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Composition of algal pigments in surface freshen layer after ice melt in the central Arctic
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Yanpei ZHUANG1, Haiyan JIN1, 2, *, Fan GU1, Yang ZHANG1, Youcheng BAI1, Zhongqiang JI1, Yong LU1, Jianfang CHEN1, 2
Acta Oceanologica Sinica | 2017, 36(8) : 122 - 130
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Acta Oceanologica Sinica | 2017, 36(8): 122-130
• •
Composition of algal pigments in surface freshen layer after ice melt in the central Arctic
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Yanpei ZHUANG1, Haiyan JIN1, 2, *, Fan GU1, Yang ZHANG1, Youcheng BAI1, Zhongqiang JI1, Yong LU1, Jianfang CHEN1, 2
Affiliations
  • 1 Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China
  • 2 State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China
Published: 2017-08-01 doi: 10.1007/s13131-017-1024-0
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Seasonal meltwater input creates a thin freshen layer in surface seawater under ice, which largely shifts the algae assemblages. Our recent observation of photosynthetic pigments in the high Arctic showed that ice bottom and 5 m of seawater under ice contained relatively high concentration of fucoxanthin, while chlorophyll b and lutein were the major diagnostic pigments in ice-water interface and 0 m of seawater under ice. Additionally, a notable change of dominant phytoplankton occurred in the top 5 m of seawater under ice, from chlorophytes-dominated at surface to diatoms-dominated at 5 m depth, which might attribute to the sharp salinity gradient (salinity from 12.5 to 28.1) in the surface seawater under ice. Our results imply that phytoplankton community in surface layer under ice would become more chlorophytes in the future warming Arctic Ocean.

the Arctic Ocean  /  seawater under ice  /  pigments  /  nutrients  /  phytoplankton community
Yanpei ZHUANG, Haiyan JIN, Fan GU, Yang ZHANG, Youcheng BAI, Zhongqiang JI, Yong LU, Jianfang CHEN. Composition of algal pigments in surface freshen layer after ice melt in the central Arctic[J]. Acta Oceanologica Sinica, 2017 , 36 (8) : 122 -130 . DOI: 10.1007/s13131-017-1024-0
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1 Introduction
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Accelerated decline of the Arctic sea ice over the last two decades was one of the most prominent signals of global climate change (Johannessen et al., 1999; Deser and Teng, 2008). Based on the satellite records, the decline rate of Arctic sea ice coverage had already rise from 2.2%–3.0% per decade during the 1979–1996 period to 10.1%–10.7% per decade in present (Comiso et al., 2008), and the ice cover in summer of 2012 declined by at least 40% compared to the average ice cover during 1979–2000 (Parkinson and Comiso, 2013). A freshening trend caused by increased freshwater storage associated with melting of sea ice (Rabe et al., 2011), resulting in a significant change on physical and ecosystem environment in the Arctic Ocean.
How phytoplankton response to sea ice retreat is of central concern due to its ecological importance in marine food web and biological pump. Early studies reported that freshening in the seasonal ice-open basin would favor picophytoplankton thrive but larger cells languish via enhancement of water stability and deepen of nutricline (Li et al., 2009; He et al., 2012). Coupel et al. (2012) also found that distinct distribution of phytoplankton abundance and biomass in marginal ice zone between low ice cover and heavy ice cover in summer. However, information about ecological impact of climate change in the high Arctic is still parse (e.g., Gosselin et al., 1997; Anderson et al., 2003; Rysgaard and Nielsen, 2006; Laney et al., 2013) due to the lack of field work. Therefore it was considered as one of the most required study regions in the Arctic Ocean (Wassmann, 2011).
Thus, it is necessary to have a detailed understanding of phytoplankton response to ice melting and surface freshening in the permanently ice cover water in the high Arctic. In the central Arctic, summer sea ice melting would thin the ice pack, producing a large freshwater input which would lead to dramatic salinity gradient and surface freshening under ice. During the Chinese Arctic cruise in summer 2014, nutrients and phytoplankton observations at a fixed floating ice pack were carried out in order to examine the change of dominant algae at ice bottom and the surface freshening layer under ice. This helps us better understand the ecological and biogeochemical dynamics after ice melting in the high Arctic.
2 Materials and methods
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2.1 Study sites and sampling
During 19 to 23 August 2014 (CHINARE2014), ice cores and water samples were collected at six sampling sites (IT1–IT6) at a floating ice station in the high Arctic. The GPS track of ice drift and sampling sites were shown in Fig. 1. Ice cores were taken with a Mark ice corer and then seawater of ice-water interface was collected immediately. The bottom 5 cm of ice cores were sectioned and melted in pre-filter saline seawater, to avoid algae cell damage by osmotic pressure change (Garrison and Buck, 1986). Ice cores and water samples of IT1 and IT2 were taken on 19 August, IT3 and IT4 on 20 August, and IT5 and IT6 on 21 August. Seawater under sea-ice was collected at 0 m, 2 m and 5 m water depth on 23 August, of which the salinity was measured with WTW ProfiLine Cond 197i portable salinity sensor (Germany).
2.2 Nutrients analysis
Nutrient samples (nitrate plus nitrite, silicate, phosphate) for seawater and ice cores were filtered through pre-washed cellulose acetate membranes (0.45 μm) and measured immediately using a continuous flow analyzer Skarlar San++ (Holland, Breda). Analysis methods for nutrients were referred to the Specification for Oceanographic Survey (General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China (AQSIQ) and Standardization Administration of the People’s Republic of China, 2008) and Grasshoff et al. (1999). The detection limits were 0.1 μmol/L for NO3–+NO2–, 0.1 μmol/L for SiO32–, and 0.03 μmol/L for PO43–, respectively.
2.3 Pigments analysis
For pigment samples, 4–8 L seawater and 1–2 L ice melting water were filtered through GF/F filters under gentle vacuum (<5×104 Pa and dim light condition, and then stored at –80°C until analysis. Pigments were extracted with 3 mL of 100% HPLC-grade methanol at –20°C for 1 h, sonicated (ice-bath) for 30 s and extracted again for 1 h. The extracts were filtered through 0.22 μm microporous membrane. Before 200 μL extract was injected into HPLC system, the extract was premixed with 28 mmol/L tetrabutyl ammonium acetate (TBAA) (1:1 v/v). Pigment was analyzed by HPLC (Waters 600) system equipped with an Eclipse SDB C8 column (150 mm×4.6 mm, 3.5 μm) and with photodiode array detector (Waters 2998), using a solvent system proposed by van Heukelem and Thomas (2001) consisting of Solvent A (methanol) and Solvent B (methanol and TBAA, 70:30, v/v), at a flow rate of 1 mL/min and the column temperature of 45°C. The gradient systems used (min, A%, B%) was as follows: (0, 90, 10), (36, 5, 95), (41, 5, 95), (45, 90, 10), (55, 90, 10). Pigments were qualified and quantified by absorption wavelength at 450 nm for chlorophylls and carotenoids. The peaks were identified by comparing their retention time and spectra with those of pigment standards (DHI water and environment, Demark). Pigments measured were listed in Table 1.
2.4 Relative contributions of different algae assemblagesto chlorophyll a
Matrix factorization program CHEMTAX proposed by Mackey et al. (1998) was the most widely used method to reveal phytoplankton community based on diagnostic pigment ratios. However it is inaccurate for the small dataset of this study, thus a specific pigment ratios method (Marty et al., 2008) was applied to estimate the relative contributions of phytoplankton groups. In this method, the specific ratios of taxonomic pigment to chlorophyll a were selected to calculate algae assemblages. Besides, the calculated algae assemblages were classified as three major groups (Not et al., 2005) based on pigment markers: (1) Diatom-group, refers to fucoxanthin-containing group, mainly diatoms, but also including chrysophytes andprymnesiophytes; (2) Green-group, characterized by the presence of Chl b and lutein, mainly members of green algae (chlorophytes and prasinophytes share several pigments, but not prasinoxanthin); (3) Cyano-group, including cyanophytes and prochlorophytes. The specific pigment ratios for algae groups’ identification were based on Zhuang et al. (2014), which was used on the northern Bering Shelf. The output ratios of diagnostic pigments and chlorophyll a were 0.61 for Fuco, 0.26 for Chl b and 0.35 for Zea, respectively. The empirical formulas were as follows:
CTChla=3.85CChlb+1.64CFuco+2.86CZea,
Fdiatom=1.64CFuco/CTChla,
Fgreen=3.85CChlb/CTChla,
Fcyano=2.86CZea/CTChla,
where Fgreen, Fdiatom and Fcyano represented the relative contribution of Green-group, Diatom-group and Cyano-group to total Chl a biomass, respectively. CChlb, CFuco and CZea represented the concentration of Chl b, Fuco and Zea, respectively.
3 Results
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3.1 Nutrients distribution
The concentrations of nutrients in the bottom section of the ice core were similar at six sampling sites (Fig. A1) and characterized by severe oligotrophic condition, with concentration in average (0.1±0.1) μmol/L (NO3+NO2), (0.04±0.01) μmol/L (PO4) and (1.3±0.0) μmol/L (SiO2), respectively (Table 2). In contrast, phosphate and silicate concentration in ice-water interface were slightly higher than those in ice bottom, with mean value of (0.20±0.11) μmol/L and (1.6±0.2) μmol/L, while inorganic nitrogen was under detected (0.1 μmol/L), suggesting that nitrogen was the absolute limiting nutrient.
As shown in Table 2, seawater under ice (0–5 m) also suffered the nitrogen limitation with inorganic nitrogen ranged from 0 to 0.5 μmol/L, which was lower than phytoplankton growth threshold (defined by 1 μmol/L). Phosphate and silicate in seawater under ice (0–5 m) were relatively abundant with a range from 0.16 to 0.71 μmol/L and 1.8 to 2.4 μmol/L, respectively. Compared to ice bottom and ice-water interface, seawater under ice had relatively high nutrients stocks, with a mean concentration of (0.52±0.19) μmol/L (PO4) and (2.1±0.3) μmol/L (SiO2) respectively.
3.2 Algal pigments
Pigments analysis revealed that Chl a, Fuco, Diadino and Diato were major pigments detected in the bottom segment of the ice cores, with average values of (82±53) ng/dm3, (35±30) ng/dm3, (23±17) ng/dm3 and (5±6) ng/dm3 respectively (Fig. A2), indicating a dominance of diatoms in the algae assemblages of the ice bottom.
Chlorophyll a concentration in ice-water interface ranged from 59 to 198 ng/dm3, with a mean concentration of (112±52) ng/dm3 (Table 2). The highest amount was encountered at IT6 (Fig. A2). Lut was the most abundant carotenoids with an average value of (29±17) ng/dm3, while the averaged concentrations of Chl b and Viola were up to (26±23) ng/dm3 and (16±15) ng/dm3 respectively. Since prasinoxanthin was not detected (Prasinoxanthin was the diagnostic pigment of prasinophyts), the high abundance of Chl b and Viola indicated that chlorophytes was the dominant algae in ice-water interface. Besides, Fuco had a mean concentration of (17±4) ng/dm3 and Zea, a diagnostic pigment of cyano-group, had a mean value of (5±6) ng/dm3.
In the seawater under ice, both the amount and composition of photosynthetic pigments had a significant change along the water depth. Pigments at 0 m depth reached the highest concentration, with Chl a ranged from 62 ng/dm3 to 285 ng/dm3. Chl b and Lut was the major diagnostic pigments, with averaged concentration of (60±34) ng/dm3 and (46±41) ng/dm3 respectively, indicating the distribution of chlorophytes. Algal pigments at 5 m depth were relatively low compared to those at 0 m depth. However pigments at different water depths vary widely. Chl a and Fuco were major components of pigments with average concentration of (38±7) ng/dm3 and (18±3) ng/dm3, whereas others diagnostic pigments were quite low or undetected, suggesting a diatoms-dominated at 5 m depth. While at 2 m depth, two opposite distributed pattern of pigments composition were found in seawater. Fuco was the main diagnostic pigments at Stas IT1 and IT3, while Chl b and Lut were relatively high at the others station. The average concentration of pigments at 0 m depth were (55±8) ng/dm3 (Chl a), (13±7) ng/dm3 (Fuco), (11±13) ng/dm3 (Chl b) and (8±7) ng/dm3 (Lut).
3.3 Algae assemblages
The relative contributions of algae assemblages calculated based on the specific pigment ratios were shown in Table 3. As mentioned above, diatoms were major contributor of diatoms-group and chlorophytes were major contributor of green-group. A high percentage of diatoms (up to 90%) were found in ice bottom and at 5 m depth of seawater under ice. Meanwhile, in ice-water interface and at 0 m depth of seawater under ice, chlorophytes contributed 77% and 87%, respectively, to thetotal chlorophyll a biomass. At 2 m depth of seawater under ice, diatoms and chlorophytes co-dominated the phytoplankton community. Cyanobacteria had a significant distribution in ice-water interface and at 0 m depth of seawater under ice, with a relative contribution of 6% and 3%.
4 Discussion
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4.1 Dramatic change of dominant algae in ice ecosystem
As shown in Fig. 2, pigment-induced phytoplankton community shown that most of algae biomass in ice bottom was contributed by diatoms, with a relative contribution higher than 90%, which was consistent with previous observation in the central Arctic. Gradinger (1999) also found that pennate diatoms dominated in the bottom layer of ice cores, while phototrophic flagellates ruled the upper parts. Besides, pigments biomass of ice bottom in the central Arctic was two or three orders of magnitude lower than that in Chukchi shelf (Gradinger, 2009), which probably ascribed to nutrients availability in the bottom layer.
Phytoplankton community in ice-water interface was dominated by chlorophytes, which was different from ice bottom (Fig. 2), suggesting a distinct mechanism of algal physiology between ice and water. The low salinity in ice-water interface might benefit chlorophytes and others flagellates. Also a green algae bloom was recorded in under-ice ponds with salinity of ice-water interface as low as 9.1 (Gradinger, 1996). It has been reported that the coverage of under-ice ponds accounted for 5% of the Arctic sea ice cover (Eicken, 1994). However, nutrients stock indicated ice-water interface might hardly sustain an algae bloom in the study area.
Chlorophyll a biomass in seawater under ice decreased gradually with the increase of depth, which might be related to light intensity (Fig. 2). With the increase of depth and salinity, the chlorophytes biomass decreased whereas the diatoms biomass increased. Thus, a significant shift of dominant phytoplankton was observed at the top 5 m of seawater under ice, with the algae assemblages shifted from dominance of chlorophytes at 0 m depth to co-dominate by diatoms and chlorophytes at 2 m depth, and then to diatoms-dominated at 5 m depth (Fig. 2). The rapid change of phytoplankton composition in seawater under ice was unique in the global ocean.
Generally, nutrients availability played an important role in phytoplankton selection. For instance large diatoms usually dominated in the nutrients-rich region and picophytoplankton dominated in the oligotrophic water. In here, spearman correlation coefficient analysis showed that change of algae assemblages significantly correlated with environmental variables, such as depth, salinity, phosphate and silicate, but not related with inorganic nitrogen (Table 4). Extremely low concentration of inorganic nitrogen absolutely limited the phytoplankton growth. Thus nutrients were not the major cause of the rapid change of dominant phytoplankton. The salinity change, however, might be the key factor for the phytoplankton shift in such thin layer of seawater under ice. As mentioned, a strong salinity gradient formed in the top 5 m of seawater under ice, with salinity increase from in average 12.5 at 0 m to 28.1 at 5 m (Fig. 2). Apparently, phytoplankton responses promptly to the surface freshening layer in the sea-ice system. Therefore ice melt in summer was an important factor influencing the algae assemblage in the central Arctic.
4.2 Comparison of dominant algae in ice-system with others oligotrophic waters
As in the other oceans, nitrogen limitation constrains sustainability of primary production in the Arctic Ocean (Falkowski, 1997). The surface seawater under ice was considered as the most nitrogen limitation part in the Arctic Ocean (Cota et al., 1990). In tropical and temperate oceans, prochlorophytes and cyanobacteria were usually the dominant algae in oligotrophic surface waters (Table 5) owing to their low nutrients demand. However, distribution of prochlorophytes and cyanobacteria were limited in the Arctic Ocean, due to the low temperature and light availability. Previous study (Coupel et al., 2012) suggested that pico-flagellates (mainly prasinophytes) dominated in phytoplankton community at the ice edge of the Arctic Ocean (Table 5). While in perennially ice-covered central Arctic, algae assemblages of surface water under ice was dominate by chlorophytes. Chlorophytes were widely distributed in the freshwater, thus the extremely low salinity in surface water under ice might beneficial to chlorophytes. In other words, environment factors such as salinity significantly influence the phytoplankton community in different oligotrophic waters, although primary production was subject to nutrients deficiency.
4.3 Impact of freshening on the algal community in the high Arctic
The consequences of the freshening on phytoplankton dynamics in the Arctic Ocean have been well studied in recent years. As shown in Fig. 3, the surface freshening by sea ice reduction and/or higher river runoffs (Yamamoto-Kawai et al., 2009) as well as accelerated nutrient consumption in surface layer, resulted in a more oligotrophic Arctic Ocean with a deepened nutricline (Coupel et al., 2014). Consequently phytoplankton became smaller (Li et al., 2009) and subsurface chlorophyll maximum (SCM) deeper (McLaughlin and Carmack, 2010). In perennially ice-covered area, a strong salinity gradient (from salinity about 5 to 28) formed in the surface layer under sea ice and then a second salinity gradient in halocline layer. Ashift of dominant algae associated with salinity change occurred, from a chlorophytes-dominated community to a diatoms-dominated one. Therefore the increased freshening in the surface layer under sea ice caused by the global warming might shift the phytoplankton community to more chlorophytes in the central Arctic in the future.
5 Conclusions
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In our observation, a dramatic salinity gradient together with an alternation of dominant algae occurred at the top 5 m of the seawater under ice in the high Arctic Ocean. Chlorophytes dominated at 0 m in the seawater with low salinity. The phytoplankton rapidly shifted to diatom-dominated at 5 m with relatively high salinity. Our results imply that phytoplankton community in the surface layer under ice would become more chlorophytes in the future freshening Arctic Ocean. This shift might alter the food web in the perennially ice-covered Arctic Ocean since the community size and structure are strong determinants of the ecosystem carbon flux. A chlorophytes-based system tended not to support large exports of biogenic carbon. Our observation in top 5 m of the seawater under ice was a complement of study on phytoplankton dynamics response to the freshening in the high Arctic Ocean.
Acknowledgements
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The authors appreciate all crews of the R/V Xuelong icebreaker during the 6 th Chinese National Arctic Expedition for their kind help. Thanks are also given to Lin Ling from the Polar Research Institute of China for the help with the field work and Ren Jian from the Second Institute of Oceanography of SOA for critical comments on English manuscript.
Funding
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  • The National Natural Science Foundation of China under contract Nos 41276198 and 41506222; Chinese Polar Environment Comprehensive Investigation & Assessment Programs under contract Nos Chinare-03-04 and Chinare-04-03; Scientific Research Fund of Second Institute of Oceanography, SOA under contract No. JG1323.
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Year 2017 volume 36 Issue 8
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doi: 10.1007/s13131-017-1024-0
  • Receive Date：2016-03-29
  • Online Date：2026-04-16
  • Published：2017-08-01
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History
  • Received：2016-03-29
  • Accepted：2016-09-29
Funding
The National Natural Science Foundation of China under contract Nos 41276198 and 41506222; Chinese Polar Environment Comprehensive Investigation & Assessment Programs under contract Nos Chinare-03-04 and Chinare-04-03; Scientific Research Fund of Second Institute of Oceanography, SOA under contract No. JG1323.
Affiliations
    1 Laboratory of Marine Ecosystem and Biogeochemistry, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China
    2 State Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, State Oceanic Administration, Hangzhou 310012, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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