INTRODUCTION
Coastal ecosystems are zones of high productivity and biodiversity. The hydrographic regime within coastal bays is complex, and includes estuarine circulation, formation of fronts, internal waves and wind, tidal mixing, and vertical density gradients (Cembella et al. 2005). Zooplankton is a key component in coastal ecosystems, primarily because of their important role in material and energy fluxes from phytoplankton to higher trophic levels (David et al. 2006). In general, zooplankton density has been associated with changes in phytoplankton standing stocks, and with the combined effects of regional climatology and local hydrography.
Gamak Bay is surrounded by Yeosu city and Dolsan Island, Korea. Since the 1990s, it has been exposed to environmental pollution, such as eutrophication, harmful algal blooms, and decomposition of sediments caused by increased urban sewage discharged from the metropolitan city of new town development and by-products from fishery farming (Lee and Kim 2008). The sediment has been organically enriched and contaminated with anthropogenic pollutants in the northern area of Gamak Bay. For the reason, the polluted sediments have been dredged for a long time from 2001 to 2006 (Seo et al. 2012). Nevertheless, hypoxia and/or anoxia continuously occurs during summer when the water column is stratified, and bottom waters are isolated from oxygen input in the northern region of Gamak Bay (Kim et al. 2006;Lee and Moon 2006;Moon et al. 2006a).
Study of zooplankton is important for better understanding of the functioning of coastal ecosystems (Chisholm and Roff 1990;Leandro et al. 2007). Most information on zooplankton in Gamak Bay is based on seasonal sampling of an adjacent region since the 1980s (Shim and Ro 1982;Soh et al. 2002;Moon et al. 2006a, b;Moon et al. 2009;Kang et al. 2018). A previous study on zooplankton populations in Gamak Bay described seasonal community, taxonomic composition, and density at inner region of Gamak Bay (Soh et al. 2002;Moon et al. 2006b). Studies of zooplankton communities are strongly influenced by temperature, salinity, dissolved oxygen, and phytoplankton standing stocks of different water masses in Gamak Bay (Soh et al. 2002;Moon et al. 2006b). However, estimates of spatial and temporal variation of zooplankton density have not been reported for Gamak Bay.
The major objective of this study was to evaluate zooplankton variability in spatial and temporal terms in relation to physical and chemical factors and biotic factors along inner, central, and outer regions of Gamak Bay. The study examines the spatial and temporal patterns of density by dominant taxonomic groups.
MATERIALS AND METHODS
1. Experimental methods
Seasonal variation of the zooplankton community and hydrographic conditions were examined at three regions (inner, central, and outer regions) of Gamak Bay, Korea (Fig. 1). Filtered sampling was conducted at 7 fixed stations monthly from January to December 2006 in Gamak Bay, Korea. Temperature, salinity, and dissolved oxygen (DO) were measured using YSI 6600 model water quality system calibrated against Winkler titrations (Winkler et al. 2003). Water samples were collected with a 5 L Niskin-type sampler from 1 m below the surface and 1 m above the bottom at each station. Chemical oxygen demand (COD) was analyzed by Alkali method (The Oceanographic Society of Japan 1980). For the determination of total chl-a concentrations, a 500 mL sub-sample was gently filtered (vacuum<5 cm Hg) through a GF/F filter (Whatman Inc., USA), and extracted with 90% acetone for 24 h in dark. Chl-a concentrations were determined fluorometrically by Cary 300 model (Varian Co., USA) spectrophotometry (Parsons et al. 1984).
Zooplankton samples were collected by vertical hauls from the bottom to the surface using a conical net (0.45 m mouth diameter, 200 μm mesh). The net was fitted with a flow meter (Model 438115, Hydro-bios, Germany) to determine the amount of water filtered during each tow. Zooplankton samples were immediately preserved in seawater- buffered formaldehyde (5% final concentrations) for enumeration and identification. In laboratory, subsamples were made with a Folsom plankton splitter, and dispensed into Bogorov-Rass counting chambers. Taxonomic composition within each zooplankton group was then determined. Copepods were identified, and counted to species level if possible. Subsamples for identification and enu-meration were at least 10% of total samples. Zooplankton identification was made to the lowest taxon possible, and counts were made by Olympus SZ-40 stereomicroscopy. Zooplankton density was expressed as the number of individuals per cubic meter (ind. m-3). The Shannon-Weaver diversity index (H′; Shannon and Weaver 1963) was calculated using PRIMER (Clarke and Warwick 2001).
2. Statistical analysis
Two-way analysis of variance (ANOVA) was used to examine the spatial and temporal differences, i.e., between the sampling stations and between months in all hydrographic variables, zooplankton taxa, density, and diversity. Two-way ANOVA was used also to analyze the spatial and temporal variations in each dominant species. Zooplankton density data were natural log transformed to meet assumptions of normality (i.e., to minimize the influence of highly abundant species). Small deviations from normality or homogeneity after transformation were accepted, because ANOVA is considered to be robust to such violations (Underwood 1997). Pearson’s correlation coefficient was calculated to characterize the relationships of different hydrographic variables, zooplankton taxon, density, and diversity. The effects of hydrographical factors on the seasonal and spatial variations of zooplankton were analyzed by multiple regressions based on correlation coefficients among parameters obtained from the sampling data. Parameters selected for all statistical analyses were mean temperature, salinity, DO, COD, and chl-a concentrations within the surface and bottom depths from January to December, 2006. All statistical analyses were conducted using SPSS ver. 18.0 for windows.
RESULTS
1. Hydrographic environment
Figure 2 shows the spatial and temporal variations in hydrographical parameters. Temperature did not show significant spatial variation. However, surface layer (F=346.72, p<0.001) and bottom layer (F=402.07, p<0.001) showed significant seasonal variations. The mean temperature values ranged ((4.8±1.2) to (27.2±0.9))°C in January to August, respectively. Surface and bottom salinity did not show significant spatial variation. The lowest value of mean salinity of (28.3±1.0) psu was recorded in July while the highest of (35.0±0.2) psu was found in April. Surface (F=54.75, p<0.001) and bottom (F=61.74, p<0.001) salinity showed significant seasonal variations. Surface and bottom DO concentrations did not show significant spatial variations. The highest mean DO concentration of (9.1± 1.3) mg L-1 was recorded at S6. It did not significantly differ between stations. Surface (F=19.05, p<0.001) and bottom (F=18.91, p<0.001) DO concentrations showed significant seasonal variation. The lowest value at the bottom of (3.9±2.4) mg L-1 was recorded in June, while the highest value at the surface of (11.2±0.6) mg L-1 was found in February. The highest value of mean COD concentrations of (1.4±0.6) mg L-1 was recorded at S1 surface. Spatial variability of surface temperature was not significant. However, that of bottom temperature was significant (F=2.47, p=0.031). Surface (F=4.87, p<0.001) and bottom (F=5.04, p<0.001) COD concentrations showed significant seasonal variations, with the lowest value of (0.5± 0.2) mg L-1 recorded in January, while the highest value detected at the surface of (1.9±0.7) mg L-1 was in June. The highest value of chl-a concentrations of (9.7±10.4) μg L-1 was recorded at S1 surface. It decreased slightly toward the bay. The lowest value of chl-a concentrations of (2.5±0.9) μg L-1 was recorded at S7 surface. The spatial variability of chl-a concentrations was not significant. However, the seasonal variabilities of surface (F=4.14, p<0.001) and bottom (F=4.67, p<0.001) chl-a concentrations were significant. The lowest value of chl-a concentrations was recorded at surface of (2.5±0.9) μg L-1 in December, while the highest value was found at surface (11.6±11.8) μg L-1 in July.
The results of Pearson’s correlation analysis showed some significant associations among the number of species, density, diversity index (H′), and hydrographical factors (Table 1). Temperature showed significant correlations with all dependent and independent values. Salinity showed significant positive correlations with DO, but significant negative correlations with COD, chl-a concentrations, number of taxa, and density of zooplankton. DO concentrations had significant negative correlation with number of species, while COD concentrations had significant positive correlations with chl-a concentrations, number of taxa, and density of zooplankton.
2. Zooplankton community structure, density and diversity
A total of 65 taxa of zooplankton were recorded. Of zooplankton identified to species level, number of individuals of Noctiluca scintillans (mean 1,082 ind. m-3), Paracalanus parvus s. l. (mean 851 ind. m-3), Acartia omorii (mean 418 ind. m-3), Eurytemora pacifica (mean 199 ind. m-3), cirriped larvae (mean 133 ind. m-3), Oithona similis (mean 130 ind. m-3), and Pseudevadne tergestina (mean 88 ind. m-3) were found (Table 2). Noctiluca scintillans was the overwhelmingly dominant species based on overall density contribution. This species alone contributed as high as 30.9% of the total zooplankton density. The low temperature assemblage was dominated by only a few species, such as E. pacifica, A. omorii, and C. abdominalis. At the inner region (S1), mainly E. pacifica was found during January to March while the high-temperature assemblage was mainly dominated by P. parvus s. l. during almost the entire study period (Fig. 3). In contrast, the outer region was dominated by some species that were seasonally variable. Major species of this assemblage were N. scintillans, P. parvus s. l., O. similis, cirriped larvae, A. crassa, and other common calanoid copepods. N. scintillans dominated overwhelmingly during January, February, June, and November, while P. parvus s. l. and O. similis dominated in January, February, and December (Fig. 3). During the whole period, zooplankton density varied by two species of magnitude, whereas copepods were the dominant taxon in terms of numerical density. Noctiluca scintillans and P. parvus s. l. followed zooplankton in relative density. However, they were numerically the most dominant, contributing 55.2% of total zooplankton. The most dominant zooplankton taxa were N. scintillans, P. parvus s. l., A. omorii, E. parcifica, cirriped larvae, O. similis, P. tergestina, and O. dioica.
Spatial and temporal variations of zooplankton density, copepods density, diversity, and the most dominant taxon of zooplankton were significant (Table 3). Of the 3 dominant species, N. scintillans, A. omorii, and C. affinis showed the most significance between seasonal and spatial variation. There were two groups based on spatial distribution: those showing significantly higher density at inner region (e.g., N. scintillans, A. omorii, A. erythraea, E. pacifica, and P. marinus); those showing no significant spatial variation; and those showing significantly low density in the outer regions (P. avirostris, P. tergestina, A. erythraea, E. pacifica, and P. marinus) (Fig. 4). The monthly variations in the density of dominant species showed that the most dominant species were generally highly abundant during June to October, corresponding to the period of high temperature. However, their co-occurrence was different (Fig. 5). The results of Pearson’s correlation analysis showed some significant associations among the dominant taxa of zooplankton, temperature, salinity, DO, COD, and chl-a concentrations (Table 4). The density of N. scintillans correlated positively with COD, but negatively with salinity; whereas, the density of P. parvus s. l. correlated negatively with temperature and COD. The density of E. pacifica and A. omorii correlated negatively with temperature. On the other hand, the density of A. erythraea and Penilia avirostris correlated positively with temperature and COD, but negatively with salinity.
Zooplankton density showed no significant spatial variation, having the highest mean density of (7,074±12,616) ind. m-3 at S1, and the lowest mean density of (1,908± 1,433) ind. m-3 at S3. There were two major spatial areas based on zooplankton density: a high-density area at inner region (S1 and S2), and a lower density area at central and outer regions (S4 to S7). However, the value of diversity index showed significant spatial variations (F=2.4, p=0.04), with the highest mean diversity index at S5, and the lowest mean diversity index at S1. The numbers of species and den-sity did not show significant spatial variations (Fig. 6). However, the number of species (F=10.21, p<0.001), density (F=2.30, p=0.018), and diversity (F=3.60, p<0.001) showed significant seasonal variations. Higher number of species and density were observed during June to September excluding August, while higher diversity index was observed during August to October. There were two distinct regions based on all diversity indices used. The inner region (S1 and S2) had significantly lower diversity than the central to outer regions.
3. Relationship of hydrographical factors in the zooplankton community
The influence of the hydrographic environment on the number of taxa, zooplankton density, diversity, and on the density of the three dominant species (N. scintillans, P. parvus s. l., and A. omorii) were characterized using multiple regression analysis. Temperature, salinity, DO, COD, and chl-a concentrations were used as independent factors in the multiple regression model to characterize their influence on the dependent variables of number of taxa, zooplankton density, diversity, and dominant species. Significant multiple regression models were produced for the number of taxa (F=16.67; adjusted R2=0.292; p<0.0001), zooplankton density (F=14.12; adjusted R2=0.147; p<0.0001), diversity (F=6.11; adjusted R2=0.186; p<0.0001), N. scintillans (F=12.29; adjusted R2=0.233; p<0.0001), P. parvus s. l. (F=18.51; adjusted R2=0.184; p<0.0001), and A. omorii (F=24.33; adjusted R2=0.375; p<0.0001) (Table 5). The model showed that temperature was the common predictor for diversity, and for N. scintillans and A. omorii of the dependent variables (P values were 0.008, 0.001, and 0.001 for diversity, N. scintillans, and A. omorii, respectively). For the number of taxa and zooplankton density, two additional variables of DO and salinity for the number of taxa (p<0.05) and COD for zooplankton density (p<0.05) were found as significant predictors (Table 5). Temperature was the significant common predictor variable for both N. scintillans (p<0.05) and A. omorii (p<0.05), and one additional variable of salinity (p<0.05) was a significant predictor for P. parvus s.l. Multiple regression models with other species were not significant, suggesting that the species were strongly influenced by the hydrographical variables.
In Gamak Bay, the five acartiid species (A. erythraea, A. omorii, A. ohtsukai, A. pacifica, and A. sinjiensis) displayed distinct spatial and temporal distribution patterns. Of these, two showed seasonal fluctuation during the study period. Acartia omorii occurred from October to July when temperature ranged (4.8 to 24.8)°C (Fig. 7). The spatial and temporal variability of P. parvus s. l. in Gamak Bay was characterized as being continuous in the zooplankton throughout the year, showing a high peak in summer to autumn, but lowest in winter. High density of two cladocerans (Pseudevadne tergestina and Penilia avirostris) was found in July. It is possible that seasonal differences in the density and peaks in Gamak Bay are related to temperature and COD concentrations (Table 4).
The Temperature - Salinity - Density diagram showed differences in ecological requirements of the dominant species of zooplankton communities in Gamak Bay (Fig. 7). Noctiluca scintillans occurred intermittently throughout the year, as temperature and salinity of the regions again increased above 20°C and below 32 psu, respectively. The density of P. avirostris and P. tergestina peaked when temperature and salinity were 23°C and 29 psu, respectively. In summer, A. erythraea showed high density when temperature and salinity ranged (22 to 28)°C, and from (30 to 32) psu, respectively, while A. omorii was most abundant at temperature of below 20°C and salinity of almost 33 psu. Eurytemora pacifica is stagnant in eutrophic waters at the inner region. Its density is higher at temperature of below 10°C and salinity of almost 33 psu. Paracalanus parvus s. l. was predominant in the whole bay area throughout the year. The density of P. parvus s. l. increased when the salinity decreased, and temperature ranged (10 to 25)°C. Pseudodiaptomus marinus and O. similis had similar periods of density in the inner region. Their density was sharply decreased when temperature was below 23°C. Regarding occurrence, P. marinus showed high density at temperature of 23°C, and salinity of 29 psu. Small cyclopoid copepod O. similis showed high density during warm seasons in Gamak Bay, when temperature and salinity were 20°C and 32 psu, respectively. Among zooplankton found in Gamak Bay, only Aidanosagitta crassa occurred during the study period. Mass occurrences of A. crassa were observed in spring and autumn. High density of O. dioica was found when temperature and salinity ranged (17 to 24)°C, and (30 to 33) psu, respectively. The density of N. scintillans was also positively correlated with COD concentration, indicating that density of zooplankton might be largely influenced by high chl-a concentration.
DISCUSSION
Gamak Bay presented considerable spatial and temporal variability for hydrographic conditions and zooplankton community during the study period. Differences in the hydrographic conditions and trophic status between the inner and outer regions of Gamak Bay were apparent. Zooplankton showed higher density at the inner region, but lower density at the outer region in Gamak Bay. Spatial and temporal variability of zooplankton by a few dominant species can sometimes occur in Gamak Bay under unstable situations (Soh et al. 2002;Moon et al. 2006b). The zooplankton assemblages in Gamak Bay were dominated by N. scintillans (30.9%), P. parvus s. l. (24.3%), A. omorii (12.0%), E. pacifica (5.7%), and cladocerans (4.1%). A similar dominance pattern by these same species also occurred in Gwangyang Bay (Jang et al. 2004) and Jinhae Bay (Soh and Choi 2004). Noctiluca scintillans was found throughout the year, excluding September. It had high density when temperature increased above 20°C, salinity decreased below 30 psu, and when chl-a was high while oxygen level was low. Noctiluca scintillans contributed largely to the decrease of copepods at low salinity, because it was the only taxon exceeding the density of copepods in Gamak Bay (Soh et al. 2002;Moon et al. 2006b). Increased density of N. scintillans may affect short-term variations of phytoplankton biomass through predation on eggs and copepods nauplii, thus influencing copepod populations (Sekiguchi and Kato 1976;Kimor 1979; Daan 1987; Nakamura 1998). In Gamak Bay, diatoms were the most dominant phytoplankton group during June to September (Lee and Kim 2008). These results support an association between the population of N. scintillans and hydrographical factors, given their high spatial and temporal heterogeneity of zooplankton density in Gamak Bay.
The density of copepods was negatively impacted by eutrophic condition in this study. Zooplankton communities with eutrophic condition appeared successively at inner region, correlating well with the timing of autochthonous species that dominated, such as E. pacifica and acartiid species. Of these, E. pacifica was a predominant species at the inner region during winter to early spring. This species has long been considered as abundant in the zooplankton community in Japanese Inlet waters (Ueda 1982;Uye et al. 2000) and the estuarine and coastal waters of Korea (Kim and Huh 1983;Kang et al. 1996;Soh et al. 2002;Moon et al. 2006b). Eurytemora species can produce resting eggs, which allows them to lie dormant in the sediment, and appear suddenly when conditions are favorable (Uye 1985;Ban and Minoda 1994;Viitasalo 1994). Most coastal copepods spend a portion of their life cycle in the sediment as resting eggs (Uye 1985;Marcus 1996). This might profoundly influence the dynamics of the zooplankton community (Hairston Jr et al. 2000). When the habitat environment is recovered, resting eggs are hatched. Our results support the notion that low temperature (<20°C) may be an important cue to induce resting egg production of E. pacifica in Gamak Bay.
The spatial and temporal variability of five acartiids are similar to the thermal range for the occurrence of this species in the zooplankton found in previous work carried out in the central part of the Inland Sea of Japan (Liang and Uye 1996a), and the southern coasts of Korea (Park et al. 2001; Soh and Jeong 2003; Part et al. 2015). The seasonal variability of A. omorii is significantly correlated with temperature, probably resulting from its seasonal cycle and ecological requirement rules (Liang and Uye 1996a; Soh and Jeong 2003, Park et al. 2015). Temperature and salinity appear to provide A. erythraea a competitive advantage, allowing them to extend their distribution to the inner region during summer. Acartia erythraea is predominant in the shallow coastal waters of Korea during summer and autumn (Han et al. 1995;Kang et al. 1996;Soh and Choi 2004;Moon et al. 2006b) and the bottom in coastal waters during day, to maintain their position against weak water currents (Ueda et al. 1983). The spatial and temporal segregation and continued coexistence of Acartia species might be due to slight difference between species in terms of their adaptation abilities and preferences for certain hydrographical conditions, such as temperature, salinity, and tidal exchange. These factors may play a key role in determining their spatial and temporal distributions ( Jeffries 1962; Ueda 1987; Soh and Jeong 2003; Moon et al. 2008; Park et al. 2015). These results suggest that Gamak Bay is a preferred place with suitable temperature, salinity, and food for the five acartiids to control their populations.
Jang et al. (2004) investigated the seasonal distribution of P. parvus s. l. in Gwangyang Bay of Korea, which has a temperate domain similar to Gamak Bay. This species is one of the most dominant copepods in the estuarine and coastal habitat (Soh and Suh 1993;Han et al. 1995;Liang and Uye 1996b, Rong et al. 2002;Jang et al. 2004, 2015). The occurrence pattern of Paracalanus sp. (as P. parvus s. l.) in Fukuyama Harbor had a temperature range of (8.9 to 28.2)°C, with a high peak at temperature ranging (20.4 to 25.4)°C. The egg production rate of the natural population of P. parvus s. l. was constant. It did not show any district reduction until temperature warmed up to 25°C, showing acclimation to higher temperature (Liang and Uye 1996b). Cladocerans can be the numerically dominant components of the zooplankton community in temperate, tropical, and subtropical regions (Clarke and Roff 1990;Kim and Onbé 1995). They are usually dominated by phytoplankton density in coastal waters, especially cryptophytes in eutrophic Tolo Harbor in the eastern coastal waters of Hong Kong (Wong et al. 2006). According to Lee and Kim (2008), there is a high density of phytoplankton, such as diatoms, in June to September in Gamak Bay. This result indicates that they are favored by water stratification during summer, when small-sized phytoplankton dominates because of relatively high chl-a concentrations in the surface layer, which occurs in the inner region.
Temperature and salinity were the main hydrographical factors regulating the spatial and temporal patterns of zooplankton in estuaries and coastal waters (Badylak and Phlips 2008;Sun et al. 2011;Park et al. 2015). In this study, the multiple regression for the association of hydrographical factors with number of taxa, zooplankton density, diversity, and dominant species differed, depending on the zooplankton community considered. In Gamak Bay, copepods (such as A. omorii , P. parvus s. l., and E. pacifica) and diversity co-varied with temperature (p<0.05), salinity (p<0.05), and DO concentration (p<0.05), indicating a tight coupling between temperature and neritic copepods density, which had high values around the inner region (S1 to S3). Therefore, temperature is the most important variable that can describe the observed variability in diversity, and of N. scintillans, and A. omorii in Gamak Bay as a whole; and COD concentration is the additional variable for zooplankton density and diversity in the inner region. Several studies that described spatial and temporal patterns of zooplankton density in Korean estuaries and coastal waters considered the influence of both abiotic (e.g., temperature and salinity) and biotic (phytoplankton and N. scintillans density) factors (Yoon and Choi 2002; Soh and Jeong 2003; Jang et al. 2004;Lee et al. 2006;Moon et al. 2006b;Park et al. 2015). In Gamak Bay, seasonal temperature, salinity, DO, and COD concentrations typically have important effects on the zooplankton community. Therefore, these factors were considered in this study to determine their possible impacts on the zooplankton community in Gamak Bay.
CONCLUSION
The present analysis showed that the seasonal cycle of zooplankton density and taxonomic composition was probably determined mainly by their preferences and tolerances for specific temperature, salinity, chl-a, and COD concentrations. High nutrient input by freshwater discharge from near metropolitan city and Seomjin River into Gamak Bay resulted in significantly higher N. scintillans density, and also affected zooplankton density. The marked increase in the zooplankton density at the inner region during summer to autumn, when freshwater discharge was at its peak, suggested that the density was strongly related to temperature and freshwater inputs that could drive nutrient inputs, consequently affecting food supply in the system, due to intense continental drainage. Nevertheless, future studies that combine information on the density of N. scintillans and zooplankton and their daily consumption rates are needed, to quantitatively determine the extent to which predation influences the density and community structure of zooplankton in Gamak Bay.