Sources and distribution of particulate organic carbon in Great Wall Cove and Ardley Cove, King George Island,West Antarctica

TIAN Shichao, JIN Haiyan,3*, GAO Shengquan, ZHUANG Yanpei,ZHANG Yang, WANG Bin & CHEN Jianfang,3

1 Second Institute of Oceanography, State Oceanic Administration (SOA), Hangzhou 310012, China;

2 Laboratory of Marine Ecosystem and Biogeochemistry, SOA, Hangzhou 310012, China;

3 State Key Laboratory of Satellite Ocean Environment Dynamics, Hangzhou 310012, China

1 Introduction

Particulate organic carbon (POC) is a key component of the marine food web and plays an important role in the global carbon cycle. Its flux is controlled by primary productivity and other biological activities[1], and it is the main component of precipitation, transformation and transport of marine organisms[2]. The relationship between carbon, nitrogen and phosphorus in POC provides information regarding the sources and biogeochemical processes controlling the POC. In the Antarctic ocean, POC distribution varies both geographically and with depth[3-4]. POC is more abundant in surface waters than in bottom waters[5-7].

Changes to glacial ablation, permafrost degradation and other effects of recent global warming have altered the nature of organic carbon input into the ocean. This may have affected primary productivity, phytoplankton communities and the input of ancient organic carbon stored in land soil in the Antarctic region.

King George Island is the biggest island of the South Shetland Islands[8]. Near to the northwestern tip of the Antarctic Peninsula, the island is within one of the most rapidly warming regions on Earth[9]. This region has a typical maritime climate, with little annual variation in atmospheric temperature, high relative humidity and constant cloud cover[10]. Great Wall Cove (GWC) is located at the southwest end of King George Island, east of Great Wall Station. GWC runs north to south, from the shared territory between Ardley Island and Fields Peninsula, to Maxwell Bay. It is 1.3 km long and 0.7 km wide, with an area of 0.71 km2[11]. Ardley Cove (AC) lies to the north of Ardley Island. It has an area slightly larger and is deeper than GWC. The depth of GWC is variable with complex bathymetry. The depth inside the bay is～35 m, with depths ＞50 m outside the bay[12]. Both coves are extensions of Maxwell Bay.

Many studies have been conducted at the Great Wall Station, including research regarding meteorological conditions[13], snow accumulation and melt processes[14], land pollution[15], ecosystem dynamics[16], and the hydrological conditions of GWC[11,17-18]. Biogeochemistry parameters such as dissolved oxygen[19], nutrient levels, phytoplankton[20-22],chlorophyll-a(Chl-a)[23-26], and their relationships[27-28]have also been investigated. International research in this area includes examination of the biogeochemistry conditions in the adjacent Antarctic Peninsula[29-31]and King George Island coastal areas[9,32-34]. All these studies indicate that global climate change impacts upon these marine ecosystems, and will further affect the composition of marine organisms as well as burial efficiency.

To improve the current understanding of carbon cycling in the Antarctic region, this study examines the hydrogeochemical conditions and biogeochemical parameters such as POC/Chl-aand the POC stable carbon isotope (δ13C)signatures within GWC and AC, with the aim of determining the distribution and sources of POC in these coves.

2 Materials and methods

2.1 Sampling and sample preparation

Nutrients, POC, Chl-a, temperature and salinity were observed in GWC and AC on 17 and 23 January 2013, during the twenty-ninth Chinese National Antarctic Research Expedition(29th CHINARE). There were five sampling stations in each cove, named G1-G5 in GWC and A1-A5 in AC (Figure 1).Seawater was sampled with a 5-L Niskin sampler. For POC collection, 0.5-2.0 L seawater was filtered on GF/F filters(47 mm, 0.7 μm) that had been pre-combusted for 4 h at 450°C. For Chl-aanalysis, 0.5 L seawater was filtered on GF/F filters (47 mm, 0.7 μm). All samples were stored at -20°C.

2.2 Analytical methods

Filters for detecting POC were dried at 50°C until constant weight and then de-carbonated by fumigating with hydrochloric acid. Carbon concentrations were analyzed using an Elementar Vario MICRO cube elemental analyzer and δ13C was analyzed using a Thermal MAT 253 isotope ratio mass spectrometer. The filters for Chl-aanalysis were extracted in 90% acetone and kept in the dark at -20°C for 24 h. Chl-aconcentrations were determined according to fluorescence readings using a Turner fluorometer (Turner10-AU). Dissolved oxygen was measured using the Winkler titration method according to the Chinese “Specification for Oceanographic Survey” (State Bureau of Quality and Technical Supervision, 2007). Seawater temperature and salinity were measuredin situwith a conductivity,temperature and depth logger (RBRconcerto CTD).

3 Results

3.1 Temperature, salinity and nutrients

Water temperature in GWC was in the range 0.49-1.15°C(mean: 0.72°C) and 0.72-1.36°C (mean: 1.02°C) in AC.Salinity in GWC ranged from 34.02 to 34.21 and from 33.97 to 34.14 in AC. One-way ANOVA tests show that the differences in temperature and salinity between the two coves are both statistically significant (p＜0.05). This indicates a difference in the hydrological regimes of the two coves, most likely because of differences in river discharge and variations in bathymetry.

Both temperature and salinity showed similar trends in the two coves: Temperature decreased with depth,while salinity increased from the inner regions to the outer regions of the coves. Higher temperatures and lower salinities were at depths ＜10 m in both coves. As shown in Figure 2, temperature and salinity show a negative correlation(r=-0.79,p＜0.01,n=37) where higher seawater temperature corresponds to lower salinity. Although no runoff records are available for this region, this pattern implies that meltwater discharge from King George Island affects both coves,especially the upper layer of seawater.

Concentrations of nitrate (GWC: 24.94 μmol∙L-1, AC:24.92 μmol∙L-1), phosphate (GWC: 1.94 μmol∙L-1, AC:1.96 μmol∙L-1) and silicate (GWC: 78.61 μmol∙L-1, AC:79.32 μmol∙L-1) showed little difference between the two coves. Concentrations of these compounds in the river discharge into the two coves are in the range of 0.95-3.10 μmol∙L-1for nitrate, 0.12-0.21 μmol∙L-1for phosphate and 19.32-39.02 μmol∙L-1for silicate, much lower than those of GWC and AC (Gao et al, 2015, submitted).Nitrate shows a weak positive correlation with salinity(r=0.54,p＜0.01,n=37) because of the greater difference between the river and seawater nitrate concentrations.No significant correlations between salinity and phosphate (r=0.13,p＞0.05,n=37) and silicate (r= 0.05,p＞0.05,n=37) were found. The patterns of temperature,salinity and nutrient levels suggest that river runoff dilutes nutrient concentration in these two coves.

3.2 Distributions of POC, Chl-a and δ13C

Distributions of POC, Chl-aand δ13C in GWC and AC are shown in Figure 3. POC was in the range of 50.51-115.41 μg∙L-1(mean: 77.69±17.27 μg∙L-1) in GWC and 63.42-101.79 μg∙L-1(mean: 82.67±11.83 μg∙L-1) in AC. The concentration of POC in GWC gradually increased from the inner cove to the outer cove. The highest concentration was recorded at station G5, but this station also had a low POC concentration in the surface layer. However, the distribution of POC in AC exhibited higher concentrations at station A1 and A4, with the lowest concentration observed at station A3,in the middle of the cove.

Chl-awas in the range of 0.42-3.08 μg∙L-1(mean: 1.29±0.60 μg∙L-1) in GWC and 0.81-1.48 μg∙L-1(mean: 1.08±0.20 μg∙L-1) in AC. Higher concentrations of Chl-awere found in the inner cove region of GWC, while in AC, higher concentrations were found in the middle of the cove.

δ13C was in the range of -30.83‰--26.12‰ (mean:-27.40‰±0.96‰) in GWC and -28.21‰--26.65‰ (mean:-27.45‰±0.47‰) in AC. As Figure 3 shows, the minimum δ13C value was observed in the surface water of station G2 whereas the maximum value was observed in the surface water of G4. δ13C in AC shows a vertical distribution pattern, with more negative values at station A2 and A3. The minimum value was observed at 10 m depth at station A2,and the maximum value was observed at 5 m depth at A5.

4 Discussion

4.1 Influence of hydrological and chemical conditions on POC distribution

During the austral summer, the south of the South Shetland Islands is occupied by the “shelf surface water” with salinity of 34.1-34.2[35]. The northern waters of the Brans field Strait,where King George Island is located, mainly originate from the surface water of the Bellingshausen Sea, which is a warm water mass with lower salinity[36]. The monthly mean precipitation at the Great Wall Station was ～50-60 mm during January and February, which are typically the wettest months of the year[37]. Warmer fresh water from river runoff flowing into the two coves, along with solar radiation heating, causes water in the inner cove regions and the upper layer of seawater to be comparatively fresher and warmer.The patterns of temperature and salinity of homologous positions in GWC and AC were roughly similar (Figure 4a). As shown in Figure 4b, POC concentrations at station G5 were distinctly higher, with higher salinity and lower temperature. POC in the surface water is higher in other Antarctic areas than in GWC (Table 1), and it is most likely that the lateral transportation of a water mass with high POC by the Brans field Current contributed to the high POC value of station G5. POC concentrations were distinctly lower in the surface water of G1 and G3 because of dilution by fresh water.

Phytoplankton is an important source of POC. In shallow Antarctic waters, light limitation due to high turbidity and the strong mixing of the upper water layers (a consequence of the heavy winds) have been suggested as controls upon phytoplankton abundance[33]. Antarctic coastal waters are usually considered to be replete with nutrients,except during local phytoplankton blooms in areas west of the Antarctic Peninsula[39]or close to receding ice edges[40].The concentrations of nitrate, phosphate and silicate in GWC and AC are high, similar to the high nutrient concentrations in Antarctic and sub-Antarctic waters in general. The average N/P ratio was 13.60±0.26 in GWC and 13.20±0.27 in AC.Normally, phytoplankton in the ocean uptake dissolved inorganic nitrogen (DIN) and dissolved inorganic phosphorus(DIP) according to the Redfield ratio, which is a ratio of carbon, nitrogen and phosphorus of 106:16:1. Justić[41]suggested that an N/P ratio close to the Red field ratio (10-22)is indicative of high productivity. As nutrient concentrations are not the limiting factors for phytoplankton growth in the two coves, there is no significant relationship between nutrient levels and POC.

Additionally, although differences in temperature and salinity between the two coves were both statistically significant (p＜0.05), differences between Chl-aand POC concentrations were not significant (p＞0.05). This indicates that hydrological conditions do not strongly influence the distribution of Chl-aand POC.

Table 1 Concentrations of POC in different regions, Antarctica

4.2 δ13C of particulate organic matter

Particulate organic matter (POM) in the ocean originates largely from plankton in the euphotic zone and reflects living plankton populations[42]. The δ13C value of marine organic matter represents a mixed isotope signal from land plant detritus, primary production by aquatic organisms,and microbial biomass[42]. A culture experiment with marine microalgae[43]showed that phytoplankton δ13C depends on several factors, including cell wall permeability, growth rate, cell size and the ability of the cell to actively assimilate inorganic carbon. It has been reported that between 40°N and 40°S, δ13C of POM varies between -18.5‰ and -22‰, with significantly lighter values in cold Arctic waters and the high latitudes of the Southern Ocean[43]. This is consistent with the reported trend of increasing surface ocean δ13C toward the tropics in both hemispheres[44-45](Table 2). For example,in Prydz Bay, latitude 64°-69°S, phytoplankton is the major contributor of POC[5-6,38], and the POC δ13C is ～-28.01‰.

As described above, terrestrial organic matter is a significant contributor to marine POC and strongly influences the δ13C. There are no available δ13C data for the Fields Peninsula; however, it has been reported that it has similar vegetation to that of other ice-free regions around Maxwell Bay[16,46]. The vegetation is predominantly composed of lichens and mosses[15], along with some algae and macro fungi, and a single type of phanerogam namedDeschampsia Antarctica. Lee et al.[46]reported that terrestrial plants on Barton Peninsula showed species-specific carbon and nitrogen isotope compositions, with δ13C values ranging between -26.9‰±0.5‰ and -23.6‰±2.5‰. Along the coast of Admiralty Bay, the largest fjord-like embayment on King George Island, δ13C of lichens ranges from -21.13‰to -18.43‰ and mosses from -25.99‰ to -21.64‰[47].However, the average POC δ13C value for GWC and AC was-27.43‰±0.74‰, lighter than that of the terrestrial plants δ13C mentioned above.

Furthermore, the average δ13C value given by Fry and Sherr[48]for 12 species of benthic macroalgae sampled in AC was -22.41‰±6.97‰ (n=26), implying that phytodetritus ofbenthic macroalgae is likely not a major source of POC.

Table 2 δ13C of phytoplankton from various latitudes

Although runoff made distinct contributions to other seawater parameters in GWC and AC, the amount of organic carbon washed into the sea from the Fields Peninsula is negligible. Although more riverine and phytoplankton samples would be required to better constrain the various terrestrial POC sources, our results suggest that terrestrial organic matter and benthic macroalgae do not significantly influence POC in these two coves. This indicates that the POC is of predominantly marine origin.

4.3 Contribution of phytoplankton and heterotrophic organisms to POC

Antarctic coasts are usually considered productive areas.However, some shallow coastal areas are known to be high-nutrient, low-chlorophyll (HNLC) systems where even with favorable conditions for phytoplankton growth,phytoplankton biomass remains low[33]. Chl-aconcentration is taken as representative of the living phytoplankton biomass, which is an important source of POC. In GWC,the main source of Chl-awas primary producers such as phytoplankton (namely diatoms, dinoflagellates and chrysophyceae) and benthic algae[16]. Reported diatom to total phytoplankton ratios are 93%[20]-96.63%[16], with dominant in summer. The POC/Chl-aof fresh phytoplankton ranges between 33 and 100[52], which is close to the range seen in regions of high primary productivity. In rivers,lakes and regions where primary productivity is not a major contributor to POC, the POC/Chl-awill be high, reaching～250-2 500[53]. The POC/Chl-ain GCW and AC was 74.62± 27.97, which is higher than that of sub-Antarctic water(50-60)[54]but lower than that of the Ross Sea (116-150)[55]and Prydz Bay (～118)[5]. The POC/Chl-aprofile (Figure 5)exhibits a similar pattern to that of POC.

Strong linear relationships between Chl-aand POC(r=～0.89) have been reported in Prydz Bay and the Ross Sea[5-7,38]. This correlation was not seen in either GWC or AC,where POC did not increase as Chl-aincreased (r=-0.40,p＜0.05). This indicates that other marine organisms as well as phytoplankton also contributed to POC in these two coves.

The process of phytoplankton photosynthesis releases dissolved oxygen (DO) and POC rich in phytoplankton is generally consistent with higher DO values. A weak positive correlation between Chl-aand DO (r=0.48,p＜0.01) was found for GWC and AC. In general, when POC sinks through the water column, the degradation of organic matter results in lower POC concentrations and higher apparent oxygen utilization (AOU). However, in GWC and AC, POC and DO showed a negative correlation (r=-0.43,p＜0.01), while POC and AOU showed a positive correlation (r=0.53,p＜0.01),although neither correlation was significant. This indicates POC formation in these two coves is a strong DO-consuming process, most likely respiration or the heterotrophic synthesis of POC. Within the microbial food loop, heterotrophic bacteria play a key role in the formation of organic carbon,because unlike other organisms, they can transform dissolved organic carbon (DOC) into POC[56-57]. The increase in DOC released during rapid phytoplankton growth stimulates bacteria growth[58]. Bacteria biomass comprises more than one third of the microbial community biomass in GWC and AC, with values of 10.770 μgC∙L-1reported for the upper 10 m of GWC and 10.424 μgC∙L-1for AC[56]. In the sea adjacent to King George Island, only ～2% of phytoplankton are consumed by zooplankton. At least 90% of phytoplankton are mineralized in the water or sink down through the water column[59]. Therefore, it is possible that the high nutrient concentrations and phytoplankton biomass provided support to the heterotrophic organisms, which consumed DO.

Additionally, seashore organisms may also play a role.On land and in the shore zone macroalgae are a source of organic matter and nutrients[60]. During our survey, there was visible macroalgae washed up on the beach and deposited on the shores of GWC and AC. After being deposited on land,the macroalgae are subject to decomposition and join the material cycle between sea and land[60].

There are also large penguin populations living on Ardley Island that produce a considerable volume of excreta,much of which is deposited in the coastal region of AC.However, there are no penguin colonies around the shores of GWC. Despite this, the POC concentrations of the two coves are similar, indicating the penguins’ impacts are minimal in the two coves.

While the contributions of all the various POC sources are difficult to quantify, it can be concluded that phytoplankton, organic detritus and heterotrophic organisms all contributed to POC in GWC and AC.

5 Conclusions

This study studied the distribution and sources of POC in GWC and AC in January 2013, during the 29th CHINARE.Our observations illustrate that the higher concentration of POC at station G5 is the result of lateral transport of the Brans field Strait current on the outer cove, whereas the lower concentration of POC in surface waters of stations G1 and G3 indicates dilution of surface waters in the inner cove.

Although temperature and salinity values for the two coves display clear runoff signals, δ13C values and POC distributions indicate that the amount of organic carbon from riverine and terrestrial sources was negligible. The δ13C values also suggest that POC was of predominantly marine origin. Based on the relationship between POC and Chl-a,it can be concluded that phytoplankton, organic detritus and heterotrophic organisms all contribute to POC in GWC and AC.

1 Song J M, Xu Y, Zhang Y, et al. Progress of marine biog eochemical processes in China. Mar Sci, 2006, 30: 69-77

2 Jin H Y, Lin Y A, Chen J F, et al. Analysis of driving factors and distribution of particulate organic carbon in the Huanghai Sea and the East China Sea. Acta Oceanol Sin (Chinese Edition), 2006, 27: 46-53

3 Liu Z L, Ning X R, Zhu G H, et al. Size-fractionated biomass and productivity of phytoplankton and particulate organic carbon in the surface on the routine encicling the Antarctica. Antarctic Research(Chinese Edition), 1993, 5: 63-72

4 Pęcherzewski K. Distribution and quantity of suspended matter in Admiralty Bay (King George Island, South Shetland Islands). Polish Polar Res, 1980, 1: 75-82

5 Hu C Y, Zhang H S. The biogeochemistry of carbon cycle in summer of the Prydz Bay, Antarctica II: characteristics of POC distribution.Chin J Polar Res(Chinese Edition), 2001, 13: 195-204

6 Yu P S, Hu C Y, Zhu G H, et al. Characteristics of particulate organic carbon in the Prydz Bay of Antarctica. Acta Oceanol Sin (Chinese Edition), 2011, 33: 181-186

7 Fabiano M, Povero P, Danovaro R. Distribution and composition of particulate organic matter in the Ross Sea (Antarctica). Polar Biol,1993, 13: 525-533

8 Knap W H, Oerlemans J, Cadee M. Climate sensitivity of the ice cap of king George Island, South Shetland Islands, Antarctica. Ann Glaciol, 1996, 23: 154-159

9 Schloss I R, Abele D, Moreau S, et al. Response of phytoplankton dynamics to 19-year (1991-2009) climate trends in Potter Cove(Antarctica). J Marine Syst, 2012, 92: 53-66

10 Ferron F A, Simões J C, Aquino F E, et al. Air temperature time series for King George Island, Antarctica. Pesquisa Antártica Brasileira,2004, 4: 155-169

11 Qin D H. Developing and physical characteristics of first-year sea ice in Great Wall Bay and its adjacent area by King George Island,Antarctica. Journal of Glaciology and Geocryology(Chinese Edition),1991, 13: 115-130

12 Song D K. Geomorphology of the beach and sea floor. Mar Sci, 1987,4: 18-21

13 Yang Q H, Wang X Q, Zhang L. The features of meterological elements in 2006 at the Great Wall Staion, Antarctica. Marine Forecasts (Chinese Edition), 2007, 24: 55-64

14 Chen X B, Zhang Y P. Snow accumulation and melting progesses at the Great Wall Staion, Antarctica. Antarctic Research(Chinese Edition), 1991, 3: 8-14

15 Pu J B, Li Z P, Shao M H, et al. A survey of the environmental contamination state in King George Island, Antarctica. Antarctic Research(Chinese Edition), 1995, 7: 51-58

16 Shen J, Xu R M, Zhou G F, et al. Reasearch on the structure and relationship of terrestrial, freshwater, interridaland shallow sea ecosystems in Fildes Peninsula, Antarctica. Chin J Polar Res(Chinese Edition), 1999, 11: 100-112

17 Sun H L. Analysis of characteristics of the tide at the Great Wall Station, Antarctica. Antarctic Research(Chinese Edition), 1992, 4:102-108

18 Sun H L. Analysis of characteristics of the tide at the Great Wall Staion, Antarctica. Antarctic Research(Chinese Edition), 1990, 2: 66-72

19 Li F R. Distribution of oxygen-minimum layer and factors controlling on it in aeras adjacent to South Shetlands and north of Adelaide,Antarctica, in summer. Antarctic Research(Chinese Edition), 1989, 4:21-27

20 Li R X, Yu J L, Lv P D. The quantitative distribution of the net phytoplankton in the Great Wall Bay, Antarctica. Antarctic Research(Chinese Edition), 1992, 4: 12-16

21 Yu J L, Li R X, Huang F P. A preliminary study of the ecology of the phtyoplankton in Great Wall Bay, Antarctica. Antarctic Research(Chinese Edition), 1992, 4: 34-39

22 Yu J L, Zhu M Y, Li R X, et al. The phytoplankton in the Antarctic Great Wall Bay In summer. Chin J Polar Res(Chinese Edition), 1999,11: 39-45

23 Li B H. The subaltern of chlorophyll a maxma in the Great Wall Bay and adjacent sea, Antarctica. Chin J Polar Res(Chinese Edition), 2004,16: 127-134

24 Li B H. Variation of chlorophyll a contents at the water of the Great Wall Station, Antarctica. Chin J Polar Res(Chinese Edition), 2004: 16:332-337

25 Li B H, Zhu M Y. Analysis of variation of chlorophyll-a content in the intertidal zone of Great Wall Bay, Antarctica during Dec., 1992 to Mar., 1993. Journal of oceanography of Huanghai & Bohai Seas,1999, 17: 38-42

26 Zhu M Y, Li B H, Huang F P, et al. A study on cholorophyll-a content and its variation in Great Wall Bay, Antarctica during the aurtral summers from 1992 to 1995. Chin J Polar Res(Chinese Edition),1999, 11: 113-121

27 Zhou G F, Xu R M, Shen J, et al. Study on the spatial distribution of organic salt and chlorophyll-a in Great Wall Bay, Antarctica. Chin J Polar Res(Chinese Edition), 1998, 10: 144-151

28 Wu B L, Zhu M Y, Huang F P. Seasonal variations of chlorophyll-ain Great Wall Bay in Antarctica. Antarctic Research(Chinese Edition),1992, 4: 14-17

29 Whitehouse M, Priddle J, Symon C. Seasonal and annual change in seawater temperature, salinity, nutrient and chlorophyll a distributions around South Georgia, South Atlantic. Oceanographic Literature Review, 1996, 44: 425-443

30 Clarke A, Holmes L, White M. The annual cycle of temperature,chlorophyll and major nutrients at Signy Island, South Orkney Islands, 1969-82. Br Antarct Surv Bull, 1988, 80: 65-86

31 Brandini F P, Boltovskoy D, Piola A, et al. Multiannual trends in fronts and distribution of nutrients and chlorophyll in the southwestern Atlantic (30-62°S). Deep Sea Res: Part I, 2000, 47: 1015-1033

32 Yoon H, Park B-K, Domack E, et al. Distribution and dispersal pattern of suspended particulate matter in Maxwell Bay and its tributary,Marian Cove, in the South Shetland Islands, West Antarctica. Mar Geol, 1998, 152: 261-275

33 Schloss I R, Ferreyra G A, Ruiz-Pino D. Phytoplankton biomass in Antarctic shelf zones: a conceptual model based on Potter Cove, King George Island. J Marine Syst, 2002, 36: 129-143

34 Nędzarek A. Sources, diversity and circulation of biogenic compounds in Admiralty Bay, King George Island, Antarctica. Antarct Science,2008, 20: 135-145.

35 Li J H. The charictaristics and factors of CWB near South Shetland Islands ajacent area in Southern Hemisphere summer, 1987. Acta Oceanol Sin(Chinese Edition), 1991, 1: 13-25

36 Yang T Z, Zhao J S, Xu J P. Water masses and circulation around the South Shetland Islands in summer. Proceedings of China first symposium on Southern Ocean expedition (Hangzhou, China), the Academic Committee on Antarctic Research of China and the Second Institute of Oceanography, SOA, 1988

37 Bian L G, Ma Y F, Lu C G, et al. Climate characteristics of precipitation and wind as well pressure and cloud amount at the Great Wall Staion (1985-2008) and Zhong Shan Station (1989-2008),Antarctic. Chin J Polar Res(Chinese Edition), 2010, 22: 321-333

38 Yin X J, Li Y H, Qiao L, et al. Distribution of particulate organic carbon(POC) and δ13CPOCin surface waters in semmer in Prydz Bay,Antarctica. Chin J Polar Res(Chinese Edition), 2014, 26: 159-166

39 Moline M, Prézelin B. High-resolution time-series data for 1991/1992 primary production and related parameters at a Palmer LTER coastal site: implications for modelling carbon fixation in the Southern Ocean. Polar Biol, 1997, 17: 39-53

40 Smith W O, Nelson D M. Phytoplankton bloom produced by a receeding ice edge in the Ross Sea: spatial coherence with the density field. Science, 1985, 227: 163-166

41 Justić D, Rabalais N N, Turner R E, et al. Changes in nutrient structure of river-dominated coastal waters: stoichiometric nutrient balance and its consequences. Estuarine Coastal Mar Sci, 1995, 40:339-356

42 Hoefs J. Stable Isotope Geochemistry, Sixth Edition. Berlin: Springer-Verlag, 2009

43 Laws E A, Popp B N, Bidigare R R, et al. Dependence of phytoplankton carbon isotopic composition on growth rate and CO2aq: theoretical considerations and experimental results. Geochim Cosmochim Acta, 1995, 59: 1131-1138

44 Goericke R, Fry B. Variations of marine plankton δ13C with latitude, temperature, and dissolved CO2in the world ocean. Global Biogeochem. Cycles, 1994, 8: 85-90

45 Hofmann M, Wolf-Gladrow D A, Takahashi T,et al. Stable carbon isotope distribution of particulate organic matter in the ocean: a model study. Mar Chem, 2000, 72: 131-150

46 Lee Y I, Lim H S, Yoon H I. Carbon and nitrogen isotope composition of vegetation on King George Island, maritime Antarctic. Polar Biol,2009, 32: 1607-1615

47 Cipro C V, Yogui G T, Bustamante P, et al. Organic pollutants and their correlation with stable isotopes in vegetation from King George Island, Antarctica. Chemosphere, 2011, 85: 393-398

48 Fry B, Sherr E B. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. Contrib Mar Sci, 1984, 27: 13-47

49 Zhang R, Chen M, Guo L, et al. Variations in the isotopic composition of particulate organic carbon and their relation with carbon dynamics in the western Arctic Ocean. Deep Sea Res: Part II, 2012, 81-84: 72-78

50 Brown K A, McLaughlin F, Tortell P D, et al. Determination of particulate organic carbon sources to the surface mixed layer of the Canada Basin, Arctic Ocean. J Geophys Res: Oceans, 2014: 1084-1102

51 Cai D L, Zhang S F, Zhang J. Esosystem Tropic Dynamics Studies as Traced by Natural Carbon and Nitrogen Stable Isotopes. J Chin Mass Spectrom Soc, 2003, 24: 434-439

52 Welschmeyer N A, Lorenzen C J. Chlorophyll budgets: Zooplankton grazing and phytoplankton growth in a temperate fjord and the Central Pacific Gyres. Limnology, 1985, 30: 1-21

53 Cifuentes L, Coffin R, Solorzano L, et al. Isotopic and elemental variations of carbon and nitrogen in a mangrove estuary. Estuarine Coastal Mar Sci, 1996, 43: 781-800

54 Copin-Montegut C, Copin-Montegut G. Stoichiometry of carbon,nitrogen, and phosphorus in marine particulate matter. Deep-Sea Res:Part A, 1983, 30: 31-46

55 Smith W O, Nelson D M, DiTullio G R, et al. Temporal and spatial patterns in the Ross Sea: Phytoplankton biomass, elemental composition, productivity and growth rates. J Geophys Res: Oceans(1978-2012), 1996, 101: 18455-18465

56 Dai J C. The Composition and Function of the Main Group of Microbial Food Loop in Offshore of Polar Region. 2006

57 Jiao N Z, Herndl G J, Hansell D A, et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol, 2010, 8: 593-599

58 Karl D M. Microbial processes in the Southern Oceans//Friedman E I,Antarctic Microbiology, Wiley: New York, 1993: 1-63

59 Knox G A. The Biology of the Southern Ocean. Cambridge:Cambridge University Press, 1994

60 Ndzarek A, Rakusa-Suszczewski S. Decomposition of macroalgae and the release of nutrient in Admiralty Bay, King George Island,Antarctica. Polar Biosci, 2004, 17: 26-35