Next Article in Journal
The Effects of Particle Gradation on Salinized Soil in Arid and Cold Regions
Next Article in Special Issue
Marine Nitrogen Fixation and Phytoplankton Ecology
Previous Article in Journal
Surface Water Flow Balance of a River Basin Using a Shallow Water Approach and GPU Parallel Computing—Pescara River (Italy) as Test Case
Previous Article in Special Issue
Spatial Patterns of Macromolecular Composition of Phytoplankton in the Arctic Ocean
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Water
Volume 14
Issue 2
10.3390/w14020235
water-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Contribution of Small Phytoplankton to Primary Production in the Northern Bering and Chukchi Seas

by
Jung-Woo Park
1,*,
Yejin Kim
2,
Kwan-Woo Kim
2,
Amane Fujiwara
3,
Hisatomo Waga
1,4,
Jae Joong Kang
2,
Sang-Heon Lee
2,
Eun-Jin Yang
5 and
Toru Hirawake
1,6
1
Faculty/Graduate School of Fisheries Sciences, Hokkaido University, Hakodate 041-8611, Japan
2
Department of Oceanography, Pusan National University, Busan 46241, Korea
3
Research Institute for Global Change, Japan Agency for Marine-Earth Science and Technology, Yokosuka 237-0061, Japan
4
International Arctic Research Center, University of Alaska Fairbanks, Fairbanks, AK 99775, USA
5
Division of Polar Ocean Sciences, Korea Polar Research Institute, Incheon 21990, Korea
6
National Institute of Polar Research, Tachikawa 190-8518, Japan
*
Author to whom correspondence should be addressed.
Water 2022, 14(2), 235; https://doi.org/10.3390/w14020235
Submission received: 30 November 2021 / Revised: 7 January 2022 / Accepted: 8 January 2022 / Published: 14 January 2022
(This article belongs to the Special Issue Marine Nitrogen Fixation and Phytoplankton Ecology)
Browse Figures
Versions Notes

Abstract

:
The northern Bering and Chukchi seas are biologically productive regions but, recently, unprecedented environmental changes have been reported. For investigating the dominant phytoplankton communities and relative contribution of small phytoplankton (<2 µm) to the total primary production in the regions, field measurements mainly for high-performance liquid chromatography (HPLC) and size-specific primary productivity were conducted in the northern Bering and Chukchi seas during summer 2016 (ARA07B) and 2017 (OS040). Diatoms and phaeocystis were dominant phytoplankton communities in 2016 whereas diatoms and Prasinophytes (Type 2) were dominant in 2017 and diatoms were found as major contributors for the small phytoplankton groups. For size-specific primary production, small phytoplankton contributed 38.0% (SD = ±19.9%) in 2016 whereas 25.0% (SD = ±12.8%) in 2017 to the total primary productivity. The small phytoplankton contribution observed in 2016 is comparable to those reported previously in the Chukchi Sea whereas the contribution in 2017 mainly in the northern Bering Sea is considerably lower than those in other arctic regions. Different biochemical compositions were distinct between small and large phytoplankton in this study, which is consistent with previous results. Significantly higher carbon (C) and nitrogen (N) contents per unit of chlorophyll-a, whereas lower C:N ratios were characteristics in small phytoplankton in comparison to large phytoplankton. Given these results, we could conclude that small phytoplankton synthesize nitrogen-rich particulate organic carbon which could be easily regenerated.

1. Introduction

The biologically productive northern Bering Sea and the Chukchi Sea are important conduit of water masses and organic matters from the North Pacific Ocean transported into the Arctic Ocean and biologically productive regions [1,2,3,4,5]. Over the past few decades, many environmental changes have been reported in the regions [4,6,7,8]. Unprecedented high sea surface temperature was reported in the Bering Sea in 2014 and persisted in 2018 and 2019 [8; refs therein]. The Pacific origin freshwater flux with increasing northward volume transport into the Arctic Ocean had been increased over the 1991–2015 period [9]. Moreover, seasonal sea ice cover has been retreating earlier and forming later in the Pacific Arctic region over the last decade [10]. These current and ongoing changes in environmental conditions could subsequently cause changes in biogeochemical processes and consequently alter marine ecosystem structure in the northern Bering and Chukchi seas [11,12]. Indeed, the prior studies indicate that the variation in primary productivity of phytoplankton is mainly governed by freshwater content variability in the Pacific Arctic region [13,14]. Moreover, the seasonal sea ice cover could largely influence phytoplankton community composition [15], phytoplankton bloom period [16] and primary productivity [17].
Refs. [13,18,19,20] reported that pico-phytoplankton increased whereas larger cells declined in the Arctic Ocean because of stronger stratification and consequently lower nutrient supply into the upper water column caused by freshening surface waters. Based on the phytoplankton size classes derived from satellite ocean color data in the northern Bering and southern Chukchi seas [21], observed increasing trends in pico-phytoplankton in the Chirikov and St. Lawrence Island Polynya regions whereas an increasing trend in micro-phytoplankton in the southeastern Chukchi Sea from 1998 to 2016. The physiological conditions and subsequently photosynthetic end-products of phytoplankton affected by the recent environmental conditions were also previously reported in the northern Bering and southern Chukchi seas [21,22,23]. Phytoplankton as important primary producers in marine ecosystems can be a good indicator of environmental changes. These long-term changes in the functional phytoplankton group are strongly related to increasing annual sea surface temperature [13]. Therefore, monitoring the phytoplankton community responses such as shifts in dominant phytoplankton species and biomass to the current environmental changes is crucial to observe marine ecosystem alterations in the northern Bering and Chukchi seas [12,18,19,20].
Especially, the contribution of small phytoplankton could be necessary to understand potential impacts on the total primary production and, thus, whole marine ecosystems [12,20,21]. Moreover, the biochemical characteristics of phytoplankton such as C:N ratio are critical for understanding marine biogeochemical processes responding to environmental conditions. Ref. [24] reported higher C:N ratio related with low chlorophyll-a concentration and lower C:N ratio to high chlorophyll-a concentration in the Arctic Ocean. The C:N ratio could differ in various environmental conditions related to nutrients. However, little information on the small phytoplankton contribution to the total primary production and their biochemical traits such as C:N ratio is currently available in the northern Bering and Chukchi seas.
In this study, our objectives are to investigate the dominant phytoplankton communities and to assess the relative contribution of small phytoplankton (0.7–2.0 µm; pico-phytoplankton) to the total primary production and their biochemical characteristics (e.g., C:N ratio) in the northern Bering and Chukchi seas.

2. Materials and Methods

2.1. Study Area and Water Sampling

The ARA07B cruise was conducted in the northern Bering Sea and the Chukchi Sea during 5–19 August, 2016 onboard the Icebreaker R/V Araon (Figure 1; Table 1). As a total of 16 stations during the ARA07B cruises, only one station (st. 1) was located in the northern Bering Sea and 15 stations were in the Chukchi Sea. Water was sampled by Niskin bottles on conductivity-temperature-depth (CTD)/rosette sampler for the total chlorophyll-a and size-fractionated chlorophyll-a concentration. Euphotic depths were measured by a Secchi disk [25]. The OS040 cruise was executed mostly in the northern Bering Sea (8 stations) and partly in the southern Chukchi Sea (2 stations) during 9–21 July, 2017 onboard T/S Oshoro-Maru (Figure 1; Table 1). Physical properties and water samples were collected by CTD/rosette with Niskin bottles. The euphotic depths were calculated by comparing downward irradiance and surface irradiance measured by compact optical profiling system (C-OPS; Biospherical instrument Inc., San Diego, CA, USA).

2.2. Chlorophyll-a Analysis

The water samples were obtained from 6 different light depths (100%, 50%, 30%, 12%, 5% and 1% of the surface photosynthetically active radiation (PAR) for measuring the chlorophyll-a concentration. For the total chlorophyll-a concentration, 300 mL of seawater was filtered through 25 mm glass fiber filter (GF/F; Whatman). To obtain size-fractionated chlorophyll-a concentration, 500 mL seawater was filtered through 20 μm and 2 μm pore size membrane filters and then 47 mm GF/F sequentially. After the filtration was done, the filters were wrapped with aluminum foil and stored at −80°C freezer until analysis at the home laboratory. Chlorophyll-a extractions were followed by [26] and the concentrations were measured with a fluorometer (Turner Designs 10AU).

2.3. High-Performance Liquid Chromatography Analysis for Accessory Pigment Concentration

For high-performance liquid chromatography (HPLC) analysis, the water from 3 light depths (100%, 30% and 1%) were sampled during the ARA07B and OS040 cruises. Seawater (0.8–2.5 L) was passed through 2 μm membrane filter and 47 mm diameter GF/F filters to measure pigments concentration of small size phytoplankton (<2 μm) under gentle vacuum pressure (<100 mmHg). Seawater (0.5–1.5 L) was filtered onto GF/F for pigments of total phytoplankton during the ARA07B. For the OS040, samples were obtained only for total phytoplankton. For avoiding degradation, the filters for HPLC analysis were immediately frozen and stored in liquid nitrogen at −80°C freezer until analysis at home laboratory. In the laboratory, the filter samples were broken into small pieces and then soaked in 3 mL of N’N-dimethylformamide (DMF) with canthaxanthin served as an internal standard. After 20 min of sonication, the filters were extracted at 4°C in dark for 24 h and then extracts were filtered through a 0.45 μm pore membrane filter to remove GF/F particles. For minimizing photo-degradation of pigments, all the procedures were conducted under a low light condition. Pigments were analyzed using HPLC (Agilent Infinite 1260 in operation by JAMSTEC, Mutsu, Japan) with a ternary linear gradient system to separate each pigment. The pigment concentrations were calculated by the function of peak area, standard response factors and peak area of the internal standard following [27]. All the standards for each pigment were purchased from DHI in Denmark.
The CHEMTAX software based on a factorization program was used for estimating the relative contributions of different phytoplankton communities to the total chlorophyll-a concentration [28]. The ratios of accessory pigments to chlorophyll-a for each phytoplankton taxon for the CHEMTAX program were based on marker pigment concentrations of algal groups present in the Arctic Ocean [13,29] (Table 2). Since our two research cruises were in different periods and years, the final ratio matrix was separated for phytoplankton communities (Table 2). The contributions of Diatoms. Dinoflagellates, Cryptophytes, Pelagophytes, Prasinophytes (Type 2 and 3), Chlorophytes, Haptophytes and Phaeosystis were estimated by the CHEMTAX program. Small phytoplankton community was estimated from HPLC results by the equations described in the literature [28,29]. The relative proportions of the three size classes are derived from the concentrations of phytoplankton diagnostic pigments for the Chukchi and Bering seas using the equations described in [30,31].

2.4. Particulate Organic Carbon and Primary Productivity

The water samples for particulate organic carbon (POC) and primary productivity were obtained from 6 light depths (100, 50, 30, 12, 5 and 1% of PAR). 300 mL of seawater was filtered through 0.7 μm GF/F (pre-combusted at 450 °C for 4 h) for total POC and 500 mL was passed through 2 μm pore size membrane filter and then filtered onto GF/F filter for small POC (0.7–2 μm). Carbon and nitrogen uptake experiments were conducted using a 13C-15N dual isotope tracer technique previously reported from the Chukchi Sea [3,33]. After a 4 h incubation on deck, 300 mL water was filtered onto pre-combusted GF/F for total primary productivity and 500 mL water was filtered through 2 μm pore size membrane filter and sequentially onto GF/F filter for small phytoplankton productivity (0.7–2 μm). The filters were immediately preserved and stored in a freezer (−20 °C) until further mass spectrometric analysis using a Delta V+ Isotope Ratio Mass Spectrometers of Alaska Stable Isotope Facility at the University of Alaska Fairbanks, USA for ARA07B samples and using a 20–22 Isotope Ratio Mass Spectrometer (SERCON) at Japan Agency for Marine-Earth Science and Technology (JAMSTEC, Mutsu, Japan) for OS040 samples after HCl fuming overnight to remove carbonate. The carbon and nitrogen uptake rates were calculated based on [34].

2.5. Statistical Analysis

Student’s t-test was applied to verify correlations among factors and differences between the mean values of POC:chlorophyll-a ratio, PON:chlorophyll-a ratio, C:N ratio of each cruise and size group. The agglomerative hierarchical clustering (AHC) with Ward’s method (XLSTAT software, Addinsoft, Boston, MA, USA) was performed to calculate the dissimilarity in observed 20 variables; temperature and salinity), size-fractionated primary productivity, particulate organic carbon of each size, size-fractionated chlorophyll-a and accessory pigments, among stations.

3. Results and Discussion

3.1. Spatial Distribution of Temperature and Salinity

The temperature and salinity ranged from −1.5 °C to 9.2 °C (mean ± standard deviation (SD) = 0 ± 2.7 °C) and from 26.5 to 32.3 (mean ± SD = 29.9 ± 1.6) during the ARA07B cruise (Figure 2). The temperature during the OS040 were from –1.1 to 13.3 °C (mean ± SD = 6.2 ± 3.6 °C) and the salinity ranged from 28.9 to 32.9 (mean ± SD = 31.7 ± 0.9). Water mass at the most stations in the northern Chukchi corresponded to melting glacier water, which called Ice melt water (IMW; temperature < 2.0 °C and salinity < 30.0) and Bering Chukchi winter water (BCWW; −2–0 °C and <30–33.5 for temperature and salinity; [35]) during the ARA07B cruise. Other stations during the ARA07B were influenced by Bering shelf water (BSW; 0.0–10.0 °C and 31.8–33.0 for temperature and salinity). During the OS040 cruise, the relatively warm and low salinity Alaskan coastal water (ACW; 2.0–13.0 °C and <31.9 for temperature and salinity) and the warm and saline Bering shelf water (BSW) were predominant (Figure 2). The Bering shelf Anadyr water (BSAW; −1.0–2.0 °C and 31.8–33.0 for temperature and salinity), which is a mixed BSW with cold/saline Anadyr water (AW; [36,37]), was observed at some stations for the OSO40 cruise.

3.2. Chlorophyll-a Concentration and Different Size Chlorophyll-a Compositions in the Northern Bering and Chukchi Seas

The average euphotic depths were 45.6 m (SD = ±22.2 m) for the ARA07B cruise and 23.8 m (SD = ±9.1 m) for the OS040 cruise, respectively. In ARA07B, Chlorophyll-a concentrations were 0.02–1.3 mg chl-a m−3 (mean ± SD = 0.2 ± 0.3 mg chl-a m−3) at surface, 0.02–15.0 mg chl-a m−3 (mean ± SD = 1.0 ± 2.5 mg chl-a m−3) for euphotic layer. In OS040, Chlorophyll-e concentrations were 0.002–5.5 mg chl-a m−3 (mean ± SD = 0.7 ± 1.4 mg chl-a m−3) at surface, 0.002–5.5 mg chl-a m−3 (mean ± SD = 1.6 ± 2.2 mg chl-a m−3) for euphotic layer. Within the euphotic zone, integral chlorophyll-a concentrations were 3.2–172.1 mg chl-a m−2 (mean ± SD = 34.2 ± 48.0 mg chl-a m−2) during the ARA07B and 12.3–107.8 mg chl-a m−2 (mean ± SD = 45.4 ± 34.1 mg chl-a m−2) for the OS040, respectively (Figure 3). The average euphotic-depth integral chlorophyll-a concentrations in this study are within the range reported previously in the northern Bering Sea and the Chukchi Sea [3,14,21].
The chlorophyll-a contributions of each size phytoplankton (pico-, nano- and micro-phytoplankton) to the total phytoplankton were plotted in Figure 4 for the three different depths (100, 30 and 1% of light depths) at every station of the ARA07B and only surface for the OS040. The contributions of small phytoplankton to the total chlorophyll-a concentrations were found largely variable among the stations during both cruises.
The contributions of small phytoplankton to the total chlorophyll-a concentrations ranged from 2.9% to 71.1% with a depth-integrated average of 32.2% (SD = ±23.1%) during the ARA07B. In the ARA07B, the dominant size group of phytoplankton was micro-phytoplankton (mean ± SD = 43.5 ± 29.7% of chlorophyll-a concentration) followed by pico-phytoplankton (32.1 ± 23.1%) and nano-phytoplankton (24.3 ± 9.1%) during the observation period. In the Chukchi Sea, large phytoplankton are generally dominant although the areal distribution of their contribution mostly depends on local water masses in different nutrient conditions [3,21]. Normally, large phytoplankton growing under nutrient-enriched conditions are predominant in AW or BSW, whereas small phytoplankton are dominant in nutrient-depleted ACW [3,21]. Our average contribution of small phytoplankton is relatively higher than that (24.8 ± 23.0%) previously reported by [21] in the Chukchi Sea during the middle of August to early September, 2004. By contrast, our average contribution of small phytoplankton is relatively lower than that (55.1 ± 26.8%) from the study by [38] that was conducted in the northern Chukchi Sea during mid-July–mid-August, 2012. This difference among the studies could be caused by different regions with non-homogeneous nutrient conditions and different observation periods with a seasonal phytoplankton succession. The relative contribution of small phytoplankton could be caused by freshwater content in the Chukchi Sea since the nutrient concentrations and primary production rates of phytoplankton are largely governed by the nutrient-depleted freshwater content in the Chukchi Sea [14,39].
In comparison to the Chukchi Sea, the contributions of small phytoplankton were 0.7–80% (mean ± SD = 37.2 ± 31.0%) to the total chlorophyll-a concentration in the northern Bering Sea for the OS040 in this study. The proportions of different size chlorophyll-a were 40.2% (±35.4%), 22.5% (±10.5%) and 37.2% (±31.3%) for micro-, nano- and pico-phytoplankton, respectively, during our observation period in 2017. In the northern Bering Sea, the dominant size groups of phytoplankton are generally nano- and micro-phytoplankton based on phytoplankton size class results derived from satellite ocean color data from 1998 to 2016 [12]. The overall dominant size of phytoplankton is composed of nano-phytoplankton (49.0 ± 9.6%), followed by micro-phytoplankton (34.9 ± 8.0%) and pico-phytoplankton (16.1 ± 7.3%) in the Chirikov Basin of the northern Chukchi Sea [12]. However, the chlorophyll-a contributions of small phytoplankton are largely variable among different seasons [40]. The average contribution of small phytoplankton was 14.8% in late May to early June during the phytoplankton bloom period and largely increased up to 50.0% in middle June after the bloom [41]. Consistently, [13] found a seasonal increasing contribution of small phytoplankton in the northern Bering Sea (around Chirikov Basin) from May (5.2%) to July (31.8%). In addition to the seasonal variation, spatially the biochemical environmental conditions in the northern Bering Sea are also generally influenced by northward advection of AW, BSW and ACW [3,5]. Over recent decades, several environmental changes have been reported in the northern Bering Sea [4,5]. A steady increasing trend in the annual contribution of small phytoplankton is distinct in the Chirikov Basin from 1998 to 2016, although no significantly strong relationship was observed between the annual contribution of small phytoplankton and sea surface temperature [12]. Long-term changes in dominant phytoplankton communities should be monitored for Arctic marine ecosystems under ongoing environmental changes. Especially, the contribution of small phytoplankton could be used as one of indicators for changing marine ecosystems.

3.3. Pigment Composition and Major Dominant Phytoplankton Groups

The euphotic depth-integral concentrations of marker pigments from the two cruises are shown in Figure 5. Fucoxanthin (a marker pigment of diatoms), chlorophyll-c1+c2 and chlorophyll-b (a marker pigment of chlorophytes) were major accessory pigments during the ARA07B, although the pigment compositions spatially varied significantly across the stations. Among the pigments, fucoxanthin was the most dominant pigment with an average value of 12.58 ± 21.8 mg m−2 and the second and third predominant pigments were chlorophyll-c1+c2 (4.04 ± 4.83 mg m−2) and chlorophyll-b (2.64 ± 2.53 mg m−2). Previous studies reported that fucoxanthin dominating the Chukchi shelf is a typical characteristic during fall [13,31]. For the small phytoplankton group for the ARA07B (data not shown), major predominant pigments were chlorophyll-b (1.59 ± 1.83 mg m−2), fucoxanthin (1.46 ± 1.47 mg m−2) and chlorophyll-c1+c2 (0.65 ± 0.62 mg m−2). In comparison, fucoxanthin, chlorophyll-c1+c2 and peridinin (a marker pigment of dinoflagellates) were major accessory pigments for the OS040. Fucoxanthin was the most dominant pigment with an average value of 23.03 ± 19.89 mg m−2, followed by chlorophyll-c1+c2 (9.35 ± 7.23 mg m−2) and peridinin (7.54 ± 9.89 mg m−2) for the OS040. High proportions of diatom-related pigments (fucoxanthin, chlorophyll-c1+c2) were observed in both cruise periods. Small diatoms appeared to be major phytoplankton communities for the small phytoplankton group during the ARA07B, based on the high proportions of chlorophyll-b and fucoxanthin. No pigment data were available for the small phytoplankton during the OS040 cruises.
Based on the CHEMTAX results, eight major phytoplankton communities were identified in the study area (Figure 6). Diatoms (43.1% ± 31.5%) and Phaeocystis (33.2% ± 14.9%) were co-dominated during the ARA07B. In comparison, Diatoms were the most dominant community (46.1 ± 17.3%) and the second dominant community was Prasinophyte (Type 2) (11.8% ± 5.3%) for the OS040. Micro-phytoplankton communities were most dominant (59.7 ± 30.5%), followed by nano-phytoplankton (11.5 ± 9.7%) and pico-phytoplankton (28.9 ± 23.5%) during the ARA07B. For the OS040, micro-phytoplankton contributed 51.5% (±18.2%) of the total chlorophyll a concentration. In comparison, nano-phytoplankton and pico-phytoplankton contributed 11.0% (±10.5%) and 37.5% (±15.7%), respectively. The relative proportions of the three size classes based on the diagnostic pigments from HPLC are different from those of the size-fractionated chlorophyll-a concentrations (Figure 4). This is probably due to a simple assumption that diatom-related pigments belong to the micro-phytoplankton although small diatoms (<2 µm) could contribute to the phytoplankton group.

3.4. Primary Production Contribution of Small Phytoplankton and Their Ecological Roles

The daily primary productivities of total phytoplankton which were integrated over the euphotic zone at each station were 33.9–811.8 mg C m−2 d−1 (mean ± SD = 142.6 ± 205.7 mg C m−2 d−1) for the ARA07B and 202.1–3100.1 mg C m−2 d−1 (mean ± SD = 942.1 ± 969.9 mg C m−2 d−1) for the OS040 (Figure 7). In comparison, the daily primary productivities of small phytoplankton ranged from 4.9 to 227.7 (mean ± SD = 42.3 ± 53.1 mg C m−2 d−1) and 56.1 to 322.2 mg C m−2 d−1 (mean ± SD = 152.8 ± 85.2 mg C m−2 d−1) for the ARA07B and the OS040, respectively (Figure 8). The contribution of small phytoplankton to the total primary productivity ranged from 8.1 to 71.7% (mean ± SD = 38.0 ± 19.9%) for the ARA07B and from 6.0 to 40.3% (mean ± SD = 25.0 ± 12.8%) for the OS040 (Figure 9).
Overall, the primary productions of total and small phytoplankton communities during the study period were different depending on the sea area. Indeed, agglomerative hierarchical clustering (AHC) analysis based on 25 stations and phytoplankton size-related variables sorted stations into four distinct groups (Figure 10; Table 3). Cluster 1 include station 1 of OS040 that was high primary productive region (1992.9 mg C m−2 d−1) near Bering strait. Cluster 1 had a relative low contribution of small phytoplankton in primary productivity (5.9%) and surface chlorophyll-a (2.9%). Cluster 2 was station 7 of OS040 that was an extremely high productive station (3100.0 mg C m−2 d−1) and represented the lowest contribution of small phytoplankton among clusters. Small phytoplankton contribution to primary production was 6.9% and the contribution to surface chlorophyll-a concentration was only 0.7% for clusters 2. The physical properties of Cluster 1 (3.5 °C and 32.7 psu) and 2 (5.5 °C and 32.7 psu) were similar. These two clusters are influence by BSW [3,21]. Cluster 3 contains all the stations of the northern Chukchi Sea and two stations of the Bering Sea. The stations form Cluster 3 had a lower productivity and lower concentration of surface chlorophyll-a. In Cluster 3, small phytoplankton contribution was the highest among the clusters. 40.5% of primary production, 39.1% of surface chlorophyll-a and 40.9% of POC were contributed by small phytoplankton. Dominant water mass, IMW can explain the high contribution of small phytoplankton in Cluster 3 because IMW has nutrient-depleted water from sea ice melting [34]. Cluster 4 includes most of the stations in the Bering Sea and 3 stations of the southern Chukchi sea in ARA07B. Cluster 4 had a lower productivity (559.2 mg C m−2 d−1) than cluster 1 and 2 but higher than cluster 3. Cluster 4 seems to be affected by nutrient-depleted ACW but not too low productivity for Cluster 4. This suggests that water masses that had an effect on Cluster 4 were not only ACW but also other source such as mixed water of AW, ACW and BSW.
The primary production contributions of small phytoplankton are rather different from their chlorophyll-a contributions in this study. Normally, the contributions of small phytoplankton are higher to primary production in comparison to those in chlorophyll-a concentrations in the polar oceans [21,41] and temperate oceans [42]. This is probably due to the considerably higher POC contribution of small phytoplankton (and consequently higher production contributions of small phytoplankton) than the chlorophyll-a contribution [21,40,42]. We also observed the higher POC:chlorophyll-a ratio in small phytoplankton than large phytoplankton during both cruises (Figure 11) as discussed later. However, the case in the northern Bering Sea in this study is against the general pattern previously reported. The lower contribution of small phytoplankton was observed in the primary production rather than chlorophyll-a concentration in the northern Bering Sea. This indicates higher standing stock (represented by chlorophyll-a concentrations) of small phytoplankton but their significantly lower contribution to the primary productions in the northern Bering Sea during this study than in other studies. Ref. [20] argued that seasonal increasing contribution of small phytoplankton is not caused by their increasing biomass and photosynthetic rate but caused by relative declining in biomass and photosynthetic rate of large phytoplankton in the Amundsen Sea, Antarctic Ocean. Based on these results, the biomass of large phytoplankton could have had decreased faster than their photosynthetic rate in the northern Bering Sea during our observation period.
The regional contributions of small phytoplankton to the primary production are summarized at various regions in the Arctic Ocean (Table 4). The average contribution of small phytoplankton in this study is comparable to the previous results in the Chukchi Sea. However, it is considerably lower than those (average ± SD = 56.7 ± 20.0%) in the Kara, Laptev and East Siberian Seas [43]. Similarly, reference [41] found a similar contribution (average ± SD = 60 ± 7.9%) of small phytoplankton in the high northern Chukchi Sea and Canada Basin. Because of no data in the northern Bering Sea, the small phytoplankton contribution to the primary production in this study could not be compared. Regionally, the primary production contribution of small phytoplankton in the northern Bering Sea (average ± SD = 25.0 ± 12.8%) is considerably lower than those in others (Table 4). At this point, we do not know whether this is a latitudinal pattern (i.e., increasing contribution of small phytoplankton in higher latitude) or simply seasonal difference among the different regions in the Pacific Arctic Ocean. Indeed, [12] found a seasonal patterns of different phytoplankton size compositions with increasing contribution of small phytoplankton in the northern Bering Sea. Since the seasonal contribution of small phytoplankton to the primary production would be different, further seasonal observations on the small phytoplankton contribution to the primary production will be warranted for better understanding their ecological roles in the Bering and Chukchi Seas.
Table
Table 4. Small phytoplankton contributions to the total primary production in the Arctic Ocean.
Table 4. Small phytoplankton contributions to the total primary production in the Arctic Ocean.
Study AreaYearSeasonSmallcontributionMethodsSizeReferences
Northern Chukchi Sea and Canada Basin2008August–September19.8–60.3%In situ<5 μm[41]
Bering Strait and Chukchi Sea2004August–September31.72 ± 23.59%In situ<5 μm[22]
Kara, Laptev and East Siberian Sea2013August–September52.7–71.2%In situ<5 μm[43]
Barents Sea2003–2005Early to late bloom period31–87%In situ<10 μm[44]
North water polynya1998April–July19%In situ<5 μm[45]
Chukchi Sea and Bering Strait2016August38.0 ± 19.9%In situ<2 μmThis study
Northern Bering Sea and Bering Strait2017July25.0 ± 12.8%In situ<2 μm
Biochemical compositions (POC:chlorophyll-a, PON:chlorophyll-a and C:N ratios) were compared between small and large phytoplankton in Figure 11. Large phytoplankton group has relatively lower POC:chlorophyll-a ratios (t-test, p < 0.01) which were 78.0–3549.0 (mean ± SD = 1358.6 ± 1170.8) for the ARA07B and 41.4–340.2 (mean ± SD = 173.8 ± 110.4) for the OS040 (Figure 9a). In comparison, POC:chlorophyll-a ratios of small phytoplankton were 408.5–6547.4 (mean ± SD = 2590.2 ± 1523.0) for ARA07B and 274.9–2303.6 (mean ± SD = 623.4 ± 639.2) for the OS040. The PON:chlorophyll-a ratio of large phytoplankton was 1.9–184.2 (mean ± SD = 62.4 ± 48.7) whereas the ratio of small phytoplankton ranged from 50.0 to 328.7 (mean ± SD = 211.9 ± 88.3) for the ARA07B (no data for OS040). The C:N ratios were 7.5–251.9 (mean ± SD = 34.1 ± 58.9) for large phytoplankton and 7.0–19.9 (mean ± SD = 11.9 ± 3.8) for small phytoplankton during the ARA07B cruise. Small phytoplankton showed a comparatively higher POC:chlorophyll-a ratio than large phytoplankton during both cruises (Figure 11). This result is consistent with the previous result in the Chukchi Sea, which suggests that higher carbon contents per unit of chlorophyll-a concentration in small phytoplankton in comparison to large phytoplankton [21]. In the Antarctic Ocean, [41] observed the consistent results in non-polynya and polynya regions in the Amundsen Sea. A similar pattern was observed for the PON:chlorophyll-a ratio in this study. However, the C:N ratios of small phytoplankton were lower than those of large phytoplankton in this study. Similarly, the overall C:N assimilation ratio of small phytoplankton was previously reported as significantly lower than that of large phytoplankton [21]. These results are consistent with the result in the Gulf of St. Lawrence, Canada [44]. In the Antarctic Ocean, the similar result was obtained in the Amundsen Sea [41]. The C:N ratios were negatively correlated with chlorophyll-a concentrations for small and large phytoplankton in this study (R2 > 0.6). However, there was no statistically significant difference in the relationship between small and large phytoplankton (p > 0.05; Figure 11).

4. Summary and Conclusions

For determining the dominant phytoplankton communities and the relative contribution of small phytoplankton (<2 µm) to the total primary production, two arctic research cruises were conducted in the Chukchi Sea onboard the icebreaker R/N Araon in 2016 (ARA07B) and mainly in the northern Bering Sea onboard T/S Oshoro-Maru in 2017 (OS040) for this study. The dominant phytoplankton communities were diatoms and phaeocystis during the ARA07B, whereas diatoms and Prasinophyte (Type 2) during the OS040. Based on the AHC analysis, the primary productions of total and small phytoplankton communities were different depending on the sea area. Overall, high primary productions and low contributions of small phytoplankton during both study periods were distributed in the Bering Strait region which was affected by nutrient-enriched BSW. Different biochemical compositions between small and large phytoplankton were observed in this study. The small phytoplankton group had a higher POC:chlorophyll-a (t-test, p <0.01) and PON:chlorophyll-a ratio than large phytoplankton in this study, which suggests that small phytoplankton have higher carbon and nitrogen contents per unit of chlorophyll-a concentration [21]. In addition, small phytoplankton had lower C:N ratios than large phytoplankton in this study. Together with these results, we could conclude that small phytoplankton incorporate more nitrogen in relation to carbon into their bodies and thus produce nitrogen-rich organic matters [43] which could be relatively faster regenerated than carbon-rich organic matters such as carbohydrates [46]. Therefore, the study for small phytoplankton which could be an important basic food source in the Arctic ecosystem should be further conducted under the current warming ocean scenario.

Author Contributions

Conceptualization, J.-W.P., T.H. and S.-H.L.; methodology, J.-W.P., A.F., Y.K., K.-W.K. and H.W.; software, J.-W.P.; validation, J.-W.P. and T.H.; formal analysis, J.-W.P., A.F., J.J.K. and T.H.; investigation, K.-W.K., J.-W.P. and E.-J.Y.; writing—original draft, J.-W.P.; writing—review and editing, T.H. and J.J.K.; visualization, J.-W.P., Y.K. and K.-W.K.; supervision, T.H. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Arctic Challenge for Sustainability (ArCS; JPMXD1300000000) and Arctic Challenge for Sustainability II (ArCS-II; JPMXD1420318865) Project of the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) and by the Global Change Observation Mission-Climate (GCOM-C; 17RSTK001714) project of the Japan Aerospace Exploration Agency (JAXA). This research also was part of the projected titled “Korea-Arctic Ocean Warming and Responses of Ecosystem (K-AWARE, KOPRI, 1525011760)”, funded by the Ministry of Oceans and Fisheries, Korea.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data Availability Statements in section “MDPI Research Data Policies” at https://www.mdpi.com/ethics, accessed on 7 January 2022.

Acknowledgments

The austhors thank the captains and crew members for our field observations. In addition, We thanks to ArCS-II project for funding this publication.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Sambrotto, R.N.; Goering, J.J.; McRoy, C.P. Large yearly production of phytoplankton in the western Bering Sea. Science 1984, 225, 1147–1150. [Google Scholar] [CrossRef] [PubMed]
  2. Springer, A.M.; McRoy, C.P. The paradox of pelagic food webs in the northern Bering Sea. III. Patterns of primary production. Cont. Shelf Res. 1993, 13, 575–599. [Google Scholar] [CrossRef]
  3. Lee, S.H.; Whitledge, T.E.; Kang, S.H. Recent carbon and nitrogen uptake rates of phytoplankton in Bering Strait and the Chukchi Sea. Cont. Shelf Res. 2007, 27, 2231–2249. [Google Scholar] [CrossRef]
  4. Bluhm, B.; Gradinger, R. Regional Variability in Food Availability for Arctic Marine Mammals. Ecol. Appl. 2008, 18, S77–S96. [Google Scholar] [CrossRef] [PubMed]
  5. Grebmeier, J.M.; Bluhm, B.A.; Cooper, L.W.; Denisenko, S.G.; Iken, K.; Kędra, M.; Serratos, C. Time-series benthic community composition and biomass and associated environmental characteristics in the Chukchi Sea during the RUSALCA 2004–2012 Program. Oceanography 2015, 28, 116–133. [Google Scholar] [CrossRef]
  6. Overland, J.; Stabeno, P. Is the Climate of the Bering Sea Warming and Affecting the Ecosystem? EOS Trans. AGU 2004, 85, 309–316. [Google Scholar] [CrossRef] [Green Version]
  7. Grebmeier, J.; Cooper, L.; Feder, H.; Sirenko, B. Ecosystem Dynamics of the Pacific-Influenced Northern Bering and Chukchi Seas in the Amerasian Arctic. Prog. Oceanogr. 2006, 71, 331–361. [Google Scholar] [CrossRef]
  8. Danielson, S.L.; Ahkinga, O.; Ashjian, C.; Basyuk, E.; Cooper, L.W.; Eisner, L.; Farley, E.; Iken, K.B.; Grebmeier, J.M.; Juranek, L.; et al. Manifestation and consequences of warming and altered heat fluxes over the Bering and Chukchi Sea continental shelves. Deep-Sea Res. II Top. Stud. Oceanogr. 2020, 177, 104871. [Google Scholar] [CrossRef]
  9. Woodgate, R. Increases in the Pacific inflow to the Arctic from 1990 to 2015, and insights into seasonal trends and driving mechanisms from year-round Bering Strait mooring data. Prog. Oceanogr. 2018, 160, 124–154. [Google Scholar] [CrossRef] [Green Version]
  10. Frey, K.E.; Moore, G.W.K.; Cooper, L.W.; Grebmeier, J.M. Divergent patterns of recent sea ice cover across the Bering, Chukchi, and Beaufort seas of the Pacific Arctic Region. Prog. Oceanogr. 2015, 136, 32–49. [Google Scholar] [CrossRef]
  11. Grebmeier, J.M. Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic Seas. Annu. Rev. Mar. Sci. 2012, 4, 63–78. [Google Scholar] [CrossRef] [Green Version]
  12. Lee, S.H.; Ryu, J.; Lee, D.; Park, J.W.; Kwon, J.I.; Zhao, J.; Son, S. Spatial variations of small phytoplankton contributions in the Northern Bering Sea and the Southern Chukchi Sea. GISci. Remote Sens. 2019, 56, 794–810. [Google Scholar] [CrossRef]
  13. Coupel, P.; Matsuoka, A.; Ruiz-Pino, D.; Gosselin, M.; Marie, D.; Tremblay, J.-É.; Babin, M. Pigment signatures of phyto- plankton communities in the Beaufort Sea. Biogeosciences 2015, 12, 991–1006. [Google Scholar] [CrossRef] [Green Version]
  14. Yun, M.S.; Whitledge, T.E.; Stockwell, D.; Son, S.H.; Lee, J.H.; Park, J.W.; Lee, D.B.; Park, J.; Lee, S.H. Primary production in the Chukchi Sea with potential effects of freshwater content. Biogeosciences 2016, 13, 737–749. [Google Scholar] [CrossRef] [Green Version]
  15. Fujiwara, A.; Hirawake, T.; Suzuki, K.; Eisner, L.; Imai, I.; Nishino, S.; Kikuchi, T.; Saitoh, S.-I. Influence of timing of sea ice retreat on phytoplankton size during marginal ice zone bloom period on the Chukchi and Bering shelves. Biogeosciences 2016, 13, 115–131. [Google Scholar] [CrossRef] [Green Version]
  16. Kahru, M.; Brotas, V.; Manzano-Sarabia, M.; Mitchell, B.G. Are phytoplankton blooms occurring earlier in the Arctic? Glob. Chang. Biol. 2011, 17, 1733–1739. [Google Scholar] [CrossRef]
  17. Arrigo, K.R.; van Dijken, G.L. Continued increases in Arctic Ocean primary production. Prog. Oceanogr. 2015, 136, 60–70. [Google Scholar] [CrossRef]
  18. Li, W.; McLaughlin, F.; Lovejoy, C.; Carmack, E. Smallest Algae Thrive as the Arctic Ocean Freshens. Science 2009, 326, 539. [Google Scholar] [CrossRef] [Green Version]
  19. Neeley, A.; Harris, L.; Frey, K. Unraveling phytoplankton community dynamics in the Northern Chukchi Sea under sea-ice covered, and sea-ice-free conditions. Geophys. Res. Lett. 2018, 45, 7663–7671. [Google Scholar] [CrossRef]
  20. Lim, Y.J.; Kim, T.W.; Lee, S.; Lee, D.; Park, J.; Kim, B.K.; Lee, S.H. Seasonal Variations in the Small Phytoplankton Contribution to the Total Primary Production in the Amundsen Sea, Antarctica. J. Geophys. Res. Ocean. 2019, 124, 8324–8341. [Google Scholar] [CrossRef]
  21. Lee, S.H.; Yun, M.S.; Kim, B.K.; Joo, H.T.; Kang, S.H.; Kang, C.K.; Whitledge, T.E. Contribution of small phytoplankton to total primary production in the Chukchi Sea. Cont. Shelf Res. 2013, 68, 43–50. [Google Scholar] [CrossRef]
  22. Joo, H.T.; Park, J.W.; Son, S.H.; Noh, J.H.; Jeong, J.Y.; Kwak, J.H.; Saux-Picart, S.; Choi, J.H.; Kang, C.K.; Lee, S.H. Long-term annual primary production in the Ulleung Basin as a biological hot spot in the East/Japan Sea. J. Geophys. Res. Ocean. 2014, 119, 5. [Google Scholar] [CrossRef] [Green Version]
  23. Yun, M.S.; Joo, H.T.; Park, J.W.; Kang, J.J.; Kang, S.H.; Lee, S.H. Lipid-rich and protein-poor carbon allocation patterns of phytoplankton in the northern Chukchi Sea, 2011. Cont. Shelf Res. 2018, 158, 26–32. [Google Scholar] [CrossRef]
  24. Frigstad, H.; Andersen, T.; Bellerby, R.G.J.; Silyakova, A.; Hessen, D. Variation in the seston C:N ratio of the Arctic Ocean and pan-Arctic shelves. J. Mar. Syst. 2014, 129, 214–223. [Google Scholar] [CrossRef] [Green Version]
  25. Kirk, J.T.O. Effects of suspensoids (turbidity) on penetration of solar radiation in aquatic ecosystems, in Perspectives in Southern Hemisphere. Hydrobiologia 1985, 28, 195–208. [Google Scholar] [CrossRef]
  26. Parsons, T.R.; Maita, Y.; Lalli, C.M. A manual of chemical & biological methods for seawater analysis. Mar. Pollut. Bull. 1984, 1, 101–112. [Google Scholar]
  27. Suzuki, K.; Hinuma, A.; Saito, H.; Kiyosawa, H.; Liu, H.; Saino, T.; Tsuda, A. Responses of phytoplankton and heterotrophic bacteria in the northwest subarctic Pacific to in situ iron fertilization as estimated by HPLC pigment analysis and flow cytometry. Prog. Oceanogr. 2005, 64, 167–187. [Google Scholar] [CrossRef]
  28. Wright, S.W.; Jeffrey, S.W.; Mantoura, R.F.C.; Llewellyn, C.A.; Bjørnland, T.; Repeta, D.; Welschmeyer, N. Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Mar. Ecol. Prog. Ser. 1991, 77, 183–196. [Google Scholar] [CrossRef]
  29. Vidussi, F.; Roy, S.; Lovejoy, C.; Gammelgaard, M.; Thomsen, H.A.; Booth, B.; Tremblay, J.-É.; Mostajir, B. Spatial and temporal variability of the phytoplankton community structure in the North Water Polynya, investigated using pigment biomarkers. Can. J. Fish. Aquat. Sci. 2004, 61, 2038–2052. [Google Scholar] [CrossRef]
  30. Fujiwara, A.; Hirawake, T.; Suzuki, K.; Saitoh, S.-I. Remote sensing of size structure of phytoplankton communities using optical properties of the Chukchi and Bering Sea shelf region. Biogeosciences 2011, 8, 3567–3580. [Google Scholar] [CrossRef] [Green Version]
  31. Fujiwara, A.; Hirawake, T.; Suzuki, K.; Imai, I.; Saitoh, S.-I. Timing of sea ice retreat can alter phytoplankton community structure in the western Arctic Ocean. Biogeosciences 2014, 11, 1705–1716. [Google Scholar] [CrossRef] [Green Version]
  32. Ardyna, M.; Mundy, C.J.; Mills, M.M.; Oziel, L.; Grondin, P.-L.; Lacour, L.; Verin, G.; Dijken, G.; Ras, J.; Alou-Font, E.; et al. Environmental drivers of under-ice phytoplankton bloom dynamics in the Arctic Ocean. Elem. Sci. Anthr. 2020, 8, 30. [Google Scholar] [CrossRef]
  33. Lee, S.H.; Kim, H.J.; Whitledge, T.E. High incorporation of carbon into proteins by the phytoplankton of the Bering Strait and Chukchi Sea. Cont. Shelf Res. 2009, 29, 1689–1696. [Google Scholar] [CrossRef]
  34. Hama, T.; Miyazaki, T.; Ogawa, Y.; Iwakuma, T.; Takahashi, M.; Otsuki, A.; Ichmura, S. Measurement of photosynthetic production of a marine phytoplankton population using a sTable 13C isotope. Mar. Biol. 1983, 73, 31–36. [Google Scholar] [CrossRef]
  35. Danielson, S.A.; Eisner, L.; Ladd, C.; Mordy, C.; Sousa, L.; Weingartner, T.J. A comparison between late summer 2012 and 2013 water masses, macronutrients, and phytoplankton standing crops in the northern Bering and Chukchi Seas. Deep-Sea Res. Part II 2017, 135, 7–26. [Google Scholar] [CrossRef] [Green Version]
  36. Coachman, L.K.; Aagaard, K.; Trip, R.B. Bering Strait: The Regional Physical Oceanography; University of Washington Press: Seattle, WA, USA, 1975. [Google Scholar]
  37. Springer, A.M.; McRoy, C.P.; Turco, K.R. The paradox of pelagic food webs in the northern Bering Sea—II. Zooplankton communities. Cont. Shelf Res. 1989, 9, 359–386. [Google Scholar] [CrossRef]
  38. Yun, M.S.; Kim, B.K.; Joo, H.T.; Yang, E.J.; Nishino, S.; Chung, K.H.; Kang, S.H.; Lee, S.H. Regional productivity of phytoplankton in the Western Arctic Ocean during summer in 2010. Deep Sea Res. II 2015, 120, 61–71. [Google Scholar] [CrossRef]
  39. Yun, M.S.; Whitledge, T.E.; Kong, M.; Lee, S.H. Low primary production in the Chukchi Sea shelf, 2009. Cont. Shelf Res. 2014, 76, 1–11. [Google Scholar] [CrossRef]
  40. Lee, S.H.; Joo, H.M.; Yun, M.S.; Whiteledge, T.E. Recent phytoplankton productivity of the northern Bering Sea during early summer in 2007. Polar Biol. 2012, 35, 83–98. [Google Scholar] [CrossRef]
  41. Lee, S.H.; Kim, B.K.; Lim, Y.J.; Joo, H.; Kang, J.J.; Lee, D.; Park, J.; Ha, S.-Y.; Lee, S.H. Small phytoplankton contribution to the standing stocks and the total primary production in the Amundsen Sea. Biogeosciences 2017, 14, 3705–3713. [Google Scholar] [CrossRef] [Green Version]
  42. Lee, S.H.; Joo, H.T.; Lee, J.H.; Lee, J.H.; Kang, J.J.; Lee, H.W.; Lee, D.B.; Kang, C.K. Seasonal carbon uptake rates of phytoplankton in the northern East/Japan Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 2017, 143, 45–53. [Google Scholar] [CrossRef]
  43. Bhavya, P.S.; Lee, J.H.; Lee, H.W.; Kang, J.J.; Lee, J.H.; Lee, D.B.; Ahn, S.H.; Stockwell, D.; Whitledge, T.E.; Lee, S.H. First in situ estimations of small phytoplankton carbon and nitrogen uptake rates in the Kara, Laptev, and East Siberian seas. Biogeosciences 2018, 15, 5503–5517. [Google Scholar] [CrossRef] [Green Version]
  44. Hodal, H.; Kristiansen, S. The importance of small-celled phytoplankton in spring blooms at the marginal ice zone in the northern Barents Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 2008, 55, 2176–2185. [Google Scholar] [CrossRef] [Green Version]
  45. Mei, Z.-P.; Legendre, L.; Gratton, Y.; Tremblay, J.-É.; LeBlanc, B.; Klein, B.; Goseelin, M. Phytoplankton production in the North Water Polynya: Size-fractions and carbon fluxes, April to July 1998. Mar. Ecol. Prog. Ser. 2003, 256, 13–27. [Google Scholar] [CrossRef]
  46. Kim, J.-M.; Lee, K.; Suh, Y.-S.; Han, I.-S. Phytoplankton Do Not Produce Carbon-Rich Organic Matter in High CO2 Oceans. Geophys. Res. Lett. 2018, 45, 4189–4197. [Google Scholar] [CrossRef]
Water 14 00235 g001 550
Figure 1. Sampling locations of (a) ARA07B and (b) OS040 cruises.
Figure 1. Sampling locations of (a) ARA07B and (b) OS040 cruises.
Water 14 00235 g001
Water 14 00235 g002 550
Figure 2. T–S diagram in the ARA07B (Red) and OS040 (Green). Alaskan coastal water (ACW), Bering Shelf water (BSW), ice melt water (IMW), Bering–Chukchi winter water (BCWW), Bering Sea Anadyr water (BSAW).
Figure 2. T–S diagram in the ARA07B (Red) and OS040 (Green). Alaskan coastal water (ACW), Bering Shelf water (BSW), ice melt water (IMW), Bering–Chukchi winter water (BCWW), Bering Sea Anadyr water (BSAW).
Water 14 00235 g002
Water 14 00235 g003 550
Figure 3. Spatial distributions of column-integrated chlorophyll-a concentration of (a) ARA07B and (b) OS040.
Figure 3. Spatial distributions of column-integrated chlorophyll-a concentration of (a) ARA07B and (b) OS040.
Water 14 00235 g003
Water 14 00235 g004 550
Figure 4. Total chlorophyll-a concentration of (a) ARA07B and (b) OS040.
Figure 4. Total chlorophyll-a concentration of (a) ARA07B and (b) OS040.
Water 14 00235 g004
Water 14 00235 g005 550
Figure 5. Pigment compositions of total phytoplankton in the (a) ARA07B (b) OSO040.
Figure 5. Pigment compositions of total phytoplankton in the (a) ARA07B (b) OSO040.
Water 14 00235 g005
Water 14 00235 g006 550
Figure 6. Phytoplankton community compositions of (a) ARA07B and (b) OS040.
Figure 6. Phytoplankton community compositions of (a) ARA07B and (b) OS040.
Water 14 00235 g006
Water 14 00235 g007 550
Figure 7. Primary production of total phytoplankton during the (a) ARA07B and (b) OS040.
Figure 7. Primary production of total phytoplankton during the (a) ARA07B and (b) OS040.
Water 14 00235 g007
Water 14 00235 g008 550
Figure 8. Primary production of small phytoplankton during the (a) ARA07B and (b) OS040.
Figure 8. Primary production of small phytoplankton during the (a) ARA07B and (b) OS040.
Water 14 00235 g008
Water 14 00235 g009 550
Figure 9. Primary production of small phytoplankton of (a) ARA07B and (b) OS040.
Figure 9. Primary production of small phytoplankton of (a) ARA07B and (b) OS040.
Water 14 00235 g009
Water 14 00235 g010 550
Figure 10. Dendrogram stands for sampling stations were divided into four clusters by agglomerative hierarchical clustering (AHC).
Figure 10. Dendrogram stands for sampling stations were divided into four clusters by agglomerative hierarchical clustering (AHC).
Water 14 00235 g010
Water 14 00235 g011 550
Figure 11. Comparison of (a) POC:chlorophyll-a ratios, (b) PON:chlorophyll-a ratios and (c) C:N ratios between small and large phytoplankton in the northern Bering and Chukchi seas. Only POC:chlorophyll-a data available for the OS040. (d) C:N ratio and chlorophyll-a of each size group.
Figure 11. Comparison of (a) POC:chlorophyll-a ratios, (b) PON:chlorophyll-a ratios and (c) C:N ratios between small and large phytoplankton in the northern Bering and Chukchi seas. Only POC:chlorophyll-a data available for the OS040. (d) C:N ratio and chlorophyll-a of each size group.
Water 14 00235 g011
Table
Table 1. Sampling locations in the Northern Bering and Chukchi Seas.
Table 1. Sampling locations in the Northern Bering and Chukchi Seas.
StationDateLatitude (°N)Longitude (°E)Bottom depth (m)
ARA07Bst. 15 Aug 201665.17−168.6949
st. 36 Aug 201667.67−168.9650
st. 66 Aug 201668.01−167.8752.3
st. 128 Aug 201672.36−168.6755
st. 149 Aug 201674.80−167.90223
st. 1517 Aug 201675.24−171.98512
st. 1610 Aug 201675.15−176.00331.57
st. 1811 Aug 201675.77177.07486
st. 1912 Aug 201676.00173.60282
st. 2012 Aug 201677.00176.571232
st. 2113 Aug 201678.00177.281693
st. 2315 Aug 201677.87−175.911564
st. 2416 Aug 201677.00−175.002008
st. 2818 Aug 201677.70−169.501756
st. 2918 Aug 201677.47−164.12280
st. 3019 Aug 201676.58−165.38987
OS04019 Jul 201766.28−168.9057
511 Jul 201765.66−168.2645
712 Jul 201765.06−169.6451
914 Jul 201765.07−168.1942
U−316 Jul 201764.44−166.5227
1317 Jul 201764.50−169.5242
1518 Jul 201764.50−170.8946
1919 Jul 201763.50−173.0266
2321 Jul 201762.17−170.5046
Table
Table 2. Pigment:chlorophyll-a ratios for nine algal groups referred to [32]. CHEMTAX initial ratio matrix and final pigment ratios obtained by CHEMTAX on the pigment data.
Table 2. Pigment:chlorophyll-a ratios for nine algal groups referred to [32]. CHEMTAX initial ratio matrix and final pigment ratios obtained by CHEMTAX on the pigment data.
Classchl-bchl-c3fucoxperidallox19butfu19hexfuchl-cneoxprasinoxlut
Initial ratio matrix
Diatoms000.42500000.171000
Dinoflagellates0000.60000000
Cryptophytes00000.673000000
Chryso-Pelago00.1140.285000.83100.285000
Prasino-20.81200000000.03300.096
Prasino-30.76400000000.0780.2480.009
Chlorophytes0.33900000000.03600.187
Phaeocystis00.2080.3500000000
Hapto-700.1710.259000.0130.4910.276000
ARA07B Final ratio matrix
Diatoms000.78500000.395000
Dinoflagellates0000.60000000
Cryptophytes00000.673000000
Chryso-Pelago00.1140.285000.83100.285000
Prasino-20.59300000000.00700.007
Prasino-34.00600000000.1660.8030.027
Chlorophytes0.33900000000.03600.187
Phaeocystis00.17910.30100000000
Hapto-700.1710.259000.0130.5080.276000
OS040Final ratio matrix
Diatoms000.72200000.328000
Dinoflagellates0001.4090000000
Cryptophytes00000.673000000
Chryso-Pelago00.1140.285000.83100.285000
Prasino-20.81200000000.03300.096
Prasino-30.28000000000.1070.4710.011
Chlorophytes0.64300000000.02900.969
Phaeocystis00.5581.45700000000
Hapto-700.1710.259000.0130.6170.276000
Abbreviations: chlorophyll-b (chl-b), chlorophyll-c3 (chl-c3), fucoxanthin (fucox), peridinin (period), alloxanthin (allox), 19′-butanoyloxyfucoxanthin (19butfu), 19′-hexanoyloxyfucoxanthin(19hexfu), chlorophyll-c1+c2 (chl-c), neoxanthin (neox), prasinoxanthin (prasinox), lutein (lut). Chrysophytes and Pelagophytes (Cryso-pelago). Prasinophytes type 2 (Prasino-2), Prasinophytes type 3 (Prasino-3), Haptophytes (Hapto-7).
Table
Table 3. Mean values of properties for the 4 clusters classified by the AHC.
Table 3. Mean values of properties for the 4 clusters classified by the AHC.
ClusterT
(°C)		S
(psu)		Small
Contribution
to PP		Small
Contribution
to Surface chl-a		Small
Contribution to POC		PP
(mg C m−2 d−1)		Chl-a
(mg m−3)		POC
(mg m−3)
13.532.76.0%2.9%25.0%1992.966.3349.0
25.532.76.9%0.7%18.6%3100.1128.8479.5
30.129.740.5%39.1%40.9%79.613.9177.7
45.631.726.7%39.1%43.9%559.260.7236.1
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Park, J.-W.; Kim, Y.; Kim, K.-W.; Fujiwara, A.; Waga, H.; Kang, J.J.; Lee, S.-H.; Yang, E.-J.; Hirawake, T. Contribution of Small Phytoplankton to Primary Production in the Northern Bering and Chukchi Seas. Water 2022, 14, 235. https://doi.org/10.3390/w14020235

AMA Style

Park J-W, Kim Y, Kim K-W, Fujiwara A, Waga H, Kang JJ, Lee S-H, Yang E-J, Hirawake T. Contribution of Small Phytoplankton to Primary Production in the Northern Bering and Chukchi Seas. Water. 2022; 14(2):235. https://doi.org/10.3390/w14020235

Chicago/Turabian Style

Park, Jung-Woo, Yejin Kim, Kwan-Woo Kim, Amane Fujiwara, Hisatomo Waga, Jae Joong Kang, Sang-Heon Lee, Eun-Jin Yang, and Toru Hirawake. 2022. "Contribution of Small Phytoplankton to Primary Production in the Northern Bering and Chukchi Seas" Water 14, no. 2: 235. https://doi.org/10.3390/w14020235

APA Style

Park, J. -W., Kim, Y., Kim, K. -W., Fujiwara, A., Waga, H., Kang, J. J., Lee, S. -H., Yang, E. -J., & Hirawake, T. (2022). Contribution of Small Phytoplankton to Primary Production in the Northern Bering and Chukchi Seas. Water, 14(2), 235. https://doi.org/10.3390/w14020235

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop