Substantial primary production in the land-remote region of the central and northern Scotia Sea

Deep-Sea Research II 59-60 (2012) 47–56

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Substantial primary production in the land-remote region of the central and northern Scotia Sea M.J. Whitehouse, A. Atkinson n, R.E. Korb, H.J. Venables, D.W. Pond, M. Gordon British Antarctic Survey, Natural Environmental Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK

a r t i c l e i n f o

abstract

Available online 23 May 2011

The Scotia Sea area has high productivity relative to the Southern Ocean as a whole, but this displays strong latitudinal and longitudinal gradients. Elucidating the extent of these from a single cruise is problematic, given the high variability of bloom timing and location in this region. Therefore, this study used data from transects across the central Scotia Sea in spring, summer and autumn of 2006, 2008 and 2009, combined with satellite data, to obtain a larger-scale appreciation of the latitudinal contrasts in phytoplankton standing stock and primary production across the region. Concentrations of nitrate, phosphate and particularly silicic acid increased towards the south of the transect with the latter showing a step change at the Southern Antarctic Circumpolar Current Front (SACCF). Changes in seasonal nutrient concentrations indicated increasing phytoplankton uptake north of  571S that peaked at  531S in the Georgia Basin. Based on seasonal depletions of nitrate relative to phosphate, the highest relative nitrate uptake occurred northwest of South Georgia on the periphery of the Georgia Basin, indicating efficient nitrate use here due to iron-replete conditions. An integrative approach to examine these gradients was with the use of 10-year satellite climatology data. These showed that the lowest mean chlorophyll a (chl-a) values were in the central/northern Scotia Sea, but these were still substantial values, 67% of values within the Georgia Basin bloom. Cruise data on chl-a and on microplankton biomass from cell counts support this finding of substantial biomass in the central Scotia Sea; since these averaged half of values in the iron-fertilised bloom of the Georgia Basin downstream of South Georgia. Given that our transect was nearly 1000 km long and in parts was land remote with low iron concentrations, the relatively high production in the central and northern Scotia Sea is surprising. Iron levels may be maintained here by efficient recycling and irregular injections, possibly for example from dust deposition or shelf-derived inputs from the south. The moderate chl-a concentration across the mid-Scotia Sea and southwest of South Georgia reflect periodic, non-iceassociated blooms that occur in some years and not others. These may provide a connection between the large populations of krill inhabiting the northern and southern fringes of the Scotia Sea. & 2011 Elsevier Ltd. All rights reserved.

Keywords: Scotia Sea Antarctica Southern Ocean Productivity Nutrients Gradients Silicate Silicic acid Phosphate Nitrate

1. Introduction The SW Atlantic is one of the most productive sectors of the main Antarctic Circumpolar Current (ACC) core (Moore and Abbot, 2000; Constable et al., 2003; Atkinson et al., 2008). This productivity supports both a commercially important food web (Everson, 2001) and a significant biogeochemical role in nutrient cycling and export (Tre´guer and Jacques, 1992; Schlitzer, 2002; Sarmiento et al., 2004; Jones et al., 2012). Compared to the abyssal plain that characterises much of the ACC’s path, the SW Atlantic sector is complex with the Scotia Arc and its seamounts and shelves forming the northern, southern and eastern rims of an elongated, relatively shallow basin known as the Scotia Sea.

n

Corresponding author. E-mail address: [email protected] (A. Atkinson).

0967-0645/$ - see front matter & 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2011.05.010

This bathymetric variability is now known to be a major cause ¨ of elevated productivity within this SW Atlantic sector (Ronner et al., 1983; Jacques, 1989; Jacques and Panouse, 1991; Holm-Hansen et al., 2004a). The shelves fringing the Scotia Sea release iron (Holeton et al., 2005; Ardelan et al., 2010) and this stimulates primary production in October–November when light becomes non-limiting (Holm-Hansen et al., 2004a,b; Venables and Moore, 2010; Park et al., 2010). These blooms contrast with the High Nutrient-Low Chlorophyll (HNLC) conditions in the central Drake Passage, where waters from the deep basin of the land-remote SE Pacific enter the Scotia Sea. While these basic features of productivity within the Scotia Sea are well known, the intense inter-annual as well as spatial variability of this region are only recently being understood (Park et al., 2010). For example Holm-Hansen et al. (2004b) found high chl-a concentrations throughout the whole central Scotia Basin, whereas in a similar large-scale survey three summers later, Korb et al. (2005) found the same area to have chl-a concentrations at near-winter values.

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Recently, Park et al. (2010) used satellite data to show that predictable phytoplankton blooms were only found in small portions of the SW Atlantic sector. This variability hinders generalisations about gradients of phytoplankton and its productivity across the Scotia Sea. Conventional ship surveys struggle to cover the full extent of the Scotia Sea and logistics means that these are often just single snapshots, typically of summer. Satellite data provide a larger-scale context, but are prone to other limitations. These include underestimations of in-situ chl-a values (Korb et al., 2004), non-inclusion of deep chl-a maxima (Schlitzer, 2002; Gilpin et al., 2002; Whitehouse et al., 2008), absent data due to cloud and ice cover, plus lack of information about phytoplankton composition or productivity. The influence of sea ice in the south adds further complexity and underlines the fact that seasonal coverage, combining shipboard and satellite observations, are needed to characterise the gradients in productivity across the Scotia Sea. In this paper we consider data collected in spring, summer and autumn during three survey transects sampled from south to north across the Scotia Sea. We illustrate the large-scale picture of chl-a as measured by satellite and then consider phytoplankton abundance and growth as indicated by macronutrient depletions and in-situ chl-a values. Measurements were made across the basin from the ice-edge in the south to the Antarctic Polar Front (APF) in the north. As with previous studies in the region, samples collected with CTD bottles are considered. However, we also use high frequency surface measurements to explore the variability of phytoplankton abundance and nutrient use to gain a much higher resolution view. Our overall objective was to quantify phytoplankton biomass and productivity in the central Scotia Sea, relating these to values around the iron-fertilised Scotia Ridge that forms the outer perimeter of this sea.

12 March 2009–15 April 2009) along a  1000 km long transect between the South Orkney Islands and the Antarctic Polar Front to the north of the Georgia Basin (Fig. 1, see also Tarling et al., 2012). During the spring and summer surveys, the southern end of this transect was near the ice-edge, which during the autumn cruise was well to the south of our study area. The most southerly samples were collected near the South Orkney Islands shelf that constitutes part of the South Scotia Ridge. From south to north the transect crossed the Southern Boundary (SB) of the ACC, the Southern ACC Front (SACCF) and the North Scotia Ridge (NSR) west of South Georgia before entering the Georgia Basin and approaching the APF. At each station, vertical profiles of temperature and salinity were measured with a SeaBird 911 þ CTD (see Venables et al., 2012 for further details). Water samples were collected with 10 L Niskin bottles during the CTD’s upcast and typical sampling depths were 5, 10, 20, 30, 40, 50, 60, 80, 100, 120, 140, 160, 180, 200, 400, 600, 800, 1000, 2000 and 3000 m and within 10 m of the seabed. A similar sampling frequency within 10 m of the seabed was used in shallower shelf waters. Between CTD stations and during biological survey grids, near-surface samples were taken via an intake on the ship’s hull (at 7 m depth towards the bow) using the non-toxic supply system. 2.2. Satellite chl-a data Satellite surface chl-a data for the three cruises (Fig. 2) were from MODIS-Aqua R1.1 and SeaWiFS R2009, obtained from http:// oceancolor.gsfc.nasa.gov. Data used were one month climatologies, 9 km Level 3 mapped images. Climatological mean SeaWiFS chl-a values (1997/1998–2009/2010) were also obtained from this source using 2010 reprocessing. 2.3. Macronutrients

2. Methods 2.1. Study site and sampling Data were collected from the RRS James Clark Ross during spring (cruise JR161; 24 October 2006–2 December 2006), summer (cruise JR177; 31 December 2007–14 February 2008), and autumn (JR200;

In addition to CTD samples, nutrient concentrations in nearsurface waters sampled via the non-toxic supply were monitored continuously and logged to a computer every 10 s (Whitehouse and Preston, 1997). All samples were filtered through a mixed ester membrane (pore size 0.45 mm, Whatman), and the filtrate was analysed colorimetrically for dissolved silicic acid (Si[OH]4–Si), nitrate (NO3–N), ammonium (NH4–N) and phosphate (PO4–P)

Fig. 1. Sampling locations during (A) JR161 (spring), (B) JR177 (summer) and (C) JR200 (autumn). Major geographical features, including the Northwest Georgia Rise (NGR) are shown in panel (A), and the location of the North Scotia Ridge is indicated by the 500 m isobath around South Georgia and south of the Georgia Basin. The stations at which deep sediment traps were deployed are indicated in panel (B); 7 and 8 which were, respectively, upstream and downstream of South Georgia. Station locations are indicated according to the sub-region or water type they were in (see legend in panel (C)), and underway sampling is indicated with a grey line.

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Fig. 2. Monthly composites of MODIS imagery for the study site in (A) November 2006, (B) January 2008 and (C) March 2009. White areas represent missing data, primarily due to cloud cover. The mean positions of the Antarctic Polar Front (APF; Moore et al., 1999), the Southern Antarctic Circumpolar Current Front (SACCF; Thorpe et al., 2002) and the Southern Boundary of the Antarctic Circumpolar Current (SB; Orsi et al., 1995) are indicated with black lines and identified in (A) November 2006 panel. The 500 m isobath is also shown in black.

with a segmented-flow analyser (Technicon; Whitehouse, 1997). The nitrate measurement included nitrite (NO2), which is not considered separately as its concentration varied little and typically comprised o1% of total NO3 þNO2. We used CTD water bottle data to check how representative the underway near-surface nutrient values were of concentrations in the water column below. For 31 stations we compared the concentration at 7 m (depth of ship’s non-toxic supply intake) with a mean value derived from measurements made between 0 and 50 m. All regressions were highly significant (po0.001) and R2 values for silicic acid, phosphate and nitrate were 99.9%, 92.7% and 97.9%, respectively. Thus we consider our high resolution surface measurements to be a good proxy for conditions in the upper mixed layer. 2.4. Calculation of nutrient deficits Nutrient deficits were estimated from the difference between concentrations in the winter water (WW) layer and those in the water column above it (Jennings et al., 1984). The WW layer in Antarctic Surface Water is characterised by a well-defined potential temperature minimum (ymin), located between 70 and 140 m during the present study. On the occasions when the ymin extended across a band of depths then nutrient concentrations at the shallowest depth were used.

surveys (Fig. 2). During November 2006, elevated chl-a concentrations were notable in an extensive west–east band between the SACCF and the SB. An area centred on 58.51S and 41.51W contained particularly high values of 8 mg chl-a m  3. On the shelf of South Georgia and downstream waters in the Georgia Basin, values up to  0.5 mg chl-a m  3 were evident while the rest of the study area that was not obscured by cloud held concentrations between 0 and 0.2 mg chl-a m  3. During January 2008 the bloom within the Georgia Basin was well advanced with concentrations 45 mg chl-a m  3 over much of this area. Compared with the spring, a modest bloom with values between 1 and 2 mg chl-a m  3 occupied much of the area north of the SACCF while values were substantially lower (often o0.5 mg chl-a m  3) over much of the area to the south of this front. However, between the South Orkney shelf and the SB, chl-a concentrations were somewhat higher at  0.5–1 mg chl-a m  3. During March 2009 the bloom had persisted in the Georgia Basin but peak values (up to 8 mg chl-a m  3) were found over the Northwest Georgia Rise—a seamount to the north of South Georgia. Concentrations between the South Orkneys and the SB were similar to summer 2008 values (up to  1 mg chl-a m  3), while post-bloom conditions ( o0.5 mg chl-a m  3) were evident in much of the rest of the Scotia Sea. 3.2. CTD data

2.5. Chlorophyll-a determination Water samples for chl-a analysis were taken hourly from the ship’s non-toxic supply at 7 m depth while the ship was transecting. Samples were filtered through GF/F filters (particle retention 0.7 mm) under  70 mm Hg vacuum and immediately frozen and stored at 201C. The filtered samples were extracted with 10 ml of 90% acetone in the dark for 24 h and fluorescence was measured before and after acidification with 1.2 M HCl (Parsons et al., 1984). The fluorometer (Turner TD-700) was calibrated against chl-a standards from Sigma chemicals.

3. Results 3.1. MODIS chlorophyll-a data MODIS satellite data indicate the spatial extent of phytoplankton blooms in our study area during the three months of our

Potential temperature and salinity values were used to establish water-mass boundaries (Fig. 3A). At the resolution of our CTD casts there was good separation of the various characteristics associated with the various water masses of the Scotia Sea. The frontal positions derived from our data (Fig. 4) are in general agreement with earlier surveys (Brandon et al., 2004; Korb et al., 2005) and are either similar to, or somewhat south of the mean front positions overlaid on our MODIS plots (Fig. 2). Seasonal change is also apparent in the temperature and salinity data. There are obvious temperature increases in the surface waters but also low salinity water in summer south of the SB is indicative of ice melt at the southern end of the transect. The transect is also characterised by latitudinal and vertical silicic acid gradients, and, when plotted against salinity, these data also allow differentiation between the different water masses (Fig. 3B). This plot also demonstrates aspects of the seasonal progression. For instance, low salinity water was evident during summer south of the SB but lowest silicic acid

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the south to 4 1C near the APF. Overall, this gradient was maintained through to summer and autumn with an overall increase throughout of  2 1C. Notable exceptions to this were low temperatures at the south and north periphery of the Georgia Basin during summer and autumn. Surface salinity was reasonably consistent during the spring although higher values were measured at the southern end of the transect (Fig. 4F). During summer, a gradient at the southern end of the transect was coincident with temperature and was likely due to ice melt. During summer and autumn, low salinity water in the Georgia Basin appeared to be coincident with a temperature peak. Increased variability of salinity and temperature at 571S during autumn was also coincident with major variability of silicic acid concentrations (see below). 3.3.2. Chl-a Our hourly surface extracted chl-a data (Fig. 4G) largely concur with the MODIS measurements in Fig. 2. In spring the band of elevated values is evident at 581S and high values are also noticeable for the Georgia Basin and near the APF—however, the latter appear higher than MODIS would suggest. In summer the Georgia Basin bloom (52–541S) values are clearly evident although once again MODIS appears to underestimate concentrations between the South Orkneys and the SB and also to the south of the NSR. In the autumn there is good agreement between the extracted and MODIS chl-a data with the Georgia Basin bloom evident in both and minor elevations evident either side of the SB.

Fig. 3. (A) Potential temperature (1C) versus salinity. (B) Silicic acid (mmol m  3) versus salinity. Spring (Sp), summer (Su) and autumn (Au) measurements are differentiated for the sub-regions north of the North Scotia Ridge (N of NSR), between the Southern Antarctic Circumpolar Current Front and the NSR (SACCF-NSR), between the Southern Boundary of the Antarctic Circumpolar Current and the SACCF (SBSACCF) and south of the SB (S of SB) as identified in the legend in panel (A).

concentrations were measured during autumn when salinity was higher. Also, silicic acid reaches depletion north of NSR by autumn whereas this appears to have occurred earlier during the summer at some stations further south between the SACCF and the NSR. Winter Water (WW) values for silicic acid, nitrate and phosphate are indicated in Fig. 4A–C. As with surface values, WW nutrient concentrations were highest at the southern end of the transect, particularly so for silicic acid. Mean silicic acid concentrations of 80.4 mmol m  3 (SD 3.3) south of the SB decreased northwards to  30 mmol m  3 at the SACCF and were 32.7 mmol m  3 (SD 1.1) in the Georgia Basin. Nitrate WW concentrations were 30 mmol m  3 (SD 1.1) along most of the transect but were generally lower (mean 28.8 mmol m  3, SD 1.1) between the SACCF and the NSR, while phosphate WW values were fairly consistent throughout the transect at 2.0 mmol m  3 (SD 0.1). 3.3. Near-surface underway transecting data 3.3.1. Temperature and salinity Surface temperature data indicate the extent of latitudinal and seasonal change (Fig. 4E). Overall, on all 3 surveys there was a substantial (5–6 1C) increase in near-surface temperatures northwards along the transect. During spring, surface waters south of the SB were mostly o 1 1C. During summer there was a gradient through this area from   0.5 1C in the south to  2 1C which had warmed further and levelled out to 2 1C throughout the area in autumn. North of the SB in spring, there was a gradient from 0 1C in

3.3.3. Macronutrients A major latitudinal gradient was evident for surface silicic acid concentrations (Fig. 4A). Highest values were to the south of the SB with mean spring concentrations of 75 mmol m  3, while summer and autumn levels were similar (mostly 65– 75 mmol m  3). However, summer values dipped substantially to o40 mmol m  3 between 591 and 601S. A steep latitudinal gradient down to 30 mmol m  3 at the SACCF was evident in spring, while much greater variability was found in both summer and autumn. An anomaly encountered in autumn at  571S held a wide range of  40 mmol m  3 silicic acid concentrations. Such anomalies reflect our transect line contacting eddies or meanders in the SACCF and sampling of contrasting silicic acid concentrations on either side of it (Venables et al., 2012). Between the SACCF and the NSR, spring values of 20–30 mmol m  3 were found which decreased to o10 mmol m  3 in parts. North of the NSR spring values of  30 mmol m  3 in the Georgia Basin decreased to o10 mmol m  3 near the APF and summer and autumn values of o5 mmol m  3 were evident. Nitrate and phosphate levels were more consistent from south to north but even so, in spring the highest values were in the south (430 mmol m  3 and 42 mmol m  3 respectively; Fig. 4B and C). Although highly variable, by summer and autumn, concentrations to the south of the SACCF had decreased to 22–26 mmol m  3 nitrate and 1.2–1.5 mmol m  3 phosphate. All values decreased north of the SACCF. Spring values of 25–30 mmol m  3 nitrate were reduced to  12–25 mmol m  3 during summer and autumn while spring phosphate concentrations of 1.6–2.0 mmol m  3 were similarly reduced to 0.5–1.5 mmol m  3. The greatest nitrate and phosphate depletions were in the southern Georgia Basin but were also notable in the northern Georgia Basin and in the vicinity of the SACCF and the NSR. Note that depletion was not uniform in the Georgia Basin. A latitudinal gradient was not found for surface ammonium but increased variability and higher concentrations became evident through the seasons at particular locations (Fig. 4D). During spring, concentrations of  0.5 mmol m  3 were found south of the SB and north of the NSR with slightly higher values (0.5–1.0 mmol m  3) in

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Fig. 4. Seasonal near-surface (7 m depth) values measured along the Scotia Sea transect. Macronutrient plots, with the exception of ammonium include Winter Water (ymin) concentrations: (A) silicic acid (mmol m  3), (B) nitrate (mmol m  3), (C) phosphate (mmol m  3), (D) ammonium (mmol m  3), (E) POTENTIAL temperature (1C), (F) salinity and (G) chlorophyll a (mg m  3). Arrows indicate positions of the Southern Boundary (SB) of the Antarctic Circumpolar Current and the Southern Antarctic Circumpolar Current Front (SACCF) on each cruise (colour-coded as in legend), with the centre of the North Scotia Ridge (NSR) demarcated by a vertical line.

the waters between. Seasonal increases were noted on either side of the SB (up to 2 mmol m  3) and in the Georgia Basin in summer (41 mmol m  3), but particularly north of 531S in autumn when concentrations 43 mmol m  3 were found. 3.4. Nutrient deficits A General Linear Model (GLM) analysis of surface silicic acid, phosphate and nitrate data indicated significant (p o0.001) latitudinal and seasonal variability for all nutrients. As our data shows, this was particularly so for the latitudinal variability of silicic acid (Fig. 4A). A GLM analysis of ymin nutrient values (winter water) showed significant (p o0.001) variability with latitude for silicic acid and nitrate but not for phosphate (p¼ 0.14). However, allowing for latitudinal change, there was no significant variance between cruises (p Z0.31), indicating that our pre-bloom winter concentration estimates are robust. To enable us to consider nutrient use over the entire length of the transect ( 4101 latitude) we interpolated values between our winter water stations and incorporated actual pre-bloom

concentrations measured on a previous BAS cruise (JR25; Whitehouse et al., 2000) from between 501S and 531S. The seasonal view of nutrient use presented in Fig. 5 is derived from 0.11 latitude means and a fitted running average (Minitab Lowess line with 0.5 degrees of smoothing and number of steps ¼2). Because silicic acid distribution varies so much with latitude, our seasonal view is doubtless complicated by frontal anomalies and the transfer of nutrients via eddies and meanders (Fig. 5A). This is especially so for our autumn survey. Nevertheless, there is some indication that south of  561S the majority of silicic acid use had occurred by spring, earlier than further north. Also the difference between winter and summer concentrations clearly indicates greater utilisation between 521S and 561S. Seasonal phosphate use appears to be relatively straightforward (Fig. 5B). Highest values are evident in winter and spring, after which major depletion occurs. Uptake increases north of  571S and peaks at  531S in the Georgia Basin. Nitrate use is similar to that of phosphate (Fig. 5C), in that the seasonal deficit appears to increase north of  571S and once again possibly peaks in the Georgia Basin. However, it differs substantially in autumn, when

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3.5. Nutrient deficit ratios Our underway nutrient data are most extensive for spring and summer, so comparison of these allows us to examine further the ratios of nutrient deficits between these periods. These calculations again use 0.11 latitude means and paired observations (Fig. 6). Although there is some evidence of anomalous ratios at the SACCF and for silicic acid:nitrate at the southernmost stations, the highest nitrate:phosphate ratios (14–16:1) occurred on the southern and northern limits of the Georgia Basin and were coincidental with silicic acid:nitrate ratios of 1:1. These areas lie downstream of South Georgia—directly (southern Georgia Basin) and in the retroflection of the region’s major water flow (northern Georgia Basin). Such efficient nitrate utilisation by phytoplankton is doubtless due to relief from Fe stress, as has been documented previously (Korb and Whitehouse, 2004; Holeton et al., 2005; Whitehouse et al., 2008). 3.6. Regional contrasts in productivity across the Scotia Sea Seasonal changes in nutrient concentrations indicated the variability of phytoplankton uptake along the transect. To determine productivity based on a variety of approaches we first divided the region of our transect line into 4 sub-regions based on 21 latitudinal by 31 longitudinal boxes (see Fig. 7A). These sub-regions were entitled NW-South Georgia, SW-South Georgia, Mid-Scotia and South Scotia, and they broadly align with the microplankton community boundaries of the same names, determined by cluster analysis of microplankton taxa (Korb et al., 2012). Below we describe contrasts in phytoplankton biomass and productivity across these 4 sub-regions, based on each method in turn.

Fig. 5. Average seasonal near-surface ( 7 m depth) macronutrient trends (mmol m  3) along the Scotia Sea transect derived from 0.11 latitude bins for: (A) silicic acid, (B) phosphate and (C) nitrate. Colour coding of seasons is indicated in panel (A). The solid lines represent fitted Lowess trend lines (see Section 3.4. Nutrient deficits).

Fig. 6. Nutrient deficit ratios calculated for the decreases measured between our spring and summer cruises. The points represent 0.11 latitude binned data as in Fig. 5. Round symbols and solid trend line represent the deficit in silicic acid relative to that of nitrate and is scaled to the left axis. Crosses and dashed line represent the deficit in nitrate to that of phosphate and is scaled to the right axis. The trend lines were derived from Lowess lines from the Minitab statistical package.

3.6.1. Satellite-derived chl-a Monthly climatologies (1997–2009) of chl-a show that substantial increases in chl-a tend to occur around October, right across this latitudinal gradient (Fig. 7B). However, the intensity, timing and duration of the bloom show regional differences. While the South Georgia region has the highest mean chl-a values as expected, the chl-a maxima in both of the northern boxes occurs later in the summer than further south. To obtain a picture of the seasonally integrated chl-a value, we calculated the area under the seasonal curves for each of the 4 subregions, expressing it as a percentage of the highest value at NWSouth Georgia (Fig. 7C, black line). These Scotia Sea values were between 42% and 53% of those of the Georgia Basin bloom. 3.6.2. Survey data: chl-a values, microplankton biomass and primary production The data obtained during the spring, summer and autumn cruises also allow some overview of the mean productivity of the 3 regions of the central Scotia Sea, relative to that at South Georgia (Fig. 7C). These values, corresponding to depth-integrated primary production, depth integrated chl-a, near-surface (7 m) chl-a and Lugols cell-count-derived microplankton biomass, are presented in Korb et al. (2012). Taken together, these results suggest that lowest values tend to occur in the SW-South Georgia Zone. However, overall values within the Scotia Sea were often at least 50% of the maximum values observed NW of South Georgia in the Georgia Basin.

4. Discussion concentrations were generally 1–2 mmol m  3 higher than in summer. Again this may be due to non-biological agents but it may be indicative of a switch by phytoplankton to reduced forms of N (Fig. 4D) and remineralisation to the oxidised form.

A recent study using satellite data concluded that regular, predictable blooms occur in only a small proportion of the SW Atlantic sector (Park et al., 2010). Our three cruises need to be

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Fig. 7. (A) Position of 21 latitude by 31 longitude boxes to characterise gradients across the Scotia Sea. These boxes are superimposed upon a SeaWiFS summer chl-a climatology of October–February 2006–2009 and our transect line. (B) SeaWiFS-derived monthly 13-year climatologies (1997/1998–2009/2010), extracting mean values from within each box shown in panel (A). (C) Total integrated chl-a within each of the 4 sub-regions shown in panel (A) (i.e. data integrated from panel (B)) plus shipboard data on primary production and phytoplankton standing stock, presented in Korb et al. (2012). All values are expressed as means, plotted as percentages of the maximum value which was within the NW-South Georgia sub-region. These maximum values are 67 mg C m  3 for microplankton biomass, 89 mg m  2 for integrated chl-a, 2.3 mg m  3 for near-surface chl-a, and 1.48 g C m  2 d  1 primary production (Korb et al., 2012).

viewed from this perspective; they incorporate inter-annual—as well as seasonal and regional variability. Because any single cruise provides only a snapshot, we also used a series of independent methods to provide some generalities about productivity across the Scotia Sea. Each method reaches broadly the same conclusion—that phytoplankton biomass and production within the land remote, central/northern Scotia Sea is substantial, averaging over one-third that in the well-known hotspot in the Georgia Basin NW of South Georgia. This difference is also similar

to that found for the seasonal Dissolved Inorganic Carbon deficit by Jones et al. (2012) for stations in the summer South Georgia bloom (4.6 mol m  2) compared to low chl-a stations upstream of the island (2.2 mol m  2). That the central/northern Scotia Sea is so productive, relative to the Georgia Basin bloom, was unexpected. Satellite chl-a colour figures (including our own in Fig. 2), often portray this area in purples or blues, invoking the idea of much lower productivity than the bright orange or red hotspot downstream of South

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While nutrient deficits and satellite-based approaches integrate greater spatial–temporal scales than direct in-situ measurements, both have potential biases. For nutrient deficits, the processes of vertical mixing, alternative nutrient sources (such as ammonium) and remineralisation within the mixed layer may lead to underestimates of primary production in any region. Indeed, our own study (Fig. 6) shows variability in the relative uptake of nutrients. However, there is potential for further bias in underestimating production near South Georgia. Nutrient deficits are measured for the position of the water at the time of sampling, despite the water having flowed long distances during the seasonal timescale of the observations. Flow times from the Antarctic Peninsula area to South Georgia are measured in months rather than years (Thorpe et al., 2004; Fach et al., 2006). Thus estimates of seasonal productivity of stations near South Georgia, based on nutrient deficits integrating over 6 months, likely include the transit time across the lower belt upstream of the island. This ‘‘smearing’’ could explain why productivity gradients based on nutrient deficits tend to underestimate uptake. So while our deficit ratios (Fig. 6) provide a reasonable estimate for the water sampled, our apparent seasonal change (Fig. 5) contains a longitudinal component in addition to the latitudinal gradient. Climatologies of satellite-derived chl-a values provide an alternative way of examining this larger-scale picture, but they rely on accurate conversion factors from ocean colour to chl-a. Korb et al. (2004) show that SeaWiFS-derived chl-a underestimates in-situ chl-a more seriously at high chl-a values (30% at 45 mg m  3) than at lower values (87% at o1 mg m  3). This could lead to a roughly 50% underestimation of the South Georgia bloom chl-a concentrations based on SeaWiFS. However, even allowing for this underestimation, Scotia Sea chl-a values would still be substantial, averaging one-third of those in the Georgia Basin bloom. The shipboard data in Fig. 7C (see also Korb et al., 2012) provide snapshots of biomass and primary production, averaged across 3 times of year in 3 different seasons. Just three repeats of one transect preclude generalisation (for instance the spring cruise had anomalously low chl-a values downstream of South Georgia and the summer cruise had lower than average chl-a values in the central/ northern Scotia Sea—see Park et al., 2010). Nevertheless, they offer a complementary view on productivity gradients. Overall the picture in Fig. 7C is of lowest production and biomass in the most landremote sub-region of the transect—the SW-South Georgia region immediately upstream of South Georgia. As might be expected, productivity increases from this region towards the south, in waters seeded by iron from the Southern Scotia ridge (Ardelan et al., 2010; Dulaiova et al., 2009). Because the values are measured directly, there is no systematic bias. Taken together, our results, plus the DIC deficits from Jones et al. (2012), suggest that phytoplankton biomass density within the Scotia Sea is substantial, and is roughly half that of the major

8 7

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4.1. Measuring regional contrasts in phytoplankton and primary production

500

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Georgia. Further, this central area is land remote, being over 700 km downstream of the nearest shelf area that could supply iron. Based on data from our cruises (Nielsdottir et al. under review) and others in this area (Bucciarelli et al., 2001; Ardelan et al., 2010), dissolved iron concentrations halve every 25, 71 or 151 km from its land/shelf source (the values varying according to the study). Indeed, some of the iron values measured on these cruises were at growth-limiting concentrations in the central/ northern Scotia Sea (Nielsdottir et al., under review). Below we examine first, the factors that might lead us to underestimate the true magnitude of the productivity contrast, and second the implications of high productivity in the central/northern Scotia Sea on the wider-scale food web.

mg carbon month-1

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Fig. 8. Total monthly particulate carbon collected during 2008 by deep sediment traps deployed at sites 7 and 8, respectively, upstream and downstream of South Georgia (see Fig. 1(B)). Traps were Parflux Mark78H 21-cup, mouth area 0.66 m2. Both sediment traps were deployed at depths of 2000 m. Mean current velocities as determined with Nortek Aquadopp current metres were o 10 cm s  1 at both sites. Note that no data were available for February 2008 for the downstream trap at station 8.

bloom in the Georgia Basin. The colour scaling chosen for satellite images often over-emphasises blooms, but closer inspection of summer climatologies (e.g. Fig. 9 of Atkinson et al., 2008; Fig. 5b of Park et al., 2010) show substantial chl-a concentrations also right across the eastern half of the Scotia Sea. While these average conditions may hold, we do not want to underplay the much greater contrasts that can exist in some years. The central Scotia Sea blooms in some years but not in others—for example in the summer 2008 cruise season, conditions approaching HNLC were observed here (Jones et al. 2012, see Fig. 2B). This inter-annual variability in the central Scotia Sea is illustrated clearly in Park et al. (2010) and Korb et al. (2012). When a central Scotia Sea bloom is absent it can result in a very steep gradient in chl-a in the northern part of the region. The absence of a central Scotia Sea bloom during 2008 is illustrated in Fig. 10 of Park et al. (2010) and during this year our deep sediment traps moored at station 7 and 8 (for positions see Fig. 1B) revealed 10-fold higher deep C sequestration in the Georgia Basin bloom compared with southwest of South Georgia (Fig. 8). Obviously deep sequestration may not scale linearly with primary production, but this example is a reminder that the Georgia Basin bloom can indeed generate substantial contrasts, at least for some processes in certain seasons. 4.2. Causes and implications of elevated productivity in the central/ northern Scotia Sea The Southern Ocean is often simplified into high versus low productivity regimes; namely the iron replete seasonal ice- or shelf influenced zones versus the remote, deep ocean HNLC belts (Smetacek et al., 2004). However, large open ocean areas such as the Lazarev Sea and offshore in the Ross Sea sector experience periodic blooms and moderate productivity (Moore and Abbot, 2000; Atkinson et al., 2008). Possibly these, like the central and northern Scotia Sea, represent intermediate scenarios with periodic iron stress and enrichment. What stimulates ephemeral blooms in such areas? Possible sources of iron include advection of eddies carrying shelf-derived inputs from the south, melting icebergs, deep upwelling from

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submarine topography, and periodic dust deposits (Smith et al., 2007; Meskhidze et al., 2007; Sokolov and Rintoul, 2007). At present the relative roles of these potential sources is unknown. The shelf at the tip of the Antarctic Peninsula is one important source of iron, which may be transported into the open sea via eddies formed downstream of the Shackleton Fracture Zone north of the South Shetlands (Dulaiova et al., 2009; Ardelan et al., 2010; Zhou et al., 2010). This water is then transported eastwards by the SACCF with continued mesoscale activity, as illustrated by our variable summer silicate values (Fig. 4A). When combined with a northwards component via Ekman drift (Venables and Meredith, 2009) this seeds the central Scotia Sea. Such a scenario would result in elevated nutrient depletions such as we found at  561S where depletion ratios indicated efficient nitrate use potentially brought about by relief from iron stress. The SW-South Georgia area, being north of the SACCF, will receive less iron from this source and this is reflected in the lower spring chl-a concentrations generally found here. However, the area does have a chl-a peak much later in the season, in January and February (Fig. 2B). Enhanced chl-a at this time in this area is often episodic and the shapes of the blooms do not align with the current flow lines. This, together with the assumption of increased dust creation in late summer as South American soils and lakes dry, is suggestive of a dust-derived iron source from the grasslands to the west (Erickson et al., 2003). Gasso et al. (2010) showed that dust from Patagonia can reach Antarctica but the quantity and especially the bioavailability of iron from dust deposition is an area of ongoing investigation so it is not possible to draw any firm conclusions. Whatever the conditions that supply micronutrients to the central/northern Scotia Sea, a series of factors may allow rapid phytoplankton build-up when these events do occur. First they are relatively close to the adjacent and highly productive fringes of the Scotia Sea, as compared to the more remote HNLC belts of the open Southern Ocean. This may allow substantial seed populations of diatoms to be present in the Scotia Sea to benefit from any immediate improvement in conditions. Secondly, nutrient recycling is very efficient in iron stressed environments (Bowie et al., 2001; Sarthou et al., 2008), so even modest supplies of new iron can lead to relatively high amounts of fixed carbon. The third point is that such blooms are unpredictable in space and time (Park et al., 2010). Because of this they are more likely to escape grazing control, since the grazing and growth rates and generation times of grazers, particularly metazoans is insufficient to keep pace with ephemeral, short-lived bloom events (Shreeve et al., 2002; Atkinson et al., 1996). While all such processes are clearly speculative, they provide some basis for interpreting these bursts of central Scotia Sea production. The food web of the SW Atlantic sector is commercially important (Everson, 2001; Atkinson et al., 2001; Murphy et al., 2007), and thus the connection between its South Scotia ridge and South Georgia sub-systems is under intense study (e.g. Thorpe et al., 2004; Fach et al., 2006). The substantial primary production in the intervening ocean may thus act as a ‘‘bridge’’ between these productive northern and southern sub-systems. The moderately productive waters of the central/northern Scotia Sea already have high zooplankton biomass (Ward et al., 2006, 2012a, 2012b; Mackey et al., 2012). These waters receive a further injection of iron as they transit the north Scotia Ridge, leading to biomasses of zooplankton and krill over 20 g dry mass m  2, comparable to the most productive ecosystems worldwide (Ward et al., 1995; Atkinson et al., 2001). The high biomass of krill at South Georgia and its winter fishery are sustained by krill that have transited the central latitudes of the Scotia Sea, and these benefit from being able to continue feeding and growing in its moderate chl-a concentrations (Atkinson et al., 2006, 2012; Schmidt et al., 2006,

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2012). The spring blooms of the central Scotia Sea were also highlighted by Schmidt et al. (2012) as being un-associated with the marginal ice zone, yet being the prime spawning ground for krill in the Southern Ocean. Therefore the elevated productivity that extends across the middle reaches of the Scotia Sea is significant for food web connectivity within this system.

Acknowledgments We first thank the officers and crew of the James Clark Ross for their professional support, as well as the Chief Scientists of the 3 cruises, Rachael Shreeve, Geraint Tarling and Rebecca Korb. We are grateful to Alex Poulton for microplankton cell count data and the NASA Ocean Biology Processing Group for MODIS and SeaWiFS chlorophyll data. References Ardelan, M.V., Holm-Hansen, O., Hewes, C.D., Reiss, C.S., Silva, N.S., Dulaiova, H., Steinnes, E., Sakshaug, E., 2010. Natural iron enrichment around the Antarctic Peninsula in the Southern Ocean. Biogeosciences 7 (1), 11–25. Atkinson, A., Shreeve, R.S., Pakhomov, E.A., Priddle, J., Blight, S.P., Ward, P., 1996. Zooplankton response to a phytoplankton bloom at South Georgia, Antarctica. Marine Ecology Progress Series 144, 195–210. Atkinson, A., Whitehouse, M.J., Priddle, J., Cripps, G.C., Ward, P., Brandon, M.A., 2001. South Georgia, Antarctica: a productive, cold water, pelagic ecosystem. Marine Ecology Progress Series 216, 279–308. Atkinson, A., Shreeve, R.S., Hirst, A.G., Rothery, P., Tarling, G.A., Pond, D.W., Murphy, E.J., Watkins, J.L., 2006. Natural growth rates in Antarctic krill (Euphausia superba): II. Predictive models based on food, temperature, body length, sex, and maturity stage. Limnology and Oceanography 51, 973–987. Atkinson, A., Siegel, V., Pakhomov, E.A., Rothery, P., Loeb, V., Ross, R.M., Quetin, L.B., Schmidt, K., Fretwell, P., Murphy, E.J., Tarling, G.A., Fleming, A.H., 2008. Oceanic circumpolar habitats of Antarctic krill. Marine Ecology Progress Series 362, 1–23. Atkinson, A., Schmidt, K., Fielding, S., Kawaguchi, S., Geissler, P.A., 2012. Variable food absorption by Antarctic krill: relationships between diet, egestion rate and the composition and sinking rates of their fecal pellets. Deep-Sea Research II 59–60, 147–158. Bucciarelli, E., Blain, S., Treguer, P., 2001. Iron and manganese in the wake of the Kerguelen Islands (Southern Ocean). Marine Chemistry 73, 21–36. Bowie, A.R., Maldonado, M.T., Frew, R.D., Croot, P.L., Achterberg, E.P., Mantoura, R.F.C., Worsfold, P.J., Law, C.S., Boyd, P.W., 2001. The fate of added iron during a mesoscale fertilisation experiment in the Southern Ocean. Deep-Sea Research II 48, 2703–2743. Brandon, M.A., Naganobu, M., Demer, D.A., Chernyshkov, P., Trathan, P.N., Thorpe, S.E., Kameda, T., Berezhinskiy, O.A., Hawker, E.J., Grant, S., 2004. Physical oceanography in the Scotia Sea during the CCAMLR 2000 survey, austral summer 2000. Deep-Sea Research II 51, 1301–1321. Constable, A.J., Nicol, S., Strutton, P.G., 2003. Southern Ocean productivity in relation to spatial and temporal variation in the physical environment. Journal of Geophysical Research 108 (C4), 8079. doi:10.1029/2001JC001270. Dulaiova, H., Ardelan, M.V., Henederson, P.B., Charettte, M.A., 2009. Shelf-derived iron inputs drive biological productivity in the Southern Drake Passage. Global Biogeochemical Cycles 23, GB4014. doi:10.1029/2008GB003406. Erickson III, D.J., Hernandez, J.L., Ginoux, P., Gregg, W.W., McClain, C., Christian, J., 2003. Atmospheric iron delivery and surface biological activity in the Southern Ocean and Patagonian region. Geophysical Research Letters 30 (12), 1609. doi:10.1029/2003GL017241. Everson, I., 2001. Southern Ocean fisheries. In: Steele, J., Turekian, K., Thorpe, S.A. (Eds.), Encyclopedia of Ocean Sciences. Academic Press, San Diego, California, USA, pp. 2858–2865. Fach, B.A., Hofmann, E.E., Murphy, E.J., 2006. Transport of Antarctic krill (Euphausia superba) across the Scotia Sea. Part II: krill growth and survival. Deep-Sea Research I 53, 1011–1043. Gasso, S., Stein, A., Marino, F., Castellano, E., Udisti, R., Cerrato, J., 2010. A combined observational and modeling approach to study modern dust transport from the Patagonia desert to East Antarctica. Atmospheric Chemistry and Physics 10, 8287–8303. Gilpin, L.C., Priddle, J., Whitehouse, M.J., Savidge, G., Atkinson, A., 2002. Primary production and carbon uptake dynamics in the vicinity of South Georgia—balancing carbon fixation and removal. Marine Ecology Progress Series 242, 51–62. Holeton, C.L., Ne´de´lec, F., Sanders, R., Brown, L., Moore, C.M., Stevens, D.P., Heywood, K.J., Statham, P.J., Lucas, C.H., 2005. Physiological state of phytoplankton communities in the southwest Atlantic sector of the Southern Ocean, as measured by fast repetition rate fluorometry. Polar Biology 29, 44–52. Holm-Hansen, O., Kahru, M., Hewes, C.D., Kawaguchi, S., Kameda, T., Sushin, V.A., Krasovski, I., Priddle, J., Korb, R., Hewitt, R.P., Mitchell, B.G., 2004a. Temporal

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