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In Situ Rates of Carbon and Nitrogen Uptake by Phytoplankton and the Contribution of Picophytoplankton in Kongsfjorden, Svalbard

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In Situ Rates of Carbon and Nitrogen Uptake by Phytoplankton and the Contribution of Picophytoplankton in Kongsfjorden, Svalbard water Article In Situ Rates of Carbon and Nitrogen Uptake by Phytoplankton and the Contribution of Picophytoplankton in Kongsfjorden, Svalbard Bo Kyung Kim, Hyoung Min Joo, Jinyoung Jung, Boyeon Lee and Sun-Yong Ha * Division of Polar Ocean Sciences, Korea Polar Research Institute, 26 Songdomirae-ro, Yeonsu-gu, Incheon 21990, Korea; [email protected] (B.K.K.); [email protected] (H.M.J.); [email protected] (J.J.); [email protected] (B.L.) * Correspondence: [email protected] Received: 20 August 2020; Accepted: 15 October 2020; Published: 17 October 2020 Abstract: Rapid climate warming and the associated melting of glaciers in high-latitude open fjord systems can have a significant impact on biogeochemical cycles. In this study, the uptake rates of carbon and nitrogen (nitrate and ammonium) of total phytoplankton and picophytoplankton (<2 µm) were measured in Kongsfjorden in early May 2017 using the dual stable isotope technique. The daily 2 1 uptake rates of total carbon and nitrogen ranged from 0.3 to 1.1 g C m− day− , with a mean of 0.7 0.3 g C m 2 day 1, and 0.13 to 0.17 g N m 2 day 1, with a mean of 0.16 0.02 g N m 2 day 1. ± − − − − ± − − Microphytoplankton (20–200 µm) accounted for 68.1% of the total chlorophyll a (chl-a) concentration, while picophytoplankton (<2 µm) accounted for 19.6% of the total chl-a, with a high contribution to the carbon uptake rate (42.9%) due to its higher particulate organic carbon-to-chl-a ratio. The contributions of picophytoplankton to the total nitrogen uptake rates were 47.1 10.6% for nitrate and 74.0 16.7% ± ± for ammonium. Our results indicated that picophytoplankton preferred regenerated nitrogen, such as ammonium, for growth and pointed to the importance of the role played by picophytoplankton in the local carbon uptake rate during the early springtime in 2017. Although the phytoplankton community, in terms of biovolume, in all samples was dominated by diatoms and Phaeocystis sp., a higher proportion of nano- and picophytoplankton chl-a (mean SD = 71.3 16.4%) was observed in the ± ± relatively cold and turbid surface water in the inner fjord. Phytoplankton production (carbon uptake) decreased towards the inner fjord, while nitrogen uptake increased. The contrast in carbon and nitrogen uptake is likely caused by the gradient in glacial meltwater which affects both the light regime and nutrient availability. Therefore, global warming-enhanced glacier melting might support lower primary production (carbon fixation) with higher degrees of regeneration processes in fjord systems. Keywords: phytoplankton productivity; carbon and nitrogen; stable isotopes; Kongsfjorden; Svalbard 1. Introduction Marine phytoplankton play a critical role in global carbon and nitrogen cycling [1,2]. They uptake carbon dioxide from the atmosphere through photosynthesis and transform it into organic matter as well as uptaking nitrogen and other nutrients (e.g., phosphorous, silicate, trace metals), and they contribute approximately 50% of global primary production (carbon fixation) [3]. In marine systems, production depends on allochthonous inputs of nutrients (new production based on nitrate), while the remainder is mainly driven by the remineralization of nutrients (regenerated production; based on ammonium and urea) [4]. This distinction provides useful information for the proportion of the organic carbon exported out of the euphotic zone or into higher trophic levels because new production is assumed to be equivalent to the fraction of total production under steady-state conditions [5]. Water 2020, 12, 2903; doi:10.3390/w12102903 www.mdpi.com/journal/water Water 2020, 12, 2903 2 of 22 Climate change is expected to considerably influence the upper ocean in marine ecosystems, such as through rising temperatures and declining ice cover, altering the structure of phytoplankton communities, magnitudes of carbon, nitrogen, and export production, and the efficiency of the biological carbon pump [6–10]. Particularly, changes are more pronounced in the Arctic [11,12]. For example, patterns of increasing picophytoplankton (<2 µm) biomass and a decline in larger cells (2–20 µm) were found in the Canada Basin due to strong vertical stratification with a lower nitrate supply [11]. Although smaller phytoplankton is more competitive under low nutrient concentrations, picophytoplankton-dominated systems do not provide large carbon exports to the deep sea (carbon sequestration). Because picophytoplankton have a high surface-area-to-volume ratio and are more resistant (they do sink, form aggregates and such). As a result, picophytoplankton is considered a critical component of carbon and nitrogen cycling in high-latitude marine ecosystems and likely more important in warmer freshened ocean [11,13,14]. Our study area, Kongsfjorden, is located in the open fjords in western Spitsbergen and geographically belongs to the Arctic. The hydrological condition of this area is characterized by Atlantic water (T > 3 ◦C, S > 34.9), glacial meltwater, and Arctic water (T = 0.5–2 ◦C, S = 34.7–34.9) ([15–17] and references therein). The mixing process of these water masses influences the spatial and temporal variation in the food web [18,19]. Generally, phytoplankton biomass in Kongsfjorden begins to increase in early spring (March) and then decreases dramatically in late summer and early autumn [16,20]. The progress of the spring bloom is controlled by light and grazing pressure [21], and the primary production of phytoplankton can influence zooplankton production [22,23]. Therefore, knowing the local primary production and the contribution of the picophytoplankton fraction to the total primary production in the Arctic Ocean is useful for assessing the potential impacts caused by environmental changes, such as an intense ice melt season [12,24,25]. A number of studies have reported the composition of coupled pico- and nanoplankton communities (including heterotrophic bacteria) in water masses and/or phytoplankton bloom dynamics in Kongsfjorden [20,26,27]. Unfortunately, only a few in situ measurements of primary production have been conducted in Kongsfjorden [16,20,21,28]. Hence, the purposes of this study were (i) to investigate spatial variation in the phytoplankton community structure and the rates of carbon and nitrogen uptake and (ii) to estimate the contribution of picophytoplankton to the total biomass and carbon and nitrogen uptake rates during the spring period in Kongsfjorden, Svalbard. 2. Materials and Methods 2.1. Study Area and Sampling Kongsfjorden is a fjord in western Spitsbergen and is located on the Svalbard archipelago. All of the samples except for the carbon and nitrogen uptake rates were collected at a total of ten stations in Kongsfjorden from 4–8 May 2017 onboard the Teisten (Figure1 and Table1). Our sampling stations were divided into three zones based on species distribution, substrate and the overriding environmental gradient described by Hop et al. [16]: the inner zone (St. 1, St. 2, and St. 3), the transition zone (St. 4, St. 5, and St. 6), and the middle zone (St. 7, St. 8, St. 9, and St. 10) (Table1). At each station, we used a conductivity-temperature-depth (CTD) system with a turbidity sensor and Niskin bottles to obtain the water temperature, turbidity, and water samples, respectively. The water samples for the nutrients, chl-a concentrations, and taxonomy were obtained using a Niskin sampler from the surface to a depth of up to 100 m (Table1). The characteristics of each station are summarized in 2 Table1. To estimate the daytime uptake rate, daily solar irradiance (W m − ) data were obtained from the Baseline Surface Radiation Network (BSRN) for the sampling period. The daily solar irradiance was calculated using a 1 h resolution. One percent of the surface irradiance was defined as the euphotic zone, and different light levels were determined (100, 50, 30, 12, 5, and 1%) by a Secchi disc using the vertical attenuation coefficient (Kd = 1.7/Secchi depth) from Poole and Atkins [29]. The euphotic depth was measured only at experiment stations (St. 3, St. 5, St. 7, St. 9, and St. 10). Water 2020, 12, x FOR PEER REVIEW 3 of 23 disc using the vertical attenuation coefficient (Kd = 1.7/Secchi depth) from Poole and Atkins [29]. The Watereuphotic2020, depth12, 2903 was measured only at experiment stations (St. 3, St. 5, St. 7, St. 9, and St. 10). 3 of 22 Figure 1. (A) Sampling stations in Kongsfjorden. The blue dots indicate productivity stations. Surface Figure 1. (A) Sampling stations in Kongsfjorden. The blue dots indicate productivity3 stations. Surface distribution of (B) water temperature (◦C), (C) chlorophyll a (chl-a) (mg m− ), and (D) turbidity (FTU) distribution of (B) water temperature (°C), (C) chlorophyll a (chl-a) (mg··m−3), and (D) turbidity (FTU) in Kongsfjorden (Ocean Data View (ODV) version 5.1.0) (AWI, Bremerhaven, Germany, Schlitzer, R.). in Kongsfjorden (Ocean Data View (ODV) version 5.1.0) (AWI, Bremerhaven, Germany, Schlitzer, R.). Table 1. Sample location with corresponding sampling depth for nutrient, chl-a, andphytoplankton Tabletaxonomy 1. Sample samples location in Kongsfjorden with corresponding in 2017. sampling depth for nutrient, chl-a, andphytoplankton taxonomy samples in Kongsfjorden in 2017. Latitude Longitude Date Bottom Euphotic Sampling Station Zone (◦N) (◦E) (Day,Date Month Year) Depth (m) Depth (m) Depth (m) Latitude Longitude Bottom Euphotic Sampling Station (day, month Zone St. 1(° 78.91N) 12.39(°E) 4 May 2017Depth (m) 63 Depth - (m) 0,Depth 10, 30, (m) 50 Inner St. 2 78.93 12.39 4year May) 2017 47 - 0, 10, 20, 40 Inner St.St. 1 378.91 78.98 12.39 12.32 4 May 7 May 2017 2017 63 55- 16 0,0,4, 10, 16, 30, 40 50 InnerInner St.St. 2 478.93 78.96 12.39 12.22 4 May 7 May 2017 2017 47 14- -0, 0, 10, 5, 1020, 40 TransitionInner St.St.
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