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<front>
<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Mar. Sci.</journal-id>
<journal-title>Frontiers in Marine Science</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Mar. Sci.</abbrev-journal-title>
<issn pub-type="epub">2296-7745</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="doi">10.3389/fmars.2022.887909</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Marine Science</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Variability in the Carbon and Nitrogen Uptake Rates of Phytoplankton Associated With Wind Speed and Direction in the Marian Cove, Antarctica</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Kim</surname>
<given-names>Bo Kyung</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/593112"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Jeon</surname>
<given-names>Misa</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Park</surname>
<given-names>Sang-Jong</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kim</surname> <given-names>Hyun-Cheol</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Min</surname>
<given-names>Jun-Oh</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Park</surname>
<given-names>Jisoo</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1207365"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Ha</surname>
<given-names>Sun-Yong</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn001">
<sup>*</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/519459"/>
</contrib>
</contrib-group>
<aff id="aff1">
<sup>1</sup>
<institution>Division of Ocean Sciences, Korea Polar Research Institute</institution>, <addr-line>Incheon</addr-line>, <country>South Korea</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>Division of Atmospheric Sciences, Korea Polar Research Institute</institution>, <addr-line>Incheon</addr-line>, <country>South Korea</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>Center of Remote Sensing and Geographic Information System, Korea Polar Research Institute</institution>, <addr-line>Incheon</addr-line>, <country>South Korea</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>Edited by: Mi Sun Yun, Tianjin University of Science and Technology, China</p>
</fn>
<fn fn-type="edited-by">
<p>Reviewed by: Ya-Wei Luo, Xiamen University, China; Andrew Mcminn, University of Tasmania, Australia</p>
</fn>
<fn fn-type="corresp" id="fn001">
<p>*Correspondence: Sun-Yong Ha, <email xlink:href="mailto:syha@kopri.re.kr">syha@kopri.re.kr</email>
</p>
</fn>
<fn fn-type="other" id="fn002">
<p>This article was submitted to Aquatic Microbiology, a section of the journal Frontiers in Marine Science</p>
</fn>
</author-notes>
<pub-date pub-type="epub">
<day>25</day>
<month>07</month>
<year>2022</year>
</pub-date>
<pub-date pub-type="collection">
<year>2022</year>
</pub-date>
<volume>9</volume>
<elocation-id>887909</elocation-id>
<history>
<date date-type="received">
<day>02</day>
<month>03</month>
<year>2022</year>
</date>
<date date-type="accepted">
<day>16</day>
<month>06</month>
<year>2022</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2022 Kim, Jeon, Park, Kim, Min, Park and Ha</copyright-statement>
<copyright-year>2022</copyright-year>
<copyright-holder>Kim, Jeon, Park, Kim, Min, Park and Ha</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>Quantifying the temporal variability in phytoplankton productivity is essential for improving our understanding of carbon (C) and nitrogen (N) dynamics and energy flows in natural aquatic ecosystems. Samples were collected at three-day intervals from December 2018 to January 2019 from fixed station in Marian Cove, Antarctica to determine the C and N (NO<sub>3</sub>
<sup>-</sup> and NH<sub>4</sub>
<sup>+</sup>) uptake by phytoplankton. Considerable fluctuations in the total C and N productivities were observed, which led to dynamic changes in the phytoplankton communities and a stronger coupling between the phytoplankton biomass. The increased rate of NO<sub>3</sub>
<sup>-</sup> uptake coincided with an enhanced C uptake mainly by microphytoplankton (&gt;20 &#xb5;m), followed by an increase in NH<sub>4</sub>
<sup>+</sup> uptake towards the end of sampling period. However, the &lt;2 &#xb5;m fraction (picophytoplankton) showed little variation in C and NO<sub>3</sub>
<sup>-</sup> uptake, and the proportions of assimilated NH<sub>4</sub>
<sup>+</sup> contributed to more than half of the total assimilated inorganic N. The increased NH<sub>4</sub>
<sup>+</sup> did not increase the total phytoplankton biomass and C production. Interestingly, after January 9 (maximum chlorophyll a, C, and N uptake) there was a shift to a predominantly easterly wind (&gt;6&#xa0;m s<sup>-1</sup>), which rapidly decreased the total chl-a, C and N uptake rate to ~4% of the highest values (0.6 mg m<sup>-3</sup>, 1.0 mg C m<sup>-3</sup> h<sup>-1</sup>, 0.1 mg N m<sup>-3</sup> h<sup>-1</sup>, respectively) on January 12. The phytoplankton community was also replaced by neritic and ice-related species. These findings suggest that strong temporal shifts in phytoplankton C and N assimilation are strongly influenced by external forces (wind stress).</p>
</abstract>
<kwd-group>
<kwd>phytoplankton</kwd>
<kwd>carbon</kwd>
<kwd>nitrogen</kwd>
<kwd>stable isotope</kwd>
<kwd>Marian Cove</kwd>
<kwd>Antarctica</kwd>
</kwd-group>
<counts>
<fig-count count="5"/>
<table-count count="1"/>
<equation-count count="1"/>
<ref-count count="87"/>
<page-count count="14"/>
<word-count count="6913"/>
</counts>
</article-meta>
</front>
<body>
<sec id="s1" sec-type="intro">
<title>Introduction</title>
<p>The Southern Ocean plays a critical role in Earth&#x2019;s carbon cycle as a significant carbon sink, accounting for ~43% of the total oceanic inventory of anthropogenic CO<sub>2</sub> south of 30&#xb0; S (<xref ref-type="bibr" rid="B27">Fr&#xf6;licher et al., 2015</xref>). This is a region of seasonal extremes, with large fluctuations in phytoplankton productivity. Coastal Antarctic is considered to have high productivity, with large summer blooms phytoplankton representing the most important annual input to pelagic food webs (<xref ref-type="bibr" rid="B38">Kang et al., 1997</xref>; <xref ref-type="bibr" rid="B26">Fiala et al., 1998</xref>; <xref ref-type="bibr" rid="B40">Kang et al., 2002</xref>; <xref ref-type="bibr" rid="B5">Arrigo et al., 2008</xref>; <xref ref-type="bibr" rid="B81">Vernet et al., 2012</xref>; <xref ref-type="bibr" rid="B8">Biggs et al., 2019</xref>).</p>
<p>Phytoplankton bloom dynamics in coastal Antarctic waters are governed by irradiance, temperature, stratification, anticyclones, and nutrient supply (<xref ref-type="bibr" rid="B72">Saba et al., 2014</xref>; <xref ref-type="bibr" rid="B74">Schloss et al., 2014</xref>; <xref ref-type="bibr" rid="B34">H&#xf6;fer et al., 2019</xref>, and references therein). They consists of a series of sequential blooms of different phytoplankton species and sizes that utilize different forms of dissolved inorganic N (DIN) for optimal growth, depending on the ambient nutrient concentration and cell phases. Usually, high primary productivity (C uptake) phytoplankton blooms are seasonal in ice-covered regions and occur after sea ice melts. These blooms are composed of large phytoplankton cells (&gt;20 &#xb5;m, e.g., diatoms) that utilize nitrate (NO<sub>3</sub>
<sup>-</sup>; so-called &#x201c;new&#x201d;) as their nitrogen (N) source. Smaller cells and haptophytes, which use regenerated forms of N compounds, e.g., ammonium (NH<sub>4</sub>
<sup>+</sup>) to sustain growth, become important under post-bloom conditions (<xref ref-type="bibr" rid="B22">Dugdale and Goering, 1967</xref>; <xref ref-type="bibr" rid="B37">Kanda et al., 1990</xref>; <xref ref-type="bibr" rid="B46">Kristiansen et al., 1994</xref>; <xref ref-type="bibr" rid="B9">Bode et al., 2002</xref>; <xref ref-type="bibr" rid="B13">Clarke et al., 2008</xref>). Therefore, changes in the productivity and size classes of marine phytoplankton reflect environmental conditions and affect the flow of dietary energy from lower to upper trophic levels.</p>
<p>The coastal ecosystems of Antarctica on the western Antarctic Peninsula (WAP), where significant changes in sea ice and terrestrial ice sheet dynamics, temperature, nutrients, and salinity have been observed, are more vulnerable to climate change than other regions (<xref ref-type="bibr" rid="B68">Pr&#xe9;zelin et al., 2000</xref>; <xref ref-type="bibr" rid="B15">Cook et al., 2005</xref>; <xref ref-type="bibr" rid="B52">Martinson et al., 2008</xref>; <xref ref-type="bibr" rid="B76">Stammerjohn et al., 2008</xref>; <xref ref-type="bibr" rid="B3">Annett et al., 2015</xref>; <xref ref-type="bibr" rid="B16">Cook et al., 2016</xref>; <xref ref-type="bibr" rid="B50">Llanillo et al., 2019</xref>). These changes are directly linked to observed changes in coastal ecosystems (<xref ref-type="bibr" rid="B6">Atkinson et al., 2004</xref>; <xref ref-type="bibr" rid="B54">Moline et al., 2004</xref>; <xref ref-type="bibr" rid="B57">Moon et al., 2015</xref>; <xref ref-type="bibr" rid="B4">Arrigo et al., 2017</xref>; <xref ref-type="bibr" rid="B34">H&#xf6;fer et al., 2019</xref>; <xref ref-type="bibr" rid="B67">Plum et al., 2020</xref>; <xref ref-type="bibr" rid="B31">Gutt et al., 2021</xref>). In particular, Marian Cove is one of the fastest glacier retreat fronts in the WAP (<xref ref-type="bibr" rid="B71">R&#xfc;ckamp et al., 2011</xref>), and is a marine biological hotspot, as it is a fjord experiencing ecosystem changes due to global warming-induced glacier retreat and ice-melt (<xref ref-type="bibr" rid="B31">Gutt et al., 2021</xref>). Most studies in the area have focused primarily on benthic genera and bacterial community structures (<xref ref-type="bibr" rid="B57">Moon et al., 2015</xref>; <xref ref-type="bibr" rid="B2">Ahn et al., 2016</xref>; <xref ref-type="bibr" rid="B32">Ha et al., 2019</xref>; <xref ref-type="bibr" rid="B43">Kim et al., 2020</xref>; <xref ref-type="bibr" rid="B7">Bae et al., 2021</xref>), with numerous studies dealing with phytoplankton in the Marian Cove (<xref ref-type="bibr" rid="B38">Kang et al., 1997</xref>; <xref ref-type="bibr" rid="B40">Kang et al., 2002</xref>; <xref ref-type="bibr" rid="B49">Lee et al., 2015</xref>). However, limited phytoplankton productivity data are available from the same area (<xref ref-type="bibr" rid="B83">Yang, 1990</xref>; <xref ref-type="bibr" rid="B41">Kim et al., 2021</xref>). Studies on <sup>15</sup>N-based uptake of phytoplankton have not been conducted in the Marian Cove till date. Therefore, the temporal pattern of phytoplankton succession in the Marian Cove, as influenced by their C and N uptake dynamics were undertaken to better understand the ecosystem structures and functions. The aim of this study was to describe the temporal variations in the C and N (new and regenerated) uptake rates of phytoplankton and associated chlorophyll a (chl-a) during summertime in the Marian Cove. The present study also constitutes the first measurement of <italic>in-situ</italic> N productivity in the study area and mainly focuses on the mechanisms controlling C and N dynamics related to environmental conditions.</p>
</sec>
<sec id="s2" sec-type="materials|methods">
<title>Materials and Methods</title>
<sec id="s2_1">
<title>Study Site and Field Sampling</title>
<p>The Marian Cove is 4.5&#xa0;km long, 1.5&#xa0;km wide, ~110 m deep, and is located in the Maxwell Bay, southwest of the King George Island, WAP. The area has experienced ~1.7 km of glacial retreat for 50 years (<xref ref-type="bibr" rid="B62">Park et al., 1998</xref>; <xref ref-type="bibr" rid="B48">Lee et al., 2008</xref>; <xref ref-type="bibr" rid="B71">R&#xfc;ckamp et al., 2011</xref>). Recent (1956&#x2013;1957 and 2020&#x2013;2021) glacier retreat velocity was ~27.2 m/yr in the Marian Cove (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). The phytoplankton biomass (chl-a) in the area started to increase from October to November peaking (i.e., a &#x201c;bloom&#x201d;) around January, whereas the lowest values occurred during winter (June&#x2013;August) (<xref ref-type="bibr" rid="B40">Kang et al., 2002</xref>; <xref ref-type="bibr" rid="B49">Lee et al., 2015</xref>; <xref ref-type="bibr" rid="B35">Jeon et al., 2021</xref>). Marian Cove is characterized by intense summer blooms with high primary production in January (<xref ref-type="bibr" rid="B41">Kim et al., 2021</xref>). The general pattern of seasonal phytoplankton succession is that diatoms (&gt;20 &#xb5;m) dominate in summer and, pico- and nanophytoplanktons (&lt;20 &#xb5;m) dominate in winter (<xref ref-type="bibr" rid="B38">Kang et al., 1997</xref>; <xref ref-type="bibr" rid="B40">Kang et al., 2002</xref>; <xref ref-type="bibr" rid="B49">Lee et al., 2015</xref>; <xref ref-type="bibr" rid="B35">Jeon et al., 2021</xref>).</p>
<fig id="f1" position="float">
<label>Figure&#xa0;1</label>
<caption>
<p>Map showing the location of the <bold>(A)</bold> South Shetland Islands, <bold>(B)</bold> King George Island, and <bold>(C)</bold> Marian Cove. Glacier termini overlaid on remote sensing images and aerial photographs acquired in 1956-2021. The maps <bold>(A</bold>, <bold>B)</bold> were generated by using Ocean Data View v. 5.3.0 (<uri xlink:href="https://odv.awi.de">https://odv.awi.de</uri>) (AWI, Bremerhaven, Germany, Schlitzer, R.).</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-09-887909-g001.tif"/>
</fig>
<p>The study site was conducted from a fixed-point coastal monitoring site for marine ecosystem near King Sejong Station (62&#xb0;13&#x2019; S, 58&#xb0;47&#x2019; W; KSS), Korea (<xref ref-type="fig" rid="f1">
<bold>Figure&#xa0;1</bold>
</xref>). Experiments for C and N uptake by phytoplankton were conducted from December 19, 2018, to January 26, 2019, and results were compared with the environmental parameters (water temperature, salinity, chl-a, nutrients, and phytoplankton taxonomy). The water depth at the site is between 5 and 10&#xa0;m, and is vertically well-mixed owing to wind- and tide-induced currents (<xref ref-type="bibr" rid="B49">Lee et al., 2015</xref> and references therein). Surface water samples were collected every third day around solar noon at a depth of 0.5&#xa0;m using a sampler. Average three&#x2013;hour meteorological data (wind speed and wind direction) were collected during the sampling period from the automatic meteorological observation system (AMOS-3) of the KSS. The wind vane was located 10&#xa0;m above ground (<xref ref-type="bibr" rid="B63">Park et al., 2013</xref>). Ten-minute interval data were averaged into hourly and daily data.</p>
</sec>
<sec id="s2_2">
<title>Surface Seawater Temperature, Salinity, Macronutrient, and Chl-a Analyses</title>
<p>Water temperature and salinity were measured using a YSI Model 30 (Yellow Springs Inc. Ohio, USA). For dissolved inorganic nutrient (NO<sub>2</sub>
<sup>-</sup> + NO<sub>3</sub>
<sup>-</sup>, NH<sub>4</sub>
<sup>+</sup>, PO<sub>4</sub>
<sup>3-</sup>, and SiO<sub>2</sub>) concentrations, the seawater was filtered through GF/F filters (pre-combusted at 450&#xb0;C for 4&#xa0;h, nominal 0.7 &#xb5;m, Whatman, UK). The filtered seawater samples were preserved at approximately -20&#xb0;C until analysis. Major inorganic nutrients were measured using a 4-channel continuous autoanalyzer (QuAAtro, SEAL Analytical, UK), according to the manufacturer&#x2019;s instructions. Standard curves were run for each sample batch using freshly prepared standards with concentrations in the range of that of the samples. For total chl-a analysis, seawater was filtered through GF/F filters (pre-combusted at 450&#xb0;C for 4&#xa0;h). For size-fractionated chl-a analysis, water was passed sequentially through a nucleopore membrane filter (20 &#xb5;m and 2 &#xb5;m) and GF/F filters. All filters were extracted overnight with 90% acetone, and the extracts were analyzed using a fluorometer (Trilogy, Turner Designs, Sunnyvale, CA, USA) (<xref ref-type="bibr" rid="B64">Parsons et al., 1984</xref>).</p>
</sec>
<sec id="s2_3">
<title>Experiments for Carbon and Nitrogen Uptake Rate</title>
<p>The sampled seawater was prefiltered through a 200 &#xb5;m mesh to remove zooplankton. <sup>13</sup>C-labeled sodium bicarbonate (Cambridge Isotope Laboratories, USA), <sup>15</sup>N-labeled potassium nitrate and sodium ammonium (Sigma&#x2013;Aldrich, USA) were added to the surface water samples in 1 L polycarbonate bottles. The <sup>13</sup>C and <sup>15</sup>N levels were ~4&#x2013;20% of the total dissolved inorganic C and ambient nitrogenous nutrient concentrations. The bottles were incubated for 4&#x2013;5 h in ambient seawater. The incubated seawater was filtered (0.3 L) through 450&#xb0;C pre-combusted GF/F filters (25&#xa0;mm). A fraction of the picophytoplankton and water passed through 2 &#x3bc;m nucleopore filters (47&#xa0;mm) and the filtrate was passed through GF/F filters (25&#xa0;mm). The filters were immediately stored at -80&#xb0;C until further analysis. The C and N (nitrate and ammonium) uptake rates of the phytoplankton were measured according to the protocol described by <xref ref-type="bibr" rid="B41">Kim et al. (2021)</xref>. The samples were placed overnight in an acid fume to remove carbonates. C and N isotope abundances were determined using Elemental Analysis (Euro EA3028, EuroVector, Milan, Italy) - Isotope Ratio Mass Spectrometry (Isoprime 100, EIementar, Manchester, UK) in a stable isotope laboratory at Hanyang University, Korea. Carbonate alkalinity of the water sample was determined by titration with 0.01&#xa0;N HCl, and the total CO<sub>2</sub> content was calculated according to the method of <xref ref-type="bibr" rid="B64">Parson et al. (1984)</xref>. The C or N uptake rates (mg C (or N) m<sup>-3</sup> h<sup>-1</sup>) of phytoplankton were calculated based on <xref ref-type="bibr" rid="B33">Hama et al. (1983)</xref> and <xref ref-type="bibr" rid="B22">Dugdale and Goering (1967)</xref>, respectively, using the following formula (1):</p>
<disp-formula>
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<mml:mrow>
<mml:mo>(</mml:mo>
<mml:mi>t</mml:mi>
<mml:mo>)</mml:mo>
</mml:mrow>
</mml:mrow>
<mml:mi>t</mml:mi>
</mml:mfrac>
</mml:mtd>
</mml:mtr>
</mml:mtable>
</mml:math>
</disp-formula>
<p>where <italic>&#x394;POC</italic>(<italic>orPON</italic>)(<italic>t</italic>) is the increase in particulate organic C or N concentration during incubation (mg C (or N) m<sup>-3</sup>), respectively, t is the incubation time, <italic>a<sub>is</sub>
</italic> is the atomic % of <sup>13</sup>C (or <sup>15</sup>N) in the incubated sample, <italic>a<sub>ns</sub>
</italic> , is the atomic % of <sup>13</sup>C (or <sup>15</sup>N) in the natural sample, <italic>a<sub>ic</sub>
</italic> is the atomic % of <sup>13</sup>C (or <sup>15</sup>N) in the total inorganic C (or N). The specific uptake rate can be defined as the rate of uptake or transport of the product (h<sup>-1</sup>). Unlike the C uptake samples (duplicates), single samples were analyzed for the N uptake rates.</p>
</sec>
<sec id="s2_4">
<title>Data Analysis</title>
<p>Pearson&#x2019;s correlation was used to investigate the relationship between environmental variables and C and N uptake rates. In this study, we estimated the time series of temporally cumulative zonal wind stress (&#x3c4;<sub>x,</sub> in N m<sup>-2</sup>) from December 19, 2018 to January 26, 2019, to identify cumulative force exerted on the surface. The cumulative zonal wind stress at a particular time is calculated as the sum of the wind stresses over the previous days (1-day to 5-day in this study). Positive and negative values indicate eastward and westward wind stress, respectively.</p>
</sec>
</sec>
<sec id="s3" sec-type="results">
<title>Results</title>
<sec id="s3_1">
<title>Temporal Patterns of Temperature, Salinity, Chl-a, and Inorganic Macronutrients</title>
<p>The surface water temperature at the sampling site in the Marian Cove was the highest (2.2&#xb0;C) and lowest (0.3&#xb0;C) on December 19, 2018 and January 26, 2019, respectively (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2A</bold>
</xref>). With the exception of a few days (&#x2264;0.6&#xb0;C) in December to January, most recorded temperatures were above &gt;1&#xb0;C. The surface salinity ranged from 29.6 to 34.5. Salinity was stable throughout the study period, except a low salinity period in January 12&#x2013;20. Salinity was positively correlated with the water temperature (r = 0.615, p&lt; 0.05; <xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>).</p>
<fig id="f2" position="float">
<label>Figure&#xa0;2</label>
<caption>
<p>Temporal variability of <bold>(A)</bold> water temperature and salinity, <bold>(B)</bold> total chlorophyll a concentration and percentage contribution of size-fractionated chlorophyll a, concentration of <bold>(C)</bold> NO<sub>x</sub> (NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup>) and SiO<sub>2,</sub>
<bold>(D)</bold> PO<sub>4</sub>
<sup>3-</sup> and NH<sub>4</sub>
<sup>+</sup>, <bold>(E)</bold> molar ratio of N:P and N:Si at surface water during sampling period.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-09-887909-g002.tif"/>
</fig>
<table-wrap id="T1" position="float">
<label>Table&#xa0;1</label>
<caption>
<p>Pearson correlation coefficients between the environmental parameters on productivity.</p>
</caption> 
<table frame="hsides">
<thead>
<tr>
<th valign="top" align="center">
</th>
<th valign="top" align="center">Temp</th>
<th valign="top" align="center">Sal</th>
<th valign="top" align="center">Chl</th>
<th valign="top" align="center">T_C</th>
<th valign="top" align="center">Sp_T_C</th>
<th valign="top" align="center">P_C</th>
<th valign="top" align="center">Sp_P_C</th>
<th valign="top" align="center">T_Ni</th>
<th valign="top" align="center">T_Am</th>
<th valign="top" align="center">P_Ni</th>
<th valign="top" align="center">P_Am</th>
<th valign="top" align="center">NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup>
</th>
<th valign="top" align="center">NH<sub>4</sub>
<sup>+</sup>
</th>
<th valign="top" align="center">PO<sub>4</sub>
<sup>3-</sup>
</th>
<th valign="top" align="center">SiO<sub>2</sub>
</th>
<th valign="top" align="center">DIN</th>
<th valign="top" align="center">Micro</th>
<th valign="top" align="center">Nano</th>
<th valign="top" align="center">Pico</th>
</tr>
</thead>
<tbody>
<tr>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Temp</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Sal</td>
<td valign="top" align="left">0.615*</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Chl</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">T_C</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.973**</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Sp_T_C</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.859**</td>
<td valign="top" align="left">0.930**</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">P_C</td>
<td valign="top" align="left">0.769**</td>
<td valign="top" align="left">0.623*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Sp_P_C</td>
<td valign="top" align="left">0.748**</td>
<td valign="top" align="left">0.640*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.957**</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">T_Ni</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.939**</td>
<td valign="top" align="left">0.987**</td>
<td valign="top" align="left">0.943**</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">T_Am</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.880**</td>
<td valign="top" align="left">0.923**</td>
<td valign="top" align="left">0.905**</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.927**</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">P_Ni</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">P_Am</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.836**</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">NH<sub>4</sub>
<sup>+</sup>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.567*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">PO<sub>4</sub>
<sup>3-</sup>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.586*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.929**</td>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">SiO<sub>2</sub>
</td>
<td valign="top" align="left"/>
<td valign="top" align="left">0.746**</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.577*</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">DIN</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.616*</td>
<td valign="top" align="left">-0.595*</td>
<td valign="top" align="left">-0.601*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.982**</td>
<td valign="top" align="left"/>
<td valign="top" align="left">0.938**</td>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Micro</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.748**</td>
<td valign="top" align="left">0.771**</td>
<td valign="top" align="left">0.831**</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.784**</td>
<td valign="top" align="left">0.688**</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.553*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Nano</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.678*</td>
<td valign="top" align="left">-0.672*</td>
<td valign="top" align="left">-0.693**</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.684**</td>
<td valign="top" align="left">-0.605*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.953**</td>
<td valign="top" align="left">1</td>
<td valign="top" align="left"/>
</tr>
<tr>
<td valign="top" align="left">Pico</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.651*</td>
<td valign="top" align="left">-0.724**</td>
<td valign="top" align="left">-0.849**</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">-0.736**</td>
<td valign="top" align="left">-0.637*</td>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left"/>
<td valign="top" align="left">0.588*</td>
<td valign="top" align="left">0.718**</td>
<td valign="top" align="left"/>
<td valign="top" align="left">0.614*</td>
<td valign="top" align="left">-0.769**</td>
<td valign="top" align="left"/>
<td valign="top" align="left">1</td>
</tr>
</tbody>
</table>
<table-wrap-foot>
<p>The r-values shown in this table indicate statistical signifificance when p-values are&lt; 0.05 (*) and&lt; 0.001 (**). Blanks indicate that r-values are not signifificant. Temp; temperature, Sal; salinity, Chl; chlorophyll a, T_C; total carbon uptake rate, P_C; picophytoplankton carbon uptake rate, Sp_T_C; specifific total carbon uptake rate, Sb_P_C; specifific picophytoplankton carbon uptake rate, T_Ni; total nitrate uptake rate, T_Am; total ammonium uptake rate, P_Ni; picophytoplankton nitrate uptake rate, P_Am; picophytoplankton ammonium uptake rate, DIN; sum of NO3-+NO2-+NH4+; Micro; microphytoplankton (%), Nano; nanophytoplankton (%), Pico; picophytoplankton contribution (%) of total chl-a.</p>
</table-wrap-foot>
</table-wrap>
<p>
<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2B</bold>
</xref> shows the temporal variability of the total chl-a content and the relative contribution of size-fractionated phytoplankton (micro-, nano-, and picophytoplankton). The highest total phytoplankton biomass (chl-a) was recorded on January 6 and 9, 2019 (14.6 and 20.0 mg m<sup>-3</sup>, respectively). Average chl-a was 4.4 mg m<sup>-3</sup> (SD = &#xb1; 6.0 mg m<sup>-3</sup>) during the period from December 19, 2018 to January 26, 2019 (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2B</bold>
</xref>). Microphytoplankton constituted the dominant size fraction during the sampling period, accounting for 16.5-93.6% of the total chl-a content, with a mean of 57.2% (&#xb1; 26.2%), followed by nano- (30.3%), and picophytoplankton (12.5%). At peak chl-a content, microphytoplankton (&gt;20 &#x3bc;m) contributed &gt;90% of the total chl-a. In comparison, the contribution of picophytoplankton (&lt;2 &#x3bc;m) to the total biomass was always low, reaching peak values (28%) on December 25, 2018. The total chl-a concentration was positively correlated with microphytoplankton (p&lt; 0.05, r = 0.748) and negatively correlated with picophytoplankton (p&lt; 0.05, r = -0.651) (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>).The daily concentrations of NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup> and SiO<sub>2</sub> were 11.4&#x2013;26.2 &#x3bc;M and 41.6&#x2013;73.5 &#x3bc;M, respectively, although they differed widely on each sampling date. PO<sub>4</sub>
<sup>3-</sup> displayed the same pattern as NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup> (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2C</bold>
</xref>). However, the PO<sub>4</sub>
<sup>3-</sup> concentration was relatively lower (0.8-1.8 &#x3bc;M). Decrease in nutrient concentrations during sampling were common with substantially increased chl-a concentration, such as from early to mid-January. The largest decrease in nutrient concentration in the surface water from the initial values was observed during January 12&#x2013;20. NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup> and PO<sub>4</sub>
<sup>3-</sup> concentrations decreased from 19.2 to 11.4 &#x3bc;M and 1.7 to 0.8 &#x3bc;M, respectively (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2C</bold>
</xref>). Similarly, low NH<sub>4</sub>
<sup>+</sup> was observed (&lt;1 &#x3bc;M) at peak chl-a. Interestingly, SiO<sub>2</sub> concentrations further decreased between January 9 and 23, which was not observed for other inorganic nutrients (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2D</bold>
</xref>). Overall, the NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup>+NH<sub>4</sub>
<sup>+</sup>:PO<sub>4</sub>
<sup>3-</sup> (N:P) and NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup>+NH<sub>4</sub>
<sup>+</sup>:SiO<sub>2</sub> (N:Si) molar ratios ranged from 11.7 to 15.4 (average &#xb1; SD = 13.2 &#xb1; 1.1) and 0.2 to 0.7 (average &#xb1; SD = 0.3 &#xb1; 0.1), respectively (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2E</bold>
</xref>).</p>
</sec>
<sec id="s3_2">
<title>Wind Speed and Direction</title>
<p>
<xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3</bold>
</xref> shows the three-hourly average wind speed and direction. The average wind speed during the study period was 6&#xa0;m s<sup>-1</sup>. A large change was observed in the average wind speed in the Marian Cove during the sampling period, reaching 14.4&#xa0;m s<sup>-1</sup>. The overall wind direction was WNW during the sampling period. Meanwhile, an easterly wind prevailed from January 10 and 13, with highest wind speeds (&gt;6&#xa0;m s<sup>-1</sup>) (<xref ref-type="fig" rid="f3">
<bold>Figures&#xa0;3A, B</bold>
</xref>). The colored curve in <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3C</bold>
</xref> shows the accumulated &#x3c4;<sub>x</sub> values, there were two strong eastward episodes. The pulses of accumulated &#x3c4;<sub>x</sub> match well with the wind speed through December 19, 2018 to January 26, 2019 (<xref ref-type="fig" rid="f3">
<bold>Figures&#xa0;3A, C</bold>
</xref>). It exhibits clearly that the overall intensity of the eastward in 2-day is the strongest from 1-day to 5-day (see red curve in <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3C</bold>
</xref>). The accumulated intensity of easterly wind in 2-day between January 11 and 13 is the most prominent.</p>
<fig id="f3" position="float">
<label>Figure&#xa0;3</label>
<caption>
<p>Time series of <bold>(A)</bold> wind direction, <bold>(B)</bold> wind speed and <bold>(C)</bold> cumulative zonal wind stress during sampling period. In <bold>(C)</bold>, the black line indicates the prescribed climatological wind stress (&#x3c4;<italic>
<sub>x</sub>
</italic> ) for the 1-day. The red, green, yellow, and blue lines are cumulative wind stress forcing for 2-, 3-, 4-, and 5-day, respectively. The circle and square symbols represent the sampling time of January 6 and 12, respectively.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-09-887909-g003.tif"/>
</fig>
</sec>
<sec id="s3_3">
<title>Time Series in Surface-Water Uptake of Total C and N</title>
<p>The total C and N (sum of NO<sub>3</sub>
<sup>-</sup> and NH<sub>4</sub>
<sup>+</sup> uptake) uptake rates (mg C (or N) m<sup>-3</sup> h<sup>-1</sup>) by phytoplankton in the surface water were measured during summer (December&#x2013;January) (<xref ref-type="fig" rid="f4">
<bold>Figures&#xa0;4</bold>
</xref>, <xref ref-type="fig" rid="f5">
<bold>5</bold>
</xref>), and were 0.3&#x2013;24.5 mg C m<sup>-3</sup> h<sup>-1</sup> and 0.06&#x2013;3.27 mg N m<sup>-3</sup> h<sup>-1</sup>, respectively. The average C and N uptake rates were 6.8 mg C m<sup>-3</sup> h<sup>-1</sup> (SD = &#xb1; 7.9 mg C m<sup>-3</sup> h<sup>-1</sup>) and 1.0 mg N m<sup>-3</sup> h<sup>-1</sup> (SD = &#xb1; 1.1 mg N m<sup>-3</sup> h<sup>-1</sup>), respectively, with the highest rates observed on January 9 and the lowest on January 26 (<xref ref-type="fig" rid="f4">
<bold>Figures&#xa0;4A</bold>
</xref>, <xref ref-type="fig" rid="f5">
<bold>5A</bold>
</xref>). The temporal pattern of N uptake was very similar to that of C uptake and chl-a content (<xref ref-type="fig" rid="f4">
<bold>Figures&#xa0;4A</bold>
</xref>, <xref ref-type="fig" rid="f5">
<bold>5A</bold>
</xref>). Moreover, the specific uptakes (h<sup>-1</sup>) of total C and NO<sub>3</sub>
<sup>-</sup> were the highest on January&#xa0;6, after which they gradually decreased, peaked on January 17, and then steadily decreased until the end of the observation period (<xref ref-type="fig" rid="f4">
<bold>Figures&#xa0;4B</bold>
</xref>, <xref ref-type="fig" rid="f5">
<bold>5C</bold>
</xref>). Relative contributions of the different N compounds to the measured total N uptake varied for on each sampling date (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5D</bold>
</xref>). Compared to total N, proportion of the NO<sub>3</sub>
<sup>-</sup> uptake fraction was 15.2% at the beginning (in the middle of December) but increased gradually to 64.7% on January 3.</p>
<fig id="f4" position="float">
<label>Figure&#xa0;4</label>
<caption>
<p>Hourly <bold>(A)</bold> carbon and <bold>(B)</bold> specific uptake rates for total and picophytoplankton, and <bold>(C)</bold> the relative contribution of size-fractionated phytoplankton each sampling date.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-09-887909-g004.tif"/>
</fig>
<fig id="f5" position="float">
<label>Figure&#xa0;5</label>
<caption>
<p>Hourly rates of <bold>(A)</bold> nitrogen, <bold>(B)</bold> nitrate (NO<sub>3</sub>
<sup>-</sup>) and ammonium (NH<sub>4</sub>
<sup>+</sup>) uptake, <bold>(C)</bold> specific nitrate (NO<sub>3</sub>
<sup>-</sup>) and ammonium (NH<sub>4</sub>
<sup>+</sup>) uptake, and <bold>(D)</bold> the relative contribution of different N forms in total phytoplankton, <bold>(E)</bold> nitrate (NO<sub>3</sub>
<sup>-</sup>) and ammonium (NH<sub>4</sub>
<sup>+</sup>) uptake in picophytoplankton, <bold>(F)</bold> the relative contribution of size-fractionated phytoplankton for different N forms on each sampling date. The blue squares in <bold>(A)</bold> and triangles in <bold>(B</bold>, <bold>E)</bold> represent total chl-a concentration and <italic>f</italic>-ratio, respectively.</p>
</caption>
<graphic mimetype="image" mime-subtype="tiff" xlink:href="fmars-09-887909-g005.tif"/>
</fig> 
<p>Although both NO<sub>3</sub>
<sup>-</sup> and NH<sub>4</sub>
<sup>+</sup> were taken up by phytoplankton, the C and dominant N sources varied between the growth phases and blooms. During the sampling period, the 31-fold change in biomass was lower than the 84-fold change in total C uptake, and growth acceleration was much faster in this region. Simultaneously, a more substantial (462-fold) change in the total NO<sub>3</sub>
<sup>-</sup> uptake rate was observed, whereas the total NH<sub>4</sub>
<sup>+</sup> uptake (31-fold) was similar to that of the chl-a content. The total and specific C uptake rates were inversely correlated with DIN (NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup>+NH<sub>4</sub>
<sup>+</sup>, p&lt; 0.05, r = -0.595, and r = -0.601, respectively) but positively correlated with phytoplankton biomass (chl-a, p&lt; 0.05, r = 0.973, and r = 0.859, respectively) (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>). This suggests that the nutrients were alomost simultaneously used by the Marian Cove phytoplankton.</p>
</sec>
<sec id="s3_4">
<title>Relative Contribution of the Picophytoplankton (&lt; 2 &#xb5;m) Fraction to the Total Productivity</title>
<p>Decrease in the C uptake rate was mainly due to the decline in chl-a values for the total phytoplankton; however, the picophytoplankton fraction showed little variation in chl-a. We found that picophytoplankton productivity remained relatively constant during the sampling period compared to the total uptake, even with nutrient fluctuations (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4A</bold>
</xref>). The average surface C uptake by picophytoplankton was 0.2 mg C m<sup>-3</sup> h<sup>-1</sup> (SD = &#xb1; 0.2 mg C m<sup>-3</sup> h<sup>-1</sup>), the highest being on December 22 (0.7 mg C m<sup>-3</sup> h<sup>-1</sup>), and the lowest (0.02 mg C m<sup>-3</sup> h<sup>-1</sup>) at the end of the observation period. The contribution of picophytoplankton to the total phytoplankton C uptake ranged from a minimum of 0.6% to a maximum of 27.9% on January 9 (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4C</bold>
</xref>). However, the average C uptake by picophytoplankton was up to 8.6% (SD = &#xb1; 8.7%) of the total measured C uptake. The specific uptake rate (h<sup>-1</sup>) of picophytoplankton showed a similar trend to the uptake rate of C, and decreased with decreasing surface C uptake (<xref ref-type="fig" rid="f4">
<bold>Figure&#xa0;4B</bold>
</xref>). A positive relationship was observed between the picophytoplankton C uptake, temperature, and salinity (p&lt; 0.05), while a negative relationship was found between the picophytoplankton relative contribution to total biomass an the total C uptake (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>).</p>
<p>NO<sub>3</sub>
<sup>-</sup> uptake by picophytoplankton in the surface waters varied from&lt;0.01 to up to 0.04 mg N m<sup>-3</sup> h<sup>-1</sup>, with a mean of 0.01 mg N m<sup>-3</sup> h<sup>-1</sup> (SD = &#xb1; 0.01 mg N m<sup>-3</sup> h<sup>-1</sup>) (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5E</bold>
</xref>). The surface NH<sub>4</sub>
<sup>+</sup> uptake rates varied from 0.005 to 0.257 mg N m<sup>-3</sup> h<sup>-1</sup>, whereas the NO<sub>3</sub>
<sup>-</sup> uptake rates showed a relatively narrow range (0.001-0.035 mg N m<sup>-3</sup> h<sup>-1</sup>) (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5E</bold>
</xref>). The NH<sub>4</sub>
<sup>+</sup> uptake rate was higher than the NO<sub>3</sub>
<sup>-</sup> uptake rate in picophytoplankton, suggesting that it preferred NH<sub>4</sub>
<sup>+</sup> over NO<sub>3</sub>
<sup>-</sup> (average NH<sub>4</sub>
<sup>+</sup> to NO<sub>3</sub>
<sup>-</sup> uptake ratio of 9.1). Unlike the C uptake, neither NO<sub>3</sub>
<sup>-</sup> nor NH<sub>4</sub>
<sup>+</sup> uptake showed any trend (data not shown). No statistical relationship was observed between picophytoplankton N productivity and hydrography and/or dissolved inorganic nutrient concentrations (<xref ref-type="table" rid="T1">
<bold>Table&#xa0;1</bold>
</xref>).</p>
</sec>
</sec>
<sec id="s4" sec-type="discussion">
<title>Discussion</title>
<p>We measured the <italic>in-situ</italic> C and N uptake rates of phytoplankton at a fixed monitoring site during the summer of 2018&#x2013;2019 using a dual-stable isotope method. The Marian Cove is a semi-enclosed water body that has a tidal, turbid, wind-induced circulation current with high nutrient concentrations, water temperature, and organic matter load (<xref ref-type="bibr" rid="B1">Ahn et al., 1997</xref>; <xref ref-type="bibr" rid="B85">Yoo et al., 2003</xref>; <xref ref-type="bibr" rid="B35">Jeon et al., 2021</xref>). Freshwater discharge from glacier melt is an important control of phytoplankton production, and the accompanying high input of suspended particulate matter (SPM) in the inner Cove changes the optical conditions (<xref ref-type="bibr" rid="B41">Kim et al., 2021</xref>). During the study period, SPM concentration did not show any correlation with chl-a, C, or N uptake (p &gt; 0.05, data not shown). However, phytoplankton C and N uptake rates and dominant species may be affected by the form of N supplied, nutrient levels, and wind-driven transport processes, such as glacial outflow in the cove. For the present study, we assumed a negligible influence of tidal forces because all sampling was conducted during flood tides.</p>
<sec id="s4_1">
<title>Phytoplankton Bloom and the Highly Variable C Uptake in Summer 2018</title>
<p>Relatively high phytoplankton biomass (up to 45 mg m<sup>-3</sup> near-shore waters adjacent to Palmer station; <xref ref-type="bibr" rid="B30">Goldman et al., 2014</xref>) and productivity have been observed in coastal and shelf areas (<xref ref-type="bibr" rid="B28">Garibotti et al., 2003</xref>; <xref ref-type="bibr" rid="B5">Arrigo et al., 2008</xref>; <xref ref-type="bibr" rid="B21">Ducklow et al., 2012b</xref>; <xref ref-type="bibr" rid="B53">Mendes et al., 2012</xref>). Particularly during the summer growing period, the phytoplankton species composition varied seasonally, with species abundance related to changes in environmental conditions based on 15 years of monitoring data (1996&#x2013;2011) (<xref ref-type="bibr" rid="B35">Jeon et al., 2021</xref>). For example, seasonal nutrient depletion reflects diatom-dominated phytoplankton communities in regions where blooms are common, with a significant contribution of diatoms to the total phytoplankton biomass in the WAP (<xref ref-type="bibr" rid="B13">Clarke et al., 2008</xref>; <xref ref-type="bibr" rid="B82">Vernet et al., 2008</xref>; reviewed in <xref ref-type="bibr" rid="B20">Ducklow et al., 2012a</xref>; <xref ref-type="bibr" rid="B34">H&#xf6;fer et al., 2019</xref>, and references therein).</p>
<p>Similarly, we observed massive phytoplankton blooms (chl-a up to 20 mg m<sup>-3</sup>), which were mainly composed of microphytoplankton (&gt;20 &#xb5;m) and large diatoms (&gt;40 &#xb5;m, e.g., <italic>Thalassiosira</italic> spp.; <xref ref-type="supplementary-material" rid="SF1">
<bold>Supplementary Figure&#xa0;1</bold>
</xref>). There was a strong relationship between microphytoplankton fraction and the total chl-a concentration (p&lt; 0.05, r = 0.748, n = 13), where microphytoplankton contributed &gt;90% of the total chl-a when the latter exceeded ~14 mg m<sup>-3</sup>. When the chl-a concentration was&lt;2 mg m<sup>-3</sup>, nanophytoplankton was occasionally the dominant size class (<xref ref-type="fig" rid="f2">
<bold>Figure&#xa0;2B</bold>
</xref>). This is consistent with <xref ref-type="bibr" rid="B35">Jeon et al. (2021)</xref>, who reported that centric and pennate diatoms comprised a substantial part of phytoplankton biomass in the Marian Cove, with an ~58% contribution to the total microphytoplankton abundance during summer blooms. Therefore, seasonal blooms result primarily from increases in microphytoplankton and diatoms.We observed similar trends in the C uptake data and chl-a concentrations. During the peak bloom, the C uptake rate was much higher (24.5 mg C m<sup>-3</sup> h<sup>-1</sup>) and the macronutrient concentrations declined considerably, implying a much more active nutrient intake by the phytoplankton. Variability in macronutrient consumption is reflected in the phytoplankton biomass in the Antarctic coastal waters during summer (<xref ref-type="bibr" rid="B13">Clarke et al., 2008</xref>; <xref ref-type="bibr" rid="B87">Zhang et al., 2019</xref>, and references therein). The dominance of microphytoplankton is consistent with the total primary production, and also positively correlates with the chl-a in various coastal waters (<xref ref-type="bibr" rid="B78">Varela et al., 2002</xref>; <xref ref-type="bibr" rid="B51">Mara&#xf1;&#xf3;n et al., 2012</xref>; <xref ref-type="bibr" rid="B41">Kim et al., 2021</xref>). Previous studies have documented a markedly high chl-a and C uptake rate in the coastal ice-edge zone in Antarctic waters adjoining the Indian Ocean (up to 4.0 mg m<sup>-3</sup> and 3.3 mg C m<sup>-3</sup> h<sup>-1</sup>, respectively; <xref ref-type="bibr" rid="B80">Verlencar et al., 1990</xref>), Marguerite Bay (&gt;10 mg m<sup>-3</sup> and &gt;4.2 mg C m<sup>-3</sup> h<sup>-1</sup>, respectively; <xref ref-type="bibr" rid="B21">Ducklow et al., 2012b</xref>), Marian Cove (up to 19.5 mg m<sup>-3</sup> and 31.1 mg C m<sup>-3</sup> h<sup>-1</sup>, respectively; <xref ref-type="bibr" rid="B41">Kim et al., 2021</xref>), and South Bay (&gt;15 mg m<sup>-3</sup> and &gt;50 mg C m<sup>-3</sup> h<sup>-1</sup>, respectively; <xref ref-type="bibr" rid="B34">H&#xf6;fer et al., 2019</xref>). This is consistent with observations from the Antarctic coastal waters, and supports the theory that this is one of the most important global &#x201c;biological hotspots&#x201d;. The development of phytoplankton blooms is also an important factor affecting primary production.However, the observed temporal variability (0.3&#x2013;24.5 mg C m<sup>-3</sup> h<sup>-1</sup>) probably reflects a combination of changes in light availability due to turbidity and water stability (<xref ref-type="bibr" rid="B73">Schloss et al., 2002</xref>; <xref ref-type="bibr" rid="B41">Kim et al., 2021</xref>), as well as water movement (<xref ref-type="bibr" rid="B34">H&#xf6;fer et al., 2019</xref>). Although various environmental factors affected the C uptake rate, no statistically significant differences were observed in the direct light intensity, SPM, water temperature, and salinity during the sampling period. Low macronutrient contents were observed during the peak bloom, but the N/P ratio remained similar regardless of the growth phase and was unlikely to act as a limiting factor for phytoplankton growth. Earlier studies reported that macronutrient values in the Marian Cove are generally a non-limiting factor for phytoplankton growth (<xref ref-type="bibr" rid="B49">Lee et al., 2015</xref>; <xref ref-type="bibr" rid="B35">Jeon et al., 2021</xref>), both due to inflow from the Maxwell Bay and the penguin colonies (<xref ref-type="bibr" rid="B69">Pruszak, 1980</xref>; <xref ref-type="bibr" rid="B60">N&amp;eogon;dzarek, 2008</xref>), where turbulent mixing and wind-driven upwelling cause continuous and abundant nutrient flow into the photic layer. Additionally, lateral iron inputs from glacial meltwaters and terrestrial sources are sufficient to sustain large-scale phytoplankton blooms on the King George Island (<xref ref-type="bibr" rid="B74">Schloss et al., 2014</xref>; <xref ref-type="bibr" rid="B42">Kim et al., 2015</xref>; <xref ref-type="bibr" rid="B34">H&#xf6;fer et al., 2019</xref>), and phytoplankton growth is not limited, even during intense blooms (<xref ref-type="bibr" rid="B10">Bown et al., 2017</xref>).</p>
<p>Nevertheless, the significant reduction in biomass and total C uptake immediately after peak chl-a (on January 12) may have enhanced other phytoplankton losses, such as zooplankton predation and other loss rates (i.e., viral lysis, sinking, and aggregation) (<xref ref-type="bibr" rid="B66">Petrou et al., 2016</xref>). Grazing effects, phytoplankton sinking, and mortality rates were not explored in this study. Instead, heterotrophic activity and the physiological status of phytoplankton were estimated based on the NH<sub>4</sub>
<sup>+</sup> concentration and specific C uptake by phytoplankton. For example, being its main contributor, zooplankton excretion can boost ambient NH<sub>4</sub>
<sup>+</sup> concentrations (<xref ref-type="bibr" rid="B17">Corner and Davies, 1971</xref>). Bacterial degradation of organic matter may also result in summertime NH<sub>4</sub>
<sup>+</sup> accumulation (<xref ref-type="bibr" rid="B45">Koike et al., 1986</xref>). NH<sub>4</sub>
<sup>+</sup> and NO<sub>3</sub>
<sup>-</sup> concentrations in the area showed a rapid increase under lower C uptake on January 12 (<xref ref-type="fig" rid="f3">
<bold>Figures&#xa0;3D</bold>
</xref> and <xref ref-type="fig" rid="f4">
<bold>4A</bold>
</xref>). Simultaneously, the specific C uptake rates by phytoplankton were approximately 1/6 of the peak value (0.03 h<sup>-1</sup>). These results imply a physiological limitation of phytoplankton growth on January 12, which may have temporarily enhanced nutrient concentrations in the surface water due to less consumption by phytoplankton. This suggests the increased possibility of the influence of external forces (i.e., bottom-up control) rather than biointeractions (i.e., top-down control).</p>
</sec>
<sec id="s4_2">
<title>N Uptake Dynamics of Phytoplankton and <italic>f</italic>-Ratio</title>
<p>Utilisation of inorganic N by phytoplankton was observed to be highly variable in the Marian Cove during summer. The total NO<sub>3</sub>
<sup>-</sup> uptake was higher than the NH<sub>4</sub>
<sup>+</sup> uptake in the bloom phase, while primary production in the system evolved from NO<sub>3</sub>
<sup>&#x2013;</sup>-based to NH<sub>4</sub>
<sup>+</sup>-based at the end of sampling. This evolution is in agreement with earlier studies that reported rise in NH<sub>4</sub>
<sup>+</sup> levels during summers, when zooplankton and microbial metabolism provide regenerated N (<xref ref-type="bibr" rid="B13">Clarke et al., 2008</xref>; <xref ref-type="bibr" rid="B58">Mosseri et al., 2008</xref>). The high ambient NH<sub>4</sub>
<sup>+</sup> concentrations in conjunction with increased NH<sub>4</sub>
<sup>+</sup> uptake are indicative of an active regeneration process in the Marian Cove and are attributed to the late summer sampling. Thus, we hypothesized that NH<sub>4</sub>
<sup>+</sup> uptake occurs in relation to changes in its concentration and phytoplankton species/size composition.</p>
<p>Dependence of the NH<sub>4</sub>
<sup>+</sup> concentration on NO<sub>3</sub>
<sup>-</sup> uptake has been described in previous studies (<xref ref-type="bibr" rid="B19">Dortch, 1990</xref>; <xref ref-type="bibr" rid="B47">L&#x2019;Helguen et al., 2008</xref>; <xref ref-type="bibr" rid="B23">Dugdale et al., 2012</xref>; <xref ref-type="bibr" rid="B29">Glibert et al., 2016</xref>). For example, NH<sub>4</sub>
<sup>+</sup> concentrations &gt;1 &#xb5;M (<xref ref-type="bibr" rid="B19">Dortch, 1990</xref>) or over a certain threshold (0.2&#x2013;100 &#xb5;M; <xref ref-type="bibr" rid="B79">Varela and Harrison, 1999</xref>; <xref ref-type="bibr" rid="B23">Dugdale et al., 2012</xref>; <xref ref-type="bibr" rid="B29">Glibert et al., 2016</xref>) inhibit NO<sub>3</sub>
<sup>-</sup> uptake rates. Our data also support that a relatively higher uptake of NH<sub>4</sub>
<sup>+</sup> than that of NO<sub>3</sub>
<sup>-</sup> was observed in the presence of &gt;1 &#xb5;M NH<sub>4</sub>
<sup>+</sup> in ambient waters, which might be influenced by the inhibition of assimilated NO<sub>3</sub>
<sup>-</sup> by phytoplankton. However, the elevated NH<sub>4</sub>
<sup>+</sup> uptake did not enhance the total phytoplankton C uptake or biomass. The observed rapid NO<sub>2</sub>
<sup>-</sup>+NO<sub>3</sub>
<sup>-</sup> drawdown and uptake rate of NO<sub>3</sub>
<sup>-</sup> in January, coupled with increases in chl-a and C uptake, indicate high productivity. These results clearly suggest that NO<sub>3</sub>
<sup>-</sup> is the preferred growth- and biomass-promoting N source for the studied phytoplankton community. Notably, the NH<sub>4</sub>
<sup>+</sup> uptake by phytoplankton was higher despite the high NO<sub>3</sub>
<sup>-</sup> concentrations. Consequently, inhibition of NO<sub>3</sub>
<sup>-</sup> uptake by NH<sub>4</sub>
<sup>+</sup> (&gt;1 &#xb5;M) may be one of the factors that led to the low <italic>f</italic>-ratio (0.08&#x2013;0.24, <xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5B</bold>
</xref>) in the total phytoplankton (<italic>f</italic>-ratio= NO<sub>3</sub>
<sup>-</sup> uptake/total N uptake (NO<sub>3</sub>
<sup>-</sup> + NH<sub>4</sub>
<sup>+</sup> uptake), <xref ref-type="bibr" rid="B24">Eppley and Peterson, 1979</xref>).Another possible cause of the lower <italic>f</italic>-ratio could be the increasing contribution of the smaller cells (&lt;20 &#xb5;m). Microphytoplankton levels were higher during relatively high biomass and C and NO<sub>3</sub>
<sup>-</sup> uptake rates, reaching an <italic>f</italic>-ratio of up to 0.67 on January 9 (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5B</bold>
</xref>). The NH<sub>4</sub>
<sup>+</sup> uptake rates were the highest in the picophytoplankton fraction throughout the sampling period, resulting in an <italic>f</italic>-ratio&lt;0.5, which decreased to 0.03 at the end of the sampling period (<xref ref-type="fig" rid="f5">
<bold>Figure&#xa0;5E</bold>
</xref>). In picophytoplankton, NH<sub>4</sub>
<sup>+</sup> is preferentially assimilated over NO<sub>3</sub>
<sup>-</sup> because NO<sub>3</sub>
<sup>-</sup> assimilation is more energy consuming than NH<sub>4</sub>
<sup>+</sup> assimilation. Once NO<sub>3</sub>
<sup>-</sup> is transported into the cell, it must be further reduced to NH<sub>4</sub>
<sup>+</sup> before it can be assimilated (<xref ref-type="bibr" rid="B59">Mulholland and Lomas, 2008</xref>).More importantly, <italic>f</italic>-ratio values show that planktonic diatoms (larger cells) are replaced by small phytoplankton in surface water, causing decreased primary production and C export. This is because NO<sub>3</sub>
<sup>&#x2013;</sup>-fueled new production at steady state is equivalent to the organic C that can be exported from total production in the euphotic layer (<xref ref-type="bibr" rid="B24">Eppley and Peterson, 1979</xref>). In this regard, phytoplankton species shifts toward smaller values could substantially lower C export efficiency as well as primary production (<xref ref-type="bibr" rid="B56">Montes-Hugo et al., 2008</xref>; <xref ref-type="bibr" rid="B55">Montes-Hugo et al., 2009</xref>; <xref ref-type="bibr" rid="B49">Lee et al., 2015</xref>, <xref ref-type="bibr" rid="B53">Mendes et al., 2012</xref>; <xref ref-type="bibr" rid="B70">Rozema et al., 2017</xref>; <xref ref-type="bibr" rid="B75">Schofield et al., 2017</xref>). The undergoing reductions in diatom silica production in response to ocean acidification and shifts toward smaller cells could reduce the vertical fluxes of diatoms and diminish C export efficiency before the end of this century (<xref ref-type="bibr" rid="B65">Petrou et al., 2019</xref>). Therefore, in the neritic area of Marian Cove, nutrient utilization in the surface layer during the summer induced variations in phytoplankton size composition in terms of chl-a and C and N uptake, from summer blooms (early January) skewed toward the microsized fraction (&gt;20 &#x3bc;m) undergoing a gradual shift toward the pico sized fraction (&lt;2 &#x3bc;m) through the nanosized fraction (2&#x2013;20 &#x3bc;m) in late January. This shift in the size of the phytoplankton community probably involved the prevailing wind direction associated with physiological and morphological properties (e.g., nutrient uptake and export rate), as mentioned above.</p>
</sec>
<sec id="s4_3">
<title>Role of Wind</title>
<p>Surface wind, meltwater dynamics, and currents, as key drivers of the upper water layer structure, strongly influence nutrient availability and phytoplankton growth (<xref ref-type="bibr" rid="B18">Deppeler and Davidson, 2017</xref>). Wind speed and direction may influence the strength and duration of phytoplankton blooms (<xref ref-type="bibr" rid="B74">Schloss et al., 2014</xref>; <xref ref-type="bibr" rid="B18">Deppeler and Davidson, 2017</xref>, and references therein). High-frequency (HF) wind forcing is important for the residence time of water (<xref ref-type="bibr" rid="B44">Kohut et al., 2018</xref>). The major component of HF zonal wind forcing was the so-called easterly wind events, which played a critical role in modulating water movement. Previous, studies on the Marian Cove (<xref ref-type="bibr" rid="B86">Yoo et al., 1999</xref> and <xref ref-type="bibr" rid="B84">Yoo et al., 2015</xref>; <xref ref-type="bibr" rid="B35">Jeon et al., 2021</xref>) and the adjacent Potter Cove (<xref ref-type="bibr" rid="B36">K1&#xf6;ser et al., 1994</xref>) and Admiralty Bay (<xref ref-type="bibr" rid="B61">Nowosielski, 1980</xref>) have suggested that the prevailing easterly wind can generate outflow and upwelling near the cove head or deter the flow rate of surface influents from the Maxwell Bay. <xref ref-type="bibr" rid="B69">Pruszak (1980)</xref> observed the drift ice movement and reported that, surface water circulation can be controlled with a wind speed of &gt;4&#xa0;m s<sup>-1</sup> in the adjacent Admiralty Bay. There is also a study result that surface water flows out of the Marian Cove within one day when the east wind blows with an average wind speed of over 8&#xa0;m s<sup>-1</sup> (<xref ref-type="bibr" rid="B86">Yoo et al., 1999</xref>).</p>
<p>Similarly, in our study, the wind direction changed from west to east, and continued for approximately three days. Additionally, strong winds (&gt;6&#xa0;m s<sup>-1</sup>) blew simultaneously, which is believed to have caused low biomass and C and N uptake rates. Although easterly winds occurred on January 6, their speed was low compared to that during January 10&#x2013;12. In detail, <xref ref-type="fig" rid="f3">
<bold>Figure&#xa0;3C</bold>
</xref> shows the evolution of zonal wind stress during sampling period. As a result of the analysis of cumulative wind stress from Day 1 to Day 5, the wind forcing was higher when 2 days were considered. Overall, negative &#x2211;&#x3c4;<italic>
<sub>x</sub>
</italic> values with low wind speeds led to high chl-a, C, and N uptakes from January 2 to 9. This is because factors, such as outflowing water from the Marian Cove to the Maxwell Bay, also play a role in transporting particulate matter, including algae, near the ice wall and resuspending it (<xref ref-type="bibr" rid="B11">Brandini and Rebello, 1994</xref>; <xref ref-type="bibr" rid="B86">Yoo et al., 1999</xref>). This surface circulation influenced by the easterly wind can deliver surface water and suspended particles to the Maxwell Bay because the Coriolis effect is not important for a small bay width (~1.5 km for the Marian Cove) (<xref ref-type="bibr" rid="B84">Yoo et al., 2015</xref>). Resuspension of sediments and benthic diatoms in the inner Admiralty Bay induced by wind-driven upwelling (&lt;20&#xa0;m water depth) increases surface turbidity and nutrient concentrations (<xref ref-type="bibr" rid="B11">Brandini and Rebello, 1994</xref>); however, the effect of resuspension was not significant in the present study. As the SiO<sub>2</sub> concentration was lower than that at peak bloom, benthic diatom species (<italic>Cocconei</italic>s spp.) accounted for 8.5% of total diatom abundance (<xref ref-type="supplementary-material" rid="SF1">
<bold>Supplementary Figure&#xa0;1</bold>
</xref>). On January 12, the dominant species were small (&lt;20 &#xb5;m) <italic>Navicula</italic> spp. and <italic>Fragilariopsis</italic> spp., accounting for 72.2% to the total diatom abundance that lives mainly on the ice walls and in low-salinity coastal waters (<xref ref-type="bibr" rid="B39">Kang et al., 1999</xref>; <xref ref-type="bibr" rid="B25">Fernandes and Procopiak, 2003</xref>; <xref ref-type="bibr" rid="B35">Jeon et al., 2021</xref>). More specifically, a change in the structure of the phytoplankton community was observed during the sampling period in microscope-based phytoplankton observation (<xref ref-type="supplementary-material" rid="SF1">
<bold>Supplementary Figure&#xa0;1</bold>
</xref>). Phytoplankton communities were dominated by bacillariophytes (diatoms), which comprised &gt;60% (up to 96.3%) of the total C biomass over the sampling period. <italic>Thalassiosira</italic> spp., accounting for 67.7% of total diatom abundance at peak bloom, decreased to 1/4 of its peak bloom value on January 12 (<xref ref-type="supplementary-material" rid="SF1">
<bold>Supplementary Figure&#xa0;1</bold>
</xref>).Water column stratification and relatively weak wind speed are favorable for initiating seasonal blooms, and the presence of sea ice and glacial meltwaters influences primary production patterns (<xref ref-type="bibr" rid="B72">Saba et al., 2014</xref>; <xref ref-type="bibr" rid="B70">Rozema et al., 2017</xref>; <xref ref-type="bibr" rid="B34">H&#xf6;fer et al., 2019</xref>; <xref ref-type="bibr" rid="B41">Kim et al., 2021</xref>). In this regard, the relatively weak wind speeds observed at the beginning of January seem to enable water column stabilization, favoring an increase in the residence times of cells in the photic layer and providing more light for photosynthesis, allowing high phytoplankton accumulation in the cove.</p>
</sec>
</sec>
<sec id="s5" sec-type="conclusions">
<title>Conclusions</title>
<p>In this study, we examined the C and N uptake regimes in the Marian Cove during the austral summers of 2018&#x2013;19 using <sup>13</sup>C and <sup>15</sup>N dual isotope tracer assays. During phytoplankton blooms, the study area was generally characterized by high <italic>f</italic>-ratios (&gt;0.5), suggesting that NO<sub>3</sub>
<sup>-</sup> plays a dominant role in phytoplankton nutrition. Low <italic>f</italic>-ratios were observed at the end of the sampling period, and microphytoplankton and planktonic diatoms were replaced by nanophytoplankton and sympagic (sea-ice-associated) diatoms, causing decreased primary production and C export. Our results highlight the influence of wind on the changes in C and N uptake regimes and physical&#x2013;biological coupling in the Marian Cove. Increased regenerated production was not observed as the total phytoplankton biomass increased.</p>
<p>However, we assumed that the bacterial uptake rate was negligible in the present study. It is possible that the N uptake rate of heterotrophic bacteria may contribute to the N uptake rate in the study area. Phytoplankton and bacterial N uptake have been studied in various ecosystems (<xref ref-type="bibr" rid="B12">Bronk et al., 2007</xref>). Few records are available for the direct measurements of inorganic N uptake by bacteria in the Southern Ocean. The bacterial NH<sub>4</sub>
<sup>+</sup> demand in the coastal waters of the northern Gerlache Strait region of the Antarctic Peninsula during summer is 8~25% (mean 17%) of the total community NH<sub>4</sub>
<sup>+</sup> uptake rate (<xref ref-type="bibr" rid="B77">Tupas et al., 1994</xref>). <xref ref-type="bibr" rid="B14">Cochlan and Bronk (2001)</xref> reported similar mean value of 17% for the potential NH<sub>4</sub>
<sup>+</sup> uptake by heterotrophic bacteria in the Ross Sea during summer. The lower <italic>f</italic>-ratio could reflect more available NH<sub>4</sub>
<sup>+</sup> compared to NO<sub>3</sub>
<sup>-</sup>. However, accurately determining the contributions to bacterial N uptake using the GF/F filter method, as in this study, to distinguish them by size is still challenging. Therefore, further research is needed to clarify the contribution of bacteria to the primary production of the Marian Cove and the trophic linkages between phytoplankton assemblages and associated consumers. More observations with a longer timescale are required to better understand the C and N dynamics in the Sothern Ocean, particularly in coastal waters where rapid changes in glacial retreat and vigorous meteorological conditions take place owing to the effects of climate change.</p>
</sec>
<sec id="s6" sec-type="data-availability">
<title>Data Availability Statement</title>
<p>The original contributions presented in the study are included in the article/<xref ref-type="supplementary-material" rid="SF1">
<bold>Supplementary Material</bold>
</xref>. Further inquiries can be directed to the corresponding author.</p>
</sec>
<sec id="s7" sec-type="author-contributions">
<title>Author Contributions</title>
<p>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 carried out the analysis of the chl-a and phytoplankton community. S-JP provided meteorological data. H-CK processed and analyzed satellite imagery for glacier change detection. J-OM contributed to writing the manuscript. JP was the leader of the Korean Antarctic Research Program and provided scientific advice. All authors contributed to the article and approved the submitted version.</p>
</sec>
<sec id="s8" sec-type="funding-information">
<title>Funding</title>
<p>This study was supported by the Korea Polar Research Institute (KOPRI) and undertaken as part of &#x201c;Carbon cycle change and ecosystem response under the Southern Ocean warming (PE22110)&#x201d;.</p>
</sec>
<sec id="s9" sec-type="COI-statement">
<title>Conflict of Interest</title>
<p>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.</p>
</sec>
<sec id="s10" sec-type="disclaimer">
<title>Publisher&#x2019;s Note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
</p>
</sec>
</body>
<back>
<ack>
<title>Acknowledgments</title>
<p>We take the opportunity to thank the colleagues and 32nd King Sejong Station Overwintering Team assistance during work.</p>
</ack>
<sec id="s11" sec-type="supplementary-material">
<title>Supplementary Material</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="https://www.frontiersin.org/articles/10.3389/fmars.2022.887909/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fmars.2022.887909/full#supplementary-material</ext-link>
</p>
<supplementary-material xlink:href="Image_1.tif" id="SF1" mimetype="image/tiff">
<label>Supplementary Figure&#xa0;1</label>
<caption>
<p>Temporal variations of the <bold>(A)</bold> relative C biomass (%) of each phytoplankton group and <bold>(B)</bold> the relative cell abundance of major dominant phytoplankton species in diatoms (%) among six sampling dates (December 22 and January 6, 9,12, 23, and 26).</p>
</caption>
</supplementary-material>
</sec>
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