Estuaries and Coasts

, Volume 32, Issue 6, pp 1225–1233

Dinoflagellate Cysts in Coastal Sediments as Indicators of Eutrophication: A Case of Gwangyang Bay, South Sea of Korea

Authors

    • Environmental Science Laboratory, South Sea InstituteKorea Ocean Research and Development Institute
  • Chang-Ho Moon
    • Department of OceanographyPukyong National University
  • Hyun-Jin Cho
    • Pollution Response DepartmentMokpo Coast Guard
  • Dhong-Il Lim
    • Environmental Science Laboratory, South Sea InstituteKorea Ocean Research and Development Institute
Note

DOI: 10.1007/s12237-009-9212-6

Cite this article as:
Kim, S., Moon, C., Cho, H. et al. Estuaries and Coasts (2009) 32: 1225. doi:10.1007/s12237-009-9212-6

Abstract

Diatom densities in the surface water and dinoflagellate cysts in bottom sediments of Gwangyang Bay were studied to determine changes in the phytoplankton community structure in response to anthropogenic eutrophication and to assess the use of dinoflagellate cysts as indicators of coastal eutrophication. Our results show that, in nutrient-enriched environments, diatoms are particularly benefited from the nutrients supplied and, as a consequence, heterotrophic dinoflagellates that feed on the diatoms can be more abundant than autotrophic dinoflagellates. In short-core sediment records, a marked shift in autotrophic–heterotrophic dinoflagellate cyst compositions occurred at a depth of approximately 9–10 cm corresponding to the timing of the 1970s industrialization around Gwangyang Bay. This tentatively indicates that diatom and dinoflagellate communities here have undergone a considerable change mainly due to increased nutrient loadings from both domestic sewage effluent and industrial pollution. Our study suggests a possible potential use of dinoflagellate cysts in providing retrospective information on the long-term effects of coastal eutrophication.

Keywords

EutrophicationDinoflagellate cystsDiatomsCoastal zoneGwangyang Bay sediments

Introduction

Population growth and related human activities have severely increased nutrient inputs to streams and estuaries which commonly lead to an increase in the rate of organic matter supplies to a coastal ecosystem over natural levels. The oversupplied organic matters and nutrient inputs can produce a wide range of negative effects, including eutrophication and other deleterious effects such as phytoplankton blooms, degradation of habitat, and decreased fishery production (Conley et al. 1993; Boynton et al. 1995). Of particular concern are long-term effects of eutrophication on coastal environments as a main cause for increased water-column oxygen demand and subsequent hypoxia on continental shelves (Diaz 2001; Colman and Bratton 2003). In northern temperate aquatic ecosystems, accumulation rates of biogenic silica in sediments have been used as an index of diatom productivity for tracing long-term trends in nutrients and eutrophication (Conley et al. 1993). However, complicated relationships between biogenic silica and diatom productivity (e.g., dissolution problem, terrestrial sources of biogenic silica, and recycling effects) have been recognized especially in the nutrient-overenriched condition (Malone et al. 1996; Colman and Bratton 2003).

Dinoflagellates, one of the major phytoplankton groups, are present in both freshwater and marine systems where they often account for substantial amounts of the planktonic biomass. Approximately 10% of the around 2,000 marine species of dinoflagellates produce cysts, most of which appear to serve as a benthic resting stage. In many species, their cell wall is composed of heavy, complex organic molecules, similar to the sporopollenin of plant pollen grains which are extremely resistant to physical, chemical, and biological breakdown (Wall et al. 1977; Taylor 1987). Therefore, dinoflagellate cysts in sediments have been suggested as useful indicators for obtaining integrated records of the planktonic population, over time and space, on a scale usually not attained by conventional plankton surveys. In several studies, dinoflagellate cysts in coastal sediments have been used as indicator species in order to trace eutrophication processes (Wall et al. 1977; Dale and Fjellså 1994; Matsuoka 1999; Dale 2009).

Located in the southern coastal area of Korea (Fig. 1), Gwangyang Bay is one of the most industrial-polluted coastal areas of Korea. It is connected with the open sea by the 4-km-wide Yeosu Channel to the south and with Seomjin River to the north which annually discharges 10.7–39.3 × 108 tons of fresh water. Water depth of the bay is generally shallow, less than 5 m, except for two tidal channels which are more than 20 m (Hydrographic Office of Korea 1986). Gwangyang Bay is one of the most quickly developed coastal areas in Korea where the main estuarine delta and tidal flats along the bay were heavily reclaimed to establish diverse industrial facilities since the 1970s. As a consequence, various aquatic habitats around the Seomjin River estuary and the shallow water embayment in the bay have been severely damaged by industrial pollutants and are becoming notorious for eutrophication and frequent red tides due to discharge of industrial and sewage effluents (Lee and Yoo 1991). Gwangyang Bay is a semienclosed basin where dinoflagellate cysts are expected to be locally produced with minimum influence by long-distance transport and, therefore, is well suited for studies on the effects of coastal eutrophication on phytoplankton assemblages. The purpose of this study is to assess the utility of dinoflagellate cysts as an indicator of coastal eutrophication and comparing them with diatoms in surface water and autotrophic–heterotrophic dinoflagellate cyst compositions in bottom sediments of Gwangyang Bay.
https://static-content.springer.com/image/art%3A10.1007%2Fs12237-009-9212-6/MediaObjects/12237_2009_9212_Fig1_HTML.gif
Fig. 1

Location map of the sampling stations in Gwangyang Bay, South Sea of Korea (open circles surface water and surface sediment samples, filled circles short-core samples)

Materials and Methods

Surface sediment samples for spatial distribution analysis of dinoflagellate cysts were collected from 20 sites in Gwangyang Bay (Fig. 1) by using a TFO gravity corer (University of Tokyo, Fisheries Oceanography Laboratory) in August 2001. To analyze vertical variation of dinoflagellate cysts in sediments, we additionally collected two short-core sediment samples from St.1 and St.14 with a gravity corer equipped with a 50-cm-long, 5-cm-diameter acrylic pipe. Along with sediment samples for dinoflagellate cyst analysis, surface seawater samples were also obtained from the 20 sites in order to examine the relationship between dinoflagellate cyst assemblages in bottom sediments and diatoms in surface water.

For the analysis of diatom abundances, 1 L of each surface seawater sample was fixed with 10 ml of Lugol's iodine solution. The fixed surface seawater samples were settled in sedimentation chambers for 48 h, and then the upper water was gently removed by a siphon. The residues were suspended in 10 ml distilled water, and a 0.1 ml aliquot was examined using a light microscope (Olympus CH-2) to identify and enumerate diatom assemblages.

For the analysis of the surface distribution of dinoflagellate cysts, the top 3 cm of each TFO sediment core was taken and processed following the methods of Cho and Matsuoka (2001). Each subsample was then treated with 10% hydrochloric acid and 47% hydrofluoric acid to dissolve calcium carbonate and silicate materials in order to attain a clear view during microscopic observation. After the chemical treatment, samples were sonicated for 30 s and sieved through 125- and 20-µm-pore-sized meshes. The residue on the 20-µm mesh was suspended in 10 ml distilled water, and a 1-ml aliquot from the volume was observed under an inverted microscope (AXIOVERT 200, Zeiss) at ×200 and ×400 magnification. The dinoflagellate cyst concentration in each sample was calculated as cysts per gram of dry sediment. To examine vertical variations of dinoflagellate cysts in Gwangyang Bay sediments, core sediments from St.1 and St.14 (27.5 and 30.5 cm long, respectively) were cut into 1 cm sections. Among the subsamples, seven subsamples from 0 to 1, 2 to 3, 4 to 5, 9 to 10, 14 to 15, 19 to 20, and 24 to 25 cm depth were selected from each core and processed with the chemical treatment (Cho and Matsuoka 2001).

Results and Discussion

A total of 66 diatom taxa belonging to 27 genera was observed in surface water samples of Gwangyang Bay. The diatom density ranged from approximately 160 (St.18) to 1,170 (St.6) cells per milliliter. The predominant diatom species was Chaetoceros curvisetus, followed by Chaetoceros debilis and Stephanopyxis turris. From the surface sediment samples, a total of 30 dinoflagellate cyst taxa belonging to 17 genera was identified (Table 1). These can be divided into six taxonomic groups: protoperidinioid (13 species), gonyaulacoid (11 species), diplopsalid (two species), gymnodinioid (two species), tuberculodinioid (one species), and calciodinellid (one species). The gonyaulacoid group (Alexandrium, Lingulodinium, Operculodinium, and Spiniferites genera) and the protoperidinioid group (Brigantedinium, Protoperidinium, Quinquecuspis, Selenopemphix, Stelladinium, Trinovantedinium, and Votadinium genera) made up approximately 44.9–79.8% and 13.5–44.1% of the total dinoflagellate cysts, respectively. The predominant species was S. bulloideus, followed by S. delicatus and Alexandrium (ellipsoid-type) cysts of the gonyaulacoid group and B. simplex of the protoperidinioid group. Autotrophic dinoflagellate cysts showed their highest concentration (approximately 1,800 cysts per gram) at St.11 in the most western side of the bay, while the highest concentration of heterotrophic species was observed at St.6 (approximately 760 cysts per gram) in the middle part of the bay (Fig. 2). In the short-core analysis, a total of 25 dinoflagellate cyst taxa belonging to 14 genera (St.1 core) and 23 dinoflagellate cyst taxa belonging to 14 genera (St.14 core) were observed (Tables 2 and 3). The total dinoflagellate cyst concentrations ranged from 283 (24–25 cm depth) to 776 (2–3 cm depth) cysts per gram in St.1 core and 134 (24–25 cm depth) to 613 (4–5 cm depth) cysts per gram in St.14 core. The most frequently observed dinoflagellate cyst group in both cores was the gonyaulacoid group (genera of Alexandrium, Lingulodinium, and Spiniferites) which represented approximately 41–67% (St.1 core) and approximately 55–88% (St.14 core) of the total dinoflagellate cysts, respectively. The second most dominant dinoflagellate cyst group was the protoperidinioid group (Brigantedinium, Protoperidinium, Quinquecuspis, Selenopemphix, Stelladinium, Trinovantedinium, and Votadinium genera) representing approximately 12–39% (St.1 core) and 7–20% (St.14 core) of the total dinoflagellate cysts. The predominant species in the St.1 core was S. bulloideus followed by Diplopsalis lenticula, S. hyperacanthus, and S. delicatus, while S. hyperacanthus was the predominant cyst in St.14 core, along with S. delicatus and S. bulloideus.
Table 1

Species composition, concentrations (cysts per gram), and relative abundances (percent) of dinoflagellate cysts in the surface sediments of Gwangyang Bay

Species/station

1

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

Autotrophs

                    

 Gonyaulacoid

                    

 Alexandrium sp. (ellipsoid)

87

124

30

25

32

125

151

69

 

14

55

149

40

10

22

82

33

48

148

149

 Lingulodinium machaerophorum

     

13

   

27

37

    

12

11

   

 Spiniferites bulloideus

79

68

22

81

53

335

211

14

 

27

545

116

145

10

64

221

97

96

89

89

 Spiniferites delicatus

15

12

15

 

53

100

151

258

348

54

91

167

 

57

22

36

109

208

134

89

 Spiniferites elongatus

         

14

          

 Spiniferites hyperacanthus

 

56

8

33

53

112

60

55

251

  

34

14

29

 

105

76

112

74

75

 Spiniferites membranaceus

      

15

  

14

   

57

54

12

44

48

15

15

 Spiniferites mirabilis

 

12

8

9

 

25

136

 

20

215

218

430

27

10

 

35

11

16

15

15

 Spiniferites ramosus

22

12

   

13

166

28

 

14

653

33

66

67

   

32

30

30

 Spiniferites spp.

 

34

  

11

38

 

14

20

108

146

84

93

38

 

12

65

96

45

60

 Operculodinium centrocarpum

    

11

   

39

   

27

  

12

11

16

30

30

 Calciodinellid

                    

 Scrippsiella trochoidea

 

12

   

25

75

  

14

55

 

79

  

12

22

16

  

 Gymnodinioid

                    

 Gymnodinium capitatum

8

    

25

 

14

 

14

19

33

14

  

35

22

32

  

 Tuberculodinioid

                    

 Tuberculodinium vancampoae

   

9

 

13

 

41

39

14

 

50

14

  

12

11

16

  

Autotrophs (%)

56

58

72

67

48

52

71

51

66

73

83

72

66

48

49

79

71

60

61

57

Heterotrophs

                    

 Protoperidinioid

                    

 Brigantedinium cariacoense

15

 

8

 

95

25

15

28

58

 

37

33

14

19

 

12

11

16

30

15

 Brigantedinium simplex

36

34

   

87

121

150

136

41

109

182

79

67

107

 

22

48

104

30

 Brigantedinium spp.

8

12

 

9

11

   

20

41

37

50

27

  

35

22

48

15

45

 Protoperidinium americanum

8

  

9

11

13

30

55

 

14

19

   

11

   

59

60

 Protoperidinium latissimum

     

13

60

 

20

 

19

33

    

11

   

 Quinquecuspis concretum

8

23

8

9

22

50

 

28

  

19

33

27

67

11

  

16

 

15

 Selenopemphix alticintum

   

9

 

25

 

14

20

        

32

15

 

 Selenopemphix quanta

 

12

 

9

11

38

90

28

 

54

 

33

40

19

 

47

44

64

15

15

 Stelladinium stellatum

 

34

8

9

11

75

 

14

 

27

 

50

40

19

  

11

16

30

30

 Trinovantedinium capitatum

 

34

  

11

38

15

14

20

 

19

 

14

  

24

11

16

74

75

 Trinovantedinium palidifluvum

                

11

16

  

 Votadinium calvum

15

34

  

11

75

15

14

39

 

37

17

14

29

 

24

33

48

15

15

 Votadinium spinosum

    

11

               

 Diplopsalid

                    

 Diplopsalis lenticula

29

35

8

 

11

224

15

55

     

48

32

  

128

 

104

 Dubridinium caperatum

15

   

11

  

14

58

 

73

  

10

11

 

11

16

15

15

 Gymnodinioid

                    

 Polykrikos kofoidii

29

24

 

25

11

100

30

69

 

14

  

14

29

 

12

22

32

  

Heterotrophs (%)

44

42

28

33

52

48

29

49

34

27

17

28

34

52

51

21

29

40

39

43

Total

374

572

115

236

440

1587

1356

976

1088

720

2188

1527

788

585

334

740

721

1232

952

971

https://static-content.springer.com/image/art%3A10.1007%2Fs12237-009-9212-6/MediaObjects/12237_2009_9212_Fig2_HTML.gif
Fig. 2

Spatial distribution of dinoflagellate cyst concentrations (cysts per gram) and diatom densities (×100 cells per liter): a total dinoflagellate cysts, b autotrophic dinoflagellate cysts, c heterotrophic dinoflagellate cysts, and d diatoms

Table 2

Species composition, concentrations (cysts per gram), and relative abundances (percent) of dinoflagellate cysts observed in the short-core St.1 collected from Gwangyang Bay

Species/depths (cm)

0–1

2–3

4–5

9–10

14–15

19–20

24–25

Autotrophs

       

 Gonyaulacoid

       

 Alexandrium

sp. 1 (ellipsoid)

 

9

 

8

   

sp. 2 (ovoid)

7

27

     

 Lingulodinium machaerophorum

 

19

    

7

 Spiniferites

bulloideus

72

111

242

85

112

82

56

delicatus

43

47

41

85

59

25

57

hyperacanthus

71

74

49

29

26

74

56

membranaceus

    

7

  

mirabilis

 

9

     

ramosus

15

19

 

8

13

  

spp.

36

10

25

15

14

  

 Calciodinellid

       

 Scrippsiella trochoidea

15

      

 Tuberculodinioid

       

 Tuberculodinium vancampoae

22

28

9

8

7

17

 

Subtotal

281

353

366

238

238

198

176

Autotrophs (%)

47

45

53

60

69

66

62

Heterotrophs

       

 Protoperidinioid

       

 Brigantedinium

simplex

15

37

41

7

   

denticulatum

 

10

25

  

9

7

spp.

15

10

 

15

 

9

 

 Protoperidinium

americanum

72

140

49

22

14

9

 

latissimum

15

      

 Quinquecuspis concretum

 

10

17

  

9

13

 Selenopemphix

alticintum

8

     

7

quanta

29

37

49

29

20

9

14

 Stelladinium stellatum

 

10

    

7

 Trinovantedinium capitatum

 

19

  

7

 

7

 Votadinium calvum

29

28

 

7

 

9

7

 Diplopsalid

       

 Diplopsalis lenticula

93

94

89

71

66

50

39

 Gymnodinioid

       

 Polykrikos kofoidii/schwartzii complex

36

28

57

8

  

6

Subtotal

312

423

327

159

107

104

107

Heterotrophs (%)

53

55

47

40

31

34

38

Total

593

776

693

397

345

302

283

Table 3

Species composition, concentrations (cysts per gram), and relative abundances (percent) of dinoflagellate cysts observed in the short-core St.14 collected from Gwangyang Bay

Species/depths (cm)

0–1

2–3

4–5

9–10

14–15

19–20

24–25

Autotrophs

       

 Gonyaulacoid

       

 Alexandrium sp. 1 (ellipsoid)

    

7

  

 Lingulodinium machaerophorum

    

8

9

17

 Spiniferites

bulloideus

70

99

115

67

85

44

17

delicatus

112

113

132

41

54

70

25

hyperacanthus

70

169

115

47

93

52

41

membranaceus

    

16

  

mirabilis

 

8

 

20

8

 

9

ramosus

  

17

7

31

 

9

 Tuberculodinioid

       

 Tuberculodinium vancampoae

 

8

25

14

7

  

Subtotal

252

389

379

182

302

175

118

Autotrophs (%)

55

84

62

71

75

67

88

Heterotrophs

       

 Protoperidinioid

       

 Brigantedinium

simplex

9

      

denticulatum

  

9

 

8

 

7

spp.

18

   

8

  

 Protoperidinium

americanum

8

   

7

  

latissimum

     

9

9

Quinquecuspis concretum

 

8

58

 

8

  

 Selenopemphix

alticintum

 

8

16

 

16

  

quanta

17

8

25

 

7

  

 Stelladinium stellatum

9

7

 

7

 

8

 

 Trinovantedinium capitatum

9

 

17

7

   

 Votadinium calvum

 

15

 

7

8

  

 Diplopsalid

       

 Diplopsalis lenticula

87

22

58

41

24

71

 

 Dubridinium capetatum

35

 

9

    

 Gymnodinioid

       

 Polykrikos kofoidii/schwartzii complex

18

 

17

 

8

18

 

Subtotal

210

68

209

62

94

88

16

Heterotrophs (%)

45

15

34

24

23

33

12

Total

462

465

613

258

403

263

134

In this study, we wanted to examine the relationship between nutrient conditions and diatom densities in the overlying water and autotrophic–heterotrophic dinoflagellate cyst compositions in bottom sediments. The results show a related tendency in spatial distributions of diatom densities in surface water and heterotrophic dinoflagellate cysts in bottom sediments (Fig. 2). Given that bottom sediments of highly productive areas are usually characterized by the dominance of heterotrophic dinoflagellate cysts (e.g., Lewis et al. 1990; Hamel et al. 2002; Radi and de Vernal 2004), the higher accumulation of heterotrophic species in the sediments where rich diatom biomass was observed in the surface water is likely to reflect trophic characteristics of the upper water mass of Gwangyang Bay. Because diatoms have growth rates much higher than dinoflagellates, they are at an advantage in competition among primary producers as long as nutrients are not limiting (Chan 1978; Falkowski et al. 1985; Langdon 1987; Tang 1995) and, as a result, heterotrophic dinoflagellates feeding on diatoms can be very abundant under highly eutrophic conditions. Supporting this idea, Andren (1999) showed a massive increase of diatoms in phytoplankton assemblages in response to oversupply of nutrients to coastal areas, while grazer control of heterotrophic dinoflagellates has been found to prevent diatom blooms (Tiselius and Kuylenstierna 1996).

In view of that, the similar trend in distributions between heterotrophic dinoflagellate cyst concentrations in sediments and diatom densities in surface waters of Gwangyang Bay might be attributable to a grazing impact of heterotrophic dinoflagellates on diatoms under nutrient-enriched conditions. For instance, the highest diatom density in the surface water at St.6 coincides with the highest heterotrophic dinoflagellate cyst concentration in bottom sediment of the site, which seems to be attributed to close vicinity of the sampling site to the industrial facility (Pohang Iron and Steel Company, POSCO) subjected to both sewage effluent and heavy industrial pollution. According to Hyun et al. (2003), spatial variations of total organic carbon contents in the Gwangyang Bay sediments, which range from 0.22% to 1.29%, show high values (1.07–1.14%) in this area. Also, in Lee et al. (2007), sediment concentrations of both NO3–N (range 9.3–82.3 µM; 31.5 µM in average) and SiO2–Si (range 69.5–660.9 µM; 325.9 µM in average) show remarkably high values in this area (>75 and >460 µM, respectively). These studies support the idea that this area is under nutrient-enriched conditions, which would stimulate diatom growth and, hence, heterotrophic dinoflagellate cyst production.

On the whole, our results suggest that dinoflagellate cyst records in sediments can be utilized as an indicator of diatom productivity and, therefore, nutrient conditions in the overlying water masses. In many studies, so far, biologically bound silica in diatom remnants within sediments have been quantified to assess overall primary productivity or eutrophication in enclosed coastal areas (e.g., Conley et al. 1993; Turner and Rabalais 1994). However, the utility of biogenic silica preserved in sediments as an index of diatom productivity and phytoplankton biomass has been hampered by several factors such as recycling processes in the water column, dissolution problem in the sediments, and other terrestrial sources of biogenic silica such as phytoliths (Colman and Bratton 2003). Considering these complications, dinoflagellate cysts are useful indicators of eutrophication process-compensating biogenic silica flux, particularly for long-term periods.

In the short-core analysis, the total dinoflagellate cyst concentrations and the heterotrophic species abundance tend to be increasing towards the upper part of the cores (Fig. 3). In particular, proportional changes in dinoflagellate cyst compositions from “autotrophic species-dominated” to “heterotrophic species-dominated” commence from 9 to 10 cm sediment depth, which is clearly shown in the St.1 core. According to the sedimentation rate (approximately 0.43 cm per year) in Gwangyang Bay estimated by 210Pb dating technique (Korea Ocean Research and Development Institute 2003), we assume that the major increase in heterotrophic dinoflagellate cyst species accumulation occurred only for the last decades (approximately 20–30 years) after the time when construction of industrial complexes around Gwangyang Bay started in the 1970s. In such a context, the notable increase in heterotrophic species from 9 to 10 cm depth is likely to signal the development of eutrophication in Gwangyang Bay, which is probably not only from human waste but also from industrial activities.
https://static-content.springer.com/image/art%3A10.1007%2Fs12237-009-9212-6/MediaObjects/12237_2009_9212_Fig3_HTML.gif
Fig. 3

Vertical variations in relative frequencies of autotrophic (white bar)/heterotrophic (black bar) dinoflagellate cysts and total dinoflagellate cyst concentrations (grey line) in the sediment core St.1 (a) and St.14 (b)

According to a previous investigation on seasonal changes in phytoplankton distribution of Gwangyang Bay conducted in 1982, diatom productivity and NH3–N concentrations in both surface and bottom water were distinctively higher in the western part of the bay than the other parts (Shim et al. 1984). This result has been explained by the influence of the Yeochun Industrial Complex located at the southwest side of the bay, which seems to have played a major role in supplying nutrients into Gwangyang Bay at the early stage of industrialization. In our study, however, nutrient enrichment has been signaled in other parts of Gwangyang Bay. The signal includes high values of both diatom density in surface water and heterotrophic dinoflagellate cyst concentrations in bottom sediments from the middle part of the bay. The markedly increased heterotrophic dinoflagellate cysts in the upper part (~10 cm) of the sediment core at St.1 also probably reflects enhanced nutrient supply over the eastern side of the bay. A possible explanation of this result might be attributable to an increased nutrient supply into Gwangyang Bay according to the increase in the level of industrialization around this area since the 1970s.

Conclusion

Distribution patterns of diatoms in the surface waters and dinoflagellate cysts in the bottom sediments of Gwangyang Bay were investigated to examine phytoplankton community changes in response to anthropogenic eutrophication in coastal environments. The corresponding tendency in distributions between diatoms in surface waters and heterotrophic dinoflagellate cysts in bottom sediment seems to reflect their grazing relationship that could be related to nutrient conditions of the upper water mass. In addition to the high diatom productivity and heterotrophic dinoflagellate cyst accumulations in the middle part of the bay, the notable shifts in autotrophic–heterotrophic dinoflagellate cyst compositions of St.1 core record from the eastern part of the bay may imply increased amount of industrial effluents and sewage including both organic and inorganic nutrients since the 1970s, as the industrial complexes broadly established over the region around Gwangyang Bay. Our study suggests that dinoflagellate cysts can be utilized as tracers to provide retrospective information on the long-term effects of anthropogenic eutrophication.

Acknowledgements

We thank the anonymous reviewers for their useful suggestions to improve the quality of the manuscript and for correcting the English. This study was supported by the Korea Ocean Research and Development Institute research program under grant no. PE98314.

Copyright information

© Coastal and Estuarine Research Federation 2009