Hydrographic Control of the Marine Ecosystem in the South Shetland-Elephant Island and Bransﬁeld Strait Region

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Deep-Sea Research II 57 (2010) 519–542

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Deep-Sea Research II

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Hydrographic control of the marine ecosystem in the South Shetland-Elephant Island and Bransﬁeld Strait region

Valerie Loeb a,n, Eileen E. Hofmann b, John M. Klinck b, Osmund Holm-Hansen c a Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss Landing, CA 95039, USA b Old Dominion University, Norfolk, VA 23529, USA c Scripps Institution of Oceanography, La Jolla, CA 92093, USA article info abstract

Article history: The South Shetland-Elephant Island and Bransfield Strait region of the West Antarctic Peninsula is an Accepted 30 October 2009 important spawning and nursery ground of Antarctic krill (Euphausia superba) and is an important Available online 11 November 2009 source of krill to the Southern Ocean. Krill reproductive and recruitment success, hence supply of krill to predator populations locally and in downstream areas, are extremely variable on interannual and Topical issue on "Krill Biology and Ecology." longer time scales. Interannual ecosystem variability in this region has long been recognized and The issue is compiled and guest-edited by the North Pacific Marine Science thought related to El Ninõ Southern Oscillation (ENSO) events, but understanding of how has been Organization (PICES), International Council limited by the hydrographic complexity of the region and lack of appropriate ocean-atmosphere for the Exploration of the Sea (ICES), and interaction models. Global Ocean Ecosystem Dynamics This study utilizes multidisciplinary data sets collected in the region from 1990 to 2004 by the U.S. (GLOBEC) project. Antarctic Living Marine Resources (AMLR) Program. We focus on hydrographic conditions associated with changes in the distribution, abundance and composition of salp- and copepod-dominated Keywords: zooplankton assemblages during 1998 and 1999, years characterized respectively by a strong El Ninõ Southern Ocean event and La Ninã conditions. We provide detailed analyses of hydrographic, biological and ecological Euphausia superba conditions during these dichotomous years in order to identify previously elusive oceanographic Climate regime shifts processes underlying ecosystem variability. We found that fluctuations between salp-dominated Atmospheric-oceanic coupled processes Antarctic Dipole coastal zooplankton assemblages and copepod-dominated oceanic zooplankton assemblages result Antarctic Circumpolar Current from the relative influence of Weddell Sea and oceanic waters and that these fluctuations are associated with latitudinal movement of the Southern Antarctic Circumpolar Current Front (sACCf). Latitudinal movements of the sACCf can be explained by meridional atmosphere teleconnections instigated in the western tropical Pacific Ocean by ENSO variability and are consistent with out-of-phase forcing in the South Pacific and South Atlantic Oceans by the Antarctic Dipole high-latitude climate mode. During El Ninõ decreased northwest winds, equatorward movement of the sACCf and an intensified Weddell Gyre allow Weddell Sea water to flow into eastern Bransfield Strait. During these periods mixing between oceanic and coastal waters is reduced, chlorophyll a concentrations are low, salps numerically dominate the zooplankton, and krill recruitment success is poor. During La Ninã increased and more frequent northwest winds and poleward movement of the sACCf allows increased influence of oceanic waters and mixing of these with cold coastal waters. These periods are characterized by numerical dominance of copepods, elevated concentrations of oceanic zooplankton taxa and phytoplankton blooms that promote krill reproduction and recruitment success. Hydrographic and ecological changes after the 1998 El Ninõ are associated with a shift from frequent El Ninõs to the prevalence of La Ninã and neutral conditions and conform to a decadal-scale climate regime shift in the Antarctic Peninsula region. & 2009 Elsevier Ltd. All rights reserved.

1. Introduction 2004) and therefore plays a vital role in the krill-based food web. In particular the South Shetland-Elephant Island and Bransﬁeld The Southwest Atlantic, including the West Antarctic Peninsu- Strait region (Fig. 2) is an important krill spawning and nursery la (Fig. 1), is an important source of Antarctic krill (Euphausia ground as well as an important area for the commercial krill superba) to the Southern Ocean (Spiridonov, 1996; Atkinson et al., ﬁshery (Siegel, 2005). Krill reproductive success, population size and supply to dependent predator populations here and in downstream areas are highly variable on interannual and longer n Corresponding author. Fax: +831 632 4403. time scales (Priddle et al., 1988; Siegel and Loeb, 1995; Loeb et al., E-mail address: [email protected] (V. Loeb). 1997). Understanding of factors driving krill population variability

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Salpa thompsoni (Siegel and Loeb,1995; Loeb et al., 1997; Atkinson et al., 2004) and therefore influences two important components of the nekton/zooplankton sampled during summer months. Zooplankton in the South Shetland-Elephant Island region includes mixtures of species characteristic of coastal and oceanic environments that show significant seasonal and interannual fluctuations in total and relative abundance of dominant taxa (Siegel and Piatkowski, 1990; Park and Wormuth, 1993; Schnack- Schiel and Mujica, 1994). Notable among these are marked interannual shifts between an abundant copepod-dominated zooplankton assemblage characteristic of warm oceanic water in Drake Passage (the ‘‘West Wind Drift’’) and a less-abundant salp- dominated assemblage characteristic of cold neritic waters (the ‘‘East Wind Drift’’; Jaz˙ dz˙ ewski et al., 1982; Witek et al., 1985; Schnack-Schiel and Mujica, 1994). During surveys associated with the Biological Investigations of Marine Antarctic Systems and Stocks (BIOMASS) Program in the early 1980s, variable representation by the two assemblages was associated with latitudinal shifts in their distributions. These in turn were attributed to interannual variations in atmospheric, climatic and hydrographic conditions (Jaz˙ dz˙ ewski et al., 1982; Witek et al., 1985). As with Fig. 1. Major regions of high krill concentrations (black areas) in the Southern sea-ice extent, ENSO was believed to be a major factor driving Ocean relative to general hydrographic circulation (arrows), the Polar Front (PF), these variations (Witek et al., 1985; Priddle et al., 1988). However, Southern Antarctic Circumpolar Front (sACCf, long dashes) and Boundary (Bndy, short dashes) modified from Spiridonov (1996). establishing the linkage between ENSO and ecosystem variability in the region since that time has been severely limited by (a) the inability to identify specific hydrographic conditions associated with distribution shifts of the oceanic and coastal zooplankton has been limited due to the variable distribution and abundance assemblages and (b) lack of appropriate ocean-atmosphere patterns of relatively long-lived krill across multiple spatial and interaction models that can explain the interrelationships. temporal scales (Siegel, 2005) compounded by environmental The primary objectives of this work are to: complexity of their source regions (Fach et al., 2006) and lack of sufficiently long-term, internally consistent, multidisciplinary identify specific hydrographic conditions associated with data sets. variable representation of oceanic and coastal zooplankton The focus of the current study is the South Shetland-Elephant assemblages in the South Shetland-Elephant Island region ; Island region and adjacent Bransfield Strait and Drake Passage establish how these linked hydrographic-biological conditions (Fig. 1, Fig. 2A,B) that is annually surveyed by the U.S. Antarctic are related to the two opposite extreme ENSO phases, the Marine Living Resources (AMLR) Program. The hydrography and ‘‘warm’’ El Ninõ and ‘‘cool’’ La Ninã; and circulation of this region is complex and variable (Amos, 1984, put these linked hydrographic-biological conditions in the 2001; Priddle et al., 1994). The southern Antarctic Circumpolar context of basin-scale coupled atmosphere-oceanic processes Current front (sACCf) and southern ACC boundary (Bndy) are manifested by ENSO variability extending over decadal time present in southern Drake Passage (Orsi et al., 1995). The western scales. portion of the Weddell Sea gyre influences circulation in the Bransfield Strait and Elephant Island region (Gordon and Nowlin, 1978; Whitworth et al., 1994) and inputs from upstream regions To achieve these objectives we employ the long-term data sets along the western Antarctic Peninsula enter the region through obtained by the US AMLR Program. Gerlache Strait and western Bransfield Strait (Stein, 1986, 1988, The AMLR Program has maintained a field effort in the South 1989; Niiler et al., 1991; Capella et al., 1992; Garcia et al., 1994; Shetland-Elephant Island region since the late 1980s, and since Hofmann et al., 1996). The rugged bathymetry of the region, 1993 has focused on a relatively fixed grid of sampling stations which includes the continental shelf around the islands, deep (Fig. 2B) across which hydrographic, chlorophyll a, krill and basins of Bransfield Strait, and the South Shetland Trench and zooplankton distribution and abundance measurements have 1 Shackleton Fracture Zone ridge in Drake Passage, provides been made. The spatial and temporal resolution and multi- additional hydrographic and circulation variability (Capella et disciplinary nature of the AMLR data sets are unusual in Antarctic al., 1992). Mesoscale fluctuations in flow dynamics and between marine studies. As such, these data sets provide a framework that Weddell Sea and ACC water influence across the region occur on allows investigation of processes that produce interannual time scales ranging from several weeks to years (Makarov et al., changes in zooplankton community structure as well as identi- 1988). fication of longer term trends underlying interannual variations. The South Shetland-Elephant Island region is subject to large To achieve the first objective of this study we use the 1998 and interannual variability in the spatial and temporal extent and 1999 AMLR data sets to describe interannual variability in salp concentration of seasonal sea ice (Stammerjohn and Smith, 1996;

White and Peterson, 1996). Sea-ice variability here is character- 1 US AMLR Program Field Season Reports, published on an annual basis from ized by a four-to-five year cycle in extent and concentration that 1989 through 2002 as SWFSC Administrative Reports (1989-1999) and NOAA has been linked to El Ninõ-Southern Oscillation (ENSO) events Technical Memoranda (2000-2008). See also a series of short papers under the (Peterson and White, 1998; Kwok and Comiso, 2002a; Carleton, general heading of US AMLR Program in the 1991-1997 review issues of the Antarctic Journal of the US published by the National Science Foundation. Copies 2003; Simmonds, 2003; Stammerjohn et al., 2003; Turner, 2004). available from US AMLR Program, 8604 La Jolla Shores Drive, La Jolla, CA 92037, Interannual and longer-term variability in sea ice has significant USA. Also available on line at: http://swfsc.noaa.gov/textblock.aspx?Division= effects on krill reproductive success and on abundance of the salp, AERD&id=3154&ParentMenuId=42. ARTICLE IN PRESS

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Fig. 2. (A) Antarctic Peninsula map showing AMLR study region (solid lines), bathymetry, geographic names and abbreviations. (B) AMLR study region and sampling grid relative to climatological locations (Orsi et al., 1995) of the Southern Antarctic Circumpolar Current Front (sACCf, long dashes) and Southern Antarctic Circumpolar Current Boundary (Bndy, short dashes). Data from stations within the Elephant Island area (box) are used for long-term data analyses. The north-south transect line here is used for vertical temperature sections shown in Fig. 5. The numbered west-east transect lines are used for temperature time series plots relative to reference points (squares) shown in Fig. 11 (0 km). ARTICLE IN PRESS

522 V. Loeb et al. / Deep-Sea Research II 57 (2010) 519–542 and copepod abundance that occur in response to hydrographic due to harsh weather conditions during the February-March 1999 variability. These years, characterized by a strong El Ninõ event survey. (1998) followed by La Ninã conditions (1999), provide clear examples of between-year variability in zooplankton species 2.2. Hydrography assemblages composed of relatively short-lived (o1 year) taxa. We provide detailed analyses of hydrographic, biological and Hydrographic sampling at each station was done with a Sea- ecological conditions during these dichotomous years in order to Bird SBE-9/11 CTD system mounted on a General Oceanics identify previously elusive oceanographic processes underlying 12-bottle Rosette, or a Sea-Bird SBE32 Carousel sampler (Holm- ecosystem variability here. These analyses, not presented in a Hansen et al., 1994, 1997; Amos, 2001). The CTD profiles extended companion paper by Loeb et al. (2009), also serve as a tool kit for from the surface to 750 m or to within 10 m of the bottom at sites other researchers in their attempts to identify specific hydro- where the bottom was shallower than 750 m. Details of the CTD graphic features underlying variability in similarly complex data collection and processing are given in Amos (2001). The CTD regions of the Southern Ocean. measurements were processed using standard procedures and The hydrographic and ecological changes observed in 1998 and algorithms. Vertical profiles of temperature and salinity are 1999 are then put into the context of longer term variability to available for all surveys except for March 1997. demonstrate how these are manifestations of basin-scale atmospheric and oceanic processes. To do this we utilize the long-term 2.3. Chlorophyll a concentration measurements AMLR data sets augmented by observations made during the BIOMASS expeditions (El-Sayed, 1994) in relation to atmospheric and oceanographic indices of environmental variability. We then Water samples were obtained on each vertical profile from address the hypothesis that variation in location of the sACCf in 10-L Niskin bottles mounted on a Rosette. Water samples were Drake Passage underlies ecosystem variability in the region. taken at standard depths of 5, 10, 15, 20, 30, 40, 50, 75, 100, 200 Movements of the sACCf, and coincidental ecological changes, are and 750 m or within 10 m of the bottom at shallow stations. then linked to meridional atmosphere teleconnections instigated Estimates of phytoplankton biomass were obtained by measuring in the western tropical Pacific Ocean by ENSO variability chlorophyll a (Chl-a) concentrations in all water samples collected consistent with out-of-phase forcing in the South Pacific and between the surface and 200 m. Water samples were filtered with South Atlantic Oceans by the Antarctic Dipole high-latitude Whatman GF/F filters, extracted in absolute methanol in the dark climate mode. for four hours and fluorescence measured with a Turner Designs The final section focuses on the impacts of decadal-scale fluorometer. The 0-100 m integrated Chl-a values are used in this environmental fluctuations on ecological structure and produc- study. Detailed descriptions of the chlorophyll sampling and tivity of the Drake Passage region of the Southern Ocean. These analysis techniques are given in Holm-Hansen et al. (1994, 1997, have implications for the advective transport of krill to dependent 2000). predator populations in the South Atlantic sector (Hofmann et al., 1998; Ward et al., 2002; Trathan et al., 2003; Hofmann and 2.4. Zooplankton measurements Murphy, 2004; Murphy et al., 2004a, b; Murphy et al., 2007; Thorpe et al., 2007) as well as krill population fluctuations during Beginning in 1993 zooplankton was sampled with a 1.8 m atmospheric warming over future decades. Isaacs-Kidd Midwater Trawl fitted with a 505-mm mesh plankton net and a calibrated General Oceanics flow meter. All tows were fished obliquely from 170 m or ca. 10 m above bottom in shallow waters, monitored with a real-time depth recorder. Tows 2. Methods and materials were usually at 2 kts., ca. 20 min duration, and filtered ca. 2500-4000 m3. Zooplankton samples were processed within two 2.1. Survey area hours of net retrieval. All postlarval krill and salps were removed and enumerated from samples r2 L; for larger catches, abun- Standardized surveys, initiated around Elephant Island in 1989 dance estimates were based on 1-2 L subsamples. All postlarval by the AMLR Program, were conducted along north-south krill in samples with o100 individuals were measured, sexed and transects with stations spaced ca. 55 km intervals (Fig. 2B). The staged according to Makarov and Denys (1981); for larger samples survey was extended westward in 1993 to include King George at least 100 krill were analyzed. For clarification, ‘‘postlarval’’ krill Island and again in 1997 to include the area around Livingston includes all age/length/maturity classes from one-year old Island. A further extension into the Joinville Island area occurred juvenile and immature stages through mature adults; larvae are in 2002. The AMLR field seasons generally include two month- representatives of the current years’ reproductive effort. Other long surveys during January-February and February-March of taxa were identified to species when possible and enumerated. each year. The original Elephant Island area has been regularly Abundant taxa include large copepods (notably Metridia gerlachei, surveyed to maintain coherency of a long-term data base Calanus propinquus, Calanoides acutus and Rhincalanus gigas), salps extending back to the mid-1970s (Siegel and Loeb, 1995; Loeb (Salpa thompsoni and occasionally Ihlea racovitzai), larval and et al., 1997). Between 40-70 and 19-50 stations were occupied in postlarval stages of Euphausia superba (krill) and other euphau- the Elephant Island and South Shetland-Joinville Island areas, siids (Thysanoessa macrura and E. frigida) and chaetognaths. These respectively, during each survey that took place from 1993-2004. taxa comprise 490% of zooplankton biomass in the Antarctic Ship mechanical problems limited sampling during March 1997 to Peninsula region (Schnack-Schiel and Mujica, 1994). Zooplankton 18 net hauls, and no survey was done in this region during abundance is expressed as numbers 1000 mÀ3 filtered. January 2000. The station distribution in 1998 and 1999 was Prior to 1993, AMLR zooplankton samples were collected using similar, but with more stations occupied in 1998 (98 versus 68 0.60-m diameter bongo nets fitted with 333 and 505 mm meshes. stations total). These differences were largely due to decreased The data sets obtained from these net samples include sampling density in the Elephant Island area in 1999 (5 lines, 8 only abundance of three biomass-dominant copepod species stations per line) compared to 1998 (9 lines, 6-7 stations per line) (Calanoides acutus, Calanus propinquus and Metridia gerlachei), and stations north and south of King George Island abandoned S. thompsoni, larval and postlarval krill, and postlarval T. macrura ARTICLE IN PRESS

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60.0 1998

60.5 >2 T °C 1-2 61.0 0-1 -1-0

° S) < -1 61.5 Latitude ( 62.0

62.5

63.0 64 62 60 58 56 54 52 Longitude (°W)

60.0 1999 60.5

61.0

61.5 Latitude ( ° S) 62.0

62.5

63.0 64 62 60 58 56 54 52 Longitude (°W)

Fig. 4. Temperature distribution on the 27.6 potential density surface for (A) 1998 and (B) 1999. Negative temperatures are shown by dashed lines. Depth contours (light grey lines) are 500 and 2000 m.

2.5. Ancillary data sets

2.5.1. Sea-ice indices Sea-ice indices representing spatial and temporal extent were Fig. 3. Potential temperature-salinity diagrams for (A) 1998 and (B) 1999. Lines of derived for an area measuring 1.25 Â 106 km2 off the north- constant potential density (dotted) and the 27.6 potential density surface (dash- western side of the Antarctic Peninsula using satellite images of dot) are indicated. The freezing point of seawater as a function of salinity is shown sea ice concentrations (passive microwave radiometer data) by the horizontal dashed line. Water mass abbreviations are: UCDW-Upper Circumpolar Deep Water; LCDW-Lower Circumpolar Deep Water; AASW-Antarctic published electronically by the National Sea and Ice Data Center Surface Water; WW-Winter Water; WSW-Weddell Sea Water; BS-Bransfield Strait (http://nsidc.org/data/seaice_index). This index was developed Water. and described by Hewitt (1997) for use in initial analyses of krill recruitment success (Siegel and Loeb, 1995) and has been maintained since for internal consistency. For this study, annual anomalies were obtained by subtracting the long-term and E. frigida. Although limited, these data are adequate to 1978–2003 mean value. These indices are derived from the same demonstrate fluctuations between major zooplankton compo- source as, and are consistent with, other sea ice indices developed nents. for less and more extensive regions off the West Antarctic Analyses utilize only data collected in the Elephant Island area Peninsula (Hewitt, 1997). (Fig. 2). The 1998 and 1999 biological data and associated hydrographic data depicted here (Figs. 3-10) were derived from the mid-summer February-March surveys. However, statistical 2.5.2. ENSO indices analyses utilize Elephant Island grid station data collected during The Southern Oscillation Index (SOI) and Ninõ 3.4 index are all January-March survey efforts each year. measures of large-scale atmospheric and oceanic fluctuations ARTICLE IN PRESS

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BS DP Dynamic Height 0 60.0

1998 60.5 200

61.0 400

61.5

Depth (m) 600 Latitude ( ° S) 62.0

800 62.5 1998 1000 63.0 -200 -150 -100 -50 0 50 100 150 64 62 60 58 56 54 52 Distance (km) Longitude (°W)

BS DP 0 60.0

1999 60.5 200

61.0 400 >2 T°C 1-2 61.5

Depth (m) 600 0-1 Latitude ( ° S) -1-0 62.0 <-0 800 62.5 1999

1000 63.0 -200 -150 -100 -50 0 50 100 150 64 62 60 58 56 54 52 Distance (km) Longitude (°W) Fig. 5. Vertical temperature distributions along the north-south transect line Fig. 6. Dynamic topography at 500 m relative to the surface for (A) 1998 and (B) shown in Fig. 2B for (A) 1998 and (B) 1999. Station locations are indicated by the 1999. Depth contours (light grey lines) are 500 and 2000 m. triangles and the Bransﬁeld Strait and Drake Passage ends of the transect are indicated by BS and DP, respectively. Negative temperatures are indicated by dashed lines.

2.5.3. Historical data sets Chl-a values measured during the First International BIOMASS associated with warm El Ninõ and cold La Ninã episodes. The SOI, Experiment (FIBEX), which took place in 1981, and the Second which is the difference in air pressure anomaly between Tahiti International BIOMASS Experiment (SIBEX), which took place in and Darwin, Australia, is a measure of large-scale fluctuations in 1984 and 1985, were obtained from median integrated 0-50 m air pressure occurring between the western and eastern tropical values in the South Shetland Island area (Priddle et al., 1994). Pacific during ENSO events. The negative phase of the SOI These values, reported to be statistically similar to the means, represents below-average air pressure at Tahiti and above- were doubled to approximate 0-100 m concentrations as pre- average air pressure at Darwin. Prolonged periods of negative scribed by Priddle et al. (1994). SOI values coincide with unusually warm ocean water across the Additional Antarctic krill and salp abundance data from the eastern tropical Pacific typical of El Ninõ episodes. Prolonged Elephant Island area for 1980-1993 were taken from the data sets periods of positive SOI values coincide with unusually cold ocean reported in Siegel and Loeb (1995) and Loeb et al. (1997). Other water across the eastern tropical Pacific typical of La Ninã zooplankton abundance data collected prior to 1993 were episodes. The Ninõ 3.4 index reflects departures of sea-surface provided by John Wormuth (Texas A&M University) and temperatures from the long-term mean value in the eastern Park and Wormuth (1993). Krill recruitment indices (R1) for tropical Pacific between 51N-51S and 1701W-1201W. Time series 1980-2003 were obtained from Siegel et al. (2002) and Siegel of the SOI and Ninõ 3.4 index were obtained from the U.S. (pers. com. 2007, based on AMLR krill length-frequency and National Weather Service Climate Prediction Center and used here abundance data). Recruitment indices provide a measure of to indicate ENSO events for the time covered by the AMLR data success for a given Antarctic krill year class (Siegel et al., 2002). sets. Proportional recruitment (R1 and R2) values are derived from the ARTICLE IN PRESS

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Fig. 7. Integrated 0-100 m chlorophyll a values at stations sampled during February-March surveys during (A) 1998 and (B) 1999. Depth contours (light grey lines) are 1000, 2000 and 3000 m.

ratio of numbers of individuals in age class 1 (one-year-old) and Fig. 14E represent recruitment success associated with larval age class 2 (two-year-old), respectively, to the total number of production (Fig. 14D) each year. krill collected each season. When more than one survey is available for a season, the values represent the inverse variance weighted mean recruitment for that season (Siegel et al., 2002). 2.6. Statistical analyses Primarily R1 indices are utilized here. Because of interannual latitudinal shifts in the distribution patterns of one-year-old krill Relationships between plankton assemblages, environmental these are conservative values that may sometimes underestimate conditions, and ENSO indices were examined by computing cross actual recruitment (Siegel et al., 2002). R1 indices depicted in correlations between the mean summer concentrations of ARTICLE IN PRESS

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Fig. 8. Copepod abundance at stations sampled during February-March surveys during (A) 1998 and (B) 1999. Depth contours (light grey lines) are 1000, 2000 and 3000 m. postlarval krill, copepods, salps (S. thompsoni), larval krill, Chl-a, Between-year differences in zooplankton species abundance sea-ice extent from the previous fall-winter-spring, krill recruit- were determined by Analysis of Variance (ANOVA) of Elephant ment success (R1), and monthly values of the SOI and Ninõ 3.4 Island area data sets with significance Po0.05 based on two- indices. Correlations were computed for zero-lag and a one-year tailed tests. Comparisons between 1998 and 1999 utilized one- lag with results presented in Table 4. Probability levels are given way ANOVA applied to individual station data from both surveys for one-sided tests to demonstrate coherency within the zero- each year. A two-way ANOVA was applied to individual station lagged and one-year lagged relationships, but most of the data from all surveys conducted between 1993-1998 and correlations are significant at Po0.05 for two–sided tests. The 1999-2004 to show longer-term change with respect to zoo- dominant frequencies of individual time series were determined plankton abundance and hydrographic conditions represented at using wavelet analysis (Torrence and Compo, 1998) based on each station. The latter were based on potential temperature- Morlet wavelets (Combes et al., 1990). salinity (y–S) characteristics of five water types regularly present ARTICLE IN PRESS

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Fig. 9. Salpa thompsoni abundance at stations sampled during February-March surveys during (A) 1998 and (B) 1999. Depth contours (light grey lines) are 1000, 2000 and 3000 m. in the study area as described by Amos (2001). These are: (1) these analyses because of limited information on their y-S oceanic water of the ACC, including Antarctic Surface Water characteristics. (AASW) overlying Winter Water (WW) and deeper Circumpolar Deep Water (CDW); (2) transitional ACC-derived Mix 1 water, with modifications indicative of active mixing between CDW and 3. 1998 and 1999 survey results WW; (3) ACC-derived Mix 2 water which lacks distinct CDW but does not include water o0 1C; (4) Bransfield Strait (BS) water 3.1. Hydrography influenced by AASW, modified UCDW and Bransfield Strait deep water; and (5) cold, high-salinity water limited to eastern 3.1.1. Potential temperature-salinity Bransfield Strait (EBS) generally in the vicinity of Clarence Island. The potential temperature-salinity (y-S) characteristics in the Data from shallow water stations are generally excluded from AMLR survey region in 1998 and 1999 derive from a mixture of ARTICLE IN PRESS

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Fig. 10. Ihlea racovitzai abundance at stations sampled during February-March surveys during (A) 1998 and (B) 1999. Depth contours (light grey lines) are 1000, 2000 and 3000 m. oceanic (Drake Passage), continental shelf, Bransfield Strait and Modified CDW occurs between the WW and UCDW and is Weddell Sea waters (Fig. 3A,B). The oceanic waters consist of produced by mixing of these water masses (Whitworth et al., Antarctic Surface Water (AASW), which overlies Winter Water 1998; Hofmann and Klinck, 1998). (WW), with its characteristic temperature minimum, and the In 1998, two distinct bands joined the UCDW temperature deeper water mass, Circumpolar Deep Water (CDW). The CDW is maximum and the WW temperature minimum (Fig. 3A). The composed of two forms. Temperatures associated with salinity upper band is associated with modified CDW that is part of values 434.72 represent Lower Circumpolar Deep Water the oceanic Drake Passage water (Sievers and Nowlin, 1984). The (LCDW), indicated by the salinity maximum; LCDW is not lower band represents a modified form of CDW that overlies the represented in Fig. 3. Above this is the warm (2 1C) temperature continental shelf north of the South Shetland Islands (Hofmann et maximum representing Upper Circumpolar Deep Water (UCDW). al., 1996; Whitworth et al., 1998). This water is colder and more ARTICLE IN PRESS

V. Loeb et al. / Deep-Sea Research II 57 (2010) 519–542 529 saline than the oceanic version. The few y-S values that lie of Bransfield Strait, defined as o0 1C, occurred over the between the two bands represent water that is a transition continental shelves north and south of the South Shetland Islands between the oceanic and continental shelf types. In 1999, the in both years (Fig. 4). However, in 1998 these waters extended transition between oceanic and continental shelf waters, repre- into Drake Passage in the area around Elephant Island. This sented by an intermediate third band, was better defined (Fig. 3B) pattern is suggestive of flow of water from Bransfield Strait into indicating greater cross-shelf mixing. the southern part of Drake Passage, particularly through the The temperature and salinity variability associated with the channels between Elephant and King George and Clarence Islands. AASW in 1998 was less than observed in 1999 (Fig. 3). The WW In contrast, in 1999 northward flow of Bransfield Strait water temperature minimum in 1998 was about À1.1 1C, whereas, that extended only to the northern shelf of the South Shetland Islands in 1999 was about À0.8 1C. These differences indicate that in and southern shelf of Elephant Island. 1999 the surface waters underwent more modification through air-sea exchange and mixing. The warmer WW temperature 3.1.3. Vertical temperature distribution minimum is also suggestive of stronger mixing in 1999 than in The vertical temperature distribution along a North-South 1 1998. The cluster of points at temperatures o0 C and salinities section that extends from Drake Passage into central Bransfield of 34.5 represents Bransfield Strait water (Gordon and Nowlin, Strait (Fig. 2B) differed between 1998 and 1999 (Fig. 5). Surface- 1978). The temperature range reflects the east to west gradient, water minimum temperatures were r0 1C in 1998 and WW was with coldest water found in the eastern Bransfield Strait (Gordon present between 50 and 150 m along the entire section (Fig. 5A). and Nowlin, 1978; Hofmann et al., 1996). In 1998 the water that In 1999 the surface-water minimum temperatures were 40 1C, was cooler and less saline than Bransfield Strait waters (Fig. 3A) is the WW layer was thinner and extended poleward only to King characteristic of Weddell Sea shelf water (Whitworth et al., 1994). George Island (Fig. 5B). UCDW was present along the outer This water was sampled at two stations in southern Bransfield continental shelf in Drake Passage below 200 m in both years. In Strait and one station south of Elephant Island in 1998. Weddell 1998 the 1.8 1C isotherm was below 200 m while in 1999 it was Sea shelf water was less evident in the survey area in 1999. about 50-100 m higher in the water column. The 2.2 1C water observed at 350 m in 1998 is associated with the core of the UCDW layer; this was not present in 1999. 3.1.2. Horizontal temperature distributions The Bndy is defined by thickening of the WW layer poleward of The temperature distribution along the 27.6 potential density the sACCf, shown by deepening of the 0 1C isotherm from about surface (Fig. 4) tracks the core of UCDW (Orsi et al., 1995) and 100 to 300 m in 1998 (Fig. 5A). In this year the Bndy was located intersects the dominant water masses and water types observed over the shelf break edge. In 1999 the Bndy was shifted poleward during the 1998 and 1999 AMLR cruises (Fig. 3). The southern as indicated by the movement of the 0 1C and À0.5 1C isotherms 1 terminus of UCDW characteristics, defined by the 1.8 C isotherm into Bransfield Strait. between 200 and 500 m, provides a water mass marker for the poleward extent of the ACC and corresponds to the sACCf (Orsi 3.1.4. Dynamic topography et al., 1995). The dynamic topography fields for 1998 and 1999 (Fig. 6) show In 1998 the 1.8 1C isotherm was in the northern part of the flow to the north-northeast along the northern and southern study region in an area that corresponds to a poleward deflection flanks of the South Shetland Islands. Flow along the Drake Passage in the climatological location of the sACCf (Fig. 2B) produced by side of the South Shetland Islands is associated with the ACC. Flow the Shackleton Fracture Zone (Orsi et al., 1995). The 1.8 1C on the southern flank is associated with the northern limb of isotherm was absent elsewhere except at the outermost south- generally cyclonic (clockwise) circulation inside Bransfield Strait west station of the study region (Fig. 4A). This temperature (Niiler et al., 1991). In both years anticyclonic flow in Drake distribution suggests that the sACCf was located well offshore of Passage associated with deflection of the ACC by topography of the South Shetland Islands. As a result, oceanic waters (i.e., those the Shackleton Fracture Zone was apparent. In 1998 the antic- with temperatures 41.2 1C) were present only in a limited yclonic circulation was restricted to a narrow region in Drake portion of the study region, adjacent to the Shackleton Fracture Passage. In 1999 the region of anticyclonic flow near the Zone. In contrast, warm oceanic water was present over the entire Shackleton Fracture Zone was more expansive, extending from offshore part of the study region in 1999 (Fig. 4B). The sACCf was north of King George Island to Elephant Island. also present across most of this offshore area, suggesting that the ACC had shifted poleward in this year relative to 1998. The region of transitional waters, indicated in Fig. 4 by 3.2. Chlorophyll a distribution temperatures between 1.0 and 0 1C, was confined to a narrow band along the continental slope region in 1998. Additional The distribution of 0-100 m integrated Chl-a concentrations transitional waters were observed as a closed region downstream was similar in 1998 and 1999 (Fig. 7). Highest concentrations of Elephant Island. In 1999 the area of transitional water was also were generally located over the South Shetland Islands outer shelf along the outer shelf and slope region north of the South Shetland and south of King George and Elephant Islands within Bransfield Islands, but here this band was broader, extended further offshore Strait. Low concentrations prevailed in offshore Drake Passage and covered a more extensive area east of Elephant Island. waters (Fig. 7). However, the 1999 Chl-a concentrations were The Bndy defines the northern limit of water masses found to significantly greater than those in 1998 (ANOVA, Po0.0001) due the south of the ACC (Orsi et al., 1995) and can be identified by the to a massive phytoplankton bloom that extended from south of location of 0 1C isotherm on the 27.6 potential density surface. In King George Island to northeast of Elephant Island. The maximum 1998 the 0 1C isotherm was located along the continental slope value (460 mg mÀ2) seen in Bransfield Strait during February- north of the South Shetland Islands and extended into Drake March 1999 was the greatest observed during all of the AMLR Passage north of Elephant Island (Fig. 4A). In contrast, the 0 1C surveys. isotherm was located further south in 1999, especially in the area The high chlorophyll concentrations in Bransfield Strait during around Elephant Island (Fig. 4B). The latitudinal movement of this 1999 may have resulted from increased mixing, as suggested by isotherm is consistent with the southward displacement of ACC in the temperature-salinity properties that year (Fig. 3). Addition- 1999 compared to 1998. Waters with temperatures characteristic ally, during 1999 an unusual proportion of offshore stations ARTICLE IN PRESS

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Table 1 Abundance of the 10 numerically dominant zooplankton taxa in the Elephant Island area during 1998 and 1999.

Taxon 1998 (N=122) 1999 (N=79) ANOVA

Rank % Mean SD Rank % Mean SD P

Salpa thompsoni 1 69.3 958.5 1533.1 2 12.4 252.6 304.4 o0.0001 Thysanoessa macrura 2 10.0 138.0 196.6 6 3.5 70.7 103.9 o0.01 Euphausia superba 3 6.9 94.8 550.6 8 1.0 20.2 111.3 Copepods 4 5.5 75.8 131.7 1 60.9 1239.1 2032.4 o0.0001 Ihlea racovitzai 5 4.1 56.1 309.1 10 0.3 5.44 17.3 Vibelia antarctica 6 1.0 13.5 17.6 0.2 4.46 4.34 o0.0001 Chaetognaths 7 0.5 6.32 17.3 5 5.2 105.1 221.2 o0.0001 Cyllopus magellanicus 8 0.4 5.40 10.3 0.2 3.38 3.50 Euphausia frigida 9 0.3 4.63 19.0 7 1.0 20.3 37.0 o0.0001 Ostracods 10 0.3 4.31 12.9 9 0.4 8.97 26.4 Euphausia superba (L) 0.1 1.41 13.1 4 6.0 121.8 581.5 0.02 Thysanoessa macrura (L) 0.0 0.23 1.43 3 7.4 150.8 155.1 o0.01 Total Zooplankton 1383.4 1785.5 2034.9 2745.1 0.04

Mean concentrations (No. 1000 mÀ3) and Standard Deviations are based on total number of samples collected (N) each field season. (L) denotes larval stages. Significant between-year abundance differences (bold) are based on one-way ANOVA at the indicated probability level (P). Abundance rank and proportion of total mean abundance (%) represented by each taxon are indicated for the field seasons.

Table 2 Hydrographic afﬁliations of Copepods, Salpa thompsoni and Ihlea racovitzai based on their concentrations (No. 1000 mÀ3) at stations sampled in the Elephant Island area during January-March surveys, 1998 and 1999.

Water Type 1998 1999 Between-year differences Copepods

(N) Mean SD (N) Mean SD

ACC 35 57.3 57.8 23 2520.0 3223.2 o0.0001 Mix 1 35 75.4 108.3 20 995.4 1138.9 o0.01 Mix 2 8 24.3 20.7 5 394.6 270.1 BS 32 123.4 215.0 20 805.6 718.6 o0.05 EBS 9 44.5 58.2 5 132.1 132.7 Within-year differences ACC4All others o0.0001 Salpa thompsoni ACC 35 536.7 569.3 23 222.2 337.1 Mix 1 35 920.0 989.2 20 350.0 365.5 Mix 2 8 236.5 343.0 5 221.1 99.5 BS 32 1525.3 2497.7 20 243.1 276.8 o0.001 EBS 9 1644.0 1540.4 5 81.8 42.1 Within-year differences BS4ACC, Mix 1& 2 r0.04 Ihlea racovitzai ACC 35 0.75 2.89 23 0.00 0.00 Mix 1 35 14.2 40.2 20 0.72 2.70 Mix 2 8 16.3 33.2 5 0.00 0.00 BS 32 49.1 118.4 20 18.9 30.8 EBS 9 513.1 1060.0 5 7.41 6.41 o0.001 Within-year differences EBS4All others o0.0001

Hydrographic conditions represented at each station conform to potential temperature-salinity characteristics for five water types described by Amos (2001). Probabilities resulting from two-way ANOVA and Post Hoc tests (bold) reflect significant abundance differences of each taxon represented in the five water types within and between the two years.

evidenced shallow (20-30 m) as well as deep (80 m) chlorophyll Bransfield Strait. In 1999 the regions of maximum concentration maxima, the former attributed to enhanced mixing of Drake were expanded (Fig. 8B) and copepod abundance was in- Passage surface water with contiguous nutrient (i.e., iron) creased by an order of magnitude and significantly greater enriched continental shelf waters (AMLR, 1999; Holm-Hansen (Po0.0001; Table 1). Copepod abundance increases in 1999 et al., 2005). were most dramatic in oceanic ACC and ACC-derived Mix 1 water (Table 2). 3.3. Copepod, salp and other zooplankton distribution patterns and Salpa thompsoni distribution in 1998 showed elevated con- abundance centrations in the Elephant Island area, particularly in the eastern portion, and adjacent to the Shackleton Fracture Zone (Fig. 9A). Copepod distribution in 1998 (Fig. 8A) showed maxima Greatest concentrations here were in EBS and BS water suggesting scattered along the northern flank of the South Shetland Islands, the importance of the Weddell Sea as a source area. In 1999 between King George and Elephant Islands and within S. thompsoni was more evenly distributed across the region ARTICLE IN PRESS

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(Fig. 8B) and, while greatest concentrations again were within the Elephant Island area, overall abundance here was reduced to a LaNiña ElNiño third of that observed in 1998 (Po0.0001; Table 1) and not 2004 2004 associated with specific water characteristics (Table 2). 1.8 1.8 2 1.8 2002 The second salp species, Ihlea racovitzai, was an order of 2002 2 magnitude more abundant (Table 1) and its distribution more 1.8 2000 widespread in 1998 than in 1999 (Fig. 10A). This species, which 2000 2 occasionally occurs in Bransfield Strait (Nishikawa et al., 1995), and is typically uncommon in the AMLR survey area, is a marker 1998 2 1998 1.8 for cold, low salinity waters that come from high latitudes 1.8 1996 1996 primarily to the east of the Antarctic Peninsula (Foxton, 1971). Time (yr) 2 The largest concentrations of I. racovitzai in 1998 were clearly 1.8 1.8 1994 associated with EBS water (Po0.001; Table 2). 1994 Zooplankton assemblages sampled during 1998 and 1999 1.8 1992 differed greatly in absolute and relative abundance of dominant 1992 1.8 taxa (Table 1). Zooplankton abundance in 1998 was half of that, 1.8 1990 1990 and significantly lower than, in 1999 (Po0.05; Table 1). During 1998, S. thompsoni was the numerical dominant and postlarval stages of the euphausiids Thysanoessa macrura and krill, and 2004 2004 2 I. racovitzai were relatively abundant. Together these four categories represented 90% of the total mean zooplankton 2002 2 1.8 2002 abundance while copepods contributed another 5.5%. During 1999, copepods numerically dominated, chaetognaths and the 2000 2000 larval stages of T. macrura and krill were relatively abundant. Together these four categories represented 80% of the total mean 1998 1.8 1.8 1998 zooplankton abundance while S. thompsoni and postlarval T. macrura and krill contributed another 17%. The stark difference 1996 2 1996 Time (yr) between the zooplankton assemblages sampled each year is indicated by a low Percent Similarity Index value of 24.3. In terms 1994 1994 of overall abundance, species abundance relationships and hydrographic affiliations (Tables 1,2), the 1998 assemblage conforms to 1992 1.8 1992 that of the ‘‘East Wind Drift’’ (Antarctic coastal waters, the seasonal 0 ice zone; Hempel, 1985) while the 1999 assemblage conforms to 1990 1990 that of the ‘‘West Wind Drift’’ (ice free Antarctic oceanic waters) described by Mackintosh (1934), Jaz˙ dz˙ ewski et al. (1982), Siegel and 2004 2004 Piatkowski (1990) and Schnack-Schiel and Mujica (1994). 0 2002 2002 1.8 0 4. Long-term time series 2000 2000 0 4.1. Coupled atmospheric-oceanic processes and ecosystem 0 1998 1998 variability 1996 1996 4.1.1. Latitudinal movements of the sACCf and Bndy Time (yr) The hydrographic variability observed between 1998 and 1999 1994 1994 is in part associated with changes in location of the sACCf and 0 Bndy. Variability in frontal location was obtained from the 1992 1992 location of isotherms at 350 m along three west-east transects relative to reference points (07 km; Fig. 11) centered in the 1990 1990 Elephant Island area (lines 3, 4 and 7; Fig. 2B) for the period -150 -100 -50 0 50 100 1990-2004. These three lines were sampled each cruise and Distance (km) include the climatological location of the sACCf as well as Weddell Sea shelf water influence (Orsi et al., 1995). Here temperatures of <-0.5 -0.5-0 0-0.5 0.5-1 1-1.5 1.5-2 >2 1 1 1 2 C correspond to oceanic UCDW, 1.8 C to the sACCf and 0 Cto Fig. 11. Temperature time series constructed relative to the reference sites (black the Bndy. boxes) on three west-east transect lines shown in Fig. 2B from temperature Absence of the 2 1C isotherm along lines 3 and 4 during measurements at 350 m made from 1990 to 2004. (A) Line 3, (B) Line 4 and (C) 1990-1994 was coincident with westward displacement of the 1.8 Line 7. The bold 1.8 1C isotherm highlights movements of the sACCf across the transect lines. The 2 1C isotherm represents UCDW while the 0 1C isotherm and 0 1C isotherms along lines 4 and 7, indicating that the sACCf represents the Bndy. Bars on the Y-axis indicate the numbers of temperature and Bndy were located in the northwestern part of the AMLR measurements (i.e., surveys) used to construct each time series. White areas study region. In 1996 appearance of the 2 1C isotherm and indicate times when no measurements were made along the individual transects. eastward shifts of the 1.8 and 0 1C isotherms, indicate eastward Arrows are at midpoints of La Ninã and El Ninõ events. Eastward extension of movement of the sACCf and Bndy. The 60 km displacement of the warmer temperatures toward and beyond the reference point (0 and + km) on each line occurs when the sACCf and Bndy move into the Elephant Island area. 1 1.8 C isotherm between 1992 and 1995 is within observed These coincide with La Ninã events. Westward extension of colder temperatures variability of the sACCf location (Sprintall, 2003). In 1998 toward and beyond the reference point (0 and À km) on each line occurs when the westward movement of the 2.0, 1.8 and 0 1C isotherms were sACCf and Bndy retract and coastal waters prevail across the area. These coincide associated with an extension of colder water into the western part with El Ninõ events. ARTICLE IN PRESS

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4.1.2. ENSO-related coupled atmospheric-oceanic processes Movements of the sACCf and Bndy link ecological changes in the Antarctic Peninsula region to underlying coupled atmospheric-oceanic processes. The SOI and Nino 3.4 indices (Fig. 14A) show that between 1990 and 2004 El Ninõ conditions predominated during four periods (April 1991-August 1992, June 1994-April 1995, April 1997-May 1998 and April 2002-April 2003) and La Ninã conditions predominated during two periods (August 1995-April 1996 and June 1998-March 2001). Relatively stable Ninõ neutral conditions prevailed between the El Ninõ and La Ninã periods. During periods when La Ninã conditions prevail, the 2.0 1C isotherm, and hence the sACCf, tends to be present at, or east of, the reference site used to construct the isotherm movement patterns (e.g., Line 3; Fig. 11A). In contrast, the 0 1C isotherm, tends to be present at, or west of, the Line 7 reference site during periods when El Ninõ conditions prevail (Fig. 11C). A significant decrease in se- ice extent along the west Antarctic Peninsula has been attributed to pronounced climate warming in this portion of the Southern Ocean and Antarctic continent since the 1970s (Parkinson, 2002). This decrease was extreme between 1985 and 1990 (Jacobs and Comiso, 1993; Fig. 14B). Super- imposed on this long-term trend are interannual fluctuations in sea-ice extent that are related to the ENSO cycle (White and Peterson, 1996; Kwok and Comiso, 2002a). Sea-ice extent tends to decrease prior to the onset of El Ninõ events and increase during La Ninã events (Fig. 14B; Yuan, 2004). The extended La Ninã period in the late 1990s and early 2000s produced relatively stable sea-ice conditions (Fig. 14B). Mean Chl-a concentrations within the Elephant Island area and other portions of the AMLR survey region peaked during 1994-1996, decreased to lows in 1997-1998, and increased again in 1999-2000 and 2002 (Fig. 14C). These peak and low values correspond, respectively, to La Ninã and El Ninõ periods (Fig. 14A). Copepod and S. thompsoni abundance (Fig. 12A, 14B,D) showed an inverse relationship until the late 1990s with marked Fig. 12. Seasonal, interannual abundance and longer term fluctuations of fluctuations between years of salp or copepod dominance. The (A) copepods and Salpa thompsoni and (B) chaetognaths and Ihlea racovitzai latter portion of the time series shows elevated copepod relative to El Ninõ events (vertical bars) and intervening La Ninã and neutral abundance and dominance with positively correlated trends of periods. Copepods and chaetognaths are most abundant in oceanic water, copepod and S. thompsoni abundance. The timing of this change I. racovitzai is a marker for Weddell Sea water. Dramatic abundance and dominance changes within some summer seasons (e.g., 1994, 1997, and 2004) coincided with reduced presence of 0 1C water in the southeastern reflect hydrographic rather than biological processes. Horizontal lines are mean part of the region after 1998 and suggests the reduced importance concentrations of copepods, S. thompsoni and chaetognaths from all surveys of Weddell Sea water as a source of S. thompsoni. conducted in the Elephant Island area during 1993-1998 and 1999-2004 periods. Abundance of Ihlea racovitzai, a marker for Weddell Sea water in the study region, was highest when the species was first identified in the AMLR study region during 1998; its abundance of the region. From 1999 to 2004 the isotherm pattern was declined greatly during subsequent years characterized by La relatively stable with reduced presence of 0 1C water in the Ninã conditions and then increased again (as did S. thompsoni) eastern part of the region. after the 2002-2003 El Ninõ(Fig. 12). These fluctuations support These movements of the sACCf and Bndy can explain abrupt variable Weddell Sea water influence driven by ENSO with within- season transitions between copepod and salp dominance, enhanced westward transport into the study area during El Ninõ. and zooplankton-rich and -poor assemblages (e.g., 1994, 1997 and Krill abundance, larval production and recruitment success 2004; Fig. 12). Movements of the sACCf and Bndy can also explain (Fig. 14D,E) also showed variability associated with El Ninõ and La longer term changes in copepod and salp dominance here Ninã events. Larval krill abundance peaked during transitions to La (Fig. 12A). South and eastward movement of the sACCf Ninã events and decreased during transitions to El Ninõs. Increased (Fig. 13A) brings into the region an abundant and species-rich krill recruitment success and subsequent population growth were zooplankton assemblage dominated by copepods and chaeto- associated with La Ninã and Ninõ neutral periods while poor krill gnaths with elevated numbers of indicator species (e.g., copepods recruitment success and subsequent population declines followed Rhincalanus gigas and Calanoides acutus) characteristic of the the onset of El Ninõ periods. Three back-to-back years of good krill oceanic ‘‘West Wind Drift’’ (Mackintosh, 1934; Jaz˙ dz˙ ewski et al., recruitment success in 1978-1982 and 1998-2002 were associated 1982; Siegel and Piatkowski, 1990; Schnack-Schiel and Mujica, with extended Ninõ neutral and La Ninã periods. 1994). In contrast, westward displacement of the sACCf (Fig. 13B) allows water from Bransfield Strait and higher latitudes to expand across the region, bringing with it the comparatively depauperate 4.2. Correlation analyses of time series zooplankton assemblage (notably postlarval krill, Thysanoessa macrura and copepod Metridia gerlachei) characteristic of the Cross-correlations were calculated between the mean summer coastal ‘‘East Wind Drift’’ (i.e., seasonal sea ice zone). concentrations of postlarval krill, copepods, S. thompsoni, larval ARTICLE IN PRESS

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Fig. 13. Conceptual model of how latitudinal movements of the sACCf associated with ENSO may explain changes in representation of (A,B) oceanic and coastal zooplankton assemblages and (C,D) Chl-a (primary productivity) in the South Shetland-Elephant Island region. Dashed lines indicate the poleward and equatorward displacements of the sACCf off the Antarctic Peninsula based on Sprintall (2003). (A) Poleward movement of the sACCf allows oceanic zooplankton species assemblage to approach the island shelf region; shoaling of UCDW may facilitate increased concentrations of some species in the upper water column. (B) Equatorward movement of the sACCf , in conjunction with an energized Weddell gyre, allows coastal species assemblages from Bransfield Strait and higher latitudes to expand across the region. (C) Strong northwest winds associated with poleward movement of the sACCf enhance mixing (narrow arrows) between oceanic and coastal waters. Elevated Chl-a concentrations (cross hatching) and primary productivity result from nutrient (N,P) and iron enrichment via upwelling and mixing and favorable water column stratification. (D) Weak infrequent northwest winds (dashed arrow) associated with equatorward movement of the sACCf does not promote mixing between coastal and oceanic waters. Primary production is limited due to reduced iron enrichment of surface waters and unfavorable water column stratification.

krill, Chl-a, sea-ice extent from the previous fall-winter-spring, abundance is positively correlated with sea ice extent. Krill krill recruitment success (R1), and monthly values of the SOI and abundance is positively correlated with recruitment success. Ninõ 3.4 indices. Sea-ice extent the previous year is known to Abundance of S. thompsoni is negatively correlated with sea-ice affect spawning success and recruitment of Antarctic krill as well extent. Sea-ice extent is negatively correlated with SOI and abundance of S. thompsoni (Siegel and Loeb, 1995; Loeb et al., positively correlated with Ninõ 3.4. 1997; Fraser and Hofmann, 2003). Significant one-year lag correlations were found with the The zero-lag correlation results (Table 3A,B) showed signi- environmental and biological factors that affect krill recruitment. ficant correlations among the biological variables and between Good krill recruitment success follows summers with elevated the biological variables and SOI. Copepod and larval krill concentrations of Chl-a, copepods and krill larvae. Krill abundance abundance are positively correlated with Chl-a concentrations is negatively correlated with SOI a year before, suggesting a and with each other. Copepod abundance and Chl-a concen- population response to sea ice extent two winters ago. Wavelet trations are positively correlated with SOI and larval krill analysis of the individual time series showed significant peaks at ARTICLE IN PRESS

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3 3 2 2 1 1 0 0 Niño 3.4 °C -1 S O I -1 -2 -2 Standardized (annual) -3 -3 7 Sea Ice Extent Salpa thompsoni 4 -3 6 3 5 per mo. 2 2 4 Km Abundance 6 3 1 10

2 0 Log Mean No. 1000 m 140 Chl-a Concentrations EI 120 WBS NKG -2 100 80 60

Mean mg m 40 20 0

-3 4

Abundance 1 Copepods Krill Larvae

Log Mean No. 1000 m 0 4 -3 Postlarvae Krill Recruitment 0.8 3 0.6

2 RI 0.4 Abundance 1 0.2 Log Mean No. 1000 m 0 0 78 80 82 84 86 88 90 92 94 96 98 00 02 04 Survey Year / Year Class

Fig. 14. Time series in support of, or constructed from, observations made in the Elephant Island area, 1979-2004: (A) SOI and Nino 3.4 index, ; (B) sea ice extent and Salpa thompsoni abundance; (C) integrated 0-100 m Chl-a concentrations (including West Bransﬁeld Strait, WBS, and North King George Island, NKG, areas); (D), copepod and larval krill abundance; (E) postlarval krill abundance and recruitment (R1) of the previous year class. Shaded bars indicate El Nin˜o events.

frequencies of 10 months and three to five years, which and altered abundance relationships of copepods and S. thompso- correspond to seasonal and ENSO variability, respectively. ni, occurred in the late 1990s (Fig. 12). Examination of zooplankton concentrations represented in the Elephant Island 4.3. Longer-term considerations area during 1993-1998 and 1999-2004 shows significant differences between the two periods (Table 4) with an abundant In addition to interannual variability associated with ENSO assemblage dominated by copepods and chaetognaths replacing a fluctuations, the long-term AMLR data sets suggest ecosystem less abundant one characterized by elevated concentrations of change on a longer time scale. The temperature time series salps. These changes were directly linked to the altered (Fig. 11) indicates persistent eastward displacements of the sACCf hydrographic conditions as indicated by significant abundance and Bndy across the Elephant Island area starting in the mid- increases of taxa representative of the ‘‘West Wind Drift’’ in 1990s. Increased concentrations of copepods and chaetognaths, ACC and ACC-derived waters after 1998 (Fig. 16). Furthermore, ARTICLE IN PRESS

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Table 3 (A) Cross-correlations coefﬁcients (r2) between indicated time series, 1980-2004. (B) Summary of signiﬁcant correlations between the time series (probability levels for one-sided tests).

Zero-Lag

Krill Klarvae R1 Chl-a Copepod Salpa Sea Ice SOI Niño 3.4 Krill -0.047 0.648 -0.173 -0.141 -0.182 0.278 0.037 0.177 (22) (22) (28) (27) (31) (22) (34) (34) Klarvae -0.019 .410 0.397 0.732 -0.114 0.850 0.030 -0.057 (19) (13) (19) (22) (22) (13) (22) (22) R1 0.063 0.913 -0.016 0.369 -0.333 0.342 0.225 0.043 (20) ( 11) (18) (17) (21) (23) (23) (23) Chl-a -0.053 0.136 0.729 0.494 -0.240 0.103 0.404 -0.227

-Lag (25) (15) (17) (23) (30) r (26) (18) (30) Copepod 0.027 0.059 0.583 -0.098 0.087 0.328 0.351 -0.206 (24) (18) (15) (20) (27) (17) (27) (27) Salpa -0.003 0.046 -0.395 0.229 -0.054 -0.526 -0.206 0.133 One-Yea (29) (18) (18) (22) (23) (21) (32) (32) Sea Ice 0.084 0.221 0.300 0.519 0.205 -0.124 -0.438 0.615 (20) ( 11) (20) (17) (15) (19) (24) (24) SOI -0.517 0.290 -0.401 0.017 0.092 0.043 0.083 -0.791 (32) (20) (22) (28) (25) (30) (23) (50) Niño 3.4 0.351 -0.045 0.442 0.045 0.194 0.122 -0.054 0.193 (32) (20) (22) (28) (25) (30) (23) (48)

(N) is number of common data points in the two time series. Klarvae are krill larvae, representative of reproductive effort each year; R1 is proportional recruitment of each year class (proportions of one-year-old to total krill measured the following year). Zero-lag cross-correlations are above the diagonal; one-year-lag correlations are in italics below the diagonal. Signiﬁcant correlations are indicated by bold type.

1999-2002 marked the first time that three back-to-back years west Antarctic Peninsula (Pre´ zelin et al., 2000, 2004) and in of good krill recruitment success occurred since the early 1980s oceanic environments (Smith et al., 1992; Tynan, 1998). (Fig. 14). The sACCf can impinge on the outer continental shelf of the South Shetland Islands (Sprintall, 2003) and flow variability associated with this feature may result in circulation conditions that allow iron fertilization of coastal waters and, that in turn, 5. Discussion promotes and sustains higher primary production (Pollard et al., 2002). CDW is present north of the South Shetland Islands and 5.1. Hydrography modified CDW is found on the continental shelf of this region (Fig. 4). Nutrients associated with this water mass may support It has long been recognized that the water mass structure of large episodic phytoplankton blooms here, especially in years the South Shetland-Elephant Island region is complex (Stein, when mixing processes are strong, as happened in 1999 (Fig. 3B). 1983, 1986; Amos 1984, 2001; Niiler et al., 1991; Whitworth Evidence that CDW intrusions onto the continental shelf of the et al., 1994; Hofmann et al., 1996; Gordon et al., 2000). This South Shetland Islands do produce diatom-dominated phyto- complexity derives from the intermingling of ACC waters from the plankton assemblages is given by Kang and Lee (1995). Drake Passage, Bransfield Strait, Weddell Sea, Scotia Sea and West Characteristics of AASW are directly influenced by surface Antarctic Peninsula continental shelf. The AMLR study region forcing and as such provide an indication of interannual spans most of these input regions and this is reflected in the variability in atmospheric processes. In 1999, the temperature- complexity of its thermohaline properties (Fig. 3). salinity range associated with AASW was larger than in 1998 The primary water mass in the Drake Passage portion of the (Figs. 3A,B), which suggests greater modification in 1999. This was study region is CDW, which is the most voluminous water mass in fact a year characterized by frequent storms and periods of carried by the ACC (Sievers and Nowlin, 1984). This water mass is sustained high northwest winds (AMLR, 1999) that may promote formed in the North Atlantic and is a major component of large- upward mixing of CDW and its associated nutrients, including scale oceanic thermohaline circulation. In Drake Passage, CDW coastally supplied iron, that promote elevated phytoplankton shoals to within 150-300 m of the surface (Sievers and Nowlin, biomass in surface waters (Holm-Hansen et al., 2005). 1984; Orsi et al., 1995). CDW and its two varieties, UCDW and The WW is formed by atmospheric forcing that drives deep LCDW, are characterized by high nutrients (Sievers and Nowlin, winter mixing (Toole, 1981). The volume formed each winter is 1984; De Baar et al., 1995; Pollard et al., 2002). The presence of relatively stable because the extent of deep mixing is controlled CDW has been linked to enhanced biological production along the by the location of the permanent pycnocline. However, erosion of ARTICLE IN PRESS

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Table 4 Mean concentrations and Standard Error of numerically dominant zooplankton taxa collected in the Elephant Island area during 1993-1998 and 1999-2004 time periods.

Taxa 1993-1998 1999-2004 ANOVA probabilities

(N) Mean SE (N) Mean SE Regime Water Regimenwater

Copepods 716 1082.4 200.3 512 2986.0 236.8 o0.0001 o0.0001 Euphausia superba (L) 522 655.9 243.9 512 300.7 246.3 Salpa thompsoni 716 586.1 44.7 512 261.3 52.8 o0.0001 o0.0001 o0.0001 Thysanoessa macrura (L) 522 176.5 41.0 512 315.6 41.4 0.04 o0.0001 Thysanoessa macrura 716 97.3 34.9 512 135.9 41.3 Ihlea racovitzai 119 57.5 11.4 512 2.91 5.48 o0.0001 o0.0001 o0.0001 Chaetognaths 716 52.7 13.3 512 189.1 15.8 o0.0001 o0.001 0.01 Euphausia superba 716 50.8 12.4 512 41.5 14.7 Euphausia frigida 716 9.76 1.54 512 23.0 1.82 o0.0001 o0.0001 o0.01 Vibilia antarctica 716 4.87 0.77 512 7.66 0.91 o0.001 Limacina helicina 650 4.35 13.5 512 30.2 15.2 Themisto gaudichaudii 716 3.71 0.32 512 4.33 0.38 0.03 o0.0001 o0.001 Cyllopus magellanicus 716 3.17 0.25 512 2.18 0.30 o0.001 Cyllopus lucasii 716 1.25 0.28 512 4.38 0.34 o0.0001 o0.0001 o0.0001 Primno macropa 716 1.10 0.65 512 5.21 0.77 o0.01

Total Zooplankton 716 2532.3 388.5 512 5106.5 459.5 o0.01 o0.01

(L) denotes larval stages. Result from two-way ANOVA of the concentrations of each taxon at (N) stations sampled each time period (‘‘Regime’’) and for water types represented at each station (‘‘Water’’) are presented as probabilities associated with significant differences (bold) between Regime, Water and their combined effect. The five water types encountered in the study area are described by Amos (2001). Data from shallow stations with limited information on water characteristics are not included. Significant abundance changes in water types are depicted in Fig. 16.

WW during the subsequent austral summer provides insight into 2003). The Drake Passage region of the Southern Ocean provides a mixing intensity. In 1999 the temperature minimum associated choke point for the ACC (Fig. 1) and is shallow relative to the rest with WW was more eroded than in 1998 (Fig. 3A,B), again of the Southern Ocean. As a result, ACC frontal locations are suggesting stronger mixing in 1999. strongly constrained and the shallower depth together with The AMLR study region includes the northwestern edge of the rugged bottom topography provide triggers for mesoscale Weddell Sea (Figs. 1, 2A). Waters formed in the Weddell Sea flow variability. These conditions allow for independent mesoscale into southern Bransfield Strait (Whitworth et al., 1994) and into variability of the three ACC fronts (Sprintall, 2003). In addition, the area around Elephant Island. Weddell Sea waters are colder the ACC fronts in Drake Passage show synchronous shifting and more saline than those originating in Drake Passage and were (Hofmann and Whitworth, 1985), the reasons for which are observed in eastern Bransfield Strait during the 1998 AMLR unclear but may be linked to changes in transport (Sprintall, survey (Fig. 3A). Bransfield Strait is a meeting place for ACC- and 2003). Weddell Sea-derived waters. ACC-derived waters enter Bransfield In Drake Passage the sACCf and Bndy are located adjacent to Strait from the west through troughs that separate the South one another and are found along the continental slope region of Shetland Islands (Clowes, 1934; Capella et al., 1992). These waters the Antarctic Peninsula (Fig. 1; Orsi et al., 1995). Equatorward primarily influence the northern part of Bransfield Strait where displacement of the sACCf in Drake Passage, relative to its they impinge on the southern island shelves. The gap between climatological location, is about 0.5 degrees of latitude (Sprintall, King George Island and Elephant Island provides a major outlet for 2003 ). Poleward displacement of the sACCf is limited by the Bransfield Strait waters into Drake Passage as well as an inlet for Antarctic Peninsula continental shelf, but can be as much as Drake Passage waters into central Bransfield Strait. The southern 10 km (0.1 degree of latitude). In Drake Passage the Bndy is and eastern portions of Bransfield Strait are influenced by inputs present as a distinct feature, but at times it is overlain by the from the Weddell Sea (Whitworth et al., 1994). Inputs to the sACCf (Orsi et al., 1995; Sprintall, 2003). western portion of Bransfield Strait from the West Antarctic The variability in location of the sACCf between the 1998 and Peninsula continental shelf are mostly confined to the upper 1999 AMLR surveys is within the observed range of 0.6 degrees of water column because of the presence of a shallow sill (Stein, latitude (Figs. 4,11). The broad ACC influence over the island slope 1989). However, some connections, such as Gerlache Strait, allow region in 1999 was likely associated with poleward movement of deeper exchanges. Hence, Bransfield Strait provides a hetero- the standing meander in the sACCf front formed by flow geneous habitat, with the characteristics of a particular site being interactions with the Shackleton Fracture Zone ridge. In 1998, dependent on a combination of local and remote inputs. the sACCf was north of the AMLR study region and influence of the meander, as indicated by the 1.8 1C isotherm, was spatially limited to the Shackleton Fracture Zone axis (Fig. 4). Poleward 5.2. Frontal variability and its implications movement of the sACCf brings ACC-derived water and its associated oceanic (‘‘West Wind Drift’’) zooplankton species Variability in location and transport of ACC fronts has been assemblage into the AMLR study region (Fig. 13A). Increased described from hydrographic and moored instrument measure- concentrations of these species in the upper water column (Park ments (e.g., Nowlin et al., 1977; Whitworth, 1983; Whitworth and and Wormuth, 1993) may also be facilitated by shoaling of UCDW Peterson, 1985; Hofmann and Whitworth, 1985; Sprintall, 2003) at the sACCf. Enhanced Chl-a concentrations and primary and satellite observations (e.g., Gille, 1994; Moore et al., 1999). productivity during this time could result from nutrients supplied These studies have focused mainly on the Subantarctic and Polar to surface waters by the sACCf (Tynan, 1998), iron fertilization Fronts, but variability in the sACCf and Bndy has also been resulting from proximity of the sACCf to island and continental reported (Nowlin and Clifford, 1982; Orsi et al., 1995; Sprintall, shelves (i.e., terrestrial sources of iron; De Baar and De Jong, 2001; ARTICLE IN PRESS

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Pollard et al., 2002), shoaling and/or upwelling of UCDW and in Bransfield Strait and decreased ACC influence during warm increased mixing between oceanic and coastal waters (Holm- ENSO events. During La Ninã the South Pacific PFJ is intensified Hansen et al., 2004; Hewes et al. 2008), and water column and storm tracks move poleward whereas the strength of the stratification that promotes phytoplankton blooms in coastal Weddell Gyre is weakened due to equatorward movement and waters (Mitchell and Holm-Hansen, 1991; Fig. 13C). Good krill increased strength of the STJ. Increased eastward flow and greater reproduction and subsequent recruitment success result from storm activity near the Antarctic Peninsula during this time would favorable feeding conditions associated with elevated phyto- explain enhanced ACC influence and mixing with coastal waters. plankton biomass (Chl-a) during spring and summer (Siegel and Conceivably, latitudinal shifts in location of the sACCf and Bndy, Loeb, 1995). Conversely, an equatorward migration of the sACCf and movements in the variable boundary between the ‘‘West and Bndy allows ‘‘East Wind Drift’’ zooplankton assemblages from Wind Drift’’ and ‘‘East Wind Drift’’ zooplankton assemblages, are Bransfield Strait and higher latitudes to expand across the region driven by these ENSO related variations in the jet streams and (Fig. 13B). Low Chl-a concentrations and primary production then storm track activity. Similarly, latitudinal shifts in the sACCf and would result from reduced mixing between oceanic and coastal Bndy and variations in storm track activity can explain inter- waters, limited iron enrichment within the upper water column annual variations in primary production through their impacts on and unfavorable water column stratification (Holm-Hansen et al., shoaling and upwelling of UCDW, mixing processes and water 2004, 2005; Fig. 13D). These conditions do not favor krill column stratification during summer months (Holm-Hansen reproductive success. Thus, fluctuations in the location of the et al., 2005). sACCf appear to drive large-scale changes in the local food web The AMLR data set also indicates changes in sea-ice extent, and biological production. krill recruitment success and salp abundance that began in the Fluctuations in the location of ACC fronts in Drake Passage are mid to late 1990s (Figs. 12, 14). The 1983-1999 period was dominated by year-to-year variations (Sprintall, 2003). The time characterized by good krill recruitment success one in every three series of isotherm location within the AMLR study region (Fig. 11) to six years with population growth resulting from the successful suggests that the sACCf location varies at interannual and longer 1988/89, 1991/92 and 1995/96 year classes. After this population time scales. The year-to-year consistency in isotherm patterns growth resulted from strong recruitment of three year classes suggests that they are reflecting larger-scale changes and are not during the 1999-2002 La Ninã period A subsequent three-year the result of aliasing due to limited observations. The year-to-year period of good recruitment success also occurred during 2005- consistency in the zooplankton species assemblages and their 2008 (AMLR, 2008). Three years of back-to-back recruit- correspondence to changes in the sACCf location provide addi- ment success have not been observed here since the early 1980s tional support that frontal location fluctuations reflect large-scale (Fig. 14E). changes. The precipitous decline in krill populations in the early part of the data set was linked to the rapid decrease in sea ice extent west of the Antarctic Peninsula during the late 1980 s (Jacobs and 5.3. Large-scale climatology Comiso, 1993; Kwok and Comiso, 2002a) establishing sea ice extent as the major factor driving krill population size from 1978 The climate system in the eastern Pacific and western Atlantic to 1995 (Siegel and Loeb, 1995; Loeb et al., 1997). However, sectors of the Southern Ocean is influenced by meridional during the subsequent period of relatively stable sea ice atmosphere teleconnections instigated in the western tropical conditions (Cavalieri and Parkinson, 2008), krill recruitment Pacific Ocean by ENSO variability (Karoly, 1989; Cai and Baines, success and population size have been more directly related to 2001; White et al., 2002; Carleton, 2003). This external forcing subtler processes associated with ENSO (Table 3). These changes drives variations of sea-level pressure—the Pacific South America coincide with a shift from the 1980 to 1998 period dominated by (PSA) pattern—and corresponding Antarctic Dipole Pattern (ADP) marked oscillations between El Ninõ and La Ninã events (Fedorov of sea-surface temperature in high latitudes that are in phase with and Philander, 2000) to a six year period dominated by an ENSO (Karoly, 1989; Yuan and Martinson, 2001; Liu et al., 2002; extended La Ninã and Ninõ neutral conditions and only a modest Yuan, 2004; Fig. 15). The ENSO signal is subsequently propagated El Ninõ event (Fig. 14A). The first period provided conditions that eastward around the remainder of the Southern Ocean (White et favored salps and negatively impacted krill recruitment and al., 2002). This larger-scale climate variability influences regional abundance. The second period has been dominated by the sACCf climatic conditions in the vicinity of the West Antarctic Peninsula. off the South Shetland Islands region, and has coincided with Here cool sea-surface temperature (SST) anomalies, weak relatively stable sea ice cycles and environmental conditions that northwesterly wind anomalies and retracted sea-ice extent appear to promote krill recruitment success but are not fluctuate in phase with tropical El Ninõ. In contrast, warm SST particularly favorable for salps. Cavalieri and Parkinson (2008) anomalies, strong northwesterly wind anomalies and expanded attribute the relatively stable sea-ice conditions during this period sea-ice extent fluctuate in phase with La Ninã conditions to a more neutral phase of the SOI compared to 1992-1998. ( Gloerson and White, 2001). Significant changes after 1998 were also apparent in the Oscillations between the relative importance of eastward- Elephant Island area zooplankton assemblages and in the water flowing ACC and westward-flowing Weddell Gyre waters are mass affiliations of copepods, chaetognaths, salps and other consistent with the out-of-phase relationships of subtropical (STJ) frequent and/or abundant zooplankton taxa (Table 4, Fig. 16). and polar frontal jet (PFJ) stream strengths in the South Pacific These changes reflect a shift from interannual oscillations and South Atlantic imposed by the PSA and ADP (Rind et al., 2001; between dominance by S. thompsoni and copepods, and of taxa Martinson and Iannuzzi, 2003; Yuan, 2004). Strong STJ and weak characteristic of coastal and oceanic waters, observed during the PFJ in the South Pacific and weak STJ and strong PFJ in the South BIOMASS Program (Witek et al., 1985; Schnack-Schiel and Mujica, Atlantic are associated with El Ninõ; the opposite conditions are 1994) and early AMLR surveys to more consistent representation associated with La Ninã(Fig. 15). As a consequence, during El Ninõ by a copepod and chaetognath dominated oceanic assemblage. the South Atlantic PFJ is strengthened and swings poleward, with significantly greater concentrations of taxa in ACC and ACC- spinning up the cyclonic Weddell Gyre while the South Pacific PFJ derived waters. These results suggest increased ACC influence is weakened, STJ is strengthened and storm tracks move across the survey area in 1999-2004 than during 1980-1998. In equatorward. This would explain increased Weddell Sea water contrast, significantly reduced concentrations of S. thompsoni and ARTICLE IN PRESS

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Fig. 15. Schematic representations of the Pacific South American (PSA) and Antarctic Dipole Pattern (ADP) characterized by out-of-phase relationships between the South Pacific and South Atlantic. Shown are sea surface temperature anomaly composites, schematic jet streams (thick grey arrows) and sea surface circulation patterns (narrow black arrows), anomalous high and low atmospheric pressure centers and anomalous heat fluxes (red arrows) due to mean meridional circulation for (A) La Ninã and (B) El Ninõ conditions (modified from Yuan 2004). Oscillations between the strength of Polar Frontal Jets (PFJ) and Subtropical Jets (STJ) in the South Pacific and South Atlantic are triggered by ENSO: strengthened (weakened) PFJ in the South Pacific and strengthened (weakened) STJ in the South Atlantic occur during La Ninã (El Ninõ). Weddell Sea gyral circulation is influenced by these fluctuations, spinning up (relaxing) due to the intensified (weakened) PFJ in the South Atlantic during El Ninõ (La Ninã ) (Martinson and Iannuzzi, 2003; Yuan, 2004).

I. racovitzai after 1998,, particularly in Bransfield Strait (Table 4, 0-50 m mean water temperatures monitored across the Weddell Fig. 16), suggest reduced input from the Weddell Sea. This abrupt Scotia Confluence (WSC) between 1903 and 1981. Shifts between change between two multi-year (i.e., decadal-scale) states ‘‘cold and warm epochs’’ were attributed to variable influence of conforms to the definition of a climatic regime shift (Bakun, Weddell Sea and ACC waters. Cold periods from ca. 1911-1937 2004). and after 1975 were marked by expansion of Weddell Sea water Martinson et al. (2008) report a coincidental regime shift in the while the intervening warm period (ca. 1955-1975) was char- Western Antarctic Peninsula region studied by the Palmer Long- acterized by reduced advection of Weddell Sea water and greater Term Ecological Research program (Palmer LTER; Fig 2A), ACC influence (Fig. 17). These shifts are consistent with decadal- evidenced by a substantially increased supply of warm UCDW scale changes in the Antarctic Dipole and associated onto the shelf after the 1998 El Ninõ. Because the ACC is always intensification of the subtropical and polar frontal jets in the present along the shelf-break in this region the increased supply South Pacific and South Atlantic as depicted in Fig. 15. Presumably of warm water to the shelf is attributed to shoaling and enhanced the shift apparent after 1998 in the AMLR and LTER study regions upwelling of UCDW within the sACCf. This is consistent with the culminated the South Atlantic cold period that began in the late increased influence of the sACCf in the AMLR study region and 1970s. with the La Ninã phase of the PSA and ADP off the Antarctic It is apparent now that the decadal-scale variation in ENSO Peninsula (Fig. 15A). intensity and effect on sea ice extent overwhelmed the significant Maslennikov and Solyankin (1988) describe long-term and correlation between krill reproductive success and recruitment large-scale climate regimes that impacted the Atlantic sector of determined by Loeb et al. (1997) for the 1979-1996 period. Given the Southern Ocean during much of the 20th Century. These were the longer-term data sets krill reproductive success is now based on summertime surface air temperature anomalies at South significantly correlated with the SOI (Table 3). The implication is Georgia and South Orkney Island meteorological stations and that ENSO events are reflected in the Drake Passage region of the ARTICLE IN PRESS

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Salp thompsoni Copepods Euphausia frigida 2000 5000 50

-3 1500 3750

1000 2500 25

500 1250 Mean No. 100m

0 0 0 12345 12345 12345

Ihlea racovitzai Thysanoessa macrura Primno macropa larvae 600 800 10

-3 450 600

300 400 5

150 200 Mean No. 100m

0 0 0 12345 12345 12345 Water Type

Chaetognaths Cyllopus lucasii 300 12 Time Period 1993-1998 1999-2004 -3 225 Water Type 1 = ACC 150 6 2 = Mix 1 3 = Mix 2 4 = BS 75 5 = EBS Mean No. 100m

0 0 12345 12345 Water Type Water Type

Fig. 16. Mean concentrations of various zooplankton taxa associated with ﬁve water types in the Elephant Island area during 1993-1998 and 1999-2004 surveys. These depict the signiﬁcant changes noted in Table 4.

Southern Ocean through changes in the fronts associated with the The results of this study combined with the observations of ACC, which in turn affect regional ecosystem structure and Maslennikov and Solyankin (1988) and Martinson et al. (2008) productivity. In the South Shetland-Elephant Island region this also suggest that the relatively short-term fluctuations associated is manifested through latitudinal movements and shoaling of the with ENSO variability overlie longer-term oceanic-atmospheric sACCf the combination of which affects coupled oceanic-coastal fluctuations impacting the Southern Ocean. Like ENSO these processes that drive primary and secondary productivity. longer-term fluctuations involve processes driving large-scale The three-to-five year ENSO cycle provides variability that is fluctuations between ACC and Weddell gyre influence that are aligned with the maturation and life span of Antarctic krill (Siegel consistent with the PSA and ADP. These appear linked to decadal- and Loeb, 1994) the periodicity of which favors reproduction by scale changes of interacting climate modes of atmospheric older, larger and more fecund females. Through part of the ENSO circulation variability, notably the Southern Annular Mode (also cycle conditions prevail that are conducive to good Antarctic krill known as the Antarctic Oscillation) and ENSO that have only reproductive success and population growth. Currently these recently been recognized (Kwok and Comiso, 2002b; Lefebvre and appear to be due to proximity of the sACCf to continental and Goosse, 2005; Stammerjohn et al., 2008). island shelf regions, shoaling of UCDW, enhanced mixing between Given that good krill recruitment success has occurred during oceanic and coastal waters, increased primary production possi- six of the last 10 years (1999-2008) compared to three bly due to increased iron fertilization from continental sources intermittent individual years of good recruitment during and favorable upper water column structure, and increased 1983-1998 the current climate regime appears to favor krill zooplankton abundance (Fig. 13A,B). The latter observation population growth. This results from a more persistent and suggests the importance of zooplankton as well as phytoplankton stronger influence of the sACCf across the Antarctic Peninsula food resources for krill (Fach et al., 2006). region and weakened influence of the Weddell gyre. If so, one ARTICLE IN PRESS

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Fig. 17. Distribution of mean December water temperature in the 0-50 m layer of the Scotia Sea during (A) warm (ca. 1955-1975) and (B) cold (ca. 1911-1937) regimes in the South Atlantic (modified from Maslennikov and Solyankin, 1988). Place names: S.S.I, South Shetland Islands; E.I., Elephant Island; S.O., South Orkney Islands; S.G., South Georgia. The 0 1C isotherm is highlighted to demonstrate changes in the influence of the ACC and Weddell gyre (WG) during the two regimes which correspond to the La Ninã and El Ninõ conditions of the PSA and ADP depicted in Fig. 15. could anticipate a period of increasing krill population size Rennie Holt for facilitating the current collaborative effort and throughout the current regime which could prevail for another AMLR Chief Scientist Christian Reiss for data quality control. 10-20 years (Bakun, 2004; Loeb 2007). The increased influence of Douglas Martinson was of great assistance in supporting our the eastward flowing ACC during this regime has direct impacts appreciation of the Antarctic Dipole and establishing the climatic on the advective transport of krill from spawning and nursery regime shift after 1998. We also greatly appreciate his editorial grounds off the Antarctic Peninsula to downstream areas such as assistance during preparation of this work. Support for VJL was the South Orkney Islands and South Georgia (Hofmann et al., provided by NOAA contract no. AB5CN0003. Support for EEH and 1998; Ward et al., 2002; Trathan et al., 2003; Hofmann and JMK was provided by NOAA contract JG133F04SE0127. Support Murphy, 2004; Murphy et al., 2004a,b; Murphy et al., 2007; for OHH was provided by NOAA-JIMO grant no. 1A7RJ1231. The Thorpe et al., 2007). The ecological effect of changes in the views expressed herein are those of the authors and do not frequency, intensity and duration El Ninõ and La Ninã conditions, necessarily reflect the views of NOAA or any of its subagencies. particularly those associated with climate warming (Fedorov and Philander, 2000), are unknown, but are likely to be significant particularly in those years following a shift back to a warm References climate regime. If the late 1980s are an example, the fate of krill and their dependent predator populations then is not good. AMLR, 1999. AMLR 1998/99 Field Season Report. Southwest Fisheries Science Center Administrative Report LJ-99-10, 158 pp. AMLR, 2008. AMLR 2007/08 Field Season Report. NOAA Technical Memorandum NOAA-TM-NMFS-SWFSC-XXX, N pp. Acknowledgments Amos, A.F., 1984. The large-scale hydrography of the Southern Ocean and the distribution of Antarctic krill (Euphausia superba). Journal of Crustacean We thank the captains, crew, colleagues and multitudes of Biology 4, 306–329. Amos, A.F., 2001. A decade of oceanographic variability in summertime near shipboard assistants over the years that helped develop the long- Elephant Island, Antarctica. Journal of Geophysical Research 106, term AMLR data set. We thank also AMLR Program Director 22401–22423. ARTICLE IN PRESS

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Atkinson, A., Siegel, V., Pakhomov, E., Rothery, P., 2004. Long-term decline in krill Holm-Hansen, O., Naganobu, M., Kawaguchi, S., Kameda, T., Krasovski, I., stock and increase in salps within the Southern Ocean. Nature 432, 100–103. Tchernyshkov, P., Priddle, J., Korb, R., Brandon, M., Demer, D., Hewitt, R.P., Bakun, A., 2004. Regime Shifts. In: Robinson, A., Brink, K. (Eds.), The Sea 13. Kahru, M., Hewes, C.D., 2004. Factors influencing the distribution, biomass, and Harvard University Press, Cambridge, pp. 971–1018. productivity of phytoplankton in the Scotia Sea and adjoining waters. Deep- Cai, W., Baines, P.G., 2001. Forcing of the Antarctic Circumpolar Wave by El Ninõ- Sea Research II 51, 1333–1350. Southern Oscillation teleconnections. Journal of Geophysical Research 106, Holm-Hansen, O., Kahru, M., Hewes, C.D., 2005. Deep chlorophyll a maxima 9019–9038. (DCMs) in pelagic Antarctic waters. II. Relation to bathymetric features Capella, J.E., Ross, R.M., Quetin, L.B., Hofmann, E.E., 1992. A note of the thermal and dissolved iron concentrations. Marine Ecology Progress Series 297, structure of the upper ocean in the Bransfield Strait-South Shetland Islands 71–81. region. Deep-Sea Research 39, 1221–1229. Jacobs, S.S., Comiso, J.C., 1993. A recent sea-ice retreat west of the Antarctic Carleton, A.M., 2003. Atmospheric teleconnections involving the Southern Ocean. Peninsula. Geophysical Research Letters 20, 1171–1174. Journal of Geophysical Research 108, C4, doi:10.1029/2000JC000379. Jaz˙ dz˙ ewski, K., Kittel, W., Lotocki, K., 1982. Zooplankton studies in the southern Cavalieri, D.J., Parkinson, C.L., 2008. Antarctic sea ice variability and trends, 1979- Drake Passage and in the Bransfield Strait during the austral summer 2006. Journal of Geophysical Research 113, C07004, doi:10.1029/ (BIOMASS-FIBEX, February-March 1981). Polish Polar Research 3, 203–242. 2007JC004564. Kang, S.-H., Lee, S.-H., 1995. Antarctic phytoplankton assemblage in the western Clowes, A.J., 1934. Hydrology of the Bransfield Strait. Discovery Report 9, 1–64. Bransfield Strait region, February 1993: composition, biomass and mesoscale Combes, J.M., Grossmann, A., Tchamitchian, P.H., 1990. In: Wavelets: Time- distributions. Marine Ecology Progress Series 129, 253–267. Frequency Methods and Phase Space. Springer, Berlin, Heidelberg, New York. Karoly, D.J., 1989. Southern hemisphere circulation features associated with El De Baar, H.J.W., De Jong, J.R.M., Bakker, D.C.E., Loscher,¨ B.M., Veth, C., Bathmann, Ninõ-Southern Oscillation events. Journal of Climate 2, 1239–1252. U., Smetacek, V., 1995. Importance of iron for plankton blooms and carbon Kwok, R., Comiso, J.C., 2002a. Southern Ocean climate and sea ice anomalies dioxide drawdown in the Southern Ocean. Nature 373, 412–415. associated with the Southern Oscillation. Journal of Climate 15, 487–501. De Baar, H.J.W., De Jong, J.R.M., 2001. Distributions, sources and sinks of iron. In: Kwok, R., Comiso, J.C., 2002b. Spatial patterns of variability in Antarctic surface Seawater, IN, Turner, D.R., Hunter, K.A. (Eds.), The Biogeochemistry of Iron in temperature: connections to the Southern Hemisphere annular mode and the Seawater. John Wiley, NY, pp. 125–234. Southern Oscillation. Geophysical Research Letter 29, 1705, doi:10.1029/ El-Sayed, S.Z. (Ed.), 1994. Southern Ocean Ecology: The BIOMASS Perspective. 2002GL015415. Cambridge University Press, Cambridge. Lefebvre, W., Goosse, H., 2005. Influence of the Southern Annular Mode on the sea Fach, B.A., Hofmann, E.E., Murphy, E.J., 2006. Transport of Antarctic krill (Euphausia ice-ocean system: the role of the thermal and mechanical forcing. Ocean superba) across the Scotia Sea Part II: Krill growth and survival. Deep-Sea Science 1, 145–157. Research I, 10.1016/j.dsr.2006.03.007. Liu, J., Yuan, X., Rind, D., Martinson, D.G., 2002. Mechanism study of the ENSO and Fedorov, A.V., Philander, S.G., 2000. Is El Ninõ changing? Science 288 (5437), southern high latitude climate teleconnections. Geophysical Research Letters, 1997–2002. 29, doi:10.1029/2002/GLO15143. Fraser, W.R., Hofmann, E.E., 2003. A predators’ perspective on causal links Loeb, V., Siegel, V., Holm-Hansen, O., Hewitt, R., Fraser, W., Trivelpiece, W., between climate change, physical forcing and ecosystem response. Marine Trivelpiece, S., 1997. Effects of sea-ice extent and krill or salp dominance on Ecology Progress Series 265, 1–15. the Antarctic food web. Nature 387, 897–900. Foxton, P., 1971. On Ihlea magalhanica (Apstein) (Tunicata: Salpidae) and Ihlea Loeb, V.J., Hofmann, E.E., Klinck, J.M., Holm-Hansen, O., White, W.B., In Press. ENSO racovitzai (Van Beneden). Discovery Report 35, 1–6. and variability of the Antarctic Peninsula pelagic marine ecosystem. Antarctic Garcia, M.A., Lo´ pez, O., Sospedra, J., Espino, M., Garcia, V., Morrison, G., Rojas, P., Science. Figa, J., Puigdefabregas, J., Arcilla, A.S., 1994. Mesoscale variability in the Loeb, V.J., 2007. Environmental Variability and the Antarctic Marine Ecosystem. Bransfield Strait region (Antarctica) during austral summer. Ann. Geophysicase In: Vasseur, D.A., McCann, K.S. (Eds.), The Impact of Environmental Variability 12, 856–867. on Ecological Systems. The Peter Yodzis Fundamental Ecology Series, vol. 2. Gille, S.T., 1994. Mean sea surface height of the Antarctic Circumpolar Current Springer, Dordrecht, The Netherlands, pp. 197–225. from Geosat data: method and application. Journal of Geophysical Research 99, Mackintosh, N.A., 1934. Distribution of the macroplankton in the Atlantic sector of 18255–18273. the Antarctic. Discovery Report 9, 65–160. Gloerson, P., White, W.B., 2001. Reestablishing the circumpolar wave in sea ice Makarov, R.R., Denys, C.J.I., 1981. Stages of sexual maturity of Euphausia superba. around Antarctica from one winter to the next. Journal of Geophysical BIOMASS Handbook, 11. Research 106, 4391–4395. Makarov, R.R., Maslennikov, V.V., Solyankin, E.V., Spiridonov, V.A., Yakovlev, V.N., Gordon, A.L., Nowlin Jr., W.D., 1978. The basin waters of the Bransfield Strait. 1988. Variability in population density of Antarctic krill in the Western Scotia Journal of Physical Oceanography 8, 258–264. Sea in relation to hydrological conditions. In: Sahrhage, D. (Ed.), Antarctic Gordon, A.L., Mensch, M., Dong, Z., Smethie Jr., W.M., de Bettencourt, J., 2000. Deep Ocean and Resources Variability. Springer-Verlag, Berlin, pp. 231–236. and bottom water of the Bransfield Strait eastern and western basins. Journal Martinson, D.G., Iannuzzi, R.A., 2003. Spatial/temporal patterns in Weddell gyre of Geophysical Research 105, 11337–11346. characteristics and their relationship to global climate. Journal of Geophysical Hempel, G., 1985. On the biology of Polar Seas, particularly the Southern Ocean. Research 108 (NO. C4), 8083, doi:10.1029/200JC000538. In: Gray, J.S., Christiansen, M.E. (Eds.), Marine Biology of Polar Regions and Martinson, D.G., Stammerjohn, S.E., Iannuzzi, R.A., Smith, R.C., Vernet, M., 2008. Effects of Stress on Marine Organisms. John Wiley & Sons Ltd., pp. 3–33. Western Antarctic peninsula physical oceanography and spatio-temporal Hewes, C.D., Reiss, C.S., Kahru, M., Mitchell, B.G., Holm-Hansen, O., 2008. Control variability. Deep-Sea Research II 55, 1964–1987. of phytoplankton biomass by dilution and mixed layer depth in the western Maslennikov, V.V., Solyankin, E.V., 1988. Patterns and fluctuations in the Weddell-Scotia Confluence. Marine Ecology Progress Series 366, 15–29. hydrological conditions of the Antarctic and their effect on the distribution Hewitt, R.P., 1997. Areal and seasonal extent of sea ice cover off the northwestern of Antarctic krill. In: Sahrhage, D. (Ed.), Antarctic Ocean and Resources side of the Antarctic Peninsula: 1979 through 1995. CCAMLR Science 4, 65–73. Variability. Springer-Verlag, Berlin, pp. 210–213. Hofmann, E.E., Whitworth III, T., 1985. A synoptic description of the flow at Drake Mitchell, B.G., Holm-Hansen, O., 1991. Observations and modeling of the Antarctic Passage from year-long measurements. Journal of Geophysical Research 90, phytoplankton crop in relation to mixing depth. Deep-Sea Research 38, 7177–7187. 981–1007. Hofmann, E.E., Klinck, J.M., Lascara, C.M., Smith, D.A., 1996. Water mass Moore, J.K., Abbott, M.R., Richman, J.G., 1999. Location and dynamics of the distribution and circulation west of the Antarctic Peninsula and including Antarctic Polar Front from satellite sea surface temperature data. Journal of Bransfield Strait. In: Ross, R.M., Hofmann, E.E., Quetin, L.B. (Eds.), Foundations Geophysical Research 104, 3059–3073. for Ecological Research West of the Antarctic Peninsula, Antarctic Research Murphy, E.J., Thorpe, S.E., Watkins, J.L., 2004a. Modeling the krill transport Series, vol. 70. American Geophysical Union, Washington, DC, pp. 61–80. pathways in the Scotia Sea: spatial and environmental connections generating Hofmann, E.E., Klinck, J.M., 1998. Hydrography and circulation of the Antarctic the seasonal distribution of krill. Deep-Sea Research II 51, 1435–1456. continental shelf 1501E eastward to the Greenwich Meridian. In: Robinson, Murphy, E.J., Watkins, J.L., Meredith, M.P., Ward, P., Trathan, P.N., Thorpe, S.E., A.R., Brink, K.H. (Eds.), The Sea, The Global Coastal Ocean., Regional Studies and 2004b. Southern Antarctic Circumpolar Current front to the northeast of South Synthesis, Vol. 11. Wiley, N.Y, pp. 997–1042. Georgia: horizontal advection of krill and its role in the ecosystem. Journal of Hofmann, E.E., Klinck, J.M., Locarnini, R.A., Fach, B., Murphy, E., 1998. Krill Geophysical Research 109, C01029, doi:10.1029/2002JC001522. transport in the Scotia Sea and environs. Antarctic Science 10, 406–415. Murphy, E.J., Trathan, P.N., Watkins, J.L., Reid, K., Meredith, M.P., Forcada, J., Hofmann, E.E., Murphy, E.J., 2004. Advection, krill and Antarctic marine Thorpe, S.E., Johnston, N.M., Rothery, P., 2007. Climatically driven fluctuations ecosystems. Antarctic Science 16, 487–499. in Southern Ocean ecosystems. Proceedings of the Royal Society B 274, Holm-Hansen, O., Amos, A.F., Silva, N., Villafan˜e, V., Helbling, E.W., 1994. In situ 3057–3067. evidence for a nutrient limitation of phytoplankton growth in pelagic Antarctic Niiler, P.P., Amos, A., Hu, J.-H., 1991. Water masses and 200 m relative geostrophic waters. Antarctic Science 6, 315–324. circulation in the western Bransfield Strait region. Deep-Sea Research 38, Holm-Hansen, O., Hewes, C.D., Villafan˜e, V.E., Helbling, E.W., Silva, N., Amos, T., 943–960. 1997. Distribution of phytoplankton and nutrients in relation to different Nishikawa, J., Naganobu, M., Ichii, T., Ishii, H., Terazake, M., Kawaguchi, K., 1995. water masses in the area around Elephant Island, Antarctica. Polar Biology 18, Distribution of salps near the South Shetland Islands during austral summer, 145–153. 1990-1991 with special reference to krill distribution. Polar Biology 15, 31–39. Holm-Hansen, O., Amos, A.F., Hewes, C.D., 2000. Reliability of estimating Nowlin Jr., W.D., Whitworth III, T., Pillsbury, R.D., 1977. Structure and transport of chlorophyll a concentrations in Antarctic waters by measurement of in situ the Antarctic Circumpolar Current at Drake Passage from short-term chlorophyll a fluorescence. Marine Ecology Progress Series 196, 103–110. measurements. Journal of Physical Oceanography 7, 790–802. ARTICLE IN PRESS

542 V. Loeb et al. / Deep-Sea Research II 57 (2010) 519–542

Nowlin Jr., W.D., Clifford, M., 1982. The kinematic and thermohaline zonation of Antarctic Research Series, vol. 70. American Geophysical Union, Washington the Antarctic Circumpolar Current at Drake Passage. Journal of Marine DC, pp. 81–104. Research 40, 481–507. Stammerjohn, S.E., Drinkwater, M.R., Smith, R.C., Liu, X., 2003. Ice-atmosphere Orsi, A.H., Whitworth. III, T., Nowlin Jr., W.D., 1995. On the meridional extent and interactions during sea-ice advance and retreat in the western Antarctic fronts of the Antarctic Circumpolar Current. Deep-Sea Research 42, 641–673. Peninsula region. Journal of Geophysical Research 108 (C10), 3329, Park, C., Wormuth, J.H., 1993. Distribution of Antarctic zooplankton around doi:10.1029/2002JC001543. Elephant Island during the austral summers of 1988, 1989, and 1990. Polar Stammerjohn, S.E., Martinson, D.G., Smith, R.C., Yuan, X., Rind, D., 2008. Trends in Biology 13, 215–225. Antarctic annual sea ice retreat and advance and their relation to El Nino- Parkinson, C.L., 2002. Trends in the length of the Southern Ocean sea-ice season, Southern Oscillation and Southern Annular Mode variability. Journal of 1979-99. Annals of Glaciology 34, 435–440. Geophysical Research 112, C03S90, doi:10.1029/2077JC004269. Peterson, R.G., White, W.B., 1998. Slow oceanic teleconnections linking the Stein, M., 1983. The distribution of water masses in the South Shetland Islands Antarctic Circumpolar Wave with the tropical El Ninõ-Southern Oscillation. area during FIBEX. Memoirs National Institute Polar Research Special Issue No. Journal of Geophysical Research 103 (C11), 24,573–24,583. 27, 16–23. Pollard, R.T., Lucas, M.I., Read, J.F., 2002. Physical controls on biogeochemical Stein, M., 1986. Variability of water masses and currents off the Antarctic zonation in the Southern Ocean. Deep-Sea Research II 49, 3289–3306. Peninsula during SIBEX. Arch Fischereiwiss 37, 25–50. Pre´zelin, B.B., Hofmann, E.E., Mengelt, C., Klinck, J.M., 2000. The linkage between Stein, M., 1988. Variation of geostrophic circulation off the Antarctic Peninsula and Upper Circumpolar Deep Water (UCDW) and phytoplankton assemblages on in the southwest Scotia Sea, 1975-1985. In: Sahrhage, D. (Ed.), Antarctic Ocean the west Antarctic Peninsula continental shelf. Journal of Marine Research 58, and Resources Variability. Springer-Verlag, Berlin, pp. 81–91. 165–202. Stein, M., 1989. Seasonal variation of water masses in Bransfield Strait and Pre´zelin, B.B., Hofmann, E.E., Moline, M., Klinck, J.M., 2004. Physical forcing of adjacent waters. Arch Fischereiwiss 39, 15–38. phytoplankton community structure and primary production in continental Thorpe, S.E., Murphy, E.J., Watkins, J.L., 2007. Circumpolar connections between shelf waters of the western Antarctic Peninsula. Journal of Marine Research 62, Antarctic krill (Euphausia superba Dana) populations: investigating the roles of 419–460. ocean and sea ice transport. Deep-Sea Research I 54, 792–810. Priddle, J., Croxall, J.P., Everson, I., Heywood, R.B., Murphy, E.J., Prince, P.A., Sear, Toole, J.M., 1981. Sea ice, winter convection, and temperature minimum layer in C.B., 1988. Large-scale fluctuations in distribution and abundance of krill — a the Southern Ocean. Journal of Geophysical Research 86, 8037–8047. discussion of possible causes. In: Sahrhage, D. (Ed.), Antarctic Ocean and Torrence, C., Compo, G.P., 1998. A practical guide to wavelet analysis. Bulletin of Resources Variability. Springer-Verlag, Berlin, pp. 169–182. the American Meteorology Society 79, 61–78. Priddle, J., Brandini, F., Lipski, M., Thorley, M.R., 1994. Pattern and variability of Trathan, P.N., Brierley, A.S., Brandon, M.A., Bone, D.G., Goss, C., Grant, S.A., Murphy, phytoplankton biomass in the Antarctic Peninsula region: an assessment of the E.J., Watkins, J.L., 2003. Oceanographic variability and changes in Antarctic krill BIOMASS cruises. In: El-Sayed, S.Z. (Ed.), Southern Ocean Ecology: The (Euphausia superba) abundance at South Georgia. Fisheries Oceanography 12, BIOMASS Perspective. Cambridge University Press, Cambridge, pp. 49–61. 569–583. Rind, D., Chandler, M., Lerner, J., Martinson, D.G., Yuan, X., 2001. The climate Turner, J., 2004. The El Ninõ-Southern Oscillation and Antarctica. International response to basin-specific changes in latitudinal temperature gradients and Journal of Climatology 24, 1–31. the implications for sea ice variability. Journal of Geophysical Research 106, Tynan, C.T., 1998. Ecological importance of the Southern Boundary of the Antarctic 20161–20173. Circumpolar Current. Nature 392, 708–710. Schnack-Schiel, S.B., Mujica, A., 1994. The zooplankton of the Antarctic Peninsula Ward, P., Whitehouse, M., Meredith, M., Murphy, E., Shreeve, R., Korb, R., Watkins, region. In: El-Sayed, S.Z. (Ed.), Southern Ocean Ecology: The BIOMASS J., Thorpe, S., Woodd-Walker, R., Brierley, A., Cunningham, N., Grant, S., Bone, Perspective. Cambridge University Press, Cambridge, pp. 79–92. D., 2002. The Southern Antarctic Circumpolar front: physical and biological Siegel, V., Piatkowski, U., 1990. Variability in the macrozooplankton community coupling at South Georgia. Deep-Sea Research I 49, 2183–2202. off the Antarctic Peninsula. Polar Biology 10, 373–386. White, W.B., Peterson, R.G., 1996. An Antarctic circumpolar wave in surface Siegel, V., Loeb, V., 1994. Length and age at maturity of Antarctic krill. Antarctic pressure, wind, temperature and sea-ice extent. Nature 380, 699–702. Science 6, 479–482. White, W.B., Chen, S.C., Allan, R.J., Stone, R.C., 2002. Positive feedbacks between the Siegel, V., Loeb, V., 1995. Recruitment of Antarctic krill (Euphausia superba) and Antarctic circumpolar wave and the global El Ninõ-Southern Oscillation. possible causes for its variability. Marine Ecology Progress Series 123, 45–56. Journal of Geophysical Research 107 (C10), 3165, doi:10.1029/2000JC000581. Siegel, V., Bergstrom,¨ B., Muhlenhardt-Siegel,¨ U., Thomasson, M., 2002. Demo- Whitworth III, T., 1983. Monitoring the transport of the Antarctic graphy of krill in the Elephant Island area and its significance for stock Circumpolar Current at Drake Passage. Journal of Physical Oceanography 13, recruitment. Antarctic Science 14, 162–170. 2045–2057. Siegel, V., 2005. Distribution and population dynamics of Euphausia superba: Whitworth III, T., Peterson, R.G., 1985. Volume transport of the Antarctic summary of recent findings. Polar Biology 29, 1–22. Circumpolar Current from bottom pressure measurements. Journal of Physical Sievers, H.A., Nowlin Jr., W.D., 1984. The stratification and water masses at Drake Oceanography 15, 810–816. Passage. Journal of Geophysical Research 89, 10489–10514. Whitworth III, T., Nowlin Jr., W.D., Orsi, A.H., Locarnini, R.A., Smith, S.G., 1994. Simmonds, I., 2003. Modes of atmospheric variability over the Southern Ocean. Weddell Sea shelf water in the Bransfield Strait and Weddell-Scotia Journal of Geophysical Research 108 (No. C4, 8078), 8078, doi:10.1029/ Confluence. Deep-Sea Research 41, 629–641. 2000JC000542. Whitworth III, T., Orsi, A.J., Kim, S.-J., Nowlin Jr., W.D., 1998. Water masses and Smith, R.C., Pre´zelin, B.B., Baker, K.S., Bidigare, R.R., Boucher, N.P., Coley, T., Karentz, D., mixing near the Antarctic slope front. In: Jacobs, S., Weiss, R. (Eds.), Ocean, Ice Macintyre, S., Matlick, H.A., 1992. Ozone depletion, ultraviolet radiation and and Atmosphere: Interactions at the Antarctic Continental Margin, Antarctic phytoplankton biology in Antarctic waters. Science 255, 952–959. Research Series, vol. 75. American Geophysical Union, Washington, DC, pp. 1–27. Spiridonov, V.A., 1996. A scenario of the Late-Pleistocene-Holocene changes in the Witek, Z., Kittel, W., Czykieta, H., Zmijewska, M.I., Presler, E.., 1985. Macro- distributional range of Antarctic krill (Euphausia superba). Marine Ecology 17, zooplankton in the southern Drake Passage and in the Bransfield Strait during 519–541. BIOMASS-SIBEX (December 1983-January 1984). Polish Polar Research 6, Sprintall, J., 2003. Seasonal to interannual upper ocean variability in the Drake 95–115. Passage. Journal Marine Research 61, 27–57. Yuan, X., Martinson, D.G., 2001. The Antarctic dipole and its predictability. Stammerjohn, S.E., Smith, R.C., 1996. Spatial and temporal variability of western Geophysical Research Letter 28, 3609–3612. Antarctic Peninsula sea ice coverage. In: Ross, R.M., Hofmann, E.E., Quetin, L.B. Yuan, X., 2004. ENSO-related impacts on Antarctic sea ice: a synthesis of (Eds.), Foundations for Ecological Research West of the Antarctic Peninsula, phenomenon and mechanisms. Antarctic Science 16, 415–425.