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Limnol. Oceanogr., 59(1), 2014, 17–36 E 2014, by the Association for the Sciences of Limnology and Oceanography, Inc. doi:10.4319/lo.2014.59.1.0017

Feeding and overwintering of Antarctic krill across its major habitats: The role of ice cover, water depth, and phytoplankton abundance

Katrin Schmidt,1 Angus Atkinson,2,* David W. Pond,3 and Louise C. Ireland 1

1 British Antarctic Survey, Natural Environment Research Council, High Cross, Cambridge, United Kingdom 2 Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, United Kingdom 3 Scottish Association of Marine Science, Dunstaffnage Marine Laboratory, Oban, Argyll, Scotland, United Kingdom

Abstract Antarctic krill (Euphausia superba) were sampled in contrasting habitats: a seasonally ice-covered deep (Lazarev Sea), ice-free shelves at their northern range (South Georgia) and the Antarctic Peninsula (Bransfield Strait), and shelf and oceanic sites in the . Across 92 stations, representing a year-round average, the food volume in krill stomachs comprised 71 6 29% algae, 17 6 21% protozoans, and 12 6 25% metazoans. Fatty acid trophic markers showed that copepods were consistently part of krill diet, not a switch food. In open waters, both diatom and copepod consumption increased with phytoplankton abundance. Under sea ice, ingestion of diatoms became rare, whereas feeding on copepods remained constant. During winter, larvae contained high but variable proportions of diatom markers, whereas in postlarvae the role of copepods increased with krill body length. Overwintering differed according to habitat. Krill from South Georgia had lower lipid stores than those from the Bransfield Strait or Lazarev Sea. Feeding effort was much reduced in Lazarev Sea krill, whereas most individuals from the Bransfield Strait and South Georgia contained phytoplankton and seabed detritus in their stomachs. Their retention of essential body reserves indicates that krill experienced most winter hardship in the Lazarev Sea, followed by South Georgia and then Bransfield Strait. This was reflected in the delayed development from juveniles to adults in the Lazarev Sea. Circumpolar comparisons of length frequencies suggest that krill growth conditions are more favorable in the southwest Atlantic than in the Lazarev Sea or off East because of longer phytoplankton bloom periods and rewarding access to benthic food.

Antarctic krill, Euphausia superba, are central to the food transported by ocean currents and drifting sea ice, which web in many ecosystems. Their high interconnect Southern Ocean (Thorpe et al. 2007). abundance (. 1018 postlarvae; Atkinson et al. 2009), Population genetic analyses on E. superba have found high relatively large body size, and appearance as dispersed levels of genetic diversity, but no evidence of significant individuals as well as dense swarms makes them a favorable genetic structure even across large geographic scales food source for a range of predators, including squid, fish, (Bortolotto et al. 2011). benthic fauna, sea birds, penguins, seals, and whales. In However, environmental conditions clearly differ across turn, E. superba is ideally adapted to feed on nano- and krill habitats. At South Georgia, for instance, krill often microorganisms given their large filtering basket of very live in water depths , 300 m, summer surface temperatures fine mesh size (Suh and Nemoto 1987; Kawaguchi et al. can reach 4–5uC, elevated chlorophyll a (Chl a) concentra- 1999). However, their feeding behavior is more complex tions last on average for , 5 months yr21 (Fig. 1), predator than just filtering phytoplankton and protozoa; it includes abundance is very high, and the area is ice-free even in raptorial capture of other zooplankton, scraping algae winter. The Lazarev Sea is another extreme, where the from beneath sea ice, and diving into seabed detritus (Price water column averages depths of , 4500 m, temperatures et al. 1988; Stretch et al. 1988; Clarke and Tyler 2008). remain around 0uC, even in summer, the phytoplankton Together, their intensive grazing and excretion can affect bloom season is as short as , 1 month yr21, and the area is local nutrient cycles and phytoplankton dynamics (Smeta- ice-covered for 4–9 months yr21 (Fig. 1). The western cek et al. 2004; Schmidt et al. 2011); therefore, krill are Antarctic Peninsula, the Scotia Sea, and Prydz Bay show considered ‘‘engineers’’ of ecosystem structure and func- some intermediate features with 2–3 months of moderate to tion. high Chl a concentrations yr21 and annual sea ice cover of The circumpolar habitat of Antarctic krill spans about 1–9 months depending on latitude (Fig. 1). These specific 19 million km2, with the area around the islands South conditions most likely affect krill life cycle parameters, their Georgia and Bouvet as their northern limit (, 52uS) and feeding behavior, and their energy budget. However, only a the pack ice zone of the southeastern as their few studies address regional differences in krill biology southern limit (,75uS) (Atkinson et al. 2008). Even though beyond abundance or demography (Spiridonov 1995; areas of high and low krill abundance are interspersed, krill Kawaguchi et al. 2006). stocks are considered to mix over large areas (Thorpe et al. The western Antarctic Peninsula is the most studied krill 2007; Bortolotto et al. 2011). This is, firstly, because adult habitat, and observations from this area have often been krill migrate and second, because krill life stages are generalized because of an unawareness of regional differ- ences. An example is the seasonal onshelf–offshelf migra- * Corresponding author: [email protected] tion of adult krill (Siegel 1988), which has been considered 17 18 Schmidt et al. Krill feeding and overwintering 19 an evolved life history of krill to exploit their seasonally environmental conditions were derived from the varying variable environment (Nicol 2006). Later it was shown that proportions of diatom- [16:4(n-1)], flagellate- [18:4(n-3)], a close association of krill with the inner shelf is specific and copepod-indicating fatty acids [S 20:1, 22:1 isomers] in to the Antarctic Peninsula, whereas in the Indian-Pacific their tissues. Finally, indices of feeding activity and body sector, krill generally prevail offshore beyond the shelf conditions were used to identify overwintering mechanisms break (Atkinson et al. 2008). On the other hand, seemingly and degree of hardship across different habitats. Thereby, conflicting findings might be true reflections of local we gained an improved perspective of the conditions that differences. For instance, it was originally suggested that are conclusive to enhanced growth and overwintering. E. superba does not rely on a lipid store to survive the winter (Clarke 1984), but other studies found that the lipid Methods reserves adult krill accumulate before winter are sufficient to survive 5 months of starvation (Hagen et al. 2001). Krill sampling—Krill were sampled in the Lazarev Sea, The latter calculation was based on krill sampled in the Bransfield Strait, Scotia Sea, and at South Georgia during southeastern Weddell Sea and Lazarev Sea, where lipids various cruises of R/V Polarstern, Royal Research Ship account for up to 45% of dry mass (Hagen et al. 2001). The James Clark Ross, Marine Vessel Dorada, and krill fisheries lipid data compiled by Clarke (1984) derived mainly from vessels (January–February 2002, 2003, 2005, 2006; March South Georgia and the Antarctic Peninsula and were 2004; April 2004; July 2005; June–August 2006; November generally lower. 2006; December 2005; Fig. 2A). On research vessels, krill Even more controversial is whether krill feed during were caught with oblique target net tows in the top 200 m winter. Some studies found that their feeding rates drop of the water column or with horizontal hauls in open substantially during autumn and winter (Atkinson et al. surface waters or directly under sea ice (Flores et al. 2012). 2002; Meyer et al. 2010) and suggested that krill perform a On the fishery vessels, krill were hauled with large pelagic pseudo-dormancy (‘‘quiescence’’), wherein they remain in trawls (vessels In Sung Ho, Niitaka Maru) or continuously motion but reduce their metabolic rate, combust body pumped from the cod end of the net (vessel Saga Sea; Nicol reserves, and feed opportunistically (Torres et al. 1994). et al. 2011). Once onboard research vessels, krill were Other studies repeatedly observed food in krill stomachs immediately deep-frozen (280uC), whereas on fisheries (Morris and Priddle 1984; Kawaguchi et al. 1986; Daly and vessels, krill were stored at 220uC and transferred to a Macaulay 1991), and Huntley et al. (1994) concluded that 280uC freezer when landed at South Georgia up to 3 weeks feeding on copepods and growth, rather than starvation later. and reduced metabolism, is the usual winter behavior for krill. Drawing a conclusion from such findings is difficult Length, mass, feeding activity, and maturity stage because studies not only took part in different areas, but of krill—Krill from 13 of the total 92 stations were only also employed a range of methods, including in situ suitable for microscopic analysis of the stomach content, observations (Stretch et al. 1988), gut pigment analysis whereas krill from the remaining 79 stations were analyzed (Morris and Priddle 1984), microscopic stomach content for feeding activity, fatty acid composition, amount of analysis (Kawaguchi et al. 1986; Huntley et al. 1994), and body reserves, and stomach content. The total body length onboard feeding experiments (Huntley et al. 1994; Atkin- (from the tip of the rostrum to the tip of the uropod) and son et al. 2002; Meyer et al. 2010). the standard three body lengths (from the anterior lateral We overcame this shortage by sampling krill across edge of the carapace to the posterior edge of the sixth major habitats (South Georgia, Bransfield Strait, Scotia abdominal segment) were measured for 30 krill per station. Sea, and Lazarev Sea) throughout different seasons and The stomach fullness of these 30 krill was judged on a examining their feeding and body reserves in a methodi- semiquantitative scale between 0 (empty) and 4 (full), and cally consistent manner. Regional and seasonal differences the average stomach fullness index per station was in krill diet were established from the relative abundance of calculated. Sex and maturity stages were identified follow- different food types in their stomachs. Functional relation- ing Makarov and Denys (1981). For further analysis, 10 ships between krill diet and body length, and diet and krill with a total body length of , 40 mm and, if available,

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Fig. 1. Average season length of ice cover and open waters with elevated phytoplankton abundance ($ 0.4 mg Chl a L21) and low phytoplankton abundance (, 0.4 mg Chl a L21) for nine circumpolar habitats of E. superba (based on Atkinson et al. 2008, fig. 4). The regions are ordered in the eastward direction starting at the Greenwich meridian (0uE). Chlorophyll a values were extracted from data of SeaWiFS (8 day temporal and 9 km spatial resolution, period 1997–2010, http://oceancolor.gsfc.nasa.gov/ ). Length of the ice season was derived from Parkinson (2004, see fig. 9, period 1979–2002). Histogram bars represent 1u latitudinal steps from the north toward the Antarctic , except for the Bransfield Strait and South Georgia, where data are integrated across the latitudes shown. A Chl a concentration of , 0.4 mgL21 supports a half-saturated daily growth rate in E. superba (Atkinson et al. 2006). 20 Schmidt et al.

Fig. 2. Krill sampling. (A) Map of the sampling locations at South Georgia, the Scotia Sea, Bransfield Strait, and Lazarev Sea. Grey dots indicate stations where krill were analyzed for feeding activity, fatty acid trophic indicators, body reserves, and stomach content, and white dots show stations where only the krill stomach content has been analyzed. (B) Seasonal coverage of sampling and the body length of krill used for analysis. Each of the symbols represents a pooled sample of 10 individuals. a second set of either larger or smaller krill were selected. an index of feeding activity and the lipid content of the Overall, the analyzed krill covered a similar range in body digestive gland as a sensitive indicator of the overall lipid length throughout all seasons (Fig. 2B). Body conditions reserves. The muscle of the third abdominal segment was might vary not only with length but also with krill gender used for fatty acid analysis. This tissue integrates diet and maturity stage. Especially during summer does the signals over longer feeding periods and is unlikely to be lipid content of adult males and gravid females deviate contaminated with recently ingested food when the stomach from other krill, whereas differences between juveniles and and gut are removed. The pooled sample of each of these subadult males or subadult females are minor (Hagen et al. three components was placed in a preweighed vial. Samples 2001; Schmidt et al. 2006). Because of the main sampling were freeze-dried for 24 h and reweighed on a Sartorius in winter and the relatively small body length of 40 mm, microbalance. Solvent (chloroform : methanol; 2 : 1; v/v) was the vast majority of the krill we analyzed were juveniles added to the samples of the digestive gland and third or subadults. Only five out of the 110 batches of 10 abdominal segment, and the vials were stored at 220uC same-length individuals were dominated by adult krill. In for subsequent lipid and fatty acid analysis. To get a these cases, we included the same number of males and mass : length ratio, the dry mass of 10 krill was divided by nongravid females. their mean total body length. This ratio allows comparison The batches of 10 krill were dissected into digestive of the amount of body reserves and physiological conditions gland, third abdominal segment, and remaining body. The across similar-sized animals. digestive gland has a double function in crustaceans; it is involved in the absorption of digested food, but it is also a Lipid and fatty acid analysis—Lipids were extracted in major site of lipid storage (Dall and Moriarty 1983). chloroform : methanol (2 : 1; v/v) and weighed on a Therefore, we used the mass of the digestive gland as Sartorius microbalance. Fatty acid methyl esters (FAME) Krill feeding and overwintering 21 were prepared from aliquots of the total lipid after the category Algae includes autotrophs such as (1) the pelagic addition of an internal standard (23 : 0). FAME were diatom species Eucampia antarctica, (2) the pelagic diatom generated by transesterification of lipid samples in meth- Fragilariopsis spp., (3) benthic diatoms (Cocconeis anol and 1.5% sulfuric acid at 50uC for 16 h (Christie 1982). spp., Grammatophora arcuata), (4) pelagic spiny diatoms FAME were then purified by thin layer chromatography in (Thalassiothrix spp., Chaetoceros spp., Rhizosolenia spp., a hexane : diethyl ether : acetic acid solvent system (90 : 10 : 1; Corethron spp.), (5) pennate diatoms (Thalassionema sp., v/v/v) and analyzed with a Thermo Finnigan Trace 2000 Pseudonitzschia spp., Navicula spp., and broken parts gas chromatograph (GC). The GC was equipped with on- thereof), (6) discoid diatoms (Coscinodiscus spp., Thalas- column injection, and hydrogen was used as a carrier gas. siosira spp., Asteromphalus spp., Dactyliosolen spp.), (7) FAME were detected by flame ionization and identified by debris (small parts of broken discoid diatoms), and (8) comparing retention time data with those obtained from autotrophic flagellates (Prorocentrum spp., Ceratium spp., standard mixtures. silicoflagellates). The category Protozoan includes (9) As trophic indicators, we used 16:4(n-1) for diatoms, tintinnids (Cymatocylis spp., Codonellopsis spp., Salpingella 18:4(n-3) for autotrophic and heterotrophic flagellates, and spp., Laackmanniella spp.), (10) foraminifera (Neoglobo- 20:1, 22:1 isomers for copepods [including 20:1(n-11), quadrina pachyderma), and (11) heterotrophic flagellates 20:1(n-9), 20:1(n-7), 22:1(n-11), 22:1(n-9), 22:1(n-7)] ac- (Dinophysis spp., Protoperidinium spp.). The category cording to Dalsgaard et al. (2003). The ratio of S 20:1, 22:1/ Metazoan includes (12) copepods (Oithona spp., Calanus 16:4(n-1) was calculated to check for changes in the relative propinquus, Ctenocalanus citer, Calanoides acutus, Metridia importance of copepods compared with diatoms in the krill spp., Drepanopus forcipatus, Microcalanus pygmaeus, Ste- diet. The application of this fatty acid ratio seems valid phos longipes, and unidentified), (13) copepod nauplii, (14) because the 20:1,22:1 isomers and 16:4(n-1) have a similar eggs, and (15) nematocysts. Lithogenic particles have been status in the krill fatty acid pool: they are nonessential fatty enumerated according to Schmidt et al. (2011). acids, account for only minor proportions (, 4%), and show a similar trend with increasing lipid content (Schmidt Ambient Chl a concentration and sea ice cover—Surface et al. 2006). Chl a concentrations were derived from ocean color The sum of polyunsaturated fatty acids (PUFA) was radiometric data (sea-viewing wide field-of-view sensor calculated because this group includes a number of [SeaWiFS] and moderate-resolution imaging spectroradi- essential fatty acids. These fatty acids have a specific ometer) with 9 km spatial and 8 day temporal resolution structural role in higher organisms but are not sufficiently (http://disc.sci.gsfc.nasa.gov/giovanni/overview/index.html). synthesized within the body and have therefore to be Mean values within 50 km of the sampling site were taken up with the food (Dalsgaard et al. 2003). For diet extracted both from the nearest date to sampling and from comparison between larval and postlarval krill, additional the previous 5 weeks. However, satellite readings are analysis of fatty acid trophic indicators was carried out on hindered by ice cover, clouds, or insufficient light levels furcilia larvae. These larvae also derived from the Lazarev (June–August); therefore, Chl a data were only available for Sea cruise in June to July 2006, and sampling sites are Stas. , 50% of our sampling stations. 497, 498, 502, and 515 of Meyer et al. (2009, their fig. 2). Median values of percent sea ice cover were extracted for For each of these sites, two sets of 10 larvae were analyzed: the sampling date and at a 7 day interval for the last 5 weeks either furcilia stage IV and V or V and VI. before krill sampling. The values derived from two passive microwave radiometer data; the Microwave Scanning Microscopic analysis of the stomach content—Microscop- Radiometer– Observation System (AMSR-E) aboard ic analysis of the stomach content was carried out on two to the National Aeronautics and Space Administration’s five animals per station (i.e., 289 individuals [ind.] in total). (NASA’s) Aqua satellite and the Defense Meteorological The stomach was dissected from frozen krill, and the Satellite Program Special Sensor Microwave Imager (SSM/ content was emptied into a 4 mL water sample. The sample I; Spreen et al. 2008; http://nsidc.org/data/nsidc-0051.html). was gently mixed, transferred into an Utermo¨hl counting The medians were calculated using a 40 3 40 km window receptacle, and allowed to settle for , 2 h. Rare items (e.g., for AMSR-E data (2002–2006) and a 75 3 75 km window copepod mandibles, tintinnids, thecate dinoflagellates) for the SSM/I data (1999). Further details are given in were counted by scanning the complete receptacle at Cavalieri et al. (1996). 3200 magnification, whereas common items (e.g., small diatoms) were only enumerated from two perpendicular Results transects across the whole diameter of the receptacle. The dimensions of different food items were measured, and Seasonal trends in krill feeding activity, trophic indicators, their volume was calculated on the basis of simple and body reserves—Three indicators were used to study geometric shapes or combinations thereof (Schmidt et al. seasonal trends in krill feeding activity: the mass of the 2006). For copepods, the width of the mandible blade was digestive gland, a score of stomach fullness, and the converted into prosome length and then into body volume proportion of krill with empty stomach (Fig. 3A). For using the equations in Karlson and Ba˚mstedt (1994) and krill from South Georgia and the Scotia Sea, there is a clear Mauchline (1998). seasonal cycle in all of these parameters. The mass of the Items were grouped into three main categories—Algae, digestive gland decreases toward winter (June–August) but Protozoan, and Metazoan—comprising 15 food types. The increases again in spring. Likewise, average winter score 22 Schmidt et al.

Fig. 3. Euphausia superba, seasonal and regional differences in (A) feeding activity, (B) fatty acid trophic indicators, and (C) body reserves. The fatty acid 16:4(n-1) is characteristic for diatoms, 18:4(n-3) is synthesized by autotrophic and heterotrophic flagellates, and the 20:1 and 22:1 isomers derive from copepods. Each of the symbols represents a pooled sample of 10 individuals with the same body length. of stomach fullness is 2 (i.e., half full), whereas the score effect of body length (Table 1). Body stores either increased is often 4 (i.e., full) during spring and summer. The significantly with body length only during winter (lipid percentage of krill with an empty stomach is also slightly content of the digestive gland) or did not correlate with increased during winter, reaching , 13% on average. For body length (total amount of PUFA). Score of stomach krill from the Lazarev Sea, seasonal differences in the mass fullness was the only indicator of krill feeding activity that of the digestive gland are less pronounced, but there are correlated repeatedly with body length. Larger krill had a clear differences in the score of stomach fullness (dropping lower score of stomach fullness than smaller krill in the from , 3 in autumn to 0.5 in winter) and the percentage of Lazarev Sea in winter and at South Georgia in summer and krill with empty stomach (increasing from , 5% in autumn autumn. to up to 90% in winter). Thus, feeding activity is reduced The fatty acid trophic indicators showed significant during winter, but this reduction is more severe for Lazarev correlations with krill body length during winter. Both the Sea krill than for those at South Georgia. Krill from the diatom indicator [16:4(n-1)] and the flagellate indicator Bransfield Strait were only sampled during winter, so there [18:4(n-3)] decreased with body length, whereas the is no seasonal trend available. copepod indicator (S20:1, 22:1 isomers) increased (Fig. 4). As a consequence of the lower feeding activity during These trends were seen with the absolute amount of fatty winter, fatty acid trophic indicators (Fig. 3B) and body acids as well as with their relative proportions (Table 1). reserves (Fig. 3C) show a seasonal minimum in spring Interestingly, the furcilia larvae (body length # 10 mm) from (October to early December) in the Lazarev Sea as well as the Lazarev Sea did not match the trend lines seen in at South Georgia. Thus, krill have the lowest lipid content, postlarval krill (Fig. 4A). For some of the larvae the the lowest PUFA reserves, and the lowest mass : length proportions of the diatom indicator were clearly higher than ratio in spring. During summer these stores increase again expected from the body length correlation in postlarval krill. and reach a maximum in late summer and autumn. The same is true for the copepod indicator, whereas the proportions of the flagellate indicator remained below the The effect of body length—To explain some of the values expected from the body length correlation in variability within seasons seen in Fig. 3, we tested for the postlarval krill. This suggests that larval krill have a different Krill feeding and overwintering 23

Table 1. Results of linear regression analysis between krill body length and parameters presented in Fig. 3. The equation and p value are given for parameters, which vary significantly with body length. ns, Not significant.

Winter Summer, autumn Lazarev Sea Bransfield Strait South Georgia Lazarev Sea Scotia Sea South Georgia No. of batches of 10 krill 17 16 19 14 13 22 Body length of krill (mm) 25.5–49.3 29.8–50.6 34.3–45.9 17.6–49.6 32.6–48.1 31.4–55.0 Mass of digestive gland ns ns ns ns ns ns Score of stomach fullness ns ns ns ns n 10 19 R2 0.403 0.635 p 0.049 ,0.0001 y 20.0545x+2.397 20.1162x+7.9658 Krill with empty stomachs ns ns ns ns ns n 19 R2 0.342 p ,0.0001 y 1.2134x–39.64 16:4(n-1) (mg [mg dry mass]21)nsnsnsnsns R2 0.268 p 0.033 y 20.0099x+0.592 16:4(n-1) (% of total FA) ns ns ns ns R2 0.238 0.317 p 0.047 0.012 y 20.0135x+0.8238 20.0175x+1.2332 18:4(n-3) (mg [mg dry mass]21)nsnsns R2 0.286 0.266 0.339 p 0.027 0.041 0.009 y 20.0398x+2.6881 20.0338x+3.2156 20.0573x+3.4968 18:4(n-3) (% of total FA) ns ns ns R2 0.292 0.326 0.671 p 0.025 0.021 ,0.0001 y 20.0502x+3.6076 20.046x+4.108 20.1278x+7.1194 S 20:1, 22:1 (mg[mgdry mass]21) ns ns ns R2 0.246 0.408 0.322 p 0.043 0.008 0.011 y 0.0265x+0.1181 0.054x–0.4449 0.07x–1.6346 S 20:1, 22:1 (% of total FA) ns ns R2 0.741 0.796 0.597 0.393 p ,0.0001 ,0.0001 ,0.0001 0.016 y 0.0491x–0.2267 0.54x–0.1147 0.0908x–1.7628 0.0244x+0.5466 Lipid content of digestive gland (% dry mass) ns ns ns ns R2 0.389 0.403 p 0.007 0.003 y 0.5987x+23.34 0.7757x+5.2802 S PUFA (mg [mg dry mass]21)ns ns nsnsnsns Mass : length ratio R2 0.94 0.977 0.975 0.951 0.495 0.804 p ,0.0001 ,0.0001 ,0.0001 ,0.0001 ,0.0001 ,0.0001 y 0.0072x2.1703 0.0021x2.5465 0.002x2.5181 0.0004x2.3648 0.002x1.9333 0.0001x2.6473 feeding behavior or access different food sources than found in the data from spring, summer, and autumn postlarval krill. (Fig. 4B). Only krill from the Lazarev Sea showed a The strong correlations between fatty acid trophic correlation between the copepod indicator and body length indicators and krill body length seen in winter were not during summer and autumn (Table 1). 24 Schmidt et al.

Fig. 4. Euphausia superba correlations between krill body length and the proportion of three fatty acid trophic indicators in their muscle during (A) winter and (B) spring, summer, and autumn. Fatty acid 16:4(n-1) indicates feeding on diatoms, 18:4(n-3) feeding on autotrophic and heterotrophic flagellates, and 20:1 and 22:1 isomers feeding on copepods. A trend line is shown if correlations are significant. Equations are given in Table 1. Results for krill larvae (3–10 mm body length) are plotted for comparison but are not included in the regression analysis. Each of the symbols represents a pooled sample of 10 individuals with the same body length.

Regional differences in krill overwintering and feeding— significantly lower amounts of PUFA and 18:4(n-3) than Because of the above-mentioned influence of body length those in autumn (77% and 46%, respectively, of the autumn on feeding parameters, we used only data from 40 mm krill value), even though the overall lipid level was slightly for regional comparisons. (1) We compared the autumn-to- higher in winter (107%). Winter krill from South Georgia winter transition for krill from the Lazarev Sea and South had also lower amounts of PUFA (90%), 16:4(n-1) (77%), Georgia (Fig. 5). Winter krill from the Lazarev Sea had and 18:4(n-3) (70%) compared with autumn krill, but for each of these parameters autumn–winter differences were smaller than seen in Lazarev Sea krill. Only the difference in 16:4(n-1) was near significant (p 5 0.05). Winter lipid level and the amount of 20:1, 22:1 isomers were similar to autumn data (98%). (2) We used the winter data from the Lazarev Sea, South Georgia, and Bransfield Strait to check for regional differences in feeding and overwintering. For each of the 12 parameters tested, mean values from the three regions were significantly different (one-way ANOVA; Table 2). Krill from the Lazarev Sea and Bransfield Strait had a larger digestive gland and higher proportion of lipids than krill from South Georgia. The feeding activity was similar for krill from South Georgia and the Bransfield Strait, but the score of stomach fullness and proportion of krill with any food in the stomach were significantly lower for krill Fig. 5. Euphausia superba regional differences in the autumn- from the Lazarev Sea. All three fatty acid trophic indicators to-winter reduction in PUFA and fatty acid trophic indicators were highest in krill from the Bransfield Strait. Krill from compared with lipid levels. The calculations are based on the South Georgia had higher proportions of the fatty acids average autumn and the average winter value for 40 mm krill 16:4(n-1) and 18:4(n-3) than those from the Lazarev Sea, (data in Tables 2 and 3). Significant differences between winter and the proportions of the copepod indicator (S20:1, 22:1 and autumn data are indicated with an asterisk (Lazarev Sea, PUFA: t-test 5 22.42, df 5 7, p 5 0.046; Lazarev Sea, 18:4(n-3): isomers) were similar. Body stores on PUFA and protein t-test 5 23.04, df 5 4, p 5 0.039). Results are only presented for (indicated by the mass : length ratio vs. lipid content) were the Lazarev Sea and South Georgia because the Bransfield Strait highest in krill from the Bransfield Strait, followed by krill has not been sampled during autumn. from South Georgia. Table 2. Euphausia superba mean values (6 1 standard deviation [SD]) of parameters indicating feeding activity, diet, and body reserves of 40 mm krill sampled during winter in the Lazarev Sea (L), Bransfield Strait (B), or South Georgia (S). One-way ANOVA was used to test for overall differences between the mean values (p , 0.05), whereas the ranking of the three regions was based on t-tests. 16:4(n-1), diatom-indicating fatty acid; 18:4(n-3), flagellate-indicating fatty acid; S 20:1, 22:1 isomers, copepod- indicating fatty acids.

Lazarev Sea Bransf. Strait South Georgia One-way ANOVA Two-sample t-test

Date Jun–Aug 2006 Jun–Jul 2006 Jul–Aug 2005, Jul 2006 F25 p Comparison t df p Number of stations 8 8 10 Stomach fullness (score 0–4) 0.460.2 1.660.5 2.160.6 27.04 ,0.0001 B.L 6.72 9 ,0.0001 S.L 27.79 11 ,0.0001 Krill with empty stomach (%) 75.7610.1 16.3611.7 13.4611.3 84.6 ,0.0001 L.B 210.89 13 ,0.0001 L.S 12.35 15 ,0.0001 Body length (mm) 39.260.6 39.660.5 39.860.5 overwintering and feeding Krill Developmental stage and gender* J, MS FS, MS FS, MS Mass of digestive gland (% dry mass) 7.261.3 8.662.1 5.061.0 13.75 ,0.0001 L.S 3.93 12 0.002 B.S 4.59 9 0.001 16:4(n-1) (mg [mg dry mass]21 ) 0.260.1 0.660.1 0.460.1 38.49 ,0.0001 B.L 8.01 11 ,0.0001 S.L 25.34 15 ,0.0001 B.S 4.34 11 0.001 16:4(n-1) (% total fatty acids) 0.260.1 0.760.1 0.660.1 63.02 ,0.0001 B.L 10.91 12 ,0.0001 S.L 28.67 15 ,0.0001 B.S 3.44 13 0.004 18:4(n-3) (mg [mg dry mass]21 ) 1.060.2 1.760.2 1.260.3 13.61 ,0.0001 B.L 6.08 13 ,0.0001 B.S 3.53 15 0.003 18:4(n-3) (% total fatty acids) 1.560.2 2.160.3 2.060.3 8.94 0.001 B.L 4.63 12 0.001 S.L 23.31 15 0.005 S 20:1, 22:1 isomers (mg [mg dry mass]21 ) 1.160.4 1.660.4 1.260.4 3.76 0.039 B.L 2.69 13 0.018 B.S 2.31 15 0.036 S 20:1, 22:1 isomers (% total fatty acids) 1.760.2 2.160.2 1.960.3 3.75 0.039 B.L 3.28 12 0.007 Lipid content digestive gland (% dry mass) 47.463.2 48.462.6 36.363.8 38.84 ,0.0001 L.S 6.73 15 ,0.0001 B.S 8.09 15 ,0.0001 S PUFA (mg [mg dry mass]21 ) 19.765.2 25.863.3 20.964.2 4.68 0.02 B.L 2.83 11 0.016 B.S 2.81 15 0.013 Mass : length ratio (mg mm21 ) 20.162.1 25.661.7 22.360.6 24.89 ,0.0001 B.L 5.52 13 ,0.0001 S.L 22.47 7 0.043 B.S 5.46 7 0.001 * Stages of sexual maturity after Makarov and Denys (1981): J, juveniles (secondary sexual characteristics—petasmae and thelycum—are not visible); FS, subadult female (thelycum is present, but without color); MS, subadult male (developing petasma is visible but not fully developed, ejaculatory ducts not colored). 25 26 Schmidt et al.

Fig. 6. Euphausia superba principal component analysis of food types and lithogenic particles in krill stomach content. Food types were expressed as percentage of the total food volume in the stomach, whereas for lithogenic particles, the absolute number per stomach was used. Score plots (left) project individuals from different regions onto the PC1–PC2 plane. The fraction of unconstrained variance accounted for by each axis is given in brackets. Loading plots (right) indicate the importance of each food type for determining the scores. Food types that align together on the PC1–PC2 plane were likely ingested at the same time. Score plot and loading plot for (A) winter data from the Bransfield Strait, Lazarev Sea, and South Georgia; (B) spring, summer, and autumn data from the Lazarev Sea, Scotia Sea, and South Georgia; (C) pooled winter, spring, summer, and autumn data when food types are divided into three main categories: algae, protozoan, and metazoan. Taxonomic details of the food types are given in Methods. Each symbol represents one individual.

(3) We compared the stomach content of krill from Lazarev Sea were feeding on copepods or on mixtures of different regions. Principal component analysis clearly the diatom Fragilariopsis sp., spiny diatoms, and hetero- separates winter krill from the Bransfield Strait, the trophs such as foraminifera, heterotrophic flagellates, Lazarev Sea, and South Georgia (Fig. 6A). Krill from the cnidaria (indicated by nematocysts), and nauplii. In Krill feeding and overwintering 27

copepods. Therefore, regional differences in krill stomach fullness might partly be explained by a different feeding periodicity between filter-feeding phytoplankton or seabed detritus on one hand and catching large copepods or exploiting locally rich ice biota on the other. Using stomach content data from summer and autumn, the separation of Lazarev Sea and South Georgia krill on the principal component (PC)1–PC2 plane remains, where- as krill from the Scotia Sea overlap with both (Fig. 6B). The diet of krill from the Lazarev Sea was again dominated by Fragilariopsis sp., spiny diatoms, and foraminifera, but not by copepods. At this time of year, feeding on copepods was characteristic of krill from South Georgia, usually in combination with lithogenic particles and diatom debris. If not feeding on seabed material and copepods, the krill diet at South Georgia comprised the diatom Eucampia sp., tintinnids, and heterotrophic flagellates. Comparing sea- sons, Lazarev Sea krill fed more on algae in summer than in winter, whereas those from South Georgia fed more on heterotrophic food during summer than winter (Tables 2, 3). Krill from the Scotia Sea were on average the most herbivorous during spring and summer. Overall, most of the 289 analyzed krill contained mainly algae in their stomach (Fig. 6C). Metazoan or protozoan dominated the diet of , 22% of all krill. An almost exclusive diet of metazoans was occasionally found in winter and autumn. Based on the total identified food volume, the average proportion of the three categories was: Fig. 7. Euphausia superba feeding on copepods. (A) Fre- 71% algae, 17% protozoan, and 12% metazoan (Table 4). quency of copepod mandible width found in krill stomachs from the Lazarev Sea (58 mandibles) and South Georgia (59 mandibles) The effect of phytoplankton abundance and sea ice cover during autumn and winter. (B) Equivalent total volume of on krill diet—To study potential changes in krill diet ingested copepods. See Methods for details on the calculations. depending on the feeding environment, fatty acid trophic The data represent only the stomach content, not the absolute indicators in krill muscle were plotted against ambient feeding rates, because these also depend on gut passage time. concentration of phytoplankton (SeaWiFS-derived Chl a) and sea ice cover. However, slightly different data sets were contrast, the diet of krill from the Bransfield Strait and used for the two parameters. The correlations with Chl a South Georgia was characterized by diatom debris and include mainly data from spring and summer (due to lithogenic particles, either in combination with benthic absence of winter and some autumn data), whereas for the diatoms and tintinnids (Bransfield Strait) or with discoid correlation with sea ice, we used data from the Bransfield diatoms and autotrophic flagellates (South Georgia). Strait (winter), Lazarev Sea (late spring, autumn, winter), Overall, winter krill from the Lazarev Sea contained more and Scotia Sea (spring, summer) but excluded krill from the heterotrophic food than those from the Bransfield Strait or permanently ice-free South Georgia. The correlations South Georgia (Table 2). At South Georgia, krill also between fatty acid trophic indicator and Chl a remained ingested copepods during winter, but these were mainly relatively consistent regardless of whether the Chl a data Oithona sp. (total body length , 0.5 mm), which did not were derived from the sampling date or were integrated account for a big volume, whereas in the Lazarev Sea, krill over the last 1, 3, or 5 weeks (data not shown). In contrast, were feeding on a range of copepod sizes, including correlations between fatty acid trophic indicators and ice copepodite stages of the large C. propinquus (body length cover became stronger when data were integrated over 3 or 1.3–2.2 mm; Fig. 7). 5 weeks. Therefore we used Chl a data from the time of The number of krill with food in their stomachs was low sampling, but ice cover data that had been integrated over in the Lazarev Sea (L) in winter, but those that had been the previous 5 weeks. Correlations including only 40 mm feeding contained, on average, an order of magnitude more krill (data not shown) or all postlarval krill showed the digestible material than krill from the Bransfield Strait (B) same trends and similar coefficients of determination (R2). or South Georgia (S) (L: 6.26 6 11.3 3 1022 mm3 ind.21;S However, the latter are based on a higher number of and B: 0.74 6 0.67 3 1022 mm3 ind.21; t 5 2.48, degrees of samples and are therefore presented here. freedom [df] 5 25, p 5 0.02). This is because in the Both the diatom indictor [16:4(n-1)] and the copepod Bransfield Strait and at South Georgia, krill fed on diatom indicator (S20:1, 22:1 isomers) became more abundant in debris mixed with indigestible lithogenic particles, whereas the total fatty acid pool when Chl a concentrations in the Lazarev Sea, it was on ice biota or voluminous increased (Fig. 8A). However, the proportion of the diatom 28 Schmidt et al.

Table 3. Euphausia superba mean values (6 1 SD) of parameters indicating feeding activity, diet, and body reserves of 40 mm krill sampled during spring, summer, and autumn in the Lazarev Sea at South Georgia or in the Scotia Sea.

Lazarev Sea Lazarev Sea South Georgia South Georgia Scotia Sea Scotia Sea Dec Apr Jan, Feb 2002, Mar 2004, Nov Jan, Feb 2005 2004 2003, 2005, 2006 Apr 2007 2006 2003 No. of stations 2 5 9486 Stomach fullness (score 0–4) 2.661.3 2.660.8 3.860.2 3.460.5 3.560.8 3.760.4 Krill with empty stomach (%) 11.966.8 4.167.5 2.364.9 5.365.1 1.564.3 1.061.5 Body length (mm) 39.560.8 39.960.4 40.260.8 39.560.5 40.160.4 40.060.8 Developmental stage and gender* FS, FA1, MS J, MS J, MS, FS J, MS, FS J, FS, FA1, FA2, J, FS, FA1, MS, MA2 FA2, MS Mass of digestive gland (% dry mass) 11.060.9 8.562.2 10.662.3 6.961.8 9.462.9 13.963.7 16:4(n-1) (mg [mg dry mass]21) 0.0560.02 0.260.1 0.460.1 0.560.1 0.160.2 0.560.2 16:4(n-1) (% total fatty acids) 0.160.1 0.360.1 0.760.2 0.760.1 0.360.3 0.260.2 18:4(n-3) (mg [mg dry mass]21) 0.260.1 2.260.9 1.160.4 1.760.6 0.560.4 2.261.1 18:4(n-3) (% total fatty acids) 1.160.0 2.460.6 1.860.7 2.560.6 1.561.0 1.060.5 S 20:1, 22:1 isomers (mg[mgdrymass]21) 0.260.0 1.460.3 1.360.7 1.260.4 0.460.3 1.260.5 S 20:1, 22:1 isomers (% total fatty acids) 0.860.1 1.660.2 1.960.6 1.760.2 1.060.4 0.760.6 Lipid content of digestive gland 8.160.4 44.565.5 28.267.6 37.164.7 11.564.4 19.9612.4 (% dry mass) S PUFA (mg [mg dry mass]21) 7.764.2 25.664.8 20.564.7 23.464.0 13.564.1 18.466.9 Mass : length ratio (mg mm21) 16.761.0 25.162.7 25.664.4 22.761.0 18.961.8 22.664.4 * Stages of sexual maturity after Makarov and Denys (1981): FS, subadult female (thelycum is present, but without color); FA1, adult female 1 (thelycum is bright red, no spermatophore attached); MS, subadult male (developing petasma is visible but not fully developed, ejaculatory ducts not colored);J, juveniles (secondary sexual characteristics—petasmae and thelycum—are not visible); FA2, adult female 2 (thelycum is brownish-red due to attached spermatophore, body not swollen); MA2, adult male 2 (petasma is fully developed, ejaculatory ducts are red, spermatophores are formed). indicator increased more quickly; therefore, the copepod juveniles in the 31–45 mm size classes (male [M]: 28%, vs. diatom ratio [S20:1, 22:1 isomers/16:4(n-1)] decreased. female [F]: 17%, juvenile [J]: 55%), whereas in winter, there Different trends are seen with increasing ice cover. In were hardly any juveniles in these size classes but mainly under-ice habitats, the proportion of the diatom indicator subadult males and subadult females (M: 54%,F:45%,J: in krill muscle decreased, and the proportion of the 1%; Fig. 9A). This suggests that juveniles developed into copepod indicator remained the same (Fig. 8B). As a males and females over the winter. In the Bransfield Strait, consequence, the copepod vs. diatom ratio [S20:1, 22:1 very few juveniles were in the size classes 31–45 mm during isomers/16:4(n-1)] increased with ice cover. This suggests winter (M: 30%,F:65%,J:5%; Fig. 9B), although in that under sea ice, copepods become relatively more the Lazarev Sea, juveniles were still abundant, but the important as a food source for krill, whereas high proportion of females was low (M: 53%,F:12%,J:35%; phytoplankton abundances favor the role of diatoms. Fig. 9C). Therefore, we suggest that in the Lazarev Sea, the process of krill development from juveniles to adults, in Implications of reduced winter feeding and a copepod- particular females, is delayed during winter. dominated diet—A further difference between krill from the One possible explanation for this delayed development Lazarev Sea and either South Georgia or the Bransfield might be the loss of PUFA during winter. Figure 5 shows Strait was seen in the developmental stage and gender of that krill from the Lazarev Sea have significantly less krill sampled during winter. In summer and autumn, krill PUFA in winter than in autumn, whereas this seasonal catches from South Georgia had a high proportion of difference is less pronounced in krill from South Georgia.

Table 4. Euphausia superba proportion of algae, protozoans, and metazoans in the total volume of identified food items in krill stomach content from different regions and seasons. n, No. of individuals dissected.

Region Season n % Algae % Protozoan % Metazoan Lazarev Sea Winter 26 51636 17620 32640 Summer, autumn 30 75627 11616 14624 South Georgia Winter 22 83620 76510619 Summer, autumn 144 64631 22627 14627 Bransfield Strait Winter 19 69625 27625 4612 Scotia Sea Spring, summer 48 84617 13615 366 Overall 289 71629 17621 12625 Krill feeding and overwintering 29

Fig. 8. Euphausia superba correlations between diet and ambient conditions. (A) In situ Chl a concentration at the time of krill sampling. None of the winter data are included in this plot, as satellite data on Chl a were not available. (B) Percentage of sea ice cover over the last 5 weeks before krill sampling. Data from South Georgia were not included in this plot because South Georgia is ice-free year- round. Fatty acid 16:4(n-1) indicates feeding on diatoms, the 20:1 and 22:1 isomers indicate feeding on copepods, and the S20:1, 22:1 isomers/16:4(n-1) ratio gives the relative importance of copepods vs. diatoms. Each of the symbols represents a pooled sample of 10 individuals with the same body length.

Following on from this observation, we correlated the Discussion amount of PUFA reserves against the relative importance of copepods vs. diatoms in the krill diet. The PUFA content Krill overwintering: Business as usual, quiescence, reduced by about 50% from the lowest to the highest ratio or flexibility?—For Euphausia superba the months Novem- between copepod- and diatom-indicating fatty acids [S20:1, ber to March are the prime time of year; this is when 22:1 isomers/16:4(n-1)] in krill tissue (Fig. 10). This females spawn (Spiridonov 1995) and postlarvae grow suggests that the ingestion of diatoms rather than fastest (Kawaguchi et al. 2006). Both processes rely on a copepods favors the uptake or conservation of PUFA in sufficient food quantity and quality, which for E. superba is the krill lipid pool. However, the copepod vs. diatom ratio best met during phytoplankton blooms (Cuzin-Roudy and not only reflects food quality but, to some extent, food Labat 1992; Atkinson et al. 2006). However, in most parts quantity as well, in that high ratios of S20:1, 22:1 isomers/ of the Southern Ocean, these blooms only last for 1– 16:4(n-1) are often associated with low Chl a concentra- 3 months (Fig. 1; Arrigo et al. 2008), leaving krill to a long tions (Fig. 8A). The PUFA content in krill tissue also ‘‘overwintering’’ period. Regarding their overwintering correlates with the score of stomach fullness, but this three broad theories exist: (1) Winter conditions are not a correlation is less strong (R2 5 0.12, p , 0.0001) than that problem for krill. They find sufficient alternative food (e.g., between PUFA content and the ratio of copepod- vs. copepods and ice algae) and carry on feeding and growing as diatom-indicating fatty acids (S20:1, 22:1 isomers/16:4(n- usual (i.e., business as usual; Huntley et al. 1994); (2) food is 1), R2 5 0.233, p , 0.0001). Both factors, a copepod- always depleted during winter, and krill are genetically dominated diet and starvation, might lead to reduced adapted by entering a state of metabolic depression. PUFA levels in krill tissue. This winter depression is mediated by photoperiod and 30 Schmidt et al.

Fig. 9. Euphausia superba regional differences in the proportion of males, females, and juveniles within different length classes of krill during summer, autumn, winter, and spring. (A) South Georgia and Scotia Sea, (B) Bransfield Strait, and (C) Lazarev Sea. characterized by very low feeding activity regardless the In the present study, the seasonal cycles in lipid and actual food abundance (i.e., quiescence; Teschke et al. 2007; PUFA content and mass : length ratio (Fig. 3C) indicate Meyer 2012); or (3) there are local differences in food that winter food consumption is insufficient to balance abundance during winter, and krill overwintering strategies metabolic losses and that krill require body reserves. This vary accordingly. If available, they will feed efficiently on ice was true for krill from the Lazarev Sea (L) as well as algae, copepods, or seabed detritus. Alternatively, they can from South Georgia (S). Most of the lipid content of the survive on body reserves and reduced metabolism (i.e., digestive gland was lost between winter and spring (S: flexibility; Nicol 2006). reduction from 36% of dry mass to , 11%; L: from 47% of dry mass to , 8%). These data resemble earlier findings from the Lazarev Sea and Weddell Sea (Hagen et al. 2001). Because krill oocytes only start to grow in size in response to feeding on phytoplankton blooms (Cuzin-Roudy and Labat 1992), most of the lipid reserves must have been used for overwintering rather than reproduction. Therefore, the theory of Huntley et al. (1994) that krill rarely starve during winter has to be rejected. Even when krill carry on feeding during winter, food quantity, quality, or both seems to be suboptimal. Our findings for krill feeding activity during winter differ between South Georgia, the Bransfield Strait, and the Lazarev Sea (Table 2). More than 80% of krill from South Georgia and the Bransfield Strait contained food in their stomachs, and , 20% had a full stomach, whereas in the Lazarev Sea, only , 25% had been feeding and only 4% were scored with ‘‘full’’ stomachs. The proportions of fatty Fig. 10. Euphausia superba correlation between the content of PUFA and the S20:1, 22:1 isomers/16:4(n-1) ratio in lipids of acid trophic indicators [16:4(n-1), 18:4(n-3), S 20:1,22:1 krill muscle tissue. Grey dots indicate larval krill and black dots isomers] were also lower in Lazarev Sea krill (Table 2), postlarval krill. Each of the symbols represents a pooled sample of confirming that food uptake was more reduced in the 10 individuals with the same body length. Lazarev Sea than in the Bransfield Strait or at South Krill feeding and overwintering 31

Georgia. However, the photoperiod was similar at our of offspring), which illustrates that the energy balance of sampling stations in the Lazarev Sea (60–65uS, July– adult krill during winter can affect the population develop- August 2006, 5.5–8.5 h of daylight) and Bransfield Strait ment in the following spring and summer. (62–63uS, June–July 2006, 4.5–5.5 h of daylight), but longer at South Georgia (53–54uS, July–August 2005, 2006, 7.5– Krill feeding: Copepods as a supplementary or switch 9.5 h of day light). This suggests that photoperiod did not a food?—In feeding experiments, krill often ingest large priori determine the feeding activity of these krill. Whereas numbers of copepods (Price et al. 1988; Huntley et al. krill in the Lazarev Sea might have been in a status of 1994) and prefer feeding on copepods rather than physiological depression or inactivity, with only a few of phytoplankton (Price et al. 1988; Atkinson and Sny¨der them feeding opportunistically, the high proportion of krill 1997). However, in stomachs of freshly caught krill, with food in their stomachs at South Georgia and the copepod remains are relatively rare (Atkinson et al. 2002; Bransfield Strait suggests an active search for food. Schmidt et al. 2006). In this study, we examined the This contrasts with findings from the laboratory or stomach content of 289 postlarval krill from a wide range onboard-ship incubations, where krill show a very clear of regions and seasons and found on average 1 6 2 response to different light regimes in terms of feeding copepod mandibles stomach21 (equal copepod volume: (Teschke et al. 2007), maturation (Teschke et al. 2008; 0.009 6 0.04 mm3), with a maximum of 18 mandibles Brown et al. 2011), and gene expression (Seear et al. 2009). stomach21 (0.38 mm3 volume). When fed with the copepod In all of these studies, krill seem to shut down (low feeding- D. forcipatus (body length , 1.4 mm) in the laboratory and metabolic rates, fast rate of maturity regression, down- (Schmidt unpubl.), krill contained 20–30 mandibles stom- regulation of genes involved in metabolism, molting, and ach21 (, 0.36 mm3 volume). Thus, a very small proportion muscle use) when kept in continuous darkness compared of the in situ krill had been feeding on copepods to a similar with high or moderate light levels, but identical food extent as seen in the laboratory. Reasons might be that in concentrations. Thus, while photoperiod governs metabolic open waters krill employ a different feeding behavior or output in krill in the laboratory, most likely by synchro- copepods have a better chance to escape. nizing an endogenous clock (Teschke et al. 2011), the effect Results from our stomach content analysis suggest that is less clear in the wild. In situ, krill might gain important algae (diatoms and autotrophic flagellates) are the main environmental clues during their diurnal vertical migra- food for krill, accounting on average for 71 6 29% of the tions—a key aspect of krill behavior that is suppressed in identified food volume in krill stomachs. Protozoa or laboratory confinements. These additional clues–e.g., fine metazoa dominated the stomach content of about one- gradients in light intensity or ‘‘smell’’ of food (Schmidt quarter of the krill but played overall a smaller role 2010)—might adjust responses that are otherwise mediated (protozoa: 17 6 21%, metazoa: 12 6 25%). Other studies by photoperiod. Interestingly, the average amplitude of found the autotrophic component of the krill diet to be less krill vertical migrations is much larger in winter compared important: 22% 6 21% in summer (Perissinotto et al. with other seasons (Siegel 2005) and leads krill to potential 2000); 48% in autumn (Hopkins and Torres 1989); 20–49% feeding grounds under the ice (Flores et al. 2012) and at the in winter (Hopkins et al. 1993a) and 33–56% in spring seabed (Kawaguchi et al. 1986). (Hopkins et al. 1993b). Perissinotto et al. (2000) compared Our results show that krill employ different overwinter- the total amount of carbon in the stomach content with the ing strategies in different habitats—either relying mainly on proportion derived from algae. This approach most likely body reserves (Lazarev Sea) or on continuous feeding underestimates the role of algae because of pigment (South Georgia) or on a combination of both (Bransfield degradation (especially if gut passage is slow) and because Strait). Intensive winter feeding can occur in productive the stomach content includes wall material and enzymes shelf areas, where the seabed is rich in organic matter, even derived from krill rather than the food. Like our study, during winter (Smith and DeMaster 2008), and where those of Hopkins and Torres (1989) and Hopkins et al. migrations to the seabed are relatively short. Over deep (1993a,b) involved the microscopic examination of stomach ocean, food might be more patchy, and migration distances content. However, we tried to obtain quantitative estimates to the seabed are long. Therefore, the role of body reserves by counting and measuring food items in detail, whereas increases. How this flexibility is realized in accordance with Hopkins and Torres (1989) and Hopkins et al. (1993a,b) krill’s endogenous timing system and external signals, such recorded only the presence or absence of food categories as photoperiod, is still not completely understood. Further but studied a large range of zooplankton and micronekton attention has to be paid to the implications of different species and derived conclusions from their comparison in overwintering scenarios. In the Lazarev Sea, for instance, we clustering procedures. noticed that the winter population was short of adult krill, in Regardless of the approach, together the studies show particular females (Fig. 9). Thus, the lack of food and loss of that the relative importance of autotrophic vs. heterotro- PUFA during winter might have caused a delayed develop- phic food varies with season and sampling location. We ment from juveniles to adults. Moreover, physiological used the proportion of fatty acid trophic indicators in krill models suggest that females that grow during winter can tissue to follow the change in their diet depending on reach a body length of 53 mm at the end of their third year, phytoplankton availability and sea ice cover (Fig. 8). The whereas those that shrink will only be of , 40 mm proportion of both the diatom indicator [16:4(n-1)] and the (McClatchie 1988; Candy and Kawaguchi 2006). Body size copepod indicator [S 20:1,22:1 isomers] increased with is a predictor for various fitness parameters (e.g., the number rising Chl a concentrations. No correlation was found 32 Schmidt et al. between the lipid content of the tissue and the Chl a and might be unable to access ice biota in the small brine concentration (R2 5 0.067), which suggests that the channels. However, they have been observed breaking off simultaneous rise in the fatty acid trophic indicators is algae from the ice underside in spring, when communities are due to feeding rather than increased lipid stores. A different more developed (Marschall 1988). pattern was found with sea ice cover. The proportion of When feeding on ice biota, larval krill have not only diatom indicator decreased with increasing ice cover, access to diatoms, but also to copepods, as indicated by whereas the proportion of copepod indicator remained high proportions of the S 20:1,22:1 isomers in their tissue constant. On the basis of these results, we have to reject the (Fig. 4A) and copepod mandibles in their stomachs common hypothesis that krill switches to heterotrophic (including the ice copepod S. longipes; Meyer et al. 2009). food sources such as copepods when phytoplankton is With increasing body length of postlarval krill, the role of rare (Huntley et al. 1994; Atkinson et al. 2001). Instead, diatoms and flagellates as a winter food source reduces copepods seem to be a consistent part of the krill diet gradually, whereas that of copepods increases (Fig. 4A). during phytoplankton blooms, outside of blooms and These trends were not only seen in Lazarev Sea krill, but under sea ice. The uptake of diatoms was more variable; it also in those from the ice-free Bransfield Strait and South showed a steep increase in higher phytoplankton concen- Georgia (Fig. 4A). As the filtering area of the feeding trations but a reduction with increasing ice cover. As a basket increases by a factor of four when krill grow from 20 consequence, diatoms were relatively more important as a to 50 mm (Suh and Nemoto 1987), it could be assumed that food source for krill in phytoplankton blooms, whereas the retention efficiency of small items reduces at the same the role of copepods increased under sea ice. The latter time as catching copepods becomes more successful. observation is supported by previous studies on stomach However, in E. superba the minimum distance between content and fatty acid composition of adult winter krill filtering setae remains consistently small (, 2–3 mm), even (Hopkins and Torres 1989; Ju and Harvey 2004; O’Brien in large krill (Suh and Nemoto 1987). This means that their et al. 2011). filtering efficiency on small items is not a function of body The positive correlation between the proportion of the length. Thus, the simultaneous drop in the proportion of copepod indicator (S20:1, 22:1 isomers) in krill tissue and the diatom- and flagellate-indicating fatty acids (Fig. 4A) the ambient Chl a concentration (Fig, 8A) is mainly driven and increase in the copepod indicator cannot be explained by data from South Georgia. Excluding South Georgia by continuous filter feeding but must mean that growing data, the plot would still show a weak positive trend, but no krill spend increasingly more time in a raptorial feeding significant correlation (n 5 22, R2 5 0.05, p 5 0.31). At mode during winter. This ontogenetic switch to copepods South Georgia, phytoplankton and copepod abundances might reduce food competition among postlarval krill. are higher than in many other parts of the Southern Ocean However, outside of winter, similar trends with body length (Atkinson et al. 2001), and krill feeding on copepods has were not seen (Fig. 4B). During summer, adult krill might previously been suggested for this (Pakhomov et al. not be able to afford missing out on alga blooms because 1997). Our stomach content analysis shows that during they supply high-quality food for gonad maturation summer, krill were either feeding on a mixture of the (Cuzin-Roudy and Labat 1992). diatom Eucampia spp., tintinnids, and heterotrophic One potential drawback of feeding mainly on copepods flagellates or on copepods, lithogenic particles, and diatom might be the loss of PUFA. Krill with low S 20:1,22:1 debris (Fig. 6B). The latter combination of food items has isomers/16:4(n-1) ratios contained up to twice as much been identified as feeding on or near the seabed (Schmidt PUFA in their lipid stores as krill with high ratios (Fig. 10). et al. 2011). This behavior might be triggered by high The difference is substantial when considering that temperatures in surface water, as is typical for South individuals investing in development and growth have a Georgia in summer (Whitehouse et al. 2008) and could high demand on PUFA (Pond et al. 1996). The trend might explain why krill fed on copepods even though phyto- either be caused by the lower food uptake associated with plankton was abundant. an increased role of copepods in winter or reflect different During the cruise in the Lazarev Sea in June–August metabolic pathways when digesting these food sources. 2006, larval krill had been feeding on ice algae at three out of Support for the latter comes from long-term feeding four stations, as indicated by the high proportions of the incubations of krill in the laboratory. Individuals contained diatom marker 16:4(n-1) in their tissues (Fig. 4A). Postlarval more structural lipids (polar lipids including PUFA) when krill also contained plenty of algae in their stomachs at 3 out fed with a diatom species but produced more storage lipids of 10 stations. These krill were all small juveniles (20–30 mm (triacylglycerol) when the diatom source was partly body length), whereas larger krill from the same catch replaced by clam tissue (Hagen et al. 2007). This contained , 20 times less algae. This indicates that the ice observation cannot be explained by different PUFA levels algae distribution was patchy in the sampling area and that of the diet because both the diatom and the clam were rich larger krill did not feed on them even if available. The latter in PUFA (. 34% of total fatty acids [FA]; Hagen et al. has been suggested previously on the basis of diver’s 2007). It needs further studies to confirm whether krill observations (Daly and Macaulay 1991), stomach content metabolize lipids from diatoms and copepods in a different (Atkinson et al. 2002), and fatty acid composition (Schmidt way. Neither copepods nor ice biota can generally be et al. 2012). Compared with larvae and early juveniles, larger considered a PUFA-rich diet because their PUFA contents krill face a higher risk of predation from diving seals and are highly variable (10–60% of total FA; Kattner et al. penguins, do not require continuous feeding during winter, 1994; Ju and Harvey 2004; O’Brien et al. 2011) and overlap Krill feeding and overwintering 33

Fig. 11. Euphausia superba cumulative length frequency of individuals $ 40 mm within each of the nine habitats defined in Fig. 1. Data are from ‘‘krillbase’’ (Atkinson et al. 2009). The plot is constructed from a total of 326,716 individual krill sampled with scientific nets within these boxes. Data span throughout the year but are mainly from spring, summer, and autumn (Atkinson et al. 2009). In the legend, the regions are ordered by the body length which includes 95% of the $ 40 mm population, starting with the smallest value (50 mm, , i.e., fewest very large individuals) and ending with the highest values (58 mm, South Georgia, i.e., most very large individuals). with values reported for phytoplankton (9–55% of total Schnack-Schiel 2001). Thus, in terms of mortality, Oithona FA; Skerratt et al. 1995). spp. is probably the copepod genus most affected by krill, Little is known about which copepod species krill feed whereas in terms of ingested volume, C. propinquus is the on in situ (Hopkins and Torres 1989). Here we used the key species for krill in the Lazarev Sea. The copepod width and morphology of mandible remains in krill species C. propinquus, C. acutus, Metridia gerlachei, and stomachs to conclude copepod size and identity (Karlson Oithona spp. all contain high proportions of the 20:1 or and Ba˚mstedt 1994; Michels and Schnack-Schiel 2005). 22:1 fatty acid isomers (Kattner et al. 1994; Cripps and Hill Of 269 encountered mandibles, 65% had a small mandible 1998; Ju and Harvey 2004), which we used as a trophic width (10–30 mm, calculated copepod prosome length: indictor for copepods. , 0.15–0.4 mm), 29% had a medium width (35–100 mm, prosome length: , 0.44–1.0 mm), and 6% were large (100– Regional differences: The pros and cons of living in 190 mm, prosome length: , 1.2–2.2 mm). Over 50% of the productive shelf areas—Winter imposed more hardship on small mandibles derived from the cyclopoid copepod krill in the Lazarev Sea than on those in the Bransfield Strait Oithona spp. It has been suggested that this small copepod or at South Georgia, as indicated by their lower amounts of is passively caught by euphausiids when they filter feed on fatty acid trophic indicators and PUFA, lower mass : length phytoplankton (Schmidt 2010). Feeding on copepods was ratios and a delayed development from juveniles to subadult rare in the Bransfield Strait, and the few encountered females. These differences are most likely caused by poorer mandibles were of Oithona spp. In krill from South feeding conditions in the Lazarev Sea. With no ice cover at Georgia, the medium-sized mandibles belonged mainly to South Georgia and the Bransfield Strait sampling sites, low the copepods D. forcipatus, Metridia spp., and C. citer, levels of primary production would have occurred in the whereas the few large mandibles were of C. acutus. In the water column, even in June and July (Arrigo et al. 2008), and Lazarev Sea, most of the medium-sized mandibles and all supplied krill with some phytoplankton. Also, krill from of the large-sized mandibles derived from C. propinquus. these habitats appear to have fed at the seabed (Schmidt et This species inhabits the higher latitudes of the Southern al. 2011), which can be rewarding in highly productive shelf Ocean and is the only large copepod species that remains areas, even during winter (Smith and DeMaster 2008). In active in surface waters, even during winter (Pasternak and contrast, the Lazarev Sea is deep oceanic (, 4500 m) and 34 Schmidt et al. was heavily covered with ice for . 5 weeks at the time of stock living over deep ocean (Atkinson et al. 2008). sampling. Some larvae and juveniles contained ice biota in Therefore, addressing regional differences in life cycle their stomachs, but many postlarvae were empty. The fatty parameters (e.g., length of the spawning season, number acid trophic indicators suggest that feeding on copepods of offspring per female, the growth rate of larval and becomes relatively more important when krill overwinter juvenile krill) and potential transport within the ocean under sea ice. currents is essential to predict future development of the How do these regional differences in feeding conditions circumpolar krill populations. scale up to population processes? It has previously been noticed that krill from the southeastern Weddell Sea are of Acknowledgments smaller maximum body length than those from the Special thanks to B. Meyer, H. Flores, and E. Pakhomov Antarctic Peninsula (Siegel et al. 1990). Following on from whoprovidedfrozenkrillfromtheirLazarevSeacruisesandto this observation, we examined the body length spectrum of C.Charman,S.Clarke,M.Collins,L.Jones,A.Prior,J.Roe, krill . 40 mm from the nine regions introduced in Fig. 1. K. Ross, G. Tarling, and J. Watt for sampling krill in the The plot shows that krill from South Georgia and the Bransfield Strait, Scotia Sea, and at South Georgia. We thank M. Biszczuk for preparing the map in Fig. 2. The satellite ocean western Antarctic Peninsula grow largest, followed by krill color data are courtesy of the NASA SeaWiFS project. The from the Scotia Sea, Bransfield Strait, and Cooperation length frequency data were provided by the ‘‘krillbase’’ Sea, whereas krill from the Mawson, Cosmonaut, Somov, database. We thank all those who contributed to this database and Lazarev remain smaller (Fig. 11). and M. Jessopp for compiling it. Comments from S. Nicol and These trends in body length probably reflect two three anonymous reviewers were much appreciated. This study regional features: the annual length of the phytoplankton was funded by the Natural Environment Research Council bloom period during which krill can achieve high growth grant NE/F01547X/1. rates and the feeding conditions during the remaining, longest part of the year during which krill either grow References slowly, do not grow, or even shrink. Interestingly, the ARRIGO, K. R., G. L. VAN DIJKEN, AND S. BUSHINSKY. 2008. regions where krill grow largest (South Georgia, the Primary production in the Southern Ocean, 1997–2006. western Antarctic Peninsula, the Scotia Sea, and the J. Geophys. Res. 113: C08004, doi:10.1029/2007JC004551 /Prydz Bay) are all characterized by ATKINSON, A., B. MEYER,D.STU¨ BING,W.HAGEN,K.SCHMIDT, extensive shelf areas (, 1000 m water depth) or close AND U. V. BATHMANN. 2002. Feeding and energy budgets of connections to extensive shelf areas. Living in these areas has Antarctic krill Euphausia superba at the onset of winter—II. a twofold advantage for krill. Phytoplankton bloom periods Juveniles and adults. Limnol. Oceanogr. 47: 953–966, are relatively long (Fig. 1), because benthic iron diffusion doi:10.4319/lo.2002.47.4.0953 and sediment resuspension can repeatedly supply iron into ———, AND R. SNY¨ DER. 1997. Krill-copepod interactions at South surface waters (de Jong et al. 2012). In contrast, wintertime Georgia, Antarctica, I. Omnivory by Euphausia superba. 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