High-latitude polar regions are more vulnerable to climate change than other regions. The Western Antarctic Peninsula (WAP) is the region experiencing the greatest warming in the world (Vaughan et al., 2003; Meredith and King, 2005; Turner et al., 2005), and the temperature has increased at an average rate of 0.5 degrees per decade in some locations in the WAP (Vaughan et al., 2003; Oliva et al., 2017). These changes include shifting patterns in wind speed and direction, reductions in sea ice and in the ice shelf, and glacial retreat (Cook et al., 2005, 2016; Marshall et al., 2006; Stammerjohn et al., 2008; Montes-Hugo et al., 2009; Rückamp et al., 2011; Rignot et al., 2013; Turner et al., 2013).

Antarctic coastal ecosystems in the WAP are sensitive to climate change in which major fluctuations occur in various gradients of nutrients, temperature, and salinity, including seasonal freshwater flux associated melts from glaciers and Upper Circumpolar Deep Water (UCDW) intrusions and sea ice extent changes (Prézelin et al., 2000; Martinson et al., 2008; Annett et al., 2015; Cook et al., 2016; Llanillo et al., 2019). These changes are directly linked to observed changes in coastal water ecosystems (Atkinson et al., 2004; Moline et al., 2004; Moon et al., 2015; Arrigo et al., 2017; Bae et al., 2021; Gutt et al., 2021).

In particular, phytoplankton is the base of the food web, play critical roles in biogeochemical cycles and eventually transfer energy up through the entire marine food chain (Clarke, 1988; Pauly and Christensen, 1995; Doney et al., 2012; Deppeler and Davidson, 2017). Their growth is greatly influenced by abiotic environmental factors, and increasing irradiance, anticyclones and nutrient supplies, along with environmental factors, are the main drivers of phytoplankton blooms in the coastal waters of Antarctica (Saba et al., 2014; Schloss et al., 2014). Phytoplankton blooms in seasonally ice-covered regions are initiated after sea ice melting (Jena et al., 2019; Jena and Pillai, 2020; Turner et al., 2020) and are composed of large phytoplankton cells (>20 μm, e.g., diatoms). High primary productivity (carbon uptake) and phytoplankton blooms mainly occur in summer (Fiala et al., 1998; Biggs et al., 2019) and represent an important part of the annual primary production and chlorophyll a concentration trends (Kang et al., 1997, 2002; Arrigo et al., 2008; Vernet et al., 2012; Lee et al., 2015). In this sense, distinct changes in the productivity and biomass of phytoplankton reflect shifts in environmental conditions.

Marian Cove represents one of the fastest glacial front retreat zones in the WAP (Rückamp et al., 2011) and contains marine biological hotspots in fjords; this region experiences ecosystem changes due to warming-induced glacial retreat and melt (Gutt et al., 2021). In this area, the mean retreat of the ice cliff was 480 m (up to 680 m) from December 1956 to January 1994 (Park et al., 1998), with an accelerating rate of retreat (1.7 km) observed during the last 51 years (1956–2006) (Lee et al., 2008). Recent studies have shown that benthic and bacterial community structures are associated with glacial melting areas (Moon et al., 2015; Ahn et al., 2016; Kim S. et al., 2020; Bae et al., 2021). Intense benthic diatom blooms, an indicator of glacial retreat, are linked to thriving filter-feeding consumers in Marian Cove (Ha et al., 2019). The temporal patterns of size-fractionated chl-a concentrations were by Kang et al. (1997, 2002) and Lee et al. (2015) based on long-term monitoring at a fixed coastal site near King Sejong Station. However, the carbon uptake rate of phytoplankton has rarely been reported in previous studies. Therefore, research on phytoplankton developmental processes in Marian Cove and on the carbon dynamics of phytoplankton was undertaken to better understand the ecosystem structure and functioning. The aims of this study were (1) to examine the temporal and spatial variations in the carbon uptake rates of phytoplankton as phytoplankton succession occurred during summer (January–February 2019) in Marian Cove and (2) to investigate the mechanisms controlling the carbon dynamics that are related to environmental conditions.

The inner cove exhibited low temperatures, low salinities and high water stability, while the outer cove exhibited relatively high temperatures, high salinities and low water stability. Hydrographic changes between Maxwell Bay and Marian Cove occur due to tidal mechanisms, strong estuarine circulation, and winds over the mouth of the cove and the inner sill (c. 70 m deep) (Yoo et al., 1999, 2015; Llanillo et al., 2019). In Marian Cove, the mean tidal amplitude is 1.5 m, with the amplitude reaching up to 2.8 m (Yoon et al., 1998), and the tidal variability in salinity is higher than that of Maxwell Bay or Collins Bay (Llanillo et al., 2019). At the beginning of the investigation (on 14 January), observations of relatively cold temperatures (∼0.3°C) with fresh (<34) surface waters were most pronounced at the innermost cove close to the glacial front in our study. As the austral summer progressed, the overlying freshwater in the upper 20 m spread throughout the cove, and the water column was warmer in February than at the beginning of the study period (January). This feature is probably explained by the tides, winds, and freshwater from meltwater and precipitation and by the inward motion of warm modified upper circumpolar deep water (m-UCDW) during summer. However, this study is based on the assumption that the effects of tides and wind were negligible because sampling was performed under similar conditions (flood tides and west-northwest wind directions) (Supplementary Figure 1). Meltwater discharged from sea ice and precipitation was also not strongly affected by hydrography in our study since neither sea ice nor strong precipitation events were observed during the survey (Supplementary Figure 1). Hence, in the inner cove, freshwater inputs are sourced from glacial meltwater or stream discharge, causing significant freshening and further stabilizing the waters and creating a low-salinity water layer.

Our data suggest that the cove was influenced by glaciers, showing distinct primary productivity, phytoplankton biomass, light regime, and hydrographic conditions, as mentioned above. Antarctic continental shelf zone waters contribute to high productivity, with an average of 4.6 g C m^–2 day^–1 (Arrigo et al., 2008). Even though the spatiotemporal distribution patterns differed slightly throughout the cove, the coastal regions are more productive, reaching a maximum of 3.2 g C m^–2 day^–1 in the Gerlache Strait (Serret et al., 2001), 6.9 g C m^–2 day^–1 in Marguerite Bay (Rozema et al., 2017), and 8.8 g C m^–2 day^–1 in South Bay (Höfer et al., 2019). These results indicate that high primary productivity is one of the major characteristics of more stratified water columns primarily via freshwater input from sea ice melt and coastal glaciers. Studies on the carbon uptake rates of phytoplankton have also been conducted in some waters of King George Island (Yang, 1990; Aracena et al., 2018; Höfer et al., 2019). In the present study, the depth-integrated daily carbon uptake rates showed a wide range of variation (ranging from 0.01 to 4.52 g C m^–2 day^–1) during the investigation period that was within the range recorded in the abovementioned studies. Our measured mean daily carbon uptake rate was 0.80 g C m^–2 day^–1 (SD = ± 1.53 g C m^–2 day^–1), which was ∼5 times higher than the observation-based estimates at one point station in Marian Cove (0.14 g m^–2 day^–1; Yang, 1990) but was similar to that measured in the WAP (0.74 g C m^–2 day^–1; Vernet et al., 2008). These carbon uptake change trends were very similar to those of chl-a, suggesting that the carbon uptake rate primarily depended on the quantity of phytoplankton biomass.

The high chl-a concentrations, jointly with the high microphytoplankton and consumption of DSi, as well as the high primary production, suggest that a bloom event occurred during the 14 January sampling in Marian Cove. The maximum chl-a concentration (19.5 mg m^–3) obtained in the present study was similar to that measured by Höfer et al. (2019) (>15 mg m^–3) in Maxwell Bay. Summer chl-a concentrations typically exceed 20 mg m^–3 (up to 25 mg m^–3), with yearly variations in chl-a and a peak observed in January in Ryder Bay, northern Marguerite Bay, Antarctica (Clarke et al., 2008). These are intense blooms, and the peak total chl-a values measured during the observation period fit well with those observed in nearshore waters off Antarctica (Mitchell and Holm-Hansen, 1991; Clarke and Leakey, 1996; Vernet et al., 2008). In the present study, the samples were composed mainly of large diatoms (>20 μm, Thalassiosira spp.; >50%) during the bloom. This is consistent with previous reports of summer phytoplankton blooms, and large diatoms and colonial forms are typical for coastal waters elsewhere in Antarctica (Clarke et al., 2008; Biggs et al., 2019; Mangoni et al., 2019). The seasonal patterns of phytoplankton biomass and productivity are closely dependent on changes in sea ice, sea surface temperature, and inflow of UCDW (Kavanaugh et al., 2015; Biggs et al., 2019). In particular, the initial interleaving of m-UCDW into Maxwell Bay adjacent to Marian Cove leads to increases in the temperature, salinity and density of subsurface waters (Llanillo et al., 2019). In Marian Cove, phytoplankton biomass generally began in late November and peaked around January, when the water temperature was the warmest for an on-record year (Lee et al., 2015). Hence, our summer bloom was probably initiated by an inflow of relatively warmer water from Maxwell Bay as a means of controlling growth and stimulating phytoplankton biomass accumulation. The evidence showed that production maxima (4.52 g C m^–2 day^–1) and chl-a accumulation (174.1 mg chl-a m^–2) were high on 14 January at MC3, near the mouth of cove.

Following the bloom, the direct input of SPM occurred along with glacial meltwater and streams entering the surface; consequently, summer production was limited by turbidity and water stability. Even when comparing the specific uptake rate (h^–1), it showed a similar trend to the absolute suptake rate, suggesting that it was not only due to the difference in biomass of phytoplankton. Nutrients have an important influence on the growth of phytoplankton and are generally not limited, while there is evidence that trace metals affect production in Antarctic coastal waters more than in the open ocean (Sañudo-Wilhelmy et al., 2002). Direct measurements of nutrient concentrations (DIN, DIP, and DSi) and dissolved iron in ice or snow show that these concentrations are much lower and higher than those in seawater, respectively (Kim et al., 2015). However, in Marian Cove, major nutrients (such as DIN, DIP, and DSi) are not limiting factors for phytoplankton productivity or biomass during summer (Yang, 1990; Lee et al., 2015). Temporally, the DSi values, measured with large concentration differences between peaks and between 31 January (t-test: t = −23.1, p < 0.01) and 8 February (t-test: t = −11.5, p < 0.01), were relatively lower during intense blooms regardless of the sampling station. It was suggested that the DSi concentration is important for the growth of diatoms and that DSi is directly used by microsized phytoplankton (mainly diatoms) (Weber and Deutsch, 2010). This confirms that the comparison of nutrients between the inner cove and outer cove did not show a significant difference in our study. Therefore, in our results, the lower carbon uptake rates in the region near the glacier were not more severely affected by the additional inputs of trace metals and nutrients.

Concomitant with meltwater inputs, SPM in surface waters strongly impacts the light regime. In addition to the stability of the water column, phytoplankton entering shallow mixed layers with higher light intensities serve to enhance phytoplankton biomass and production (Mitchell and Holm-Hansen, 1991; Schloss et al., 2002); however, SPM inputs during summer could have negative effects by attenuating light penetration (Yang, 1990; Schloss et al., 2002; Kim et al., 2018). The dispersal patterns of SPM were previously reported in Marian Cove by Yoon et al. (1998), Yoo et al. (1999), and Yoo et al. (2003). These authors concluded that surface plumes (cold, freshened, and highly turbid water in the upper 2 m) result from either supraglacial discharge by meltwater streams along the coast or by waterfalls off ice cliffs. They pointed out that this discrepancy is greater in areas characterized by high levels of SPM (>28 g m^–3) occurring on the northern side of Marian Cove. In the present study, it was also shown that the SPM concentrations measured during summer led to marked spatial variations in light penetration, and these variations increased with distance to the glacier. The freshening of the surface waters coincided with high turbidity-low productivity conditions, suggesting limited light availability for phytoplankton. Because the high turbidity resulting from the high suspended material in meltwater hinders light penetration into the water, enhanced stratification also permits phytoplankton to remain within unfavorable conditions, preventing deeper mixing. It was confirmed that the comparison between the inner and outer parts of the cove in the euphotic depth, which has an important influence on the carbon uptake rates of phytoplankton, was generally low in the inner cove area. This is consistent with a previous report of summer phytoplankton in Marian Cove, in which low chl-a content and low primary productivity indebted mostly to nanophytoplankton were observed at shallow euphotic depths caused by suspended solids resulting from strong winds and ice-carried debris (Yang, 1990). The turbid water released by glacial melt and riverine discharge, can restrict phytoplankton growth, even though promoting phytoplankton growth by enhanced water column stability (Schloss et al., 2002; Kim et al., 2018). This fact suggested that reduction of light penetration into water column by high load of particulate matter can control phytoplankton bloom development in shallow coastal area (Schloss et al., 2002). Large phytoplankton blooms (dominated by diatoms) are closely dependent on light availability and the ability of phytoplankton to adapt and photosynthesize at higher light levels (Vernet et al., 2008). Smaller cells more efficiently utilize light than larger cells in light-limited conditions since they are less affected by the package effect (Kirk, 1994; Finkel, 2001). For this reason, theoretically, there is a tendency that smaller cells with greater photosynthetic efficiency can thrive under conditions of high turbidity and low light. In addition, motile flagellate is able to move, exploit different light regimes, and select for optimal light (Klais et al., 2016; Roselli et al., 2017). Likewise, phytoplankton communities showing changes in their community and cell size composition (unidentified nanophytoplankton and flagellate) were more pronounced close to the glacial front in our study. This process was suggested to be a strategic response to low light availability that gives the nanophytoplankton and flagellate (e.g., Cryptomonas sp.) a competitive advantage over microphytoplankton (diatom). Therefore, our findings provide insight that the increases in particulate matter caused by freshwater inputs determine light availability, which in turn may serve as mechanisms to control phytoplankton production, biomass accumulation and community dynamics.

The average primary production rates in Marian Cove varied by two orders of magnitude, from 0.01 to 4.52 g C m^–2 day^–1. The spatiotemporal patterns of summer phytoplankton biomass and productivity are associated with increased meltwater from glaciers and/or streams in this area. Freshwater discharges into the surface waters, increasing water column stability. The deepening of the average euphotic depth toward the slope establishes an inner-outer gradient in average productivity. In contrast, the role of nutrients cannot be clearly observed. The high variabilities in productivity and biomass reflect higher inputs of SPM loads that drive strong gradients in light availability. Thus, phytoplankton is more exposed to unfavorable light conditions, which leads to the development of smaller cells, including unidentified spp. (nanophytoplankton) and flagellate species.

The freshening of surface water has resulted in increased glacial melt, showing a shift in the size distribution of phytoplankton from diatom-dominated assemblages to cryptophytes and small flagellates in the WAP (Moline et al., 2004) and influencing changes in krill recruitment, abundance and availability to predators (Moline et al., 2004; Ducklow et al., 2017). To date, specific studies on zooplankton abundance have not been conducted in Marian Cove. Instead, in Potter Cove, a tributary basin adjacent to Marian Cove, microsized diatom blooms (> 15 mg m^–3) directly affect the large copepod abundances under cold conditions (preventing glacial melting), and nanophytoplankton and microzooplankton (aloricate ciliates and dinoflagellates) have been observed after blooms and coincide with intense glacial melting (Garcia et al., 2016).

As the WAP continues to warm, the open-water season is expected to become increasingly longer, and the glacial front is expected to retreat further. New areas of open water may be created in Marian Cove, stimulating phytoplankton blooms and increasing productivity in previously ice-related habitats. However, the high particle concentrations observed on the surface in this study highlighted interesting linkages regarding the effects of meltwater discharge and particle dynamics on primary production and phytoplankton composition in shallow coastal area; these relationships warrant further studies.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.

S-YH conceived of the study, participated in its design and helped to draft the manuscript. BK drafted the manuscript and performed the field and laboratory experiments. MJ and HJ carried out the analysis of the chl-a and phytoplankton community. T-WK processed the CTD data. S-JP provided meteorological data. JP was the leader of the Korean Antarctic Research Program and provided scientific advice. All authors have read and agreed to the published version of the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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