diaz and Rosenberg 1995; Landry et al. 2007; Shang et al. 2006; Wu 2002). Summer hypoxia will affect benthic faunal composition by promoting more tolerant benthos and by inducing community succession after hypoxia. Thus the functional composition of the macrobenthic community will be a good indicator of the ecological quality status of benthic faunal assemblages. Using this functional group composition within the benthic community, a few numerical indices for the assessment of the benthic fauna health condition have been proposed (Borja et al. 2000; Lee et al. 2003; Choi and Seo 2007). In Korean coastal waters, the occurrence of summer

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hypoxia was first reported in Masan Bay (Hong and Lee 1983), after which a few studies confirmed hypoxic events in Masan and Jinhae Bay (Hong 1987). In addition, this summer hypoxia was also found to occur in other coastal areas of Korea such as Gamak Bay (Shin 1995), Shihwa Dike (Hong et al. 1997), Chunsu Bay (Lee and Park 1998), and Youngsan River estuary (Lim et al. 2006). At the northern part of Gamak Bay, the sediment has been organically enriched and contaminated with anthropogenic pollutants. Thus sediment dredging efforts have been performed for long time between 2001 and 2006. Before the sediment dredging, a few studies had been undertaken on macrozoobenthos (Shin 1995; Koo et al. 2004; Yoon et al. 2007; Yoon et al. 2008). However, there was no seasonal benthic fauna data at the level of an entire bay after dredging work had been performed. In this study, we endeavored to determine the effects of sediment dredging on the benthic faunal community at the level of a whole bay and also to determine the structural changes in macrozoobenthic communities before and after the annual summer hypoxia at the northern part of Gamak Bay, Korea.

2. Materials and Methods Environmental variables In order to measure the bottom dissolved oxygen concentration, a modified Niskin-type water sampler which is capable of collecting bottom water above 20 cm from the surface sediment was used. The collected bottom water was immediately fixed with MnSO4 and titrated by the WinklerAzide modification method in a laboratory. Water depth, salinity and temperature of water column were measured using a CTD meter (SBE-19, Sea-Bird Electronics). For the content of total organic carbon (TOC), 50 ml of surface sediment was immediately taken on deck from the sediment samples collected by an improved van Veen grab sampler. At the same time, the temperature at a 5 cm sediment layer was measured using a metal sensor thermometer (DT400, Testo). Sediment samples were dried at 70 °C for 24 hr, and powdered in mortar. Inorganic carbon was removed with 1N hydrochloric acid. TOC was measured using a CHNS analyzer (EA1112, Thermo scientific). Macrozoobenthos sampling and analysis Macrobenthic organisms were collected seasonally at 20 sites in Gamak Bay, on the southern coast of Korea from

Fig. 1. Map showing the study area and sampling sites for macrozoobenthos in Gamak Bay, Korea

May, 2009 to February, 2010 (Fig. 1). Using van Veen grab (0.1 m2), triplicate grab samples were collected at each site, and collected sediment was sieved through a 1 mm mesh screen, and the remaining materials including macrozoobenthos were fixed with 10% formalin buffered with sea water. Benthic faunas were sorted into major taxonomic groups and their wet weight was measured. All fauna were identified into species level if possible and their individual number was counted. For species diversity measurement, Shannon’s diversity (H’) was calculated using the individual data matrix. To determine the health condition of the macrozoobenthic community, functional group classification within benthic faunal samples was conducted and the related benthic faunal indices such as BPI (Benthic Pollution Index) and AMBI (AZTI’s Marine Biotic Index) were calculated. BPI was calculated using the following equation: BPI=[1-(a×N1+b×N2+c×N3+d×N4)/(N1+N2+N3+N4)/ d]×100 where N1, N2, N3, N4 are the abundance of carnivores and filter feeders, surface deposit feeders, subsurface deposit

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Community structural changes in macrozoobenthos as a result of summer hypoxia in Gamak Bay

Table 1. The list of dominant macrobenthic fauna (more than 1.0%) assigned to the functional groups of BPI and AMBI May, 2009 July, 2009 Functional group Functional group Species % Species BPI AMBI BPI AMBI Theora fragilis N4 GIV 21.4 Eriopisella sechellensis N2 GI Musculus senhousia N4 GIV 13.2 Lumbrineris longiforia N3 GIV Lumbrineris longiforia N3 GIV 10.9 Musculus senhousia N4 GIV Eriopisella sechellensis N2 GI 10.4 Praxillella affinis N3 GI Notomastus sp. N3 GIII 5.5 Theora fragilis N4 GIV Thelepus sp. N2 GIII 4.5 Corophium sinense N2 GIII Praxillella affinis N3 GI 4.0 Notomastus sp. N3 GIII Heteromastus filiformis N3 GIV 2.2 Thelepus sp. N2 GIII Idunella chilkensis N2 GI 2.0 Nephtys ciliata N1 GII Corophium sinense N2 GIII 2.0 Nephtys oligobranchia N1 GII Nephtys oligobranchia N1 GII 1.8 Glycera chirori N1 GII Capitella capitata N4 GV 1.7 Heteromastus filiformis N3 GIV Glycera chirori N1 GII 1.5 Idunella chilkensis N2 GI Sigambra tentaculata N4 GIV 1.4 Melitidae unid. N4 GIV Pista cristata N2 GI 1.0 Sternaspis scutata N3 GIII Arcidae unid. N1 GI October, 2009 February, 2010 Functional group Functional group Species % Species BPI AMBI BPI AMBI Eriopisella sechellensis N2 GI 27.8 Eriopisella sechellensis N2 GI Lumbrineris longiforia N3 GIV 10.1 Lumbrineris longiforia N3 GIV Paralacydonia paradoxa N3 GIII 4.3 Paralacydonia paradoxa N3 GIII Idunella chilkensis N2 GI 4.3 Corophium sp. N2 GIII Raphia undulata N1 GII 3.9 Corophium sinense N2 GIII Heteromastus filiformis N3 GIV 2.7 Idunella chilkensis N2 GI Paradexamine banardi N1 GI 2.5 Heteromastus filiformis N3 GIV Praxillella affinis N3 GI 2.5 Glycera chirori N1 GII Paraprionospio cordifolia N4 GIV 2.4 Theora fragilis N4 GIV Theora fragilis N4 GIV 2.4 Polynoidae unid. N1 GII Glycera chirori N1 GII 2.2 Paradexamine banardii N1 GI Notomastus sp. N3 GIII 1.7 Tharyx sp. N2 GIII Corophium sinense N2 GIII 1.7 Musculus senhousia N4 GIV Aglaophamus sp. N1 GI 1.2 Prionospio ehlersi N2 GIV Musculus senhousia N4 GIV 1.1 Erictonius pugnax N2 GI Sigambra tentaculata N4 GIV 1.1 Ennucula tenuis N2 GII Micropodarke sp. N4 GIV 1.1 Paraprionospio cordifolia N4 GIV Terebellides horikoshii N2 GI 1.0 Notomastus sp. N3 GIII Nephtys oligobranchia N1 GII 1.0 Nephtys oligobranchia N1 GII Paraprionospio patiens N4 GIV 1.0 Aora sp. N2 GI Tharyx sp. N2 GIII 1.0 Melitidae unid. N4 GIV Anaitides koreana N1 GII Sigambra tentaculata N4 GIV Brada villosa N2 GII

feeders, and opportunistic or pollution indicative species, respectively. The weight constants in the equation, a, b, c, d,

% 15.1 13.8 10.2 7.5 6.9 4.0 4.0 3.1 2.4 2.3 2.2 2.1 2.0 1.2 1.1 1.0 % 15.9 10.7 4.9 4.7 4.4 3.2 3.1 2.8 2.7 2.4 2.2 2.1 2.0 1.8 1.8 1.7 1.6 1.4 1.4 1.2 1.1 1.1 1.1 1.0

were given as 0, 1, 2, and 3, respectively. Thus BPI is given as 0 when all macrofauna were composed of opportunistic or

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pollution indicative species, while the value of BPI is given as 100 when all specimens were carnivores or filter feeders. For the calculation of BPI, we used the information on the functional group classification of macrobenthic fauna from Shiwha Lake (Lee et al. 2003), Gwangyang Bay (Choi et al. 2003) and Masan Bay (Choi and Seo 2007). The dominant macrobenthic fauna accounted for more than 1% of total abundance and their functional group is given in Table 1. The theoretical basis of BPI comes from the ITI (infaunal trophic index) proposed by Word (1978) who used the feeding guild concept that the community structure of macrobenthic fauna may change in response to the organic enrichment of sediment. Thus the equilibrium of species with large body size and long life span such as carnivores and suspension or filter feeders with tube under normal conditions will be replaced by the subsurface deposit feeders that utilize organic matter within sediment. In our BPI, opportunistic or pioneer species were also replaced when the benthic environment was severely damaged or degraded. BPI lacks a consistency of attributes by mixing different functional groups, that is, add life strategy to the feeding guilds. Thus AMBI was also calculated using the same data in order to complement BPI. For the calculation of AMBI, we used the species-list from Borja et al. (2000) and a recently added species-list (http://ambi.azti.es). Those dominant macrobenthic fauna accounting for more than 1% of total abundance were assigned to each functional group and is given in Table 1. AMBI was calculated by the following equation: AMBI=(0.0×%GI+1.5×%GII+3.0×%GIII+4.5×%GIV +6.0×%GV)/100 Where GI, GII, GIII, GIV, and GV are the abundance of pollution sensitive, pollution insensitive, pollution tolerant species, secondary pollution indicative, and firstly pollution indicative species, respectively. Macrobenthic fauna assigned to the secondary pollution indicators mainly consisted of cirratulid worms whose populations would increase at organically enriched substrates, and those assigned to the first pollution indicators consisted of well-known pollution indicators such as Capitella capitata. The values of AMBI will be in the range of 0.0 (when all specimens are included in the GI group) to 6.0 (when all specimens are in the GV group). When no benthic fauna is found, the value of AMBI is given as 7.0. For multivariate analysis, a square-root transformation of

abundance data was performed, and cluster analysis and nMDS (Non-metric multidimensional scaling) ordination based on the Bray-Curtis similarity matrix were performed using the PRIMER software v.5.0 (Clark and Warwick 1994).

3. Results and Discussions Benthic habitat conditions Bottom DO showed a seasonal fluctuation from 1.3 mg L-1 to 14.4 mg L-1, and the lowest DO occurred at the inner part of the bay and it increased toward the bay mouth with a clear spatial gradient (Fig. 2). Bottom DO was lower than 2.0 mg L-1 at the northern part of the bay, and hypoxia occurred in July, 2009. But the concentration of bottom DO recovered from hypoxic conditions in October, 2009. Total organic carbon (TOC) contents were in the range from 1.7 to 2.4% (mean 2.0 ± 0.4%) in the hypoxic zone, and in the range from 0.7 to 1.3 (mean 1.0 ± 0.2%) in the normoxic zone (Fig. 3). Sediment temperature ranged from 5.8 to 24.0 °C during the study period. Before sediment dredging, the highest TOC content was observed in the most northern part of the bay, where the TOC values were in the range of 1.1 to 1.4% (mean 1.2 ± 0.1%) in the summer of 1999, in the range of 0.9 to 1.1% (mean 1.0 ± 0.1%) in the winter of 2000 (Yoon et al. 2007). However TOC was in the range of 1.5 to 2.1% in the winter of 2005 and 2006 just after sediment dredging (Yoon et al. 2008). The recent mean TOC of 2.0% in the hypoxic zone of Gamak Bay was higher than those before sediment dredging. This indicates that TOC had increased steadily until 2009 when sediment dredging commenced. Benthic faunal composition Total species number collected at each sampling time were in the range of 123 species (July, 2009) to 144 species (Feb., 2010) showing a similar species richness between seasons (Table 2). The total population density decreased from 1,020 ind.m-2 (May, 2009) to 567 ind.m-2 (Oct., 2009) and remained at a similar level to summer density. However, biomass increased from 35.5 g wet m-2 (May) to 132.2 g wet m-2 (July) and after then the biomass remained at a similar level to the summer biomass level. The lower density seemed to be related with hypoxia which killed the most fauna at some inner sites. The mean species richness and density were lowest in autumn, while these showed the highest values in


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Fig. 2. Spatio-temporal changes of bottom DO (mg O2/L) in Gamak Bay during the study period

spring in the hypoxic zone (Fig. 4). In the normoxic zone, however, the mean species richness was over 30 and density was in the range of 619-815 ind. m-2. Thus the macrobenthic

faunal community in the normoxic zone did not show any significant differences between seasons (Fig. 4). Hypoxia will cause some severe damage to benthic

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Fig. 4. Mean species numbers and individuals occurred at hypoxic and normoxic zones Fig. 3. Mean TOC values in Gamak Bay during the study period

faunas. In the case of the northern-central part of Tokyo Bay, when hypoxia occurred in July, defaunation of macrobenthos occurred in August (Kodama et al. 2011). In the northern Gulf of Mexico, hypoxia occurred in mid-May and lasted for four months (until mid-September), but benthic faunal densities under mild hypoxia were at a similar level with those from the normoxic areas until August (Baustianet al. 2009). However, under severe hypoxia, infaunal density

decreased one month after the occurrence of severe hypoxia (Baustian and Rabalais 2009). In Gamak Bay, mild hypoxia occurred in July and lasted for two months, but all faunas were not eliminated immediately even though their mean density decreased continuously after July. After the water column recovered from hypoxia, the larvae of macrozoobenthos could recruit on the summer hypoxic sites in October. There was a different species composition between the two zones. In the hypoxic zone, the major dominant species were Theora fragilis and Musculus senhousia (bivalves),

Table 2. Number of species (spp. 0.3 m-2), density (ind.m-2), and biomass (g wet m-2) of macrozoobenthos at each site in Gamak Bay Date Site 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Total Species 32 28 18 29 34 24 31 28 36 31 35 45 40 38 27 48 27 32 25 31 139 May, Density 2,490 2,407 900 1,543 1,213 737 1,357 623 1,617 1,387 1,260 743 410 543 657 590 417 603 297 590 1,020 09 Biomass 30.5 85.4 40.3 87.5 39.5 40.7 68.5 31.0 33.9 47.4 11.6 29.6 23.3 7.3 12.9 15.3 1.9 17.1 8.4 76.6 35.5 Species 4 3 9 16 19 39 21 31 30 38 36 31 43 30 34 41 31 31 32 29 123 Jul, Density 667 37 267 957 430 1,230 947 493 350 657 793 597 527 463 507 390 563 803 583 577 592 09 Biomass 6.2 0.7 192.4 171.7 433.6 71.0 759.0 24.8 413.5 81.7 48.8 69.2 74.8 100.5 67.2 32.6 17.4 27.6 12.6 38.0 132.2 Species 13 3 1 1 6 40 18 27 29 30 34 41 35 37 37 54 29 35 50 39 138 Oct, Density 270 13 3 3 20 537 350 367 970 710 1,493 823 480 457 823 1,377 397 590 820 820 567 09 Biomass 17.8 0.5 0.1 0.0 0.3 99.9 17.3 26.2 70.3 350.7 34.8 441.9 52.4 181.2 533.1 166.5 71.2 39.0 65.9 20.5 109.5 Species 14 7 12 19 7 18 28 49 41 37 31 35 38 32 20 52 35 23 45 28 144 Feb, Density 203 50 267 167 123 143 427 967 1110 987 737 1080 463 423 277 1363 487 243 1157 513 559 10 Biomass 5.9 1.5 1.4 7.0 0.8 13.3 74.0 44.2 86.0 144.4 46.6 53.8 28.3 37.5 79.7 116.9 27.5 122.8 1,457.6 17.1 118.3

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Table 3. Dominant species from hypoxic and normoxic zones Hypoxic zone Species Density Theora fragilis 537 Lumbrineris longiforia 348 Musculus senhousia 298 May, 2009 Thelepus sp. 195 Notomastus sp. 131 Capitella cpitata 85 Lumbrineris longiforia 175 Musculus senhousia 65 Thelepus sp. 63 Jul, 2009 Notomastus sp. 58 Nephtys oligobranchia 43 Theora fragilis 42 Micropodarke sp. 24 Hemigrapsus pecillatus 14 Hydroides ezoensis 6 Oct, 2009 Paraprionospio patiens 5 Alpheus brevicristatus 4 Harmothoe sp. 3 Erictonius pugnax 46 Theora fragilis 45 Musculus senhousia 10 Feb, 2010 Aora sp. 9 Nectoneanthes oxypoda 8 Hemileucon hinumensis 7

Lumbrineris longifolia, Micropodark sp., and Capitella capitata (polychaete worms), and Erictonius pugnax (amphipod) (Table 3). In the normoxic zone, Eriopisella sechellensis (amphipod), L. longifolia and Praxillella affinis (polychaete worms) were the typical dominant species. The lowest values in species number and density were observed at the northern area of Gamak Bay from summer to winter. But during spring, the maximum density occurred due to the massive appearance of opportunistic species such as T. fragilis, M. senhousia, Capitella capitata (Table 3). T. fragilis is known to be highly dominant where there are high levels of organic matter and also to have a high physiological tolerance to hypoxic conditions (Holmes and Miller 2006; Kodama et al. 2011). Functional group composition Macrobenthic faunas were assigned into functional groups according to their sensitivity to increasing organic matter enrichment. Dominant species assigned to each functional group accounted for more than 75% of the whole

Normoxic zone Species Theora fragilis Eriopisella sechellensis Musculus senhousia Lumbrineris longiforia Praxillella affinis Notomastus sp. Eriopisella sechellensis Musculus senhousia Lumbrineris longiforia Praxillella affinis Theora fragilis Corophium sinense Eriopisella sechellensis Lumbrineris longiforia Paralacydonia paradoxa Idunella chilkensis Raphia undulata Heteromastus filiformis Eriopisella sechellensis Lumbrineris longiforia Paralacydonia paradoxa Corophium sp. Corophium sinense Idunella chilkensis

Density 138 132 94 51 49 38 112 59 58 55 41 30 197 71 30 30 27 19 111 75 34 31 31 23

community abundance. Second-order opportunistic species (Group IV) showed their highest population density in the hypoxic zone from May, 2009 to October, 2010 (Table 1; Fig. 5). Sensitive species, whose population density decreased with organic matter loading and which were assigned into Group I, had their highest population densities in the normoxic zone. The larvae of common surface deposit feeders such as Paraprionospio sp. A (identified by Yokoyama (2007) as P. patiens) can tolerate low oxygen conditions during developmental stages and they can also delay their settlement on the substrates until oxygen levels increase in autumn (Yokoyama 1995). Paraprionospio patiens did not dominate during study period, but Group IV made up the highest proportion of the benthic community in Gamak Bay, especially in autumn. This indicated that the first benthic recruiters at the hypoxic sites in autumn were surface deposit feeders belonging to Group IV not to Group V. The values of AMBI in the hypoxic zone were in the range of 2.3 to 5.4 (Fig. 6). This means that the benthic

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Fig. 5. The functional group composition of macrozoobenthos occurred in Gamak Bay (GI: carnivores and some depositfeeder, GII: suspension feeder, less selective carnivores and scavengers, GIII: surface deposit feeder, GIV: secondorder opportunistic species, subsurface deposit-feeder, GV: First-order opportunistic feeder, deposit feeder)

fauna community was subjected to from mildly to heavily polluted conditions in winter and summer, respectively. However, the AMBI in the normoxic zone revealed that the benthic fauna was in a healthy condition or in a moderately polluted one. The values of BPI at the hypoxic zone were in the range from 15 (heavily polluted conditions) to 49 (moderately polluted conditions) in autumn and winter, respectively (Fig. 6). The AMBI showed the benthic faunal community at the hypoxic zone was subjected to very unhealthy conditions in summer whereas the BPI revealed this in autumn. Some species were assigned to different functional groups according to AMBI and BPI, so the community may be assessed as being subjected to different health environments. For example, Praxillella affinis (a polychaete worm) was deemed to be a sensitive species according to AMBI, but a second-order species according to BPI (Table 1). In previous benthic community study conducted at Gamak Bay, BPI was in the range from 50 to 62 during August, 1998, but it was very low at the hypoxic zone where there was no benthic fauna (Koo et al. 2004). BPI ranged from 4 to 72 in May, 1999. Thus the health status of macrozoobenthic communities during 1998-1999 and 20092010 was at a similar level. Species diversity The Shannon species diversity index (H’) at each site was in the range from 0.8 to 1.8 (mean 1.3±0.6) with lower values and a large variation between seasons in the hypoxic zone, while it was in the range from 2.5 to 2.6 (mean 2.5±0.4) with higher and similar annual values in the normoxic zone (Fig. 7). In previous study on the polychaete community in Gamak Bay, there was no fauna in the hypoxic sites (8 sites), and the mean value of the Shannon

Fig. 6. Mean values of AMBI and BPI at hypoxic and normoxic zones

Fig. 7. Mean values of species diversity indices (H’) at hypoxic and normoxic zones


diversity index from normoxic sites was 1.66 in the summer of 1993 (Shin 1995). During the summer of 1999, no macrofauna were collected from hypoxic sites. The mean index value of the Shannon diversity was 2.0 ± 1.1 in September, 1999 and February, 2000 (Yoon et al. 2007). In this study, there were some macrofauna at hypoxic sites in

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summer, which indicates a slight improvement in the benthic habitats compared with those from a decade ago. Spatial distributions From the results of the cluster analysis, Gamak Bay could be divided mainly into two site groups with similar species

Fig. 8. Dendrograms and MDS plots based on the macrozoobenthic abundance data

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composition (Fig. 8). Site group A belonged to the sites located in the hypoxia zone. The dominant species of this site group were Capitella capitata (Polychaeta) and Theora fragilis (Bivalvia). These species are opportunistic species whose density will increase with increments in sediment organic matter content (Grassle and Grassle 1976; Lim et al. 2006). Site group B could be subdivided into two groups. Site group B-1 included an intermediate zone located between the hypoxic and normoxic zone. In this group, the dominant species were Eriopisella sechellensis (Amphipoda), Paraprionospio cordifolia, Lumbrineris longifolia (Polychaeta). Site group B-2 included sites at the normoxic zone and some sites at the intermediate zone depending on the season. In this group, the dominant species were E. sechellensis (Amphipoda) and Theora fragilis (Bivalvia). The faunal similarity among seasons was higher than that between sites located at the hypoxic zone (Fig. 9). However, the faunal similarity between sites in the normoxic zone was higher than that in the hypoxic zone. The faunal composition at both site 5 and 6 was different from other sites in the normoxic zone during October, 2009 and February, 2010. According to previous studies, there existed three different water masses and each watermass showed a specific different community structure (Shin 1995). In this study,

Fig. 9. Two-dimensional MDS plots of macrozoobenthos occurred at hypoxic and normoxic sites in Gamak Bay

there were 3 site groups approximately corresponding to the 3 different water masses in Gamak Bay. Opportunistic species such as Capitella capitata, Theora fragilis, Lumbrineris longifolia appeared with high population densities in the northern area (hypoxic zone) of Gamak Bay. These species have been reported as being dominant fauna in the northern part of Gamak Bay during the pre-dredging periods (Shin 1995; Koo et al. 2004; Yoon et al. 2007; Yoon et al. 2008). Thus the annually repeating summer hypoxia prevented the community succession of macrozoobenthos to a mature stage at the northern part of Gamak Bay and the community structure of macrozoobenthos returned to the previous existing one before sediment dredges. Hypoxic events in Gamak Bay The northern part of Gamak Bay has a concave geographic shape with a water depth of ca 10 m, and there are many long line culturing systems (oyster and mussel) and fish cage farms located there. The annual variation of water temperature is significantly higher than open sea and congested currents occur in northern area (Lee and Cho 1990; Kim et al. 2006). Both the enhanced anthropogenic pollution loading from land and physical summer stratification have resulted in the depletion of bottom DO concentration at the northern part of Gamak Bay since the 1980’s. To improve the environment of this contaminated area around Seonso at the most inner part of the bay, sediment dredging efforts were performed from 2001 to May, 2006. There were some previous studies on polychaete worms in Gamak Bay (Table 4). Polychaete densities fluctuated from 205 ind. m-2 in May, 2010 to 2,802 ind. m-2 in February, 2000. In this study, the density of polychaete worms was the lowest among previous studies. During the hypoxic period, polychaete worms did not appear at a few sites before Aug., 2000 (Shin 1995; Koo et al. 2004; Yoon et al. 2007; MOMAF 2001) whereas there was no azoic site in this study. In the last year of the sediment dredging project in February, 2006, the abundance of benthic polychaete worms decreased to mean densities ranging from 40 ind. m-2 to 290 ind. m-2 at the hypoxic zone (Yoon et al. 2008). In February 2010, the polychaete density decreased to a lower level compared to those from four years ago, and was in the range from 13 to 40 ind. m-2 in the hypoxic zone in Gamak Bay. Before sediment dredging work commenced, the dominant benthic fauna in the hypoxic area were composed of Tharyx


Table 4. Temporal changes in the polychaeta composition of macrozoobenthic community in Gamak Bay Study Density Sampling Sample Dominant speciea period (Ind.m-2) sites (azoic) unit Capitella capitata Feb, 2000 2,802 Euchone alicaudata (15.0%) 12 0.1 m2 Pseudopolydora paucibranchiata Lumbrineris longifolia (17.8%) Capitella capitata (16.1%) Feb, 2005 854 20 0.05 m2 Mediomastus californiensis (9.9%) Euchone alicaudata (13.5%) Feb, 2006 847 20 0.05 m2 Lumbrineris longifolia (13.1%) Paraprionospio pinnata (5.3%) Before hypoxia Lumbrineris longifolia (22.6%) Paralacydonia paradoxa (10.3%) Feb, 2010 205 20 0.1 m2 Heteromastus filiformis (6.5%) Tharyx sp. (37.0%) May, 1999 582 12 0.1 m2 Capitella capitata (16.8%) Lumbrineris longifolia (6.9%) Lumbrineris longifolia (24.7%) Notomastus sp. (12.5%) May, 2009 449 20 0.1 m2 Thelepus sp. (10.3%) Tharyx sp. (31.9%) Lumbrineris longifolia (27.5%) Jul-Sep, 1993 340 47 (8) 0.1 m2 Chone sp. (4.5%) Tharyx sp. (15.0%) Aug, 1998 314 12 (1) 0.1 m2 Praxillella affinis (15.0%) Lumbrineris longifolia (14.2%) Aphelochaeta monilaris (20.6%) During hypoxia Sep, 1999 Lumbrineris longifolia (16.3%) 900 28 (5) 0.1 m2 Terebellides japonica (5.8%) Tharyx sp. (61%) Aug, 2000 2,238 20 (2) 0.1 m2 Lumbrineris longifolia (11%) Lumbrineris longifolia (27.6%) Praxillella affinis (14.9%) Jul, 2009 296 20 (0) 0.1 m2 Notomastus sp. (7.9%) Tharyx sp. (37%) Nov, 2000 2,627 Lumbrineris longifolia (11%) 20 (1) 0.1 m2 Capitella capitata After hypoxia Lumbrineris longifolia (22.9%) Paralacydonia paradoxa (9.7%) Oct, 2009 250 20 (0) 0.1 m2 Heteromastus filiformis (6.2%)

sp., Lumbrineris longifolia, Capitella capitata, Euchone alicaudata, Paraprionosio pinnata (maybe P. patiens). These fauna are known as first-order opportunistic species (C. capitata) and second-order opportunistic ones increase in abundance at disturbed areas that are high in organic matters (Borja et al. 2000). The proportion of these opportunistic species was higher than 50% at the northern

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Reference

2 grabs

Yoon et al. 2007

3 grabs

Yoon et al. 2008

3 grabs

Yoon et al. 2008

3 grabs

Present study

5 grabs

Koo et al. 2004

3 grabs

Present study

2 grabs

Shin 1995

5 grabs

Koo et al. 2004

3 grabs

Yoon et al. 2007

2 grabs

MOMAF 2001

3 grabs

Present study

2 grabs

MOMAF 2001

3 grabs

Present study

part of Gamak Bay that had been severely contaminated with organic matter before the dredging work (Shin 1995). In February 2006, the abundance of opportunistic species decreased from the level in February 2005, but the benthic community was replaced by opportunistic species such as L. longifolia and P. pinnata (Yoon et al. 2008). In this study, 3 years after the completion of sediment dredging, some

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second-order opportunistic species (Theora fragilis, Musculus senhousia, L. longifolia, Paraprionospio patiens) dominated at Seonso located in the hypoxic zone, while the abundance of C. capitata decreased compared to before the dredging work. C. capitata is known as an opportunistic, deposit feeding polychaete worm, and also a common indicator species of organic pollution and one of the early colonizers of disturbed areas with high sediment organic content (Grassle and Grassle 1976; Tsutsumi 1987). In previous studies, C. capitata became the dominant fauna with a density over 1,000 ind. m-2 in February, 1998 and 2000 (MOMAF 2001), but the density of this species was reduced to less than 15 ind. m-2 in February, 2006 just after sediment dredging efforts commenced (Yoon et al. 2008). Sediment organic matter content and AVS (Acid volatile sulfide) contents also decreased from the highly enriched conditions just after dredging began (Yoon et al. 2008).The reduced population density of C. capitata might have been caused by the reduced sulfide content because the presence of sulfides alone can induce larval settlement of C. capitata even sulfide may not be necessary for settlement (Cuomo 1985). Thus the sediment dredging seemed to be effective at reducing the abundance of opportunistic species including C. capitata. In this study, C. capitata was not collected at the hypoxic sites in February of 2009, but their population density was 85 ind.m-2 in May, 2009. The lower population density of C. capitata during the winter season may be attributed to its specific life history. C. capitata population can switch reproductive strategies by making a brood pouch or releasing free swimming larvae according to whether the water temperature is above or below 23 °C, respectively (Tsutsumi 2005).

4. Summary and Conclusion At the northern area of Gamak Bay, an annual summer hypoxia occurred (DO < 2.8 mg L-1) and TOC content of sediments showed the highest values in the study area. After hypoxia, most macrobenthid fauna died and they did not recover until late fall. Most recruited macrobenthic fauna in fall were composed of opportunistic species and they disappeared again with the next summer hypoxia. This was the general phenomenon that occurred before sediment dredging. Immediately after dredging, sediment quality and benthic communities were reported to be improved. Despite the dredging efforts to improve sediment quality, hypoxia

repeatedly occurred in the summer. The health condition of the benthic fauna community assessed by the composition of functional groups within the community also changed due to the summer hypoxia from a slightly polluted condition to a highly polluted condition. In this study, we confirmed that the macrozoobenthic community in the hypoxic area was not restored by sediment dredging and that it was very similar with those that existed before dredging efforts in Gamak Bay.

Acknowledgements The authors would like to sincerely thank Prof. H.-C. Shin at Chonnam National University for his fauna data and valuable comments on this study. We also thank anonymous reviewers for their valuable comments and critiques. This work was supported by KORDI (PE98661 and PE98745).

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