Stratification and the distribution of phytoplankton, nutrients, inorganic carbon, and sulfur in the surface waters of Weddell Sea leads

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Deep-Sea Research II 55 (2008) 988–999 www.elsevier.com/locate/dsr2

Stratification and the distribution of phytoplankton, nutrients, inorganic carbon, and sulfur in the surface waters of Weddell Sea leads H.J. Zemmelinka,b,, L. Houghtonc, J.W.H. Daceyc, J. Stefelsd, B.P. Koche, M. Schro¨dere, A. Wisotzkie, A. Scheltzf, D.N. Thomasg, S. Papadimitrioug, H. Kennedyg, H. Kuosah, T. Dittmari a

Royal Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB Den Burg, The Netherlands b University of East Anglia, NR9 7TJ Norwich, UK c Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA d Laboratory of Plant Physiology, University of Groningen, 9750 AA Haren, The Netherlands e Alfred Wegener Institute for Polar and Marine Research, Bussestr. 24, 27570 Bremerhaven, Germany f Inst. f. Polaro¨kologie,Wischhofstr. 1-3, Geba¨ude 12, D-24148 Kiel, Germany g College of Natural Sciences, Bangor University, Anglesey, UK h Tva¨rminne Zoological Station, FI-10900 Hanko, Finland i Department of Oceanography, Florida State University, OSB 311, Tallahassee, FL 32306-4320, USA Accepted 23 December 2007 Available online 12 March 2008

Abstract The distribution (fine resolution depth profiles) of major nutrients, chlorophyll-a, organic compounds, and phytoplankton (biomass and numbers) was examined in lead water in pack ice of the Weddell Sea. Samples were taken by pulling water into a syringe from a series of depths from 0.002 to 4 m. While concentrations of compounds of interest remained constant in the water column, an enhanced depletion of nutrients (ammonium, nitrate, silicate, and inorganic carbon) occurred above the pycnocline at 0.1 m. Coinciding with this depletion was an increase of organic matter and chlorophyll. The change in carbon isotopic composition showed that an enhanced primary production occurred at the sea surface. Cell counts and nutrient disappearance ratios suggest that primary production was dominated by diatoms. These results show that the sea surface can have different chemical characteristics than the deeper water column. r 2008 Elsevier Ltd. All rights reserved. Keywords: Stratification; Phytoplankton; Nutrients; Inorganic carbon; Sulfur compounds; Southern Ocean

1. Introduction Sea-ice formation is an important characteristic of both polar regions, which at its maximum extent covers 6% of the Earth’s surface (Gloersen et al., 1992). In the Southern Ocean, the annual extent of sea ice ranges from a minimum of 4  106 km2 in summer to a maximum of 19  106 km2 in winter and forms one of the largest biomes on Earth. Seaice research over the past decades has improved our understanding of many of the physical processes that transform surface waters into a matrix of ice and liquid. Corresponding author. Tel.: +31 222 369 438; fax: +31 222 319 674.

E-mail addresses: [email protected] (H.J. Zemmelink), [email protected] (B.P. Koch). 0967-0645/$ - see front matter r 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2007.12.011

Sea ice is constantly in motion driven by the wind. Wind stress drives the sea ice through frictional drag that creates a divergent stress over large areas of ice. Since ice has little strength under tension, this divergence can open up cracks that widen to form leads. The surface area of leads varies day-to-day by refreezing and with the cyclical periods of divergence and convergence caused by the wind. However, sea-ice leads are highly important for the energy flux, in the form of heat, to the atmosphere (Eisen and Kottmeier, 2000). In addition, the sea-ice habitat appears to be highly productive during spring and summer and is thought to make a major contribution to global sulfur and carbon cycling (Trevena et al., 2003; Semiletov et al., 2004; Zemmelink et al., 2005a, b, 2006a, b). Estimation of the

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annual productivity of the sea-ice flora remains inconclusive, although it is generally accepted that Antarctic sea ice sustains a significant uptake of atmospheric CO2, ranging from 0.015 to 0.024 Pg C in spring and summer (Delille, 2006). Zemmelink et al. (2006a, b) estimated from direct CO2 flux measurements that the total carbon uptake by the multi-year-ice zone of the western Weddell Sea in December 2004 could have been as high as 6.6 Tg C. However, part of the CO2 fixed by sea-ice algae may be remineralized and made to enter the surface sea water inorganic carbon pool and/or be ultimately returned to the atmosphere during the annual cycle of exchange of materials and organisms between the ice and the water column. In recent years, the high productivity of surface sea-ice assemblages, as well as assemblages in brine channels and gap layers, has been well documented (e.g., Thomas and Dieckmann, 2003, and references therein). For sea-ice algal communities transport through brine channels and gap layers is fundamental to nutrient replenishment (Golden et al., 1998). In addition, increase in ice porosity, as sea-ice warms up, may facilitate exchange of nutrients and biota with the water column. Melting sea ice will impact local and regional physical, chemical, and biological oceanographic processes. Low-salinity and low-density melt water floats on top of the higher-density seawater, forming a relatively stable surface layer (Mitchell and Holm-Hansen, 1991), unless disturbed by strong winds (Lancelot et al., 1991). During melting, solutes and particles within sea ice, including nutrients and sea-ice algae, are released to the upper water column. Phytoplankton blooms are commonly associated with the retreating sea-ice edge and polynyas and are a considerable portion of polar productivity (Smith and Nelson, 1986; Lancelot et al., 1993a, b; Schloss and Estrada, 1994; Smith and Gordon, 1997; Arrigo, 1998). In order to study sea surface characteristics, Zemmelink et al. (2005a, b) developed a system for sampling biota, nutrients, and major sulfur compounds in Weddell Sea open leads in the sea ice. First results from its application at the 2004 Ice Station POLarstern (ISPOL) cruise have been published recently by Zemmelink et al. (2005a, b) and show that the chemical characteristics (salinity and major sulfur compounds) of the near-surface seawater in Weddell Sea leads are very different from the underlying water column during periods of strong stratification caused by a decrease in salinity (see also Fig. 1). However, it was not clear whether the observed gradients were the result of physical and/or biological process, a question that can only be addressed using a more comprehensive data set. In this paper, we present depth profiles of the concentration of major nutrients (dissolved inorganic phosphorus (DIP), silicic acid, nitrate plus nitrite, and dissolved ammonium), dissolved organic nitrogen (DON), dissolved organic carbon (DOC), dissolved inorganic carbon and its stable isotope ratio (DIC and d13C-DIC, respectively), as well as chlorophyll and the major sulfur compounds (dimethyl sulfide (DMS), dimethylsulfoniopropionate (DMSP) and

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dimethylsulfoxide (DMSO)) in the water column of leads from 0.002 to 4 m depth. This paper gives a first characterization of the chemical characteristics of the near-surface water column, in open leads in the perennial ice zone of the western Weddell Sea. 2. Materials and methods 2.1. Sampling Seawater was sampled from two leads adjacent to the ISPOL ice floe. Lead 1 was newly opened and was sampled from day 350 to 359. Lead 2 was 2 weeks old when sampling started from days 362 to 001. Sampling occurred between 12:00 and 16:00 GMT and started after a period of elevated wind speeds during which waves mixed the upper water column. Samples in lead 1 were taken from 0.002, 0.25, 1, and 4 m water depth. Lead 2 was also sampled at 0.1 m depth. It is noted that we define a depth of 0.002 m as surface water, although we realize that the sample is drawn from a sphere around the sampling tube inlet. Samples were taken by suspending 0.001 m (internal diameter) Teflon sampling inlets from a small catamaran and by pulling water into a 50-mL syringe at a speed of 5 mL min1. Sample collection at different withdrawal speeds (2, 5, and 50 mL min1) and with different syringes (glass and plastic) showed no significant effect on the concentration of sulfur compounds (n ¼ 20, po0.05). It can therefore be assumed that this sampling method does not affect other parameters of interest. Sampling inlets and syringes were rinsed three times before water was collected into vials for later analysis of compounds of interest. Samples were taken in a specific order to minimize sampling artifacts: first samples were drawn for sulfur compounds (0.5–1 L), second phytoplankton (0.02 L), third nutrients (0.8 L), fourth chlorophyll (1 L), and fifth salinity

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(0.15 L). In total, about 2.5 L water were taken from close to the surface and 3 L from 1 and 4 m depth. 2.2. Analytical methods The analysis of salinity and major sulfur compounds (DMS, total DMSP, and total DMSO) was presented in detail in Zemmelink et al. (2005a, b). All samples used in microscopy were fixed with ice-cold 25% EM-grade glutaraldehyde solution (final conc. about 1%) immediately after sampling. Duplicate 5-mL samples were filtered onto black Nuclepore polycarbonate filters (pore-size 0.2 mm) after staining them with proflavine (Haas, 1982). In total, 100 mL of proflavine solution (0.033% W/V) per 5-mL sample was added and gentle filtration (o5 kPa vacuum) was started without delay. Immediately after the filtration was completed the vacuum was stopped, and the filter air-dried and mounted in paraffin oil to a glass slide. The samples were examined and counted within 24 h, and the samples kept in +4 1C before counting. All counts were made with a Leitz Dialux microscope equipped with epifluorescence light. A 50-W HBO mercury lamp and the Leitz Ploemopak filter set I2 were used. The filter set gives blue light, with which proflavine-stained cells were seen as green, and chloroplasts as red bodies inside cells. Nucleus is usually clearly visible as a green body. All cells except individual Phaeocystis were counted from the whole filter area with a 40  objective. Phaeocystis cells were enumerated from either one or two transects covering the whole diameter of the filter. Diatom cells without chloroplasts and nucleus were considered dead, and not included to counts. As the epifluorescence microscopy is rarely suitable for species identification, some samples were examined with a 100  oil immersion objective with normal light. However, the species identification was still limited. About 50 cells of the most important taxa were measured from a selected sample to get its measures. From the results mean individual cell volumes were calculated. Onboard analyses for the major dissolved inorganic nutrients, nitrate plus nitrite (hereafter, nitrate (NO 3 )), DIP, and silicic acid were done using standard calorimetric methodology (Grasshoff et al., 1983) as adapted for flow injection analysis (FIA) on a LACHAT Instruments Quick-Chem 8000 autoanalyzer (Hales et al., 2004). Dissolved ammonium (NH+ 4 ) also was determined onboard with the fluorimetric method of Holmes et al. (1999) using a HITACHI F2000 fluorescence spectrophotometer. Samples for DON were filtered through syringe filters (Whatman GD/X GMF, pore size 0.45 mm) and were kept at 18 1C until later analysis. The DON was determined by + subtraction of NO 3 and NH4 from the total dissolved nitrogen analyzed by FIA on the LACHAT autoanalyzer using on-line peroxodisulfate oxidation coupled with UV radiation at pH 9.0 and 100 1C (Kroon, 1993; Kattner and Becker, 1991). Samples for DOC were filtered through precombusted (550 1C, 6 h) glass fiber filters (GF/F, Whatman) and stored

frozen at 30 1C until analysis. DOC in the filtrate was determined by high-temperature catalytic oxidation with a Shimadzu TOC-VCPN analyzer. In the autosampler, 6 mL of sample volume were acidified with 0.12 mL HCl (2 M) and sparged with oxygen (100 mL min1) for 5 min to remove inorganic carbon. In total, 50 mL sample volume was injected directly on the catalyst (heated to 720 1C). Detection of the generated CO2 was performed with an infrared detector. Final DOC concentrations were average values of triplicate measurements. If the standard variation or the coefficient of variation exceeded 0.1 mM or 2%, respectively, up to two additional analyses were performed and outliers were eliminated. Detection limit was 7 mM C, with an accuracy of 72 mM C determined with low carbon water and seawater reference material (DOC-CRM, Hansell Research Lab, University of Miami, USA). The DIC samples were immediately filtered through a cellulose nitrate filter (0.45 mm, Sartorius) into HgCl2poisoned 10-mL glass ampoules, which were stored flamesealed under a nitrogen atmosphere for analysis in the home laboratory. The DIC concentration and d13C-DIC were determined following in-vacuo reaction with 85% H3PO4 and cryogenic CO2 gas distillation, using an in-line manometer and a EUROPA PDZ 20/20 mass spectrometer, respectively. The isotopic measurements are reported in the d notation relative to Vienna Pee Dee Belemnite, i.e., dsample ¼ 1000 [(Rsample/Rstandard)1], where R ¼ 13C/12C. The reproducibility of DIC and d13C-DIC measurements based on internal seawater standard and duplicate sample measurements was better than 5 mmol kg1 and 0.1%, respectively. For chlorophyll-a (chl-a) determination each water sample was filtered onto Whatman GF/F (Whatman plc., Brentford, Middlesex, UK) glass microfiber filters and chl-a was extracted in 96% ethanol in the dark for 24 h at room temperature. Fluorescence was measured using a Jasco FP-750 fluorometer (Jasco Inc., Tokyo, Japan) calibrated against pure chl-a (Sigma–Aldrich Company, St. Louis, MO, USA) and the concentrations were calculated according to Helcom (1988). 2.3. Data presentation In order to remove the effect of dilution with freshwater (from ice melt) all variables are scaled to a constant salinity of 34.3% (as indicated by the subscript 34) using [A]34 ¼ [S]y*[A]y/34.3, where [S]y is the salinity at depth y and [A]y the concentration of variable A at depth y. In addition, concentration changes over time are derived from ([A]yd1[A]yd2)y/([B]yd1[B]yd2)y, where ([A]yd1[A]yd2)y is the concentration difference of variable A between year days 1 and 2 at depth y. 3. Results A detailed discussion of environmental conditions, salinity, and sulfur profiles in the water column is given

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by Zemmelink et al. (2005a, b). Briefly, water temperature was about 1.8 1C and wind speed varied between 3.6 and 9.2 m s1. Aerial photography data revealed a number of significant changes in the character of the pack ice between 29 November 2004 and 1 January 2005. There was a net decrease in the concentration of thick, snow-covered floes from 96% to 90%; however, this did not reflect a net decrease in total ice concentration. Instead, we observed an increase from 1% to 7% in the amount of brash ice between the floes, much of which was brown due to the high diatom concentrations and therefore highly productive. This coincided with a net decrease in floe size, while the openwater fraction of leads averaged 5% throughout December. The relative position, of the sample site, to the direction of the wind varied from down wind to up wind. Stratification was observed from year day 354 until 359 in lead 1, and started in the second lead at year day 364, lasting until the end of our stay at the floe at year day 001. Salinity profiles are summarized in Fig. 1 and show that the water column became less saline above a depth of 0.1 m. In the mixed water column, the salinity was close to 34.3% (34.27%70.046; n ¼ 38, from 4 m depth to close to the surface). In calmer conditions, stratification occurred and salinity at the surface dropped to a minimum of 27.4%. However, water samples taken at 0.25 m and below remained at salinity around 34.3% throughout the measurement period. A similar stratification was observed in the biogeochemical parameters. Overall very little algal biomass was found throughout the water column, with maxima only occurring at the surface (Fig. 2). The distribution of phytoplankton biomass was variable and showed that single-celled Phaeocystis and autotrophic dinoflagellates were most abundant at year days 352, 354, 358 (in lead 1) and at year day 363 in lead 2. However, during most days with stratification (except year day 358) diatoms became dominant in biomass at the surface. Diatom species were dominated by Fragilariopsis cylindrus and Cylindrotheca closterium, which were both found to be dominant in ice bottom and infiltration layer in the ISPOL ice floe. (Results of sea-ice algal compositions are presented elsewhere in this special issue.) Other ice-related species were rare, and other found diatoms were mainly genuine centric planktonic diatoms (Fig. 3). Chl-a34 concentrations (Fig. 4, Table 1) in the mixed water column of lead 1 averaged 0.1570.05 mg L1 (n ¼ 16), increasing to 0.47 mg L1 towards the surface during stratification. In the second lead, chl-a34 concentrations increased from 0.1670.04 mg L1 (n ¼ 17) in the mixed column to 0.41 mg L1 during stratification. While these values are in the low range of the reported chlorophyll concentrations in the Weddell Sea (e.g., Kattner et al., 2004), the depth profiles clearly demonstrate the significant effect of stratification on the distribution of chl-a in the water column. A similar strong relationship was found between DOC and salinity but not for DON and salinity. The concentra-

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tions of DOC34 (Fig. 4, Table 1) ranged from 40.5 to 43.6 mM in the mixed water column of lead 1, increasing to a maximum of 49.0 mM near the surface during stratification. In the second lead, DOC34 values ranged from 41.3 to 44.5 during mixed conditions, increasing to 57 mM above the pycnocline. These values are typical concentrations in Antarctic seawater (Wedborg et al., 1998). The DON34 concentration (Fig. 4, Table 1) was variable in the two leads, ranging from 0.2 to 12.6 mM, with highest DON value of 12.6 mM at day 353. The DON distribution with depth in lead 1 was similar to that of DOC, with increasing concentrations towards the surface during stratification. The distribution of DON with depth in lead 2 did not show a relationship with salinity and, hence, a stratification effect. The measured DON concentrations were similar to those previously measured in the water column of the Weddell Sea (Thomas et al., 2001). The measured concentration range of the major dissolved inorganic nutrients (Fig. 4, Table 1) in the mixed water column is also typical of Weddell Sea water (Schro¨der et al., 1994; Thomas et al., 2001), with in lead 1 nitrate34, silicic acid34, and DIP34 ranging from 19.7 to 30.0 mM, 42.6 to 52.0 mM, and 1.81 to 3.81 mM, respectively. During stratification, the dissolved nutrient concentrations in lead 1 decreased to 0.9 mM for NO 3 , 8.8 mM for 34 Si34, and 0.06 for PO434. Concentrations in the second lead were similar, with nitrate34 ranging from 24.4 to 30.9 mM, silicic acid34 ranging from 48.7 to 61.4 mM and DIP34 ranging from 2.1 to 2.6 mM, respectively. During stratification, the dissolved nutrient concentrations in lead 2 decreased to 0.08 mM for NO 3 , 18.4 mM for Si34, and 0.8 34 for PO434. The DIC and d13C-DIC (Fig. 4, Table 1) were measured only in lead 2. Normalized DIC concentration was uniform in the mixed water column, averaging 229775.7 mM (n ¼ 14), decreasing at the water surface during stratification to 1223 and 1187 mM. The d13C-DIC34 was also relatively uniform in the mixed water column, with an average of 0.5970.12% (n ¼ 14). During stratification, the d13C-DIC in the surface layer increased (i.e., became enriched in 13C) to +1.2% and +4.3%. The d13C-DIC measurements are in agreement with previously reported measurements in platelet ice layers (+0.4% to +3.8%; Thomas et al., 2001) and in under-ice seawater (0.5% to 2.5%; Gibson et al., 1999). Although there is some overlap with DMS, DMSP, and DMSO data presented in Zemmelink et al. (2005a, b), here we present only data of (normalized) sulfur compounds that were collected simultaneously with samples used for analysis of nutrients, chlorophyll and biota. (Hence, data presented in this study differ from data presented in Zemmelink et al., 2005a, b.) Major sulfur compounds DMS34, DMSP34, and DMSO34 in the mixed water column of lead 1 ranged from 0.3 to 5.3 nM, 3.4 to 19.2 nM, and 2.2 to 16.0 nM, respectively. During stratification, the sulfur concentrations increased to 17.2 nM for DMS34, 68.5 nM for DMSP34, and 80.2 nM for DMSO34. Similar

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Fig. 2. Algal biomass in plasma volume (109 mm3 L1). Graphs in the left column are based on lead 1; graphs to the right are based on lead 2.

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Other diatoms (cell number l-1) Fig. 3. Abundance (cell number l1) of major phytoplankton groups. Graphs on the left site are based on lead 1 and graphs on the right are based on lead 2.

concentrations were measured in lead 2 with DMS34 in the mixed column ranging from 0.63 to 3.1 nM, DMSP34 concentrations ranging from 8.2 to 26.7 nM, and DMSO34 ranging from 2.1 to 12.7. In comparison with lead 1 slightly higher concentrations were measured above the pycnocline of lead 2 with sulfur concentrations increasing to values as high as 38.2 nM for DMS34, 70.5 nM for DMSP34, and 158.9 nM for DMSO34 (Fig. 5 and Table 1).

4. Discussion In both leads, the water column appeared to be well mixed at the first sampling days (year days 353 and 363, respectively), which was caused by the elevated wind speed and the occurrence of short breaking waves during the preceding days. No profiles were observed during such conditions but stratification rapidly occurred, and

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Table 1 Biochemical parameters measured in sea-ice leads during the ISPOL experiment Parameter

Salinity (%) Chl-a (mg L1) DoC (mM) DoN (mM) NO 3 (mM) NHx (mM) Si (mM) DIP (mM) DIC (mM) d13CDIC (%) DMS DMSP DMSO DSi:DN lead 1 DSi:DN lead 2 DN:DP lead 1 DN:DP lead 2 DC:DP lead 2 DC:DN lead 2 DMSP chl-a (nM mg1) DMSP:DMS DMS:DMSO

Stratified water column above pycnocline

Mixed water column

Lead 1

Lead 2

Lead 1

Lead 2

28.03 (27.35–28.25) 0.36 (0.3–0.41) 57 N.A. 2.0 (1.4–2.6) 11.4 (6.1–20.8) 0.33 (0.08–0.61) 26.6 (18.4–42.8) 1.2 (0.8–2.0) 1411 (1187–1823) 1.9 (0.4–4.3) 29.0 (13.4–38.2) 57.9 (21.3–70.5) 88.8 (10.0–158.9) 2.6

34.26 (24.28–34.35) 0.15 (0.07–0.23) 42.0 (40.5–43.6) 4.4 (0.2–12.6) 26.3 (19.7–30.0) 0.64 (0.14–1.78) 48.4 (42.6–52.0) 2.3 (1.81–3.81)

34.28 (34.07–34.31) 0.16 (0.07–0.21) 42.7 (41.3–44.5) 2.1 (0.5–5.2) 27.5 (24.4–30.9) 0.27 (0.05–0.65) 54.1 (48.7–61.4) 2.4 (2.1–2.6) 2297 (2292–2308) 0.59 (0.37–0.79) 1.4 (0.63–3.1) 17.4 (8.2–26.7) 7.6 (2.1–12.7)

30.27 (28.65–32.6) 0.35 (0.33–0.47) 48.6 (47.9–49.0) 5.2 (3.8–7.0) 4.9 (0.9–11.6) 0.44 (0.16–0.59) 18.6 (8.8–36.3) 0.4 (0.06–1.0)

8.7 (3.1–17.9) 66 (53.0–68.5) 34.5 (13.3–80.2) 2.0 9.2

1.1 (0.3–5.3) 10.0 (3.4–19.2) 7.6 (2.2–16.0)

8.4

740

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189 (n ¼ 4) 7.6 (n ¼ 4) 0.24 (n ¼ 4)

161 (n ¼ 3) 2.0 (n ¼ 3) 0.33 (n ¼ 3)

67 (n ¼ 16) 8.8 (n ¼ 16) 0.15 (n ¼ 16)

106 (n ¼ 17) 12.4 (n ¼ 17) 0.19 (n ¼ 17)

Presented are average values and, between parentheses, minimum and maximum values. All presented data are normalized to a salinity of 34.3%. Ratios (DA:DB) are calculated from the change between concentrations found at the sea surface during mixed conditions and minimal concentrations found during stratification. Sulfur ratios are based on the average values found in the respective water column.

enhanced with time, when breaking waves were not present. During stratification concentrations of chemical compounds changed at the surface (as sampled at 0.002 m depth), probably initialized by processes such as dilution with melt water and biological activity. Nutrients behave conservatively during freezing and melting of seawater, and, if this were the only process affecting their concentration, salinity normalization would bring them close to the respective seawater measurements in the mixed layer. However, salinity corrected concentrations of nutrients appear to be substantially depleted above the pycnocline (Fig. 4). It is therefore unlikely that dilution fully determined the disappearance of nutrients. The biological consumption of nutrients can be determined from uptake ratios (Table 1) derived from the concentration changes from the onset of stratification (year days 353 and 363) till the last sampling day (year days 359 and 001, respectively). In addition, the ratio can be used as an indication of which plankton species is most abundant. Because diatoms use large quantities of silicate to form their opal tests, the ratio of changes in silicate and nitrate concentrations, DSi34/DN34, can be used as an indication of diatom over Phaeocystis dominance. The maximum DSi34/DN34 ratio of concentration change in the surface waters of the two leads was 2.0 and 2.6 (Table 1), which, following Sweeney et al. (2000), indicates diatom dominance. Values less than 0.5 for the DSi34/DN34 ratio would

indicate a Phaeocystis dominated algal community. In addition, some studies have identified diatoms as the source of low N/P and C/P removal ratios (Arrigo et al., 1999; Sweeney et al., 2000), whereas N/P uptake ratios in Phaeocystis-dominated communities exceed the Redfield ratio (N:P ¼ 16). The observed DNOx34:DDIP34 in lead 1 of 9.2, and in the second lead DNOx34:DDIP34 of 8.4, both lower than the Redfield ratio (N:P ¼ 16), indicate a dominance of diatoms above the pycnocline of both leads. This is consistent with the general observation that phytoplankton blooms are dominated by Phaeocystis in relatively unstratified waters, while in stratified surface waters blooms are dominated by diatoms (Arrigo, 1998; Arrigo et al., 2000). Consistent with the distribution of macronutrients, concentrations of DIC34 dropped considerably between year days 363 and 001 by 1068 mM. The progress of NO 3 and DIP deficit with DIC deficit indicates the evolution of strong nutrient gradients in the surface water above the pycnocline with removal ratios DC34:DNO and 3 34 DC34:DP34 in lead 2 increasing to 49 and 740, respectively. While the DNO 3 :DPO4 ratios during ISPOL are common for diatom-dominated waters, the overall DC:DN:DP is high. Although the number of observations presented here is small, these numbers are in agreement with results published by Gleitz et al. (1996). Results show a strong drawdown of DIC that coincides the drawdown of major

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Lead

Lead

0

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1 2 3 4 5 0

5

15 10 DMS34 (nM)

20 0

10

20 30 DMS34 (nM)

40

50

0

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100

0

Depth (m)

1 2 3 4 5 0

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40 60 80 100 120 DMSO34 (nM)

0

50

100 150 DMSO34 (nM)

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Fig. 5. DMS, (total) DMSP, and (total) DMSO (nM) from 0.002 to 4 m depth in the water column of Antarctic leads. All data are normalized to a salinity of 34.3%. Symbols refer to sampling dates, presented as year day. Graphs in the left column are based on lead 1, graphs to the right are based on lead 2.

nutrients. Such a drawdown of nutrients can be expected in a closed or semi-closed environment, where nutrient replenishment (including DIC) during stratification from the mixed layer below the sea surface, or other sources (e.g., ice, atmosphere), is slow relative to the time of observation. Replenishment of the DIC pool in the stratified water column from the atmosphere by CO2 gas exchange was likely limited by diffusion-controlled transport processes under conditions of lack of turbulence at the

air–water interface, at least on the short time-scale of the present study. Enhancement of this transport by chemical reaction of atmospheric CO2 with OH at elevated pH, such as expected during intense photosynthetic events in a semi-closed system, is a possibility. However, chemical enhancement of CO2 transport across the air–sea interface is associated with faster kinetics of incorporation of 12CO2 than 13CO2 into the DIC pool of surface waters. Such strong depletion of 13C in the DIC pool is not

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supported by the current, albeit limited, number of isotopic measurements. Similar microenvironments have been described in water columns of crack pools trapped between melting ice floes (Gleitz et al., 1996). The crack pools displayed NO 3 exhaustion and were thought to have evolved due to rapid algal growth from an initially nutrient-rich and highsalinity pool. The observed nitrate exhaustion was usually associated with a significant rise in pH values from 8.3 to 9.2. Gleitz et al. (1996) estimated that the rise by one pH unit would require a decrease of 7700 mM DIC, equivalent to the DIC decrease (of 764 mM, uncorrected for salinity) observed at the surface of the lead 2 during stratification. Nutrients together with light play a major role in determining the distribution and magnitude of phytoplankton biomass and primary production. There are a few likely explanations as to why Phaeocystis in unstratified waters dominate while diatoms dominate in more stratified water columns (as discussed by Arrigo, 1998). The assimilation rate and photosynthetic efficiency of Antarctic diatoms are only 20–50% that of Phaeocystis (Tilzer et al., 1986), making them less competitive in a highly dynamic light environment of the turbulent water column. Phaeocystis exhibits both high assimilation rates and high photosynthetic efficiencies (Palmisano et al., 1986), distinct advantages in an unstable water column where light levels are changing rapidly (Richardson et al., 1983). In addition, the mucilaginous envelope surrounding Phaeocystis colonies is neutrally buoyant, allowing the colonies to remain near the surface in a mixed water column. However, it can be speculated that the mucus envelope makes Phaeocystis subject to diffusion-controlled CO2 uptake and that such colonies are in fact CO2 limited. This would become even more profound in an environment where a strong drawdown of DIC occurs, as was observed above the pycnocline in lead 2 during stratification. This could give diatoms a competitive advantage over Phaeocystis at the onset of blooms. In addition, as the onset of blooms is triggered by stratification driven by ice melt, the diatom dominance in sea ice (as found at the ISPOL floe but also in other studies, Thomas and Dieckmann, 2002; Lizotte, 2003) might outcompete Phaeocystis when diatoms are introduced in large numbers into surface waters by sea-ice melting (Smith and Nelson, 1986). Release from sea ice into the stratified surface water column suddenly exposes phytoplankton to strong irradiance, causing significant DNA damage that is likely to reduce community growth but also loss of biomass from the water column (Buma et al., 2001). The sudden enhancement of irradiance will require regulation and acclimation of light harvesting, photosynthesis, and photoprotection. The transition from low to excessive irradiance can over-reduce photosynthetic electron transport and initiate formation of reactive oxygen species. Sensitivity to excessive irradiance is strongly influenced by photoacclimation and nutrient availability because these

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conditions influence cellular pigment composition and protein turnover rates (van de Poll et al., 2005). Oxidative stress caused by factors such as ultraviolet radiation, low Fe and CO2 availability limit growth rate and can promote DMSP production (Sunda et al., 2002). In addition, in some cases, an increase of the release of DMS by some Phytoplankton species was observed (Sunda et al., 2002). These factors, along with N limitation, low temperatures, and high PAR, are all known as oxidative stress factors in plants (Winston, 1990). Sunda et al. (2002) therefore suggested that DMSP may be part of an antioxidant system in marine phytoplankton. To support this hypothesis, they presented evidence that DMSP and its known degradation products (DMS, DMSO, and acrylate) could be effective scavengers of highly toxic OH radicals. Since DMS is one of the most effective scavengers of reactive oxygen species known (about 60  better than DMSP), Sunda et al. further postulated that DMSP conversion to DMS via lyase activity might be induced by oxidative stress. Phaeocystis but also sea-ice diatoms are associated with high concentrations of DMSP and DMS (DiTullio et al., 1998; Trevena et al., 2003). The ability to use an effective radical scavenger system might explain why they are the dominant phytoplankton species in sea ice and along the retreating sea-ice edge. A profound increase of major sulfur compounds, coinciding with a rise of chl-a concentrations, was found towards the surface of the stratified water column. In the leads, the ratio between DMSP34 and chl-a34 increased from 67 nM mg1 in the water column to 189 nM mg1 above the pycnocline of lead 1. In lead, two DMSP34:chl-a34 ratios increased from 109 nM mg1 in the water column to 161 nM mg1 at the surface in the stratified water column (Table 1). In addition, the ratio between DMSP34 and DMS34 decreases by a factor two from the mixed water column towards the surface in the stratified water column of lead 2 (Table 1). From these ratios, the possibility can be inferred that DMSP production and conversion to DMS increase as a reaction to oxidative stress at the sea surface. Although the increase of DMSP and chl-a are strongly correlated, it cannot be concluded that high DMSP and DMS concentrations found at the surface are a result from in-situ production alone and thus form an active protection mechanism against oxidative stress. Sea ice could still be a source of these compounds. Trevena and Jones (2006) concluded that the source of elevated DMS and DMSP values in the water column of the Antarctic Sea ice Zone was sea ice because chl-a concentrations in the water column remained low. Photolysis is an important removal pathway for DMS (Hatton et al., 2004). By pooling data from different oceanic regions Hatton et al. (2004) found a highly significant correlation between DMS and DMSO in (near-)surface waters. The near-surface DMS and DMSO concentrations do confirm this close correlation, but also show that the ratio of DMS to DMSO (Table 1) increases

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from the mixed water column to the surface. This implies that DMS photolysis does not always result in DMSO production (as found in other studies, e.g., Kieber et al., 1996; Hatton, 2002), or that conversion pathways are of different importance at different depths of the stratified water column. For example, the light regime at the surface could well inhibit the activity of bacteria at the surface and indirectly affect conversion pathways and rates of sulfur compounds. Unfortunately, the ultimate cause of the decreased DMS:DMSO ratios and the significance of oxidative stress on the conversion and removal pathways of the major sulfur compounds in the surface waters cannot be assessed from the present study. The short field campaign in which this study took place by default only results in a brief ‘‘snap-shot’’ of the biogeochemistry of Weddell Sea leads. Concentrations of inorganic and organic compounds were found to be typical for Southern Ocean waters. However, a distinct, but not extreme, different chemical environment develops above the pycnocline during meltwater-driven stratification events. During these events, the lead surface was enriched in organic compounds and depleted in major nutrients. However, the origin of the chemical gradients observed towards the sea surface is not straightforward. Water in the newly formed leads will largely be a mixture of seawater and meltwater from the surrounding ice floes. Stratification occurs fairly rapidly and traps the biological community at the surface in a habitat that is dominated by strong gradients in light and salinity that slows down solute and particle exchange with the deeper water column. The succession of sea-ice biota in the surface layer is proposed to be comparable to a batch culture-type development (Gleitz et al., 1996). On short timescales, equivalent to the period of observation in this study, the water surface above the pycnocline can be seen as an ideal mesocosm to test hypotheses related to primary production and adaptation to oxidative stress in the high radiation environment of the polar regions. Acknowledgments This work was financially supported by the Marie Curie Training Site Fellowship (contract number HPMF-CT2002-01865) and by NERC (Award Ref. No. NER/B/S/ 2003/00844). We would like to thank the WHOI Ocean Life Institute. We would also like to thank D. Janssen (AWI), who performed the DOC analysis. The authors would like to express their deepest thanks and appreciation to the crew of the R.V. Polarstern for all their efforts in helping us throughout ANT XXII/2. Thanks also to the chief scientist Dr. M Spindler and to the AWI for making the cruise possible. References Arrigo Jr., K.R., 1998. Physical forcing of phytoplankton dynamics in the southwestern Ross Sea. Journal of Geophysical Research 103, 1007–1022.

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