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Journal of Environmental Science International - Vol. 34 , No. 6
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[ ORIGINAL ARTICLE ]
Journal of Environmental Science International - Vol. 34, No. 6, pp. 311-324
Abbreviation: J. Environ. Sci. Int.
ISSN: 1225-4517 (Print) 2287-3503 (Online)
Print publication date 30 Jun 2025
Received 11 Mar 2025 Revised 27 May 2025 Accepted 13 Jun 2025
DOI: https://doi.org/10.5322/JESI.2025.34.6.311

Seasonal Variations in Phytoplankton and Zooplankton Communities in an Estuary with Eutrophic Freshwater Inputs
Sehee Kim ; Gukhee Jo ; Yongsik Sin*
Department of Ocean System Engineering, Mokpo National Maritime University, Mokpo 58628, Korea

Correspondence to : *Yongsik Sin, Department of Ocean System Engineering, Mokpo National Maritime University, Mokpo 58628, Korea Phone：+82-61-240-7312 E-mail：yongsik@mmu.ac.kr


Ⓒ The Korean Environmental Sciences Society. All rights reserved.
This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

In the Yeongsan River estuary, anthropogenic activities, such as the construction of an estuary dike have altered hydrodynamic conditions and induced eutrophic freshwater inflow into the saltwater zone. In this study, we investigated the seasonal variations in environmental factors and their relationships with phytoplankton and zooplankton communities. Data were collected seasonally in 2014 and 2015 at three stations, located near the dike and offshore, to explore the fluctuations and associations of physical and chemical environmental factors with phyto- and zooplankton communities. A associations were examined using non-metric multidimensional scaling (nMDS) and correlation analyses. During the summer, when the maximum discharge (163.0 × 106 m3) was recorded, there was a high concentration of total chlorophyll-a and nano-sized chlorophyll-a were high and showed a significant negative correlation (p<0.05) with salinity. The zooplankton community showed a stronger correlation with water temperature than with salinity and a significant positive correlation (p<0.05) with chlorophyll-a concentrations and phytoplankton composition. The results suggest that anthropogenic and eutrophic freshwater inputs in altered estuaries affect plankton communities and potentially the food web structure.

Keywords: Yeongsan River estuary, Phytoplankton, Zooplankton, Non-metric multidimensional scaling
1. Introduction

Phytoplankton are primary producers in aquatic ecosystems and are sensitive to physical and chemical changes (Thompson et al., 2008; Guinder et al., 2013), indicating environmental change and pollution in aquatic systems (Nayar et al., 2005; Bode et al., 2017). The species composition and abundance of the phytoplankton are regulated by environmental factors such as water temperature, light, and nutrients (Reynolds, 2006; Davis et al., 2015), and by the intensity of predation by higher-level consumers such as zooplankton (Silva et al., 2014).

Zooplankton are intermediate links in the transfer of matter or energy from lower to higher trophic levels (Batten et al., 2019), and their distribution affects the growth and survival of juvenile fish, thereby determining the abundance of fish stocks (Winder and Jassby, 2011). Therefore, research regarding phytoplankton and zooplankton is essential to better understand and manage the marine ecosystem.

Estuaries are transition zones where freshwater mixes with saltwater and are highly complex physical, chemical, and biological environments that are impacted by tides, waves, and freshwater inputs. Estuaries are home to a wide variety of organisms and are known to provide highly productive water resources compared to other ecosystems (McLusky and Elliott, 2004).

In estuaries, nutrient supply from freshwater inputs can lead to algal blooms (Davis et al., 2015), where ungrazed phytoplankton and allochthonous detritus can settle out and result in hypoxia, having adverse effects on the ecosystem (Rabalais et al., 2002). As the response rate or predation pressure of zooplankton, which are consumers of phytoplankton, in particular, can regulate the abundance of primary producers that are settled, understanding their interactions is critical to understanding and managing estuarine ecology.

The Yeongsan River estuary (Fig. 1) located in the western part of Korea has a watershed area of 3,468 km2 and flows along a length of 137 km. The estuary has been transformed from a natural to an artificial estuary since the construction of a dike in 1981, separating the freshwater zone on the inner side and the saltwater zone on the outer side. In the freshwater zone, the input of domestic sewage and agricultural and livestock wastewater has accelerated the increase in nutrient concentrations and organic pollution, resulting in a deteriorating water environment and ecological health (Lee et al., 2009). Large volume of freshwater in the reservoirs is discharged into the estuary at low tide through sluice gates built in the dike when the reservoir water level peaks and is causing extreme changes in water quality including salinity, nutrients, chlorophyll-a, primary production and carbon flux in the saltwater estuary (Sin and Jeong, 2015; Kim et al., 2017; Park and Sin, 2022). Chlorophyll-a and primary production decreased in the saltwater although nutrient concentration increased during the event of freshwater discharge. Zooplankton abundance was also preliminarily reported to decrease (Sin et al., 2013) but the variation of zooplankton community relevant to the freshwater discharge is not fully understood. In this context, it is necessary to investigate the temporal and spatial variation of zooplankton as well as of phytoplankton responding to the environmental change resulting from freshwater discharge for better understanding and managing the estuarine ecosystem caused by the dike construction.


Fig. 1. 
Sampling sites in the Yeongsan River estuary.

Although studies simultaneously examining phytoplankton and zooplankton have been conducted in the Seomjin River estuary (Lee et al., 2001), Southwest Korea (Kim et al., 2010), Nakdong River (Seo et al., 2013), and Werribee River estuary, Australia (McNaughton et al., 2022), only a few studies have addressed the inter-relationship between phytoplankton and zooplankton. Furthermore, these studies were conducted in coastal waters, inland bays, and natural estuaries, and few studies have examined the relationship between phytoplankton and zooplankton in anthropogenically altered estuaries such as the Yeongsan River estuary. We expect that the anthropogenic freshwater inputs affect zooplankton as well as phytoplankton communities. In this context, this study aims to investigate the association and fluctuation of zooplankton and phytoplankton in the Yeongsan River estuary and provide foundational data for understanding the energy flow in the marine ecosystem and for managing the water quality of the altered estuary resulting from freshwater inputs.

2. Materials and Methods
2.1. Field survey

In this study, we utilized data collected in July, September, and December 2014 and April 2015 at three stations (Stations A through C) to represent salinity gradient along the main channel of the Yeongsan River estuarine waters from the lower bank of the Yeongsan River to Oedal-do (Fig. 1). The field survey was consistently conducted during high tide, based on the tide data for Mokpo Port provided by the Korea Hydrographic and Oceanographic Agency(2015).

The average water depths at the stations from A to C were 10.2±1.8 m, 18.9±2.8 m, and 7.9±2.1 m respectively. The freshwater discharge data of the estuary dike in the Yeongsan River was provided by Korea Rural Community Corporation.

Water temperature, salinity, turbidity, and dissolved oxygen were measured at the surface (0.5 m) and bottom (1.0 m off the bottom) of the water column with a conductivity, water temperature, and depth (CTD) multiparameter probe (YSI-Model 6600 V2) at each station. Water samples were also collected from the surface and bottom using a Niskin water sampler, and samples for dissolved inorganic nutrients (NO2- + NO3-, NH4+, PO43-; μM) were prepared by filtering 50 mL water sample through GF/F (dia.: 25 mm; nominal pore size: 0.7 µm; Whatman®). The filtrates were immediately stored in deep freezers (-75℃) until analyses. Nutrient concentration analyses (replicates) were performed with a QuAAtro® Autoanalyzer using the method of Parsons et al. (1984). DIN and DIP represent the sum of NO2- + NO3- and NH4+ and soluble reactive phosphate (SRP; PO43-), respectively.

2.2. Sample analyses
2.2.1. Phytoplankton

Phytoplankton were categorized as micro- (>20 µm), nano- (2–20 µm), and pico-sized (<2 µm) for chlorophyll-a measurements based on size. For size-fractionation, 200 mL of water samples were sequentially filtered using a 20 µm Nytex™ mesh, a polycarbonate membrane filter (47 mm diameter, 2 µm pore size; Whatman®), and a GF/F (25 mm diameter, 0.7 µm pore size; Whatman®). Measurement of chlorophyll-a was based on the Marine Environmental Standard Test Methods, as mandated by the Marine Environment Management Act (Ministry of Oceans and Fisheries). Sample for phytoplankton species identification was from 1 L of surface water, fixed with 5 mL of Lugol’s solution, and allowed to settle down in the dark for 1–2 days. Species identification was made under microscope (ZEISS Axioskop 2 MAT) following Korean Animal and Plant Book Vol. 9 (Jeong, 1968) and Vol. 34 (Shim, 1994). The community structure was analyzed using data (cells/mL) identified at species or genera levels and grouped at class.

2.2.2. Zooplankton collection and identification

Zooplankton were collected by horizontal hauls using a conical net (45 cm and mesh size 200 µm) attached with a flowmeter. Samples were fixed with neutral formalin to a final concentration of 5% (Sakuma et al., 2002). Zooplankton identification was performed using a dissecting microscope (Nikon SMZ 1000) with reference to Koste et al.(1978) and Smirnov and Timms(1983).

2.3. Statistical analyses

The relationship between phytoplankton and zooplankton was estimated by Pearson’s correlation analysis using SPSS Statics 26.0. Furthermore, to determine the similarities among physical and chemical environmental factors, and phytoplankton and zooplankton communities, non-metric multidimensional scaling (nMDS) analysis was performed using PRIMER 6. The impact vectors of the physical and chemical environmental factors were plotted on top of the nMDS results, where the length of the vector indicated the magnitude of the correlation between the environmental factors and the plankton community. The plankton data for nMDS and correlation analyses were log (x+1) transformed to minimize the bias of the data due to differences in population density among survey periods and species.

3. Results
3.1. Physical and chemical environmental factors
3.1.1. Freshwater discharge

The total amount of freshwater discharged during 5.0 days before the survey was 163.0×106 m3, with the maximum discharge in the summer (Table 1). The discharges in the winter and spring, respectively, were of 34.3×106 m3 and 5.0×106 m3, and no discharges were recorded in the fall.

Table 1. 
Total amount of freshwater discharged in the 5 days before the sampling date in the Yeongsan River estuary
Sampling date Discharged amount from dike (×106 m3)
D-day D-1 D-2 D-3 D-4 D-5 Total
July 23, 2014 - - 9.9 37.1 96.7 19.3 163.0
September 22, 2014 - - - - - - -
December 24, 2014 - 26.9 - - - 7.3 34.3
April 10, 2015 - - - - 5.0 - 5.0

3.1.2. Water properties

Water temperatures ranged from 6.8 to 24.7℃ at the surface and bottom layers (Fig. 2). Although water temperature was similar between the stations during the study period, in the spring, the water temperatures at the surface and bottom layers at Station A were 12.1 and 10.0℃, respectively, higher than that at the other stations. Salinity, a direct indicator of the impact of freshwater inputs, was observed to be at its lowest concentration in July, a summer month (Fig 2). The distribution of salinity ranged between 20.7 and 32.4 psu at the surface across all periods, increasing from Station A toward Station C. Salinity was higher at the bottom than at the surface, ranging from 30.8 to 33.2 psu.


Fig. 2. 
Seasonal variations of physical and chemical environmental factors in the Yeongsan River estuary.

Turbidity was higher at Stations B and C than at Station A in the winter through spring, and the surface and bottom distributions ranged from 2.8–7.0, 4.1–24.7, and 5.7–70.6 NTU (Nephelometric Turbidity Unit) at Stations A, B, and C, respectively, showing an increasing trend from Station A toward C (Fig 2).

Dissolved oxygen (DO) increased from summer (2014) to spring (2015), with the lowest reading of 4.0 mg/L at the bottom in the summer when the water temperature was high (Fig. 2). The three stations had readings ranging from 7.2 to 11.1 mg/L at the surface and 4.0 to 10.7 mg/L at the bottom.

The concentrations of nitrite+nitrate (NO2- + NO3-) and ammonium (NH4+) in the surface water peaked (Fig. 3) when salinity was low, especially at the station near the dike (Fig. 2) and decreased at station C, indicating supply of DIN (NH4++ NO2- + NO3-) by freshwater. The concentrations of phosphate (PO43-) in the surface water peaked in the winter but they peaked in the summer at the bottom. The maximum levels of DIN (86.0 μM) and DIP (1.1 μM) measured in this study can be categorized as hypereutrophic (“very poor”) and mesotrophic (“fair”), respectively, based on the criteria of Lemley et al.(2015).


Fig. 3. 
Seasonal variations of nutrient concentrations in the Yeongsan River estuary.

3.2. Phytoplankton: Chlorophyll-a and species composition

Chlorophyll-a ranged from 0.04 µg/L to 36.8 µg/L across both the surface and bottom layers (Fig. 4). In the summer, chlorophyll-a concentrations were high, ranging from 10.3 to 36.8 µg/L in the surface layer and from 1.9 to 9.8 µg/L in the bottom layer. In the other seasons, the concentrations were extremely low. Regarding the contribution of chlorophyll-a size classes (Fig. 4), nano-sized chlorophyll-a showed a high contribution (76 to 92%) at Station A in the summer; however, the contribution decreased to 31 to 49% at Stations B and C, respectively. In the fall, micro-sized chlorophyll-a was extremely dominant, ranging from 83 to 96% at all stations except for surface layer of the Station A. In the winter, micro-sized chlorophyll-a contributed the most at Stations A and B and nano-sized chlorophyll-a at Station C. In the spring, pico-sized chlorophyll-a contributed between 47 and 60% at the surface layer of Stations A and B.


Fig. 4. 
Chlorophyll-a content and the contribution (%) of size classes, including micro-, nano-, and pico-sized chlorophyll-a, to the total chlorophyll-a content in the Yeongsan River estuary.

Forty species from 6 classes (Bacillariophyceae, Chlorophyceae, Cyanophyceae, Cryptophyceae, Chrysophyceae, and Dinophyceae) were found, with highest (26 species) at Station A and 20 species at Stations B and C (Table 2). In terms of season, the highest number of species was found at Station A in the summer with 11 species, and the lowest number of species at Station C in the spring with three species. Skeletonema sp. (Bacillariophyceae) alone was dominant (>78%) at all stations in the summer whereas in other seasons, the dominant species differed among stations (Table 2). Bacillariophyceae dominated most of the study period (Table 2; Fig. 5), particularly at Station C, ranging from 99 to 100%. Chlorophyceae showed an abundance of 59% at Station B in the spring, whereas Cryptophyceae (Cryptomonas sp.) showed an abundance of 57% at Station A in the spring.

Table 2. 
Dominant species of phytoplankton in the surface water of the Yeongsan River estuary
Month Station Dominant Species Cells/mL %
July A Skeletonema sp. 4,620 78
B Skeletonema sp. 1,670 82
C Skeletonema sp. 2,030 89
September A Chaetoceros brevis 320 28
B Chaetoceros brevis 400 43
C Bacteriastrum hyalinum 210 31
December A Skeletonema costatum complex 27 30
B Nitzschia sp. 7 27
C Paralia sulcata 13 43
April A Cryptomonas sp. 77 57
B Navicula sp. / Monoraphidium contortum 7 41
C Navicula sp. 13 45


Fig. 5. 
Taxonomic composition of phytoplankton in the surface water.

3.3. Zooplankton: Community structure and species composition

Zooplankton community consisted of Chaetognatha, Copepoda, Appendicularia, Cnidaria, Ostracoda, and Cladocera, etc. (Table 3). The total abundance of zooplankton was 40,373 ind./m3, exhibiting extreme seasonal variation, with the highest abundance in spring (mean 12,536 ind./m3), followed by summer (mean 843 ind./m3), fall (mean 61 ind./m3), and winter (mean 18 ind./m3) over all stations. In particular, the abundance was the highest at Station A in the spring at 37,246 ind./m3. Copepoda dominated at 75 to 100% in most seasons at Station A, with Appendicularia contributing 59% at Station B in the summer and 53% at Station A in the fall (Fig. 6).

Table 3. 
List of zooplankton species in the Yeongsan River estuary
Chaetognatha (phylum)
　Sagitta spp.
Copepoda (subclass)
　Acartia copepodites
　Acartia hudsonica
　Acartia omorii
　Centropages copepodites
　Eurytemora pacifica
　Hemicyclops copepodites
　Oithona copepodites
　Paracalanidae copepodites
　Pavocalanus spp.
　unidentified copepodites
Appendicularia (class)
　Oikopleura spp.
Other
　Echinodermata (phylum)
　Cnidaria (phylum)
 Cladocera (subclass)


　Acartia hongi
　Acartia ohtsukai
　Calanus copepodites
　Corycaeus affinis
　Harpacticoida spp.
　Lavidocera copepodites
　Oithona spp.
　Paracalanus spp.
　Sinocalanus tenellus




Polychaeta (class)
Ostracoda (class)
Amphipoda (subclass)


Fig. 6. 
Taxonomic composition of zooplankton in the Yeongsan River estuary.

The dominant zooplankton species included Copepods Acartia spp., Eurytemora pacifica, Paracalanus spp., and Pavocalanus spp., and Appendicularian Oikopleura spp., which comprised 58 to 100% of the total zooplankton abundance (Table 4; Fig. 6). Copepods Acartia spp. dominated Station C in the winter at 96%, and E. pacifica dominated Station A in the spring at 90% (Table 4).

Table 4. 
Dominant species of zooplankton in the Yeongsan River estuary
Month Station Dominant species Zooplankton abundance
(ind./m3)
 %
July A Pavocalanus spp. 32 33
B Oikopleura spp. 384 59
C Pavocalanus spp. 696 39
September A Oikopleura spp. 5 53
B Oikopleura spp. 20 29
C Paracalanus spp. 80 76
December A Paracalanus spp. 2 82
B Acartia copepodites 4 50
C Acartia copepodites 42 96
April A Eurytemora pacifica 33,571 90
B Eurytemora pacifica 99 48
C Eurytemora pacifica 91 58

3.4. Statistical analyses

Chaetognatha showed a significant (p<0.01) positive correlation with the distribution of Chrysophyceae, whereas other zooplankton groups except Copepoda showed a significant (p<0.05) positive correlation with the distribution of phytoplankton Bacillariophyceae (Table 5). Bacillariophyceae, Appendicularia, Paracalanus spp., Pavocalanus spp. and others showed a significant (p<0.01, p<0.05) positive correlation with water temperature. Phytoplankton (chlorophyll-a) and DIN showed a significant negative correlation with salinity (p<0.05, p<0.01), whereas zooplankton show no significant correlation.

Table 5. 
Correlation matrix of phytoplankton and zooplankton with physical and chemical environmental factors in the surface water of the Yeongsan River estuary (n=12)
Temp Sal Turb DO Dis Chl-a Micro Nano Pico Bacil Chlor Cyano Crypt Chryso Dino
Temp 0.959**
Sal −0.900** −0.810** −0.847**
Turb −0.653*
DO −0.698* −0.731**
Dis 0.680*
DIN −0.744** 0.760**
DIP
Chl-a −0.637* 0.827** 0.971** 0.963** 0.713** 0.691* 0.741**
Micro 0.678* 0.793** 0.639*
Nano −0.712** 0.923** 0.691* 0.839** 0.728**
Pico −0.672* 0.618* 0.651* 0.824**
Chaet −0.656* 0.814**
Copep
Appen 0.678* 0.803** 0.641*
Acar
Eury
Para 0.576* −0.715** 0.634* 0.598*
Pavo 0.590* −0.657* 0.841** 0.916** 0.746** 0.766** 0.685*
Oth 0.709** 0.684* 0.756** 0.619* 0.655* 0.722**
*p<0.05, **p<0.01; Temp=water temperature; Sal=salinity; Turb=turbidity; DO=dissolved oxygen; Dis=total amount of discharge for 5 days; DIN=dissolved inorganic nitrogen; DIP=dissolved inorganic phosphate; Chl-a=chlorophyll-a; Micro=micro-sized chlorophyll-a; Nano=nano-sized chlorophyll-a; Pico=pico-sized chlorophyll-a; Bacil=bacillariophytes (cells/mL); Chlor=chlorophytes; Cyano=cyanophytes; Crypt= cryptophytes; Chryso=chrysophytes; Dino= dinophytes; Chaet=chaetognaths; Copep= copepods; Appen=appendicularians; Acar= Acartia sp.; Eury= Eurytemora pacifica ; Para= Paracalanus spp.; Pavo= Pavocalanus spp., Oth= others.

The nMDS analysis results indicated that the plankton communities varied significantly by season (Fig. 7). In the fall and winter, Stations B and C were associated with water temperature, turbidity, dissolved oxygen and DIP. In spring, the community at Stations A and B was largely influenced by copepods, with minimal association with environmental factors. Phytoplankton except Bacillariophyceae showed a significant negative correlation (p<0.05) with salinity (Table 5), but the nMDS results indicated that water temperature had a greater influence than salinity. The summer community showed a high correlation with size-fractionated chlorophyll-a, while the influence of environmental factors, except for salinity, had minimal impact.


Fig. 7. 
Results of the non-metric multidimensional scaling (nMDS) analysis based on the Bray-Curtis similarity. The nMDS analysis of phytoplankton (40 Species (6 genera); cells/mL) and zooplankton (25 Species (21 genera); ind./m3) species in the surface water was performed (n=68). Vectors indicate the strength and direction of water properties, including water temperature (Temp), salinity (Sal), turbidity (Turb), dissolved oxygen (DO), dissolved inorganic nitrogen (DIN), dissolved inorganic phosphate (DIP), chlorophyll-a (Chl-a), micro-sized chlorophyll-a (Micro), nano-sized chlorophyll-a (Nano), pico-sized chlorophyll-a (Pico), bacillariophyceae (Bacil, cells/mL), chlorophyceae (Chlor), cyanophyceae (Cyano), cryptophyceae (Crypt), chrysophyceae (Chryso), dinophyceae (Dino), chaetognaths (Chaet), copepods (Copep), appendicularians (Appen), and others.

4. Discussion

The community structure of phyto- and zooplankton has been reported to be strongly affected by water temperature (Gillooly, 2000; Sherman et al., 2016). The results obtained in this study also indicate a change in community structure with water temperature. Phytoplankton contributions were dominated by Bacillariophyceae during the wet season (summer to fall) at Stations A and B, whereas the contributions of Chlorophyceae and Dinophyceae increased during the dry season (winter to spring). For zooplankton, the contribution of Appendicularia increased in the wet season, with Copepoda dominating in the dry season. The results of the nMDS and correlation analyses (n=12) have revealed a high correlation of phytoplankton and zooplankton with water temperature, suggesting that phytoplankton and zooplankton communities in the Yeongsan River estuary are generally affected by water temperature.

Species composition and abundance of phytoplankton and zooplankton are also known to be affected by salinity (Muylaert et al., 2009; Paturej and Gutkowska, 2015). In this study, salinity was observed to be lowest at Station A in the summer, and the concentrations of chlorophyll-a and nano-sized chlorophyll-a were high. The negative relationship was also observed in the results of the correlation analysis between the concentrations of total and nano-sized chlorophyll-a and salinity. This is similar to the findings in previous studies between 2012 and 2013 (Sin and Jeong, 2015; Kim and Sihn, 2020, Park and Sin, 2021). Although the shift from micro-size to nano-size and increasing chlorophyll-a were frequently observed, the dominance of Bacillariophyceae such as Skeletonema sp. was not reported before. Bacillariophytes were generally dominant in the cold and dry season whereas Dinophyceae was dominant in the warm and wet season (Sin et al., 2015; Sin and Yu, 2018). Our results reinforce the idea that the seasonality of phytoplankton size and community was changed by the episodic freshwater inputs.

In contrast to phytoplankton, zooplankton showed low abundance in the summer, showing an association between salinity and abundance, with zooplankton abundance increasing toward Station C in the open ocean in this season. A rapid decrease in zooplankton abundance was also observed when freshwater was being discharged into the saltwater (Sin et al., 2013). This suggests that the anthropogenic freshwater inputs can affect zooplankton community near the estuary dike over a short term immediately after the discharge. However, the correlation and nMDS analyses showed no significant association with salinity suggesting that seasonality of zooplankton in the Yeongsan River estuary may not be disturbed by salinity unlike phytoplankton.

The phytoplankton and zooplankton form a predator–prey association wherein phytoplankton are regulated by zooplankton predation (top-down) and zooplankton can be affected by changes in the biomass of their prey (bottom-up) (Leroux and Loreau, 2015). The correlation analysis showed that zooplankton exhibited a positive correlation with the distribution of micro-sized cells and Bacillariophyceae although limited data (n=12) were analyzed. The importance of large-sized Bacillariophyta (diatoms) was also indicated in the nMDS analysis, suggesting that the main food source for zooplankton, except for a few species feeding selectively on detritus, may be the micro-sized bacillariophyte in the Yeongsan River estuary. This hypothesis is supported by the selective feeding of mesozooplankton on large-sized (20-200 µm) bacillariophyte observed in estuaries (Liu et al., 2005; Feng et al., 2020). However, the diet composition was rapidly changed in the summer when small-sized but chain-forming bacillariophytes (Skeletonema sp.) became dominant after the freshwater discharge. Nano-sized phytoplankton such as chlorophytes dominated in the freshwater reservoir were also introduced by freshwater discharge (Sin et al., 2015; Sin and Jeong, 2020). Phytoplankton biomass (chlorophyll-a) also increased greatly after the discharge. This may cause a mismatch or lag in the predator-prey consortium between phytoplankton and zooplankton and ungrazed phytoplankton may undergo heterotrophic decomposition and/or serve as a food source for micro-sized protozoa, potentially promoting microbial food web. This mismatch was also reported in a N stable isotope analysis (Kim, 2025) on phytoplankton and zooplankton collected over the short-term (daily) before and after the freshwater discharge in the Yeongsan River estuary.

5. Conclusions

In the Yeongsan River estuary, an acute decrease in salinity and an increase in DIN levels were observed after the maximum freshwater discharge in the summer. Nano-sized chlorophyll-a concentrations and Skeletonema sp. increased rapidly, responding to these changes, whereas zooplankton abundance remained low, increasing only further downstream in more saline water. This suggests that the physical and chemical environmental changes caused by eutrophic freshwater discharge through anthropogenic sluice gate operation affected phyto- and zooplankton dynamics. However, an evident plankton response was not observed in the winter despite freshwater discharge and high nutrient levels, suggesting that water temperature is also an important factor in the estuary. Statistical analysis further showed that phyto- and zooplankton were affected by water temperature, although a clear zooplankton response to episodic events such as decreasing salinity was not found in the analysis. This suggests that a short-termed investigation to examine hourly/daily variations of plankton as well as monthly/seasonal variations may be also required to better understand plankton ecology in the estuaries with episodic eutrophic freshwater inputs. The rapid increase in phytoplankton biomass as well as change in size classes derived from episodic freshwater inputs may result in a mismatch in the predator-prey interaction in the estuary. This study suggests that the anthropogenic freshwater discharge needs to be incorporated in the management strategy for the estuaries in Korea where most of major estuaries are altered by dikes. Nevertheless, further research, such as isotopic analysis, will be necessary for a better characterization of interactions, such as predation and prey, within food webs.

Acknowledgments

We thank Dr. La, Geung-hwan for his assistance with the identification of zooplankton species.

REFERENCES
1. Batten, S. D., Abu-Alhaija, R., Chiba, S., Edwards, M., Graham, G., Jyothibabu, R., Kitchener, J. A., Koubbi, P., McQuatters-Gollop, A., Muxagata, E., Ostle, C., Richardson, A. J., Robinson, K. V., Takahashi, K. T., Verheye, H. M., Wilson, W. 2019, A global plankton diversity monitoring program, Front. Mar. Sci., 6, 1-14.
2. Bode, A., Varela, M., Prego, R., Rozada, F., Santos, M. D., 2017, The relative effects of upwelling and river flow on the phytoplankton diversity patterns in the ria of a Coruña (NW Spain), Mar. Biol., 161, 94-108.
3. Chung, Y. H., 1968, Illustrated encyclopedia of fauna & flora of Korea vol. 9, Freshwater algae, 1st ed., Ministry of Education, Seoul, Republic of Korea.
4. Davis, T. W., Bullerjahn, G. S., Tuttle, T., McKay, R. M., Watson, S. B., 2015, Effects of increasing nitrogen and phosphorus concentrations on phytoplankton community growth and toxicity during Planktothrix blooms in Sandusky Bay, Lake Erie, Environ. Sci. Technol., 49, 7197-7207.
5. Feng, C., Han, M., Dong, C., Jia, J., Chen, J., Wong, C. K., Liu, X., 2020, Mesozooplankton selective feeding on phytoplankton in a semi-enclosed bay as revealed by HPLC pigment analysis, Water, 12, 2031.
6. Gillooly, J. F., 2000, Effect of body size and temperature on generation time in zooplankton, J. Plankton Res., 22, 241-251.
7. Guinder, V. A., Popovich, C. A., Molinero, J. C., Marcovecchio, J., 2013, Phytoplankton summer bloom dynamics in the Bahia Blanca Estuary in relation to changing environmental conditions, Cont. Shelf Res., 52, 150-158.
8. Kim, H. W., La, G. H., Jeong, K. S., Park, J. H., Huh, Y. J., Kim, S. D., Na, J. E., Jung, M. H., Lee, H. Y., 2010, Assessing the plankton dynamics in lakes and reservoirs ecosystem in the Southwestern parts of Korea, Korean J. Environ. Biol., 28, 86-94.
9. Kim, S. H., 2025, Trophic levels and temporal- spatial variations of phytoplankton and zooplankton in the Yeongsan River estuary, Ph. D. Dissertation, Mokpo National Maritime University, Mokpo, Korea.
10. Kim, S. H., Shin, Y. S., 2020, Daily variation of size-fractionated chlorophyll-a concentrations and water conditions associated with freshwater discharge during summer in the Yeongsan River Estuary, J. Mar. Life Sci., 5, 72-80.
11. Kim, Y. H., Hong, S. J., Song, Y. S., Lee, H. J., Kim, H. C., Ryu, J. S., Park, J. S., Kwon, B. O., Lee, C. H., Khim, J. S., 2017, Seasonal variability of estuarine dynamics due to freshwater discharge and its influence on biological productivity in Yeongsan River Estuary, Korea, Chemosphere, 181, 390-399.
12. Korea Hydrographic and Oceanographic Agency, 2015, KHOA smart tide forecast, http://www.khoa.go.kr.
13. Koste, W., 1978, Rotatoria : die Raedertiere Mitteleuropas : Ueberordnung Monogononta: ein Bestimmungswerk, Gebruder Borntraeger, Stuttgart, 445-468.
14. Lee, P. G., Park, C., Moon, C. H., Park, M. O., 2001, Biomass and species composition of phytoplankton and zooplankton along the salinity gradients in the Seomjin River Estuary, J. Korean Soc. Oceanogr., 6, 93-102.
15. Lee, Y. G., An, K. G., Ha, P. T., Lee, K. Y., Kang, J. H., Cha, S. M., Cho, K. H., Lee, Y. S., Chang, I. S., Kim, K. W., Kimj, J. H., 2009, Decadal and seasonal scale changes of an artificial lake environment after blocking tidal flows in the Yeongsan estuary region, Korea, Sci. Total Environ., 407, 6063-6072.
16. Lemley, D. A., Adams, J. B., Taljaard, S., Strydom, A. N., 2015, Towards the classification of eutrophic condition in estuaries, Estuar. Coast. Shelf Sci., 164, 221-232.
17. Leroux, S. J., Loreau, M., 2015, Theoretical perspectives on bottom-up and top-down interactions across ecosystems, 1st ed., Trophic ecology: Bottom-up and top-down interactions across aquatic and terrestrial systems, Cambridge Univ. Press, Cambridge, 3-27.
18. Liu, H., Dagg, M. J., Wu, C. J., Chiang, K. P., 2005, Mesozooplankton consumption of microplankton in the Mississippi River plume, with special emphasis on planktonic ciliates, Mar. Ecol. Prog. Ser., 286, 133-144.
19. McLusky, D. S., Elliott, M., 2004, The estuarine ecosystem: Ecology, threats and management, Oxford University Press, New York, 189.
20. McNaughton, C., Cook, P. L., Wong, W. W., Koster, W. M., Reich, P., Jenkins, G. P., Cartwright, I., Beardall, J., Woodland, R. J., 2022, Environmental flows stimulate estuarine plankton communities by altered salinity structure and enhanced nutrient recycling, Estuar. Coast. Shelf Sci., 279, 108157.
21. Ministry of Oceans and Fisheries, 2015, https://www.mof.go.kr.
22. Muylaert, K., Sabbe, K., Vyverman, W., 2009, Changes in phytoplankton diversity and community composition along the salinity gradient of the Schelde estuary (Belgium/The Netherlands), Estuar. Coast. Shelf Sci., 82, 335-340.
23. Nayar, S., Goh, B. P. L., Chou, L. M., 2005, Dynamics in the size structure of Skeletonema costatum (Greville) Cleve under conditions of reduced photosynthetically available radiation in a dredged tropical estuary, J. Exp. Mar. Biol. Ecol., 318, 163-182.
24. Park, S. J., Sin, Y. S., 2021, Artificial neural network (ANN) modeling analysis of algal blooms in an estuary with episodic and anthropogenic freshwater inputs, Appl. Sci., 11, 6921.
25. Park, S. J., Sin, Y. S., 2022, Characteristics of water quality and chlorophyll-a in the seawater zone of the Yeongsan River Estuary: Long-term (2009-2018) data analysis, Ocean. Polar Res., 44, 13-27.
26. Parsons, T. R., Maita, Y., Lalli, C. M., 1984, A Manual of chemical and biological methods for seawater analysis, Pergamon Press, Oxford, 187.
27. Paturej, E., Gutkowska, A., 2015, The effect of salinity levels on the structure of zooplankton communities, Arch. Biol. Sci., 67, 483-492.
28. Rabalais, N. N., Turner, R. E., Wiseman, Jr. W. J., 2002, Gulf of Mexico hypoxia, aka "The dead zone.", Annu. Rev. Ecol. Syst., 33, 235-263.
29. Reynolds, C. S., 2006, The ecology of phytoplankton, Cambridge University Press, Cambridge, 535.
30. Sakuma, M., Hanazato, T., Nakazato, R., Haga, H., 2002, Methods for quantitative sampling of epiphytic micro invertebrates in lake vegetation, Limnol., 3, 115-119.
31. Seo, D. I., Nam, G. S., Lee, S. H., Lee, E. H., Kim, M., Choi, J. Y., Kim, J. H., Chang, K. H., 2013, Plankton community in weir section of the Nakdong River and its relation with selected environmental factors, Korean J. Environ. Biol., 31, 362-369.
32. Sherman, E., Moore, J. K., Primeau, F., Tanouye, D., 2016, Temperature influence on phytoplankton community growth rates, Glob. Biogeochem. Cycles, 30, 550-559.
33. Shim, J. H., 1994, Illustrated encyclopedia of fauna & flora of Korea vol. 34, Marine phytoplankton, Ministry of Education, Seoul, Republic of Korea.
34. Silva, L. H., Huszar, V. L., Marinho, M. M., Rangel, L. M., Brasil, J., Domingues, C. D., Branco, C. C., Roland, F., 2014, Drivers of phytoplankton, bacterioplankton, and zooplankton carbon biomass in tropical hydroelectric reservoirs, Limnologica, 48, 1-10.
35. Sin, Y. S., Hyun, B. K., Jeong, B. K., Soh, H. Y., 2013, Impacts of eutrophic freshwater inputs on water quality and phytoplankton size structure in a temperate estuary altered by a sea dike, Mar. Environ. Res., 85, 54-63.
36. Sin, Y. S., Jeong, B. K., 2015, Short-term variations of phytoplankton communities in response to anthropogenic stressors in a highly altered temperate estuary, Estuar. Coast. Shelf Sci., 156, 83-91.
37. Sin, Y. S., Jeong, B. K., 2020, Anthropogenic disturbance of tidal variation in the water properties and phytoplankton community of an estuarine system, Estuaries and Coasts, 43, 547-559.
38. Sin, Y. S., Lee, E. J., Lee, Y. J., Shin, K. H., 2015, The river-estuarine continuum of nutrients and phytoplankton communities in an estuary physically divided by a sea dike, Estuar. Coast. Shelf Sci., 163, 279-289.
39. Sin, Y. S., Yu, H. S., 2018, Phytoplankton community and surrounding water conditions in the Youngsan River estuary: Weekly variation in the saltwater zone, Ocean. Polar Res., 40, 191-202.
40. Smirnov, N. N., Timms, B. V., 1983, A Revision of the Australian Cladocera (Crustacea), Records of Australian Museum Supplementary, The Australian Museum, Sydney, 132.
41. Thompson, P. A., Bonham, P. I., Swadling, K. M., 2008, Phytoplankton blooms in the Huon Estuary, Tasmania: Top-down or bottom-up control?, J. Plankton Res., 30, 735-753.
42. Winder, M., Jassby, A. D., 2011, Shifts in zooplankton community structure: Implications for food web processes in the upper San Francisco Estuary, Estuar. Coasts, 34, 675-690.
∙ Ph. D. Hee Se Kim

Department of Ocean System Engineering, Mokpo National Maritime Universitymks2328@naver.com

∙ M. S. Hee Gu Jo

Department of Ocean System Engineering, Mokpo National Maritime Universitycooky318@naver.com

∙ Professor. Yong Sik Sin

Department of Ocean System Engineering, Mokpo National Maritime Universityyongsik@mmu.ac.kr