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Hypoxia and benthic community recovery in Korean coastal waters
Marine Pollution Bulletin 52 (2006) 1517–1526 www.elsevier.com/locate/marpolbul
Hypoxia and benthic community recovery in Korean coastal waters Hyun-Sig Lim b
a,*
, Robert J. Diaz b, Jae-Sang Hong c, Linda C. Schaffner
b
a Department of Marine Resources, Mokpo National University, Muan, Chonnam 534-729, Republic of Korea Virginia Institute of Marine Science, College of William and Mary, 1208 Greate Road, Gloucester Point, VA 23062, USA c Department of Oceanography, Inha University, Incheon 402-751, Republic of Korea
Abstract Low dissolved oxygen (hypoxia and/or anoxia) has become a major cause of change to the benthic component of ecosystems around the world. We present the response of a benthic community to hypoxia in organically enriched environments in Korean coastal waters. Disturbances due to low dissolved oxygen (DO), and organic enrichment altered community dynamics, result in defaunation during summer hypoxia with delayed recolonization occurring in winter. As DO decreased, the number of taxa, their abundance and biomass of macrofauna dropped significantly at inner bay stations in Chinhae Bay and Youngsan River estuarine bay affected by hypoxia. With the return of normoxic conditions in Chinhae Bay, recolonization was initiated by opportunistic species, with a 1–4 months lag. The polychaetes, Sigambra tentaculata, Mesochaetopterus sp., and Lumbrineris longifolia, were most persistent under hypoxia. The first recolonizers were the polychaetes Paraprionospio pinnata, S. tantaculata, Glycinde gurjanovae and Nectoneanthes multignatha and the bivalve Theora fragilis. The second group of colonizers included the polychaetes Capitella capitata, Mesochaetopterus sp. and L. longifolia, and the bivalve Raetellops pulchella. Hypoxic and near anoxic conditions resulted in mass mortality in Chinhae Bay and Youngsan River estuarine bay, but communities did partially recover after return to normoxic conditions despite delayed recolonization. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Hypoxia; Korea; Recruitment; Benthic recovery; Opportunistic species
1. Introduction Hypoxia is worldwide in coastal areas, and has been recorded in over 140 locations from enclosed bays and estuaries to open seas (Diaz et al., 2004). Systems affected by hypoxia have increased over the last 40–50 years and are strongly associated with expanded eutrophication from industrialization and urbanization (Cloern, 2001; Diaz, 2001; Gray et al., 2002). Of the many environmental variables affecting benthic community structure, dissolved oxygen in bottom waters is most critical in structuring benthic communities (Diaz and Rosenberg, 1995; Gray et al., 2002).
*
Corresponding author. Tel.: +82 61 450 2392; fax: +82 61 452 8875. E-mail address: [email protected] (H.-S. Lim).
0025-326X/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2006.05.013
In Asia, hypoxia has been reported from Korea, China, Taiwan and Japan (Wu, 1982; Hong, 1987; Jeng and Han, 1996; Karim et al., 2002). In Korean coastal areas, hypoxia and associated red tides have been linked to catastrophic mortality of marine life (Cho, 1991; Kim, 1990). Mortality in Chinhae Bay (Hong, 1987) and the Youngsan River estuarine bay (Lim and Park, 1999) were associated with a one-time summer event, while in Chonsu Bay (Park et al., 2000) and Kamak Bay (Shin, 1995) hypoxia was mentioned as a cause of mortality but without supporting evidence. Unfortunately, the annual development and duration of hypoxia, along with benthic defaunation and recovery, have not been monitored in Korean coastal waters. We provide here a general overview of hypoxia in Korean coastal waters and the response of benthic communities, including complete defaunation due to summer hypoxia/anoxia and winter recolonization.
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2. Characteristics of the study area 2.1. Youngsan River estuarine bay The Youngsan River estuarine bay is located along the southwestern part of the Korean Peninsula and connects to the sea through the narrow Mokpogu water channel (Fig. 1). In this area, two dikes have been constructed: Youngsan dike in 1984, Kumho dike in 1994, to provide a
water supply for irrigating farm land, as well as industrial and municipal services. Prior to dike construction, the Youngsan River estuarine bay was a typical estuarine ecosystem, where seawater was diluted with freshwater from land drainage. The construction of both dikes altered the characteristics of this estuary, with a reduction in water circulation and increased deposition of organic matter and fine sediments near the dikes in the inner part of the estuary (Park, 1987).
Fig. 1. Location of sampling stations and bathymetry of Chinhae Bay and Youngsan River estuarine bay on the southern coast of Korea.
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2.2. Chinhae Bay Chinhae Bay, a semi-enclosed embayment located in the southern part of the Korean Peninsula (Fig. 1), is a spawning and nursery grounds for many commercially important finfishes. It also supported high shellfish production, e.g., intensive long-line cultures of oysters (Crassostrea gigas) and mussels (Mytilus edulis), as well as bottom culture of the arkshell (Scapharca broughtonii). About 7.5% of the total Chinhae Bay area was used for aquaculture. These industries have declined due to environmental stress from organic pollution and hypoxia. Domestic, industrial, and agricultural wastes from adjacent cities and industrial activities have contaminated Chinhae Bay since the early 1970’s; red tide blooms due to dinoflagellates and consequent hypoxia have become annual events (Kim, 1990). Hypoxia now extends over most of the bay, seasonally covering about 54% of the total 497 km2 (Hong, 1987).
Fig. 2. Spatial distribution pattern of bottom dissolved oxygen in Youngsan River estuarine bay, August 1995.
3. Materials and methods 3.1. Youngsan River estuarine bay Triplicate van Veen grab (0.1 m2) samples were collected at 40 subtidal, soft bottom sediment stations in May, August, October 1995 and February 1996 (Fig. 1). Sediments were sieved using 1-mm mesh sieves and ambient seawater and preserved with 10% neutralized formalin solution. Macrofauna were sorted from the sieve. Wet weight biomass was measured for major taxonomic groups (e.g., polychaetes, molluscs, etc.), and all macrofauna enumerated and identified to the lowest possible taxonomic level. Water temperature, salinity, and dissolved oxygen (DO) concentration in the surface and bottom water layers were measured at each station using a SCT meter (YSI-32) and DO meter (YSI-58).
was 0.8–10.2 mg/l in summer. In contrast, hypoxia has not been observed near the recently constructed Kumho dike.
4. Result
4.1.2. Chinhae Bay Hypoxia first developed in innermost areas of the Bay by May, when DO was 1.7 mg/l at station 1 (Fig. 3). By June, hypoxic areas extended out into the bay proper, with the Masan area recording 0.9 mg/l (17.9% of saturation) and 0.3 mg/l (5.5%) at stations 1 and 2, respectively (Fig. 3). The DO continued to decline in July with <0.2 mg/l (3.3% of air saturation) at station 1, 0.2 mg/l (4.0%) at station 2, 1.2 mg/l (22.9%) at station 11, and 0.7 mg/l (12.7%) at station 12. By August, DO concentrations reached their lowest levels, with 0.01 mg/l (0.2%), 0.07 mg/l (1.3%) and 0.6 mg/l (11.7%) at stations 1, 2 and 12, respectively. Central bay low DO levels remained throughout September. In October, DO concentrations in bottom waters recovered to more normal levels (>4.0 mg/l) over the entire area of the bay; higher levels of DO remained until February of the following year. Differences in DO concentration in surface and bottom waters then appeared by March, with the onset of hypoxia in bottom water again by May, with DO at station 1 in the inner most area of the bay being 0.7 mg/l (11.3% of saturation); this suggests that hypoxia in Chinhae Bay is an annual phenomenon associated with the development of a thermocline.
4.1. Hypoxia areas
4.2. Impact of hypoxia on benthos
4.1.1. Youngsan River estuarine bay Hypoxia (<2.0 mg/l) in Youngsan estuary developed first near the Youngsan dike in summer due to stratification of the water column (Fig. 2). In surface waters, DO concentrations were 5.1–11.2 mg/l, whereas bottom DO
4.2.1. Youngsan River estuarine bay In summer, August 1995, maximum numbers of taxa were recorded near Kumho dike (33 taxa at station 32) as not affected by hypoxia, whereas minimum numbers were from station 1 (nine taxa) stressed by hypoxia and
3.2. Chinhae Bay Five replicate van Veen grab (0.1 m2) samples were collected monthly at each of 12 stations, May 1989 to May 1990 (Fig. 1). The processing of grab samples was the same as for the Youngsan estuary. Water temperature, salinity and dissolved oxygen were measured simultaneously during sediment sampling using a T-S bridge (Type MC 5) and DO meter (Yellow Springs Instrument). Measurements were made 50 cm from sea bottom.
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Fig. 3. Monthly distribution pattern of bottom dissolved oxygen in Chinhae Bay from June 1989 to May 1990.
high organic content of the sediments (Fig. 4). Species numbers were lower at inner estuarine stations near the dike (<25 taxa), higher in the outer part of the estuary (>30 taxa). Low species richness in the inner estuarine bay, near the dike, was positively correlated (P < 0.001) with DO. Similarly, low densities of macrobenthic organisms with <300 ind m 2 were also observed in the area stressed by hypoxia in the inner bay. In contrast, >1000 ind m 2 of macrobenthos were observed in normoxic areas between Mokpo harbor and Youngsan dike. There was significant positive correlation between abundance and DO in the bottom water (P < 0.001). Low biomass of the macrobenthos (1.28 g wet wt m 2 at station 1) was observed near the dike, where the lowest number
of species and abundance were also recorded. Biomass was positively correlated to summer bottom dissolved oxygen (P < 0.05). These results suggested that the spatial distribution of the macrobenthos in Youngsan estuarine bay in summer season was severely influenced by summer dissolved oxygen due to reduced water circulation after dike construction. Variations in number of taxa, abundance and biomass along the hypoxic gradient was closely linked to DO concentration (Fig. 5). The number of taxa was lower at stations 1 and 10, most stressed by hypoxia, whereas it increased continuously toward the normoxic outer area. In contrast, a greater abundance of macrobenthos was observed at station 17 that was transitional between hyp-
Fig. 4. Spatial distribution of macrobenthic fauna (number of taxa, abundance and biomass) in Youngsan River estuarine bay.
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oxic and normoxic areas, with a DO of 2.9 mg/l. The deposit-feeding bivalve Theora fragilis, tolerant of low DO (Tamai, 1993), was abundant at this station. Low total abundance was found at inner stations stressed by hypoxia and also at outer normoxic stations. Greatest biomass was observed at station 30 (outer part of the bay), lowest at station 1. The proportion of polychaete species was greater in areas with hypoxia, lower in normoxic areas. The opposite was found for proportions of molluscs and crustaceans.
Dissolved oxygen (mg/I)
4.2.2. Chinhae Bay The macrobenthos were severely affected by bottom hypoxia in Chinhae Bay, with stations 1 and 2 most affected (Fig. 6). Species richness at station 1 and 2 decreased with time, as hypoxia progressed, and by August these stations were found to be azoic. With the return of normoxic conditions, recruitment occurred and species richness increased gradually from February until April when it started to decrease again. Similarly, abundance, biomass, and species diversity showed the same trend as species richness with a progression of hypoxia. Opposite 10.0 8.0 6.0 4.0 2.0 0.0 1
10
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trends in species richness, abundance, and biomass were observed at stations 3 and 4 over the summer season. At station 1, the development of hypoxia from May to September 1989 led to mass mortality of macrobenthos with complete defaunation by August, when the lowest DO was recorded. While bottom water DO at station 1 had been reoxygenated to >4.0 mg/l by October, azoic conditions persisted until December 1989, when a few individuals of seven taxa recolonized. By January 1990, however, azoic conditions returned and it was not until February that colonizing taxa persisted. Strong recruitment lagged the return of normoxia by some 4 months. Subsequently, bottom water DO began to decrease again by April 1990 when the abundance of macrobenthos was highest for station 1. By May, the abundance of macrobenthos declined, coincidental with DO declining to <2.0 mg/l. There were six species recorded in May, reduced to two species by July; azoic conditions lasted until January. However, recruitment increased the number of taxa to 23 by February. At station 2, hypoxia developed by June, 1 month later than at station 1, causing mass mortality and continuing until September, with azoic conditions for 4 months, August–November. Although bottom dissolved oxygen at station 2 had recovered by October, the benthos did not recolonize until December 1989 when eighteen taxa recolonized following a 2 months lag in recolonization after recovery of bottom DO. In contrast, stations 3 and 4, influenced by water exchange with the open sea, did not experience hypoxia, but DO decreased in summer to 3.7–3.9 mg/l (Fig. 6). Maximum abundances of macrobenthos was found during the summer season. 4.3. Dynamics of benthos in Chinhae Bay
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Fig. 5. Spatial distributions of the number of taxa, abundance and biomass of macrobenthos and community structure parameters along the gradient of bottom dissolved oxygen in Youngsan River estuarine bay.
In Chinhae Bay the dynamic fluctuations in abundance of benthos were related to DO concentration (Fig. 7). By June both stations 1 and 2 were severely hypoxic (<1 mg/ l) and total abundance was declining. Severe hypoxia persisted through September, with normoxic conditions returning by October. However, both stations remained depauperate from August to November, with recruitment beginning by December (Fig. 7). Three polychaetes, Sigambra tentaculata, Mesochaetopterus sp., and Lumbrineris longifolia were most persistent under conditions of hypoxia at stations 1 and 2 (Fig. 7). Individuals of these species survived 2–3 months of hypoxia (May, June, and July) disappearing by August, when DO reached near anoxia at station 1 (0.01 mg/l) and station 2 (0.07 mg/l). Seven taxa appeared sparsely as recruits at station 1 in December, but did not persist. These were a mix of opportunists (Paraprionospio spp., Paraprionospio pinnata, T. fragilis) and equilibrium species (Ophiura kinbergi and its commensal Ophiodromus pugettensis). Species of unknown life-history status were Nectoneanthes multignatha and Hesiospina similis. It was not until February, 5 months after the renewal of bottom water DO, that the community recovered at station
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Fig. 6. Monthly variation of the environmental and community structure parameters in Chinhae Bay. Arrow indicates azoic month during the study period. Dotted line in the dissolved oxygen indicates hypoxia (<2 mg/l).
1, with strong recruitment by the polychaetes, P. pinnata and N. multignatha, and the bivalve, T. fragilis. At station 2, with similar DO concentrations as station 1, recruitment started in December, the first recruits being P. pinnata, T. fragilis, N. multignatha, S. tentaculata, H. similes and O. kinbergi. Subsequently, additional species, i.e. Capitella capitata, Glycinde gurjanovae, L. longifolia, S. tentaculata, Mesochaetopterus sp., and Raetellops pulchella, colonized station 1, and L. longifolia and G. gurjanovae station 2 (Fig. 7). Most of these are known as opportunists and have been associated with low DO (Diaz and Rosenberg, 1995; Gray et al., 2002). In contrast, there was no defaunation at stations 3 and 4, where lowest DO concentrations were 3.3 mg/l in August, 3.6 mg/l in July, respectively (Figs. 6 and 7). During the summer when abundance, biomass, and number of
taxa at stations 1 and 2 were declining, those at stations 3 and 4 either remained unchanged or increased. Species eliminated from stations 1 and 2 during hypoxia persisted at these stations (Fig. 7). By winter, recruitment reached a peak at stations 1 and 2 with populations of P. pinnata and N. multignatha greater than those at stations 3 and 4. Mesochaetopterus sp., L. longifolia, and C. setosa recruitment at stations 1 and 2 did not reach levels of population similar to those at stations 3 and 4. Species that recruited to similar densities at the four stations included T. fragilis, S. tentaculata, R. pulchella, and G. gurjanovae (Fig. 7). 5. Discussion Hypoxia in Korean coastal waters occurred during summer season when the water column was thermally strati-
H.-S. Lim et al. / Marine Pollution Bulletin 52 (2006) 1517–1526 100
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Fig. 7. Monthly fluctuation of macrobenthos in Chinhae Bay, May 1989 to May 1990.
fied; this lead to severe effects on benthic community structure (Table 1). Detrimental effects of hypoxia (DO of <2 mg/l) on benthic communities were reported earlier from Chinhae Bay (Hong, 1987; Lim, 1993) and Youngsan River estuarine area (Lim and Park, 1999), (Fig. 1). In addition, summer hypoxia may develop in Kamak Bay (Shin, 1995) and Chonsu Bay (Park et al., 2000). Hypoxia has been reported as a worldwide phenomenon in temperate regions, with principal causal factors including: stratification of the water column (due to temperature or salinity); reduced vertical mixing; and isolation of bottom waters from oxygenation. Respiration of bottom dwelling organisms and decomposition of organic matter further lowers DO to critical levels and can lead to anoxic conditions where stratification persists. Nutrient and/or organic loading related to urbanization and industrializa-
tion have exacerbated hypoxia in estuarine and marine systems throughout the world (Gray et al., 2002; Diaz, 2001). Low DO in Korean coastal waters was first recorded in Chinhae bay in the mid-1970s. Levels of DO less than 2.0 mg/l were measured in Masan Bay, near station 1 in the present study, in September 1974 (Kim et al., 1976), September 1975 (Kweon, 1979), and May 1982 (Yang and Lee, 1983). Cho (1991) reported reduced levels of oxygen (saturation of 30–80%) at depths between 5 and 10 m in northern and western parts of Chinhae Bay in July 1977, with near anoxic conditions (<5% saturation) below ten meters depth during a Gonyaulax spp. red tide outbreak lasting for 1 week. Yang and Hong (1988) also reported that bottom DO in Chinhae Bay ranged from 0.1 to 4.5 mg/l, with lowest values in Masan Bay. Kim (1990) reported that since 1985 hypoxia in Chinhae Bay has
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Table 1 Summary of benthic effects for hypoxic systems in Korean coastal waters System
Hypoxia typea
Hypoxia levelb
Hypoxic area (km2)c
Time trends
Fauna responsed
Fauna recoverye
Fisheries response
Chonsu Bay Kamak Bay Youngsan Estuary Chinhae Bay
Seasonal Seasonal Seasonal Periodic
Moderate Moderate Moderate Severe
– –
Gradually Gradually Gradually Gradually
Mortality Mortality Mass mortality Mass mortality
Slow Slow Some Some
Reduced Reduced Reduced Reduced
2.8 (11%) 184.5 (46%)
increasing increasing increasing increasing
a
Seasonal, yearly events related to summer or autumnal stratification; periodic, events occurring at regular intervals shorter than a year. Moderate, oxygen decline to about 0.8 mg/l; Severe, decline to near anoxic levels. c Parentheses indicates percentage of whole surface area. d Mortality, moderate reductions of populations, many species survive; mass mortality, drastic reduction or elimination of the benthos. e Slow, gradual return of community structure taking more than a year; Some, recolonization occurs but community does not return to prehypoxic structure. b
of benthic organisms in the inner part of the bay in summer season. In the present study, low number of taxa, abundance, and biomass in Youngsan estuarine bay were observed during summer hypoxia, and defaunation was observed in Chinhae Bay. In Chinhae Bay, there was a 1–4 month time-lag between return of normoxia and recolonization of the benthos. The above results were based on the use of 1-mm mesh; if smaller mesh (e.g., 0.5 mm or less) was used, results would change. The 1-mm mesh screening is typical for Asian studies (Hayashi, 1991; Lim, 1993; Shin, 1995). Polychaetes are generally known to be more tolerant of hypoxia than other taxonomic groups (crustaceans) (Mangum and van Winkle, 1973). Harper et al. (1981) pointed out that amphipod and echinoderms are more severely affected by hypoxic stresses than polychaetes. Similar findings have been reported from other hypoxic events (see Diaz and Rosenberg, 1995; Gray et al., 2002). In our study, initially colonizing species following hypoxia were P. pinnata, N. multignatha and T. fragilis at station 1, P. pinnata, S. tentaculata and G. gurjanovae at station 2. Of these, P. pinnata and T. fragilis are known as broadly distributed opportunistic species tolerant of low DO (Boesch and Rabalais, 1991; Tamai, 1993). Under hypoxic conditions larvae of P. pinnata are also known to delay settlement and remain in the water column until DO increased to >2.8 mg/l (Powers et al., 2001). The ability of larvae to delay settlement and select when and where to settle would reduce postsettlement mortality (Wilson, 1952). S. tentaculata is also broadly distributed and was the third most abundant species to recolonize following hypoxia in the Gulf of Mexico (Powers et al., 2001). The ecological characteristics of G. gurjanovae and N. multignatha relative to low DO are unknown.
become an annual development in June. Fluctuations in DO are controlled by temperature, and to a lesser extent salinity, and driven by stratification. Bottom water hypoxia in Chinhae Bay first develops at inner bay areas in May, when water temperature begins to increase, and covers the widest area by September. A return to normoxic condition usually occurs by October (Table 2). The progression from aperiodic occurrence of hypoxia to predictable annual summer hypoxia that disappears in Autumn is typical of many anthropogenically oxygen stressed systems (Diaz and Rosenberg, 1995) and is related to increased organic matter reaching the bottom (Gray et al., 2002). Systems stressed by the development of annual summer hypoxia characteristically have elevated levels of organic material in surface sediments, which accelerates the reduction of DO (Degobbis, 1989; Rosenberg and Loo, 1988; Zimmerman and Canuel, 2000). Sedimentation of dead plankton and debris accelerates uptakes of dissolved oxygen via microbial activity. Similarly, the decomposition of dead macrobenthos would likely lead to even more severe DO condition. Rosenberg and Loo (1988) emphasized marine eutrophication as due to input of nutrients which induced oxygen deficiency and consequent effects on soft bottom fauna in west Sweden. In Korean waters, bottom water hypoxia resulted in an annual mass mortality of benthos and altered community structure, a response typical of systems experiencing annual hypoxia. Diaz et al. (2004) found that 54% (74 of 142) of hypoxic systems around the world were subjected to annual hypoxia with 39% of them reporting annual mass mortality of benthos. Of this 39%, annual recolonization following the dissipation of hypoxia occurred in 65% of the systems. Zarkanellas (1979) reported that hypoxia in Elefsis Bay controlled the species richness and abundance
Table 2 Monthly variations of the hypoxic area (km2) in Chinhae Bay from June 1989 to May 1990 and Youngsan estuarine bay in August, 1995 DO (mg/l)
Chinhae Bay June
July
August
September
October
November
December
January
February
March
April
May
62.0 2.0–4.0
105.9 109.0
134.0 172.5
142.0 63.0
184.5 42.0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
8.9 26.8
Youngsan estuarine bay 2.8 4.2
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Recolonization of the benthos following depauperization due to hypoxia follows patterns for other forms of disturbance, i.e. the result of larval settlement and emigration of adults (Boesch, 1977; Pearson and Rosenberg, 1978; Harper et al., 1981; Powers et al., 2001). Differences in these responses vary taxonomically. Santos and Simon (1980) suggested that adult emigration by crustaceans and larval settlement by polychaetes were paramount in recolonization following hypoxia. In this study, the occurrence of young T. fragilis and adult polychaetes were observed at station 1, suggesting emigration of adult in polychaetes, larval settlement in bivalves. Sanukida et al. (1981) reported that the abundance of P. pinnata was high in spring (before the development of hypoxia), decreasing gradually with reduced oxygen content. He also noted that abundance of P. pinnata increased dramatically during recovery of bottom DO in Harima-Nada, Japan. Similarly, Powers et al. (2001) found heavy recruitment of P. pinnata after hypoxia in the Gulf of Mexico, followed by two nereid polychaetes and S. tentaculata. The polychaete, P. pinnata, was the first species to occur after DO recovered at station 1 (Fig. 7). We concluded that recovery of this species was due not to larval settlement but movement of adults. This contrasts with findings of Powers et al. (2001), but they did not report the size of P. pinnata found in posthypoxia samples. In conclusion, macrobenthic dynamics and community structure were strongly influenced by summer hypoxia in Chinhae and Youngsan estuarine Bay. In particular, severe hypoxia caused mass mortality of benthic animals with recolonization of defaunated areas delayed by 1–4 months after the return of normoxic conditions. To what degree annual hypoxia has altered trophic transfer within these systems has yet to be determined. Acknowledgements Special thanks are given to Mr. J.G. Lim and students in the Benthic Ecology Laboratory in Mokpo National University for their support in field and laboratory studies, including sorting animals and drawing figures. This work was supported by the Mokpo National University. We also wish to thank Dr. J. Pearce and other anonymous reviewers for their constructive criticism of earlier drafts of this manuscript. References Boesch, D.F., 1977. A new look at the zonation of benthos along the estuarine gradient. In: Coull, B.C. (Ed.), Ecology of Marine Benthos. University of South Carolina Press, Columbia, pp. 245–266. Boesch, D.F., Rabalais, N.N., 1991. Effects of hypoxia on continental shelf benthos: comparisons between the New York Bight and the Northern Gulf of Mexico. In: Tyson, R.V., Pearson, T.H. (Eds.), Modern and Ancient Continental Shelf Anoxia, No. 58. Geological Society Special Publication, London, pp. 27–34. Cho, C.H., 1991. Mariculture and eutrophication in Jinhae Bay, Korea. Marine Pollution Bulletin 23, 275–279.
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Cloern, J.E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology and Progress Series 210, 223–253. Degobbis, D., 1989. Increased eutrophication of the Northern Adriatic Sea: second act. Marine Pollution Bulletin 20, 452–457. Diaz, R.J., 2001. Overview of hypoxia around the world. Journal of Environmental Quality 30 (2), 275–281. Diaz, R.J., Rosenberg, R., 1995. Marine benthic hypoxia—review of ecological effects and behavioural responses on macrofauna. Oceanography and Marine Biology: an Annual Review 33, 245– 303. Diaz, R.J., Nestlerode, J., Diaz, M.L., 2004. A global perspective on the effects of eutrophication and hypoxia on aquatic biota. In: Proceedings of the 7th International Symposium on Fish Physiology, Toxicology, and Water Quality, pp. 1–33. Gray, J.S., Wu, R.S., Or, Y.Y., 2002. Effects of hypoxia and organic enrichment on the coastal marine environment. Marine Ecology Progress Series 238, 249–279. Harper, D.E., McKinney, L.D., Salzer, R.R., Case, R.J., 1981. The occurrence of hypoxic bottom water off the upper Texas coast and its effects on the benthic biota. Contributions in Marine Science 24, 53– 79. Hayashi, I., 1991. Recent progress in polychaeta ecology-2. Distribution (1). Aquabiology 13, 366–369. Hong, J.S., 1987. Summer oxygen deficiency and benthic biomass in the Chinhae Bay system, Korea. The Journal of the Oceanological Society of Korea 22, 246–256. Jeng, W.L., Han, B.C., 1996. Coprostanol in a sediment core from the anoxic Tan-Shui Estuary, Taiwan. Estuarine, Coastal and Shelf Science 42, 727–735. Karim, M.R., Masahiko, S., Masao, U., 2002. Simulation of eutrophication and associated occurrence of hypoxic and anoxic condition in a coastal bay in Japan. Marine Pollution Bulletin 45, 280–285. Kim, H.G., 1990. Characteristics of flagellate red tide and environmental conditions in Masan Bay. Bulletin of National Fisheries Research and Development Agency 43, 1–40. Kim, J.M., Han, S.J., Lee, J.W., 1976. Environmental studies on Masan Bay 1. Physical factors and chemical contents. The Journal of the Oceanological Society of Korea 11, 25–33. Kweon, S.W., 1979. Studies on the distribution of dissolved oxygen on Jinhae Bay in Summer. Bulletin of National Fisheries Research and Development Agency 22, 7–20. Lim, H.S., 1993. Ecology of macrozoobenthos in Chinhae Bay of Korea. Ph.D. Thesis, National Fisheries University of Pusan, 311pp. Lim, H.S., Park, K.Y., 1999. Community structure of the macrobenthos in the soft bottom of Youngsan River estuary, Korea. 2. The occurrence of summer hypoxia and benthic community. Journal of the Korean Fisheries Society 31, 343–352. Mangum, C., van Winkle, W., 1973. Responses of aquatic invertebrates to declining oxygen tensions. American Zoologist 13, 529–541. Park, Y.J., 1987. Ecological survey on the marine environments in Yeongsan River estuary before and after the enclosure of a dam. M.S. Thesis, Chosun University, 68pp. Park, H.S., Lim, H.S., Hong, J.S., 2000. Spatio- and temporal patterns of benthic environment and macrobenthos community on subtidal softbottom in Chonsu Bay, Korea. Journal of the Korean Fisheries Society 33, 262–271. 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. Powers, S.P., Harper, D.E., Rabalais, N.N., 2001. Effect of hypoxia/ anoxia on the supply and settlement of benthic invertebrate larvae. In: Rabalais, N.N., Turner, R.E. (Eds.), Coastal Hypoxia: Consequences for Living Resources and Ecosystems, Coastal and Estuarine Studies, Vol. 58, pp. 211–240. Rosenberg, R., Loo, L.D., 1988. Marine eutrophication induced oxygen deficiency: effects on soft bottom fauna, western Sweden. Ophelia 29, 213–225.
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Santos, S.L., Simon, J.L., 1980. Marine soft-bottom community establishment following annual defaunation: larval or adult recruitment? Marine Ecology Progress Series 2, 235–241. Sanukida, S., Okamoto, H., Hitomi, M., 1981. On the behavior of the indicator species of marine bottom pollution. Bulletin of the Japanese Society of Scientific Fisheries 47, 863–869. Shin, H.C., 1995. Benthic polychaetous community in Kamak Bay, southern coast of Korea. Journal of the Korean Society of Oceanography 30, 250–261. Tamai, K., 1993. Tolerance of Theora fragilis (Bivalvia: Semelidae) to low concentrations of dissolved oxygen. Nippon Suisan Gakkaishi 59, 615–620. Wilson, D.P., 1952. The influence of the nature of the substratum on the metamorphosis of the larvae of marine animals, especially the larvae of Ophelia bicornis Savigny. Annals l’Institute Oc’eanographique (Nouvelle Serie) 27, 49–156.
Wu, R.S.S., 1982. Periodic defaunation and recovery in a subtropical epibenthic community, in relation to organic pollution. Journal of Experimental Marine Biology and Ecology 64, 253–269. Yang, D.B., Hong, J.S., 1988. On the biogeochemical characteristics of surface sediments in Chinhae Bay in September 1983. Bulletin of the Korean Fisheries Society 21, 195–205. Yang, D.B., Lee, K.W., 1983. Vertical distributions and diurnal variations of dissolved nutrients and chlorophyll a in Masan Bay. Bulletin of KORDI 5, 9–13. Zarkanellas, A.J., 1979. The effects of pollution induced oxygen deficiency on the benthos in Elefsis Bay, Greece. Marine Environmental Research 2, 191–207. Zimmerman, A.R., Canuel, E.A., 2000. A geochemical record of eutrophication and anoxia in Chesapeake Bay sediments: anthropogenic influence on organic matter composition. Marine Chemistry 69, 117– 137.
Hypoxia and benthic community recovery in Korean coastal waters Hyun-Sig Lim b
a,*
, Robert J. Diaz b, Jae-Sang Hong c, Linda C. Schaffner
b
a Department of Marine Resources, Mokpo National University, Muan, Chonnam 534-729, Republic of Korea Virginia Institute of Marine Science, College of William and Mary, 1208 Greate Road, Gloucester Point, VA 23062, USA c Department of Oceanography, Inha University, Incheon 402-751, Republic of Korea
Abstract Low dissolved oxygen (hypoxia and/or anoxia) has become a major cause of change to the benthic component of ecosystems around the world. We present the response of a benthic community to hypoxia in organically enriched environments in Korean coastal waters. Disturbances due to low dissolved oxygen (DO), and organic enrichment altered community dynamics, result in defaunation during summer hypoxia with delayed recolonization occurring in winter. As DO decreased, the number of taxa, their abundance and biomass of macrofauna dropped significantly at inner bay stations in Chinhae Bay and Youngsan River estuarine bay affected by hypoxia. With the return of normoxic conditions in Chinhae Bay, recolonization was initiated by opportunistic species, with a 1–4 months lag. The polychaetes, Sigambra tentaculata, Mesochaetopterus sp., and Lumbrineris longifolia, were most persistent under hypoxia. The first recolonizers were the polychaetes Paraprionospio pinnata, S. tantaculata, Glycinde gurjanovae and Nectoneanthes multignatha and the bivalve Theora fragilis. The second group of colonizers included the polychaetes Capitella capitata, Mesochaetopterus sp. and L. longifolia, and the bivalve Raetellops pulchella. Hypoxic and near anoxic conditions resulted in mass mortality in Chinhae Bay and Youngsan River estuarine bay, but communities did partially recover after return to normoxic conditions despite delayed recolonization. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Hypoxia; Korea; Recruitment; Benthic recovery; Opportunistic species
1. Introduction Hypoxia is worldwide in coastal areas, and has been recorded in over 140 locations from enclosed bays and estuaries to open seas (Diaz et al., 2004). Systems affected by hypoxia have increased over the last 40–50 years and are strongly associated with expanded eutrophication from industrialization and urbanization (Cloern, 2001; Diaz, 2001; Gray et al., 2002). Of the many environmental variables affecting benthic community structure, dissolved oxygen in bottom waters is most critical in structuring benthic communities (Diaz and Rosenberg, 1995; Gray et al., 2002).
*
Corresponding author. Tel.: +82 61 450 2392; fax: +82 61 452 8875. E-mail address: [email protected] (H.-S. Lim).
0025-326X/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2006.05.013
In Asia, hypoxia has been reported from Korea, China, Taiwan and Japan (Wu, 1982; Hong, 1987; Jeng and Han, 1996; Karim et al., 2002). In Korean coastal areas, hypoxia and associated red tides have been linked to catastrophic mortality of marine life (Cho, 1991; Kim, 1990). Mortality in Chinhae Bay (Hong, 1987) and the Youngsan River estuarine bay (Lim and Park, 1999) were associated with a one-time summer event, while in Chonsu Bay (Park et al., 2000) and Kamak Bay (Shin, 1995) hypoxia was mentioned as a cause of mortality but without supporting evidence. Unfortunately, the annual development and duration of hypoxia, along with benthic defaunation and recovery, have not been monitored in Korean coastal waters. We provide here a general overview of hypoxia in Korean coastal waters and the response of benthic communities, including complete defaunation due to summer hypoxia/anoxia and winter recolonization.
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2. Characteristics of the study area 2.1. Youngsan River estuarine bay The Youngsan River estuarine bay is located along the southwestern part of the Korean Peninsula and connects to the sea through the narrow Mokpogu water channel (Fig. 1). In this area, two dikes have been constructed: Youngsan dike in 1984, Kumho dike in 1994, to provide a
water supply for irrigating farm land, as well as industrial and municipal services. Prior to dike construction, the Youngsan River estuarine bay was a typical estuarine ecosystem, where seawater was diluted with freshwater from land drainage. The construction of both dikes altered the characteristics of this estuary, with a reduction in water circulation and increased deposition of organic matter and fine sediments near the dikes in the inner part of the estuary (Park, 1987).
Fig. 1. Location of sampling stations and bathymetry of Chinhae Bay and Youngsan River estuarine bay on the southern coast of Korea.
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2.2. Chinhae Bay Chinhae Bay, a semi-enclosed embayment located in the southern part of the Korean Peninsula (Fig. 1), is a spawning and nursery grounds for many commercially important finfishes. It also supported high shellfish production, e.g., intensive long-line cultures of oysters (Crassostrea gigas) and mussels (Mytilus edulis), as well as bottom culture of the arkshell (Scapharca broughtonii). About 7.5% of the total Chinhae Bay area was used for aquaculture. These industries have declined due to environmental stress from organic pollution and hypoxia. Domestic, industrial, and agricultural wastes from adjacent cities and industrial activities have contaminated Chinhae Bay since the early 1970’s; red tide blooms due to dinoflagellates and consequent hypoxia have become annual events (Kim, 1990). Hypoxia now extends over most of the bay, seasonally covering about 54% of the total 497 km2 (Hong, 1987).
Fig. 2. Spatial distribution pattern of bottom dissolved oxygen in Youngsan River estuarine bay, August 1995.
3. Materials and methods 3.1. Youngsan River estuarine bay Triplicate van Veen grab (0.1 m2) samples were collected at 40 subtidal, soft bottom sediment stations in May, August, October 1995 and February 1996 (Fig. 1). Sediments were sieved using 1-mm mesh sieves and ambient seawater and preserved with 10% neutralized formalin solution. Macrofauna were sorted from the sieve. Wet weight biomass was measured for major taxonomic groups (e.g., polychaetes, molluscs, etc.), and all macrofauna enumerated and identified to the lowest possible taxonomic level. Water temperature, salinity, and dissolved oxygen (DO) concentration in the surface and bottom water layers were measured at each station using a SCT meter (YSI-32) and DO meter (YSI-58).
was 0.8–10.2 mg/l in summer. In contrast, hypoxia has not been observed near the recently constructed Kumho dike.
4. Result
4.1.2. Chinhae Bay Hypoxia first developed in innermost areas of the Bay by May, when DO was 1.7 mg/l at station 1 (Fig. 3). By June, hypoxic areas extended out into the bay proper, with the Masan area recording 0.9 mg/l (17.9% of saturation) and 0.3 mg/l (5.5%) at stations 1 and 2, respectively (Fig. 3). The DO continued to decline in July with <0.2 mg/l (3.3% of air saturation) at station 1, 0.2 mg/l (4.0%) at station 2, 1.2 mg/l (22.9%) at station 11, and 0.7 mg/l (12.7%) at station 12. By August, DO concentrations reached their lowest levels, with 0.01 mg/l (0.2%), 0.07 mg/l (1.3%) and 0.6 mg/l (11.7%) at stations 1, 2 and 12, respectively. Central bay low DO levels remained throughout September. In October, DO concentrations in bottom waters recovered to more normal levels (>4.0 mg/l) over the entire area of the bay; higher levels of DO remained until February of the following year. Differences in DO concentration in surface and bottom waters then appeared by March, with the onset of hypoxia in bottom water again by May, with DO at station 1 in the inner most area of the bay being 0.7 mg/l (11.3% of saturation); this suggests that hypoxia in Chinhae Bay is an annual phenomenon associated with the development of a thermocline.
4.1. Hypoxia areas
4.2. Impact of hypoxia on benthos
4.1.1. Youngsan River estuarine bay Hypoxia (<2.0 mg/l) in Youngsan estuary developed first near the Youngsan dike in summer due to stratification of the water column (Fig. 2). In surface waters, DO concentrations were 5.1–11.2 mg/l, whereas bottom DO
4.2.1. Youngsan River estuarine bay In summer, August 1995, maximum numbers of taxa were recorded near Kumho dike (33 taxa at station 32) as not affected by hypoxia, whereas minimum numbers were from station 1 (nine taxa) stressed by hypoxia and
3.2. Chinhae Bay Five replicate van Veen grab (0.1 m2) samples were collected monthly at each of 12 stations, May 1989 to May 1990 (Fig. 1). The processing of grab samples was the same as for the Youngsan estuary. Water temperature, salinity and dissolved oxygen were measured simultaneously during sediment sampling using a T-S bridge (Type MC 5) and DO meter (Yellow Springs Instrument). Measurements were made 50 cm from sea bottom.
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Fig. 3. Monthly distribution pattern of bottom dissolved oxygen in Chinhae Bay from June 1989 to May 1990.
high organic content of the sediments (Fig. 4). Species numbers were lower at inner estuarine stations near the dike (<25 taxa), higher in the outer part of the estuary (>30 taxa). Low species richness in the inner estuarine bay, near the dike, was positively correlated (P < 0.001) with DO. Similarly, low densities of macrobenthic organisms with <300 ind m 2 were also observed in the area stressed by hypoxia in the inner bay. In contrast, >1000 ind m 2 of macrobenthos were observed in normoxic areas between Mokpo harbor and Youngsan dike. There was significant positive correlation between abundance and DO in the bottom water (P < 0.001). Low biomass of the macrobenthos (1.28 g wet wt m 2 at station 1) was observed near the dike, where the lowest number
of species and abundance were also recorded. Biomass was positively correlated to summer bottom dissolved oxygen (P < 0.05). These results suggested that the spatial distribution of the macrobenthos in Youngsan estuarine bay in summer season was severely influenced by summer dissolved oxygen due to reduced water circulation after dike construction. Variations in number of taxa, abundance and biomass along the hypoxic gradient was closely linked to DO concentration (Fig. 5). The number of taxa was lower at stations 1 and 10, most stressed by hypoxia, whereas it increased continuously toward the normoxic outer area. In contrast, a greater abundance of macrobenthos was observed at station 17 that was transitional between hyp-
Fig. 4. Spatial distribution of macrobenthic fauna (number of taxa, abundance and biomass) in Youngsan River estuarine bay.
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oxic and normoxic areas, with a DO of 2.9 mg/l. The deposit-feeding bivalve Theora fragilis, tolerant of low DO (Tamai, 1993), was abundant at this station. Low total abundance was found at inner stations stressed by hypoxia and also at outer normoxic stations. Greatest biomass was observed at station 30 (outer part of the bay), lowest at station 1. The proportion of polychaete species was greater in areas with hypoxia, lower in normoxic areas. The opposite was found for proportions of molluscs and crustaceans.
Dissolved oxygen (mg/I)
4.2.2. Chinhae Bay The macrobenthos were severely affected by bottom hypoxia in Chinhae Bay, with stations 1 and 2 most affected (Fig. 6). Species richness at station 1 and 2 decreased with time, as hypoxia progressed, and by August these stations were found to be azoic. With the return of normoxic conditions, recruitment occurred and species richness increased gradually from February until April when it started to decrease again. Similarly, abundance, biomass, and species diversity showed the same trend as species richness with a progression of hypoxia. Opposite 10.0 8.0 6.0 4.0 2.0 0.0 1
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trends in species richness, abundance, and biomass were observed at stations 3 and 4 over the summer season. At station 1, the development of hypoxia from May to September 1989 led to mass mortality of macrobenthos with complete defaunation by August, when the lowest DO was recorded. While bottom water DO at station 1 had been reoxygenated to >4.0 mg/l by October, azoic conditions persisted until December 1989, when a few individuals of seven taxa recolonized. By January 1990, however, azoic conditions returned and it was not until February that colonizing taxa persisted. Strong recruitment lagged the return of normoxia by some 4 months. Subsequently, bottom water DO began to decrease again by April 1990 when the abundance of macrobenthos was highest for station 1. By May, the abundance of macrobenthos declined, coincidental with DO declining to <2.0 mg/l. There were six species recorded in May, reduced to two species by July; azoic conditions lasted until January. However, recruitment increased the number of taxa to 23 by February. At station 2, hypoxia developed by June, 1 month later than at station 1, causing mass mortality and continuing until September, with azoic conditions for 4 months, August–November. Although bottom dissolved oxygen at station 2 had recovered by October, the benthos did not recolonize until December 1989 when eighteen taxa recolonized following a 2 months lag in recolonization after recovery of bottom DO. In contrast, stations 3 and 4, influenced by water exchange with the open sea, did not experience hypoxia, but DO decreased in summer to 3.7–3.9 mg/l (Fig. 6). Maximum abundances of macrobenthos was found during the summer season. 4.3. Dynamics of benthos in Chinhae Bay
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Fig. 5. Spatial distributions of the number of taxa, abundance and biomass of macrobenthos and community structure parameters along the gradient of bottom dissolved oxygen in Youngsan River estuarine bay.
In Chinhae Bay the dynamic fluctuations in abundance of benthos were related to DO concentration (Fig. 7). By June both stations 1 and 2 were severely hypoxic (<1 mg/ l) and total abundance was declining. Severe hypoxia persisted through September, with normoxic conditions returning by October. However, both stations remained depauperate from August to November, with recruitment beginning by December (Fig. 7). Three polychaetes, Sigambra tentaculata, Mesochaetopterus sp., and Lumbrineris longifolia were most persistent under conditions of hypoxia at stations 1 and 2 (Fig. 7). Individuals of these species survived 2–3 months of hypoxia (May, June, and July) disappearing by August, when DO reached near anoxia at station 1 (0.01 mg/l) and station 2 (0.07 mg/l). Seven taxa appeared sparsely as recruits at station 1 in December, but did not persist. These were a mix of opportunists (Paraprionospio spp., Paraprionospio pinnata, T. fragilis) and equilibrium species (Ophiura kinbergi and its commensal Ophiodromus pugettensis). Species of unknown life-history status were Nectoneanthes multignatha and Hesiospina similis. It was not until February, 5 months after the renewal of bottom water DO, that the community recovered at station
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Fig. 6. Monthly variation of the environmental and community structure parameters in Chinhae Bay. Arrow indicates azoic month during the study period. Dotted line in the dissolved oxygen indicates hypoxia (<2 mg/l).
1, with strong recruitment by the polychaetes, P. pinnata and N. multignatha, and the bivalve, T. fragilis. At station 2, with similar DO concentrations as station 1, recruitment started in December, the first recruits being P. pinnata, T. fragilis, N. multignatha, S. tentaculata, H. similes and O. kinbergi. Subsequently, additional species, i.e. Capitella capitata, Glycinde gurjanovae, L. longifolia, S. tentaculata, Mesochaetopterus sp., and Raetellops pulchella, colonized station 1, and L. longifolia and G. gurjanovae station 2 (Fig. 7). Most of these are known as opportunists and have been associated with low DO (Diaz and Rosenberg, 1995; Gray et al., 2002). In contrast, there was no defaunation at stations 3 and 4, where lowest DO concentrations were 3.3 mg/l in August, 3.6 mg/l in July, respectively (Figs. 6 and 7). During the summer when abundance, biomass, and number of
taxa at stations 1 and 2 were declining, those at stations 3 and 4 either remained unchanged or increased. Species eliminated from stations 1 and 2 during hypoxia persisted at these stations (Fig. 7). By winter, recruitment reached a peak at stations 1 and 2 with populations of P. pinnata and N. multignatha greater than those at stations 3 and 4. Mesochaetopterus sp., L. longifolia, and C. setosa recruitment at stations 1 and 2 did not reach levels of population similar to those at stations 3 and 4. Species that recruited to similar densities at the four stations included T. fragilis, S. tentaculata, R. pulchella, and G. gurjanovae (Fig. 7). 5. Discussion Hypoxia in Korean coastal waters occurred during summer season when the water column was thermally strati-
H.-S. Lim et al. / Marine Pollution Bulletin 52 (2006) 1517–1526 100
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fied; this lead to severe effects on benthic community structure (Table 1). Detrimental effects of hypoxia (DO of <2 mg/l) on benthic communities were reported earlier from Chinhae Bay (Hong, 1987; Lim, 1993) and Youngsan River estuarine area (Lim and Park, 1999), (Fig. 1). In addition, summer hypoxia may develop in Kamak Bay (Shin, 1995) and Chonsu Bay (Park et al., 2000). Hypoxia has been reported as a worldwide phenomenon in temperate regions, with principal causal factors including: stratification of the water column (due to temperature or salinity); reduced vertical mixing; and isolation of bottom waters from oxygenation. Respiration of bottom dwelling organisms and decomposition of organic matter further lowers DO to critical levels and can lead to anoxic conditions where stratification persists. Nutrient and/or organic loading related to urbanization and industrializa-
tion have exacerbated hypoxia in estuarine and marine systems throughout the world (Gray et al., 2002; Diaz, 2001). Low DO in Korean coastal waters was first recorded in Chinhae bay in the mid-1970s. Levels of DO less than 2.0 mg/l were measured in Masan Bay, near station 1 in the present study, in September 1974 (Kim et al., 1976), September 1975 (Kweon, 1979), and May 1982 (Yang and Lee, 1983). Cho (1991) reported reduced levels of oxygen (saturation of 30–80%) at depths between 5 and 10 m in northern and western parts of Chinhae Bay in July 1977, with near anoxic conditions (<5% saturation) below ten meters depth during a Gonyaulax spp. red tide outbreak lasting for 1 week. Yang and Hong (1988) also reported that bottom DO in Chinhae Bay ranged from 0.1 to 4.5 mg/l, with lowest values in Masan Bay. Kim (1990) reported that since 1985 hypoxia in Chinhae Bay has
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Table 1 Summary of benthic effects for hypoxic systems in Korean coastal waters System
Hypoxia typea
Hypoxia levelb
Hypoxic area (km2)c
Time trends
Fauna responsed
Fauna recoverye
Fisheries response
Chonsu Bay Kamak Bay Youngsan Estuary Chinhae Bay
Seasonal Seasonal Seasonal Periodic
Moderate Moderate Moderate Severe
– –
Gradually Gradually Gradually Gradually
Mortality Mortality Mass mortality Mass mortality
Slow Slow Some Some
Reduced Reduced Reduced Reduced
2.8 (11%) 184.5 (46%)
increasing increasing increasing increasing
a
Seasonal, yearly events related to summer or autumnal stratification; periodic, events occurring at regular intervals shorter than a year. Moderate, oxygen decline to about 0.8 mg/l; Severe, decline to near anoxic levels. c Parentheses indicates percentage of whole surface area. d Mortality, moderate reductions of populations, many species survive; mass mortality, drastic reduction or elimination of the benthos. e Slow, gradual return of community structure taking more than a year; Some, recolonization occurs but community does not return to prehypoxic structure. b
of benthic organisms in the inner part of the bay in summer season. In the present study, low number of taxa, abundance, and biomass in Youngsan estuarine bay were observed during summer hypoxia, and defaunation was observed in Chinhae Bay. In Chinhae Bay, there was a 1–4 month time-lag between return of normoxia and recolonization of the benthos. The above results were based on the use of 1-mm mesh; if smaller mesh (e.g., 0.5 mm or less) was used, results would change. The 1-mm mesh screening is typical for Asian studies (Hayashi, 1991; Lim, 1993; Shin, 1995). Polychaetes are generally known to be more tolerant of hypoxia than other taxonomic groups (crustaceans) (Mangum and van Winkle, 1973). Harper et al. (1981) pointed out that amphipod and echinoderms are more severely affected by hypoxic stresses than polychaetes. Similar findings have been reported from other hypoxic events (see Diaz and Rosenberg, 1995; Gray et al., 2002). In our study, initially colonizing species following hypoxia were P. pinnata, N. multignatha and T. fragilis at station 1, P. pinnata, S. tentaculata and G. gurjanovae at station 2. Of these, P. pinnata and T. fragilis are known as broadly distributed opportunistic species tolerant of low DO (Boesch and Rabalais, 1991; Tamai, 1993). Under hypoxic conditions larvae of P. pinnata are also known to delay settlement and remain in the water column until DO increased to >2.8 mg/l (Powers et al., 2001). The ability of larvae to delay settlement and select when and where to settle would reduce postsettlement mortality (Wilson, 1952). S. tentaculata is also broadly distributed and was the third most abundant species to recolonize following hypoxia in the Gulf of Mexico (Powers et al., 2001). The ecological characteristics of G. gurjanovae and N. multignatha relative to low DO are unknown.
become an annual development in June. Fluctuations in DO are controlled by temperature, and to a lesser extent salinity, and driven by stratification. Bottom water hypoxia in Chinhae Bay first develops at inner bay areas in May, when water temperature begins to increase, and covers the widest area by September. A return to normoxic condition usually occurs by October (Table 2). The progression from aperiodic occurrence of hypoxia to predictable annual summer hypoxia that disappears in Autumn is typical of many anthropogenically oxygen stressed systems (Diaz and Rosenberg, 1995) and is related to increased organic matter reaching the bottom (Gray et al., 2002). Systems stressed by the development of annual summer hypoxia characteristically have elevated levels of organic material in surface sediments, which accelerates the reduction of DO (Degobbis, 1989; Rosenberg and Loo, 1988; Zimmerman and Canuel, 2000). Sedimentation of dead plankton and debris accelerates uptakes of dissolved oxygen via microbial activity. Similarly, the decomposition of dead macrobenthos would likely lead to even more severe DO condition. Rosenberg and Loo (1988) emphasized marine eutrophication as due to input of nutrients which induced oxygen deficiency and consequent effects on soft bottom fauna in west Sweden. In Korean waters, bottom water hypoxia resulted in an annual mass mortality of benthos and altered community structure, a response typical of systems experiencing annual hypoxia. Diaz et al. (2004) found that 54% (74 of 142) of hypoxic systems around the world were subjected to annual hypoxia with 39% of them reporting annual mass mortality of benthos. Of this 39%, annual recolonization following the dissipation of hypoxia occurred in 65% of the systems. Zarkanellas (1979) reported that hypoxia in Elefsis Bay controlled the species richness and abundance
Table 2 Monthly variations of the hypoxic area (km2) in Chinhae Bay from June 1989 to May 1990 and Youngsan estuarine bay in August, 1995 DO (mg/l)
Chinhae Bay June
July
August
September
October
November
December
January
February
March
April
May
62.0 2.0–4.0
105.9 109.0
134.0 172.5
142.0 63.0
184.5 42.0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
8.9 26.8
Youngsan estuarine bay 2.8 4.2
H.-S. Lim et al. / Marine Pollution Bulletin 52 (2006) 1517–1526
Recolonization of the benthos following depauperization due to hypoxia follows patterns for other forms of disturbance, i.e. the result of larval settlement and emigration of adults (Boesch, 1977; Pearson and Rosenberg, 1978; Harper et al., 1981; Powers et al., 2001). Differences in these responses vary taxonomically. Santos and Simon (1980) suggested that adult emigration by crustaceans and larval settlement by polychaetes were paramount in recolonization following hypoxia. In this study, the occurrence of young T. fragilis and adult polychaetes were observed at station 1, suggesting emigration of adult in polychaetes, larval settlement in bivalves. Sanukida et al. (1981) reported that the abundance of P. pinnata was high in spring (before the development of hypoxia), decreasing gradually with reduced oxygen content. He also noted that abundance of P. pinnata increased dramatically during recovery of bottom DO in Harima-Nada, Japan. Similarly, Powers et al. (2001) found heavy recruitment of P. pinnata after hypoxia in the Gulf of Mexico, followed by two nereid polychaetes and S. tentaculata. The polychaete, P. pinnata, was the first species to occur after DO recovered at station 1 (Fig. 7). We concluded that recovery of this species was due not to larval settlement but movement of adults. This contrasts with findings of Powers et al. (2001), but they did not report the size of P. pinnata found in posthypoxia samples. In conclusion, macrobenthic dynamics and community structure were strongly influenced by summer hypoxia in Chinhae and Youngsan estuarine Bay. In particular, severe hypoxia caused mass mortality of benthic animals with recolonization of defaunated areas delayed by 1–4 months after the return of normoxic conditions. To what degree annual hypoxia has altered trophic transfer within these systems has yet to be determined. Acknowledgements Special thanks are given to Mr. J.G. Lim and students in the Benthic Ecology Laboratory in Mokpo National University for their support in field and laboratory studies, including sorting animals and drawing figures. This work was supported by the Mokpo National University. We also wish to thank Dr. J. Pearce and other anonymous reviewers for their constructive criticism of earlier drafts of this manuscript. References Boesch, D.F., 1977. A new look at the zonation of benthos along the estuarine gradient. In: Coull, B.C. (Ed.), Ecology of Marine Benthos. University of South Carolina Press, Columbia, pp. 245–266. Boesch, D.F., Rabalais, N.N., 1991. Effects of hypoxia on continental shelf benthos: comparisons between the New York Bight and the Northern Gulf of Mexico. In: Tyson, R.V., Pearson, T.H. (Eds.), Modern and Ancient Continental Shelf Anoxia, No. 58. Geological Society Special Publication, London, pp. 27–34. Cho, C.H., 1991. Mariculture and eutrophication in Jinhae Bay, Korea. Marine Pollution Bulletin 23, 275–279.
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