Deep-Sea Research II 49 (2002) 1881–1907

Salp/krill interactions in the Southern Ocean:spatial segregation and implications for the carbon flux

E.A. Pakhomova,*, P.W. Fronemanb, R. Perissinottoc a Department of Zoology, University of Fort Hare, P/Bag X1314, Alice 5700, South Africa b Southern Ocean Group, Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa c School of Life and Environmental Sciences, University of Natal, Durban 4041, South Africa

Abstract

Available data on the spatial distribution and feeding ecophysiology of Antarctic krill, Euphausia superba, and the tunicate, Salpa thompsoni, in the Southern Ocean are summarized in this study. Antarctic krill and salps generally display pronounced spatial segregation at all spatial scales. This appears to be the result of a clear biotopical separation of these key species in the Antarctic pelagic food web. Krill and salps are found in different water masses or water mass modifications, which are separated by primary or secondary frontal features. On the small-scale (o100 km), Antarctic krill and salps are usually restricted to the specific water parcels, or are well segregated vertically. Krill and salp grazing rates estimated using the in situ gut fluorescence technique are among the highest recorded in the Antarctic pelagic food web. Although krill and salps at times may remove the entire daily primary production, generally their grazing impact is moderate (p50% of primary production). The regional ecological consequences of years of high salp densities may be dramatic. If the warming trend, which is observed around the Antarctic Peninsula and in the Southern Ocean, continues, salps may become a more prominent player in the trophic structure of the Antarctic marine ecosystem. This likely would be coupled with a dramatic decrease in krill productivity, because of a parallel decrease in the spatial extension of the krill biotope. The high Antarctic regions, particularly the Marginal Ice Zone, have, however, effective physiological mechanisms that may provide protection against the salp invasion. r 2002 Elsevier Science Ltd. All rights reserved. Re´ sume´

Les observations disponibles sur la distribution spatiale et l’ecophysiologie! de l’alimentation du krill antractique, Euphausia superba, et du tunicier Salpa Thompsoni dans l’Ocean! Austral sont synthetis! ees! dans cette etude.! Le krill et les salpes presentent! une distribution qui se traduit en gen! eral! par une forte segr! egation! spatiale, a" toutes les echelles! d’espaces. Ceci semble etre# le resultat! d’une separation! claire des niches ecologiques! de ces deux especes" cles! du reseau! trophique antarctique. Le krill et les salpes sont observes! dans des masses d’eau differentes! qui sont separ! ees! par des frontieres" primaires et secondaires. A petite echelle! (o100 km), soit le krill antarctique et les salpes sont habituellement localisee! dans des parcelles d’eaux specifiques,! ou alors ils sont separ! es! verticalement. Les vitesses de broutage du krill et des salpes, estimees! en utilisant la technique de fluorescence in situ, sont parmi les plus elev! ees! rencontrees! au sein du reseau! trophique pelagique! antarctique. Bien que le krill et les salpes peuvent parfois consommer l’ensemble de la production primaire journaliere," l’impact de leur activite! de broutage est gen! eralement! moder! e(! p50% de la production primaire). Les consequences! ecologiques! regionales! d’annees! caracteris! ees! par des fortes densites! de salpes peuvent etre#

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

0967-0645/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved. PII:S 0967-0645(02)00017-6 1882 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 dramatiques. Si la tendance au rechauffement,! qui est observee! autour de la Peninsule! Antarctique et dans l’Ocean! Austral, continue, les salpes pourraient jouer un role# plus important dans la structuration des ecosyst! emes" marins antarctiques. A cela serait probablement associe! une diminution dramatique de la productivite! du krill, en raison d’une diminution de l’extension spatiale du biotope du krill. Cependant, aux hautes latitudes, et en particulier dans la zone marginale des glaces, il existe des mecanismes! physiologiques effectifs qui pourraient offrir une certaine protection vis a" vis d’une invasion par les salpes.

1. Introduction 1993a; Park and Wormuth, 1993; Kawamura et al., 1994; Nishikawa et al., 1995). With the exception The Antarctic krill, Euphausia superba, and the of only few areas, such as Antarctic Peninsula tunicate, Salpa thompsoni, are among the most region, spatial exclusion between Antarctic krill important filter-feeding metazoans of the Southern and salps has been widely documented (Pakhomov Ocean, ranking only after copepods in terms of et al., 1994a; Hosie, 1994; Voronina, 1998). Studies total dry pelagic biomass (Pages, 1997; Voronina, on the community structure of zooplankton 1998). These two species are also recognized as conducted in the vicinity of the Greenwich microphages of key importance, as they are able to meridian have indicated that Antarctic krill and efficiently re-package small particles into large fast salps may overlap in their distribution south of the sinking feces, thereby playing a major role in Antarctic Polar Front (Fransz and Gonzalez, channeling biogenic carbon from surface waters 1997; Pakhomov et al., 2000). Feeding studies into the long-living pools and to the ocean’s conducted in this region provided evidence that interior and seafloor (Huntley et al., 1989; Fortier these species may at times consume the entire daily et al., 1994; Schnack-Schiel and Mujica, 1994; primary production (Dubischar and Bathmann, Pakhomov et al., 1997; Le Fevre" et al., 1998; 1997; Perissinotto et al., 1997; Perissinotto and Perissinotto and Pakhomov, 1998a). As a conse- Pakhomov, 1998a; Froneman et al., 2000). Unlike quence, the ecological role of these two key species for case of krill, for which there are numerous data in the Antarctic pelagic food web has recently on its feeding ecology, there are still large gaps in received much attention (e.g., Nishikawa et al., our understanding of the biology and the ecologi- 1995; Siegel and Loeb, 1995; Siegel and Harm, cal role of salps in the Southern Ocean (Le Fevre" 1996; Dubischar and Bathmann, 1997; Loeb et al., et al., 1998). The aims of this paper are to 1997; Kawaguchi et al., 1998; Perissinotto and summarize studies on the trophic ecophysiology Pakhomov, 1998b; Ross et al., 1998). It has been of Antarctic krill and of the tunicate S. thompsoni, suggested that krill and salps may be in direct with particular emphasis to the tunicates, and to competition with one another in certain areas of discuss the phenomenon of krill/salp spatial the Antarctic Peninsula (Loeb et al., 1997) and in separation. the Lazarev and Cooperation Seas (Perissinotto and Pakhomov, 1998a, b). It also was tentatively postulated that if the increase in seawater tem- 2. Materials and methods perature, already observed in the Antarctic Penin- sula region, continues (Zwally, 1991; Rott et al., Data on ingestion rates of Antarctic krill, E. 1996), salps may spread into the high Antarctic superba, and of the tunicate, S. thompsoni, regions, with important implications for the estimated using the gut fluorescence technique regional carbon flux and the Antarctic food web were obtained mainly during the three expeditions structure (Perissinotto and Pakhomov, 1998a, b). to the southern part of the Atlantic sector of the In the Southern Ocean, S. thompsoni is generally Southern Ocean:(a) the second cruise of the South restricted to the warmer water masses (Voronina, African Antarctic Marine Ecosystem Study 1984; Nast, 1986; Siegel et al., 1992; Pakhomov, (SAAMES II) conducted aboard the mv SA E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1883

Agulhas along the Greenwich Meridian (WOCE CmÀ2) and from 1 to 1200 mg C mÀ2 (mean SR2 line) in January 1993 (Perissinotto et al., 1997; 2207320 mg C mÀ2) in the regions of dense and Froneman et al., 2000; Pakhomov et al., 2000); (b) low krill concentrations, respectively (Voronina, the SAAMES IV aboard the mv SA Agulhas in the 1998). Lazarev Sea during December 1994–January 1995 Although Southern Ocean tunicates have not (Froneman et al., 1997; Perissinotto and Pakho- been targeted specifically, over the past two mov, 1998a, b); (c) the joint Scandinavian/South decades a substantial amount of data on S. African Antarctic Research Expedition aboard the thompsoni density has been accumulated in differ- mv SA Agulhas along the 61E meridian between ent sectors of the Southern Ocean (Table 1). In 491S and 601300S (Pakhomov, 2002; Pakhomov summary, these data indicate extreme variability in and Froneman, 2002a, b). salp densities across the Southern Ocean (Table 1). In addition, numerous published and unpub- Nevertheless, throughout much of the area south lished sources (mentioned throughout the text) on of 401S, S. thompsoni densities remain moderate, krill and salps ingestion rates, abundances, bio- on average varying between o0.1 and 30 mg mass and distribution in the Southern Ocean were CmÀ2, or between o0.1 and 30 ind mÀ2. However, used for this synthesis. To convert wet weight into S. thompsoni densities in the Antarctic Peninsula carbon weight, the following conversion factors region, particularly in the Bransfield Strait and were used:(a) S. thompsoni dry weight was around Elephant Island, were found to be assumed to be 4% of wet weight, and carbon consistently elevated (Table 1). Furthermore, the weight was assumed to be 4.3% of dry weight secondary frontal systems that demarcate low and (Ikeda and Mitchell, 1982; Ikeda and Bruce, 1986; high latitude water masses around the Antarctic Hagen, 1988; Huntley et al., 1989; Donnelly et al., Continent, e.g., Weddell–Scotia Confluence, 1994); (b) E. superba dry weight was assumed to be Warm Counter Weddell Current in the Lazarev 22% of wet weight, and carbon weight assumed to Sea, the northern part of the Ross Sea, also be 45% of dry weight (Ikeda and Mitchell, 1982; showed enhanced densities of S. thompsoni. Ikeda and Bruce, 1986; Torres et al., 1994). To Foxton (1966) first mentioned this phenomenon, convert chlorophyll values into carbon values a e.g., an increased biomass of S. thompsoni at the standard chlorophyll/carbon ratio of 50 was northern limit of Antarctic krill distribution. In the applied (Booth et al., 1993). regions of high salp densities, average concentra- tions generally ranged from 22 to 1115 mg C mÀ2 and from 20 to 800 ind mÀ2, with a maximum 3. Euphausia superba and Salpa thompsoni: biomass level of 2.5 g C mÀ2 observed in the densities and distribution northern Ross Sea (Voronina et al., 1993) and abundance of ca 6000 ind mÀ2 off the Adelie Coast 3.1. Krill/salp densities: importance in the Antarctic (Chiba et al., 1998). The mean S. thompsoni pelagic ecosystem biomass, estimated using average values presented in Table 1, is 72.17189 mg C mÀ2 (N ¼ 54). There is a great deal of uncertainty in estimating For comparison, mean copepod biomass in the total stocks of Antarctic krill and salps in the Southern Ocean is estimated at E1161 mg C mÀ2. Southern Ocean due to their extremely patchy This value was obtained from Voronina (1998) by distribution (e.g., Miller and Hampton, 1989; assuming that dry weight is equivalent to 15% of Voronina, 1998). The most recent revision of wet weight and that carbon weight accounts for Antarctic krill biomass estimates obtained using 43% of dry weight (Ikeda and Mitchell, 1982; scientific and commercial trawls was presented by Ikeda and Bruce, 1986; Donnelly et al., 1994). Voronina (1998, Tables 2–4). After converting wet From the above comparative biomass estimates weight into carbon, the average biomass of E. of the three large Antarctic metazoan filter-feeder superba throughout the Southern Ocean ranges groups, it is obvious that the tunicates do not play from 400 to 37800 mg C mÀ2 (mean 595071110 mg a major role in terms of total carbon biomass. 1884 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907

Table 1 Biomass and abundance of the tunicate Salpa thompsoni in the Southern Ocean

Location Date Sampling Biomass Abundance Source depth (m) (mgC mÀ2) (ind mÀ2)

Mean Range Mean Range

Elephant Island Nov 1983 0–200 nd nd 31.7 0.8–123.4 Nast (1986) Nov 1984 0–200 nd nd 1.1 0–12.8 Nast (1986) Mar 1985 0–200 nd nd 25.0 0.1–177.8 Nast (1986) Mar 1989 0–200 65.3 F nd F Pakhomov (1993b) Jan–Feb 1988 0–160 nd nd 25.6 nd Park and Wormuth (1993) Jan–Feb 1989 0–160 nd nd 92.8 nd Park and Wormuth (1993) Jan–Feb 1990 0–160 nd nd 801.6 nd Park and Wormuth (1993) Jan 1992 0–160? nd nd 15.1 0–197 AMLR (1994) Jan 1993 0–160 nd nd 194.1 1.1–2573 AMLR (1994) Feb–Mar 1993 0–160 nd nd 253.7 0.4–2666 AMLR (1994) Jan 1994 0–160 nd nd 149.1 1.5–765 AMLR (1994) Feb–Mar 1994 0–160 nd nd 79.2 0.8–380 AMLR (1994) summers 1975–95 ? nd nd nd 1.2–3489* Loeb et al. (1997) Jan 1994 ? 570.6 0–3277 nd nd Loeb et al. (1997) Jan 1995 ? 7.8 0–75.3 nd nd Loeb et al. (1997) Jan 1996 ? 20.2 0–134.2 nd nd Loeb et al. (1997) Mar–Apr 1998 0–200? 1383 nd nd nd Minkina et al. (1999)

Antarctic Peninsula Nov–Dec 1983 0–600 409.2 272.4– nd nd Torres et al. (1984) 591.1 Feb 1982 0–300 nd nd 12.3 0–228.6 Piatkowski (1985) Mar 1984 0–200 183.5 44–671 nd nd Huntley et al. (1989) Mar 1993 0–120 9.8 nd nd nd Ross et al. (1998) Jan–Feb 1994 0–120 29.5 nd nd nd Ross et al. (1998)

Drake Passage and Dec 1983–Jan 1984 0–200 23.8 0.04–207.7nd nd Witek et al. (1985) Bransfield Strait

Bransfield Strait Mar 1989 0–200 221.1 F nd F Pakhomov (1993b) South Shetland Isl Dec 1990–Jan 1991 0–100 22.3 0–151.4 17.8 0–132 Nishikawa et al. (1995) Jan–Feb 1991 0–100 9.9 0–147.3 3.2 0–30 Nishikawa et al. (1995)

South Georgia Jan 1991 0–200 0.003 F nd F Piatkowski et al. (1994) Jan 1991 0–1000 0.02 F nd F Piatkowski et al. (1994)

APF, Scotia Sea Jan 1991 0–200 49 F nd F Piatkowski et al. (1994) Jan 1991 0–1000 71.2 F nd F Piatkowski et al. (1994)

WSC Jan 1994 0–200 nd 115–2930 nd nd Alcaraz et al. (1998) Northern Weddell Nov–Dec 1983 0–200 4.5 nd 17.5 nd Lancraft et al. (1989) Southern Scotia Seas Nov–Dec 1983 0–1000 49.5 nd 145.3 nd Lancraft et al. (1989) Mar 1986 0–200 5.9 nd 4.3 nd Lancraft et al. (1989) Mar 1986 0–1000 6.8 nd 5.6 nd Lancraft et al. (1989) Aug 1988 0–200 0.6 nd 0.23 nd Lancraft et al. (1991) Aug 1988 0–1000 6.8 nd 1.0 nd Lancraft et al. (1991) Oct–Nov 1988 0–60 0.01 nd 6.1 nd Siegel et al. (1992)

Eastern Weddell Feb 1988 0–500 11.6 nd nd nd Makarov and Solyankin (1990)

Gyre (EWG):ACC E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1885

Table 1 (continued)

Location Date Sampling Biomass Abundance Source depth (m) (mgC mÀ2) (ind mÀ2)

Mean Range Mean Range

EWG:ACC+WW Feb 1988 0–500 124.1 nd nd nd Makarov and Solyankin (1990) EWG:WCWC Feb 1988 0–500 711.8 nd nd nd Makarov and Solyankin (1990) Weddell Sea Feb–Apr 1989 0–200 0.07 0–0.32 nd nd Pakhomov (1993b) Southern Weddell Feb–Mar 1983 0–300 13.2 nd 12.3 nd Boysen-Ennen and Sea Piatkowski (1988), Boysen-Ennen et al. (1991) Lazarev Sea Jan–Feb 1990 0–200 6.6 0–45.7 22.1 0–189.2 Pakhomov et al. (1994a) Dec 1994–Jan 1995 0–300 nd nd 150.1 0–1220 Perissinotto and Pakhomov (1998b)

AS:APF Jan–Feb 1993 0–300 4.1 nd 7.3 nd Pakhomov et al. (1994a, b) AS:STC FAPF Dec 1979–Jan 1980 surface 0.004 nd o0.01 nd Pakhomov and McQuaid (1996) AS:APF F60–651S Dec 1979–Jan 1980 surface 0.03 nd 0.2 nd AS:0 1, 46–691S Jan 1993 0–300 5.97 0–45.1 41.4 0–222.6 Pakhomov et al. (2000) AS:6 1E, 49–651S Dec 1997–Jan 1998 0–300 17.5 0–126.9 44.1 0–402 Pakhomov (2002) Kerguelen Islands Feb–Mar 1988 0–150 1.1 0–22.0 2.4 0–39.7 Pakhomov (1995) Ob and Lena banks Nov–Dec 1986 0–500 7.3 nd nd nd Pakhomov (1993c)

Prydz Bay Region Feb–Mar 1985 0–52 6.2 nd 2.15 nd Pakhomov (1991) (PBR) Dec 1985–Jan 1986 0–59 0.1 nd 0.3 nd Pakhomov (1991) Feb–Mar 1986 0–67 7.7 nd 2.6 nd Pakhomov (1991) Feb–Mar 1987 0–124 0.4 nd 0.33 nd Pakhomov (1991) Dec 1987–Mar 1988 0–150 7.9 nd 7.2 nd Pakhomov (1991) Feb–Mar 1989 0–200 0.31 nd 3.2 nd Pakhomov (1991)

PBR:OC Jan 1985 0–200 nd nd 23–98 nd Hosie (1994) PBR:OC Mar 1987 0–200 nd nd 5.4 nd Hosie (1994) PBR:OC Jan–Feb 1993 0–200 nd nd 0.33 nd Hosie et al. (1997) PBR:TC Jan 1985 0–200 nd nd 1.4 nd Hosie (1994) PBR:TC Mar 1987 0–200 nd nd 0.4 nd Hosie (1994) PBR:NC Jan–Feb 1993 0–200 nd nd 0.06 nd Hosie et al. (1997) PBR:south of 65 1S Jan–Feb 1991 0–200 0000Hosie and Cochran (1994) Enderby Land Apr 1988 0–200 30.3 nd 29.3 nd Pakhomov (1991)

Cosmonaut Sea Jan–Feb 1987 0–159 0.2 nd 0.9 nd Pakhomov (1991) Feb 1988 0–100 0.5 nd 1.6 nd Pakhomov (1991) Feb 1989 0–200 0.1 nd 1.7 nd Pakhomov (1991) Mar–Apr 1989 0–200 o0.01 nd o0.1 nd Pakhomov (1991)

Pacific Sector (PS) Dec 1980 0–300 26.8 0–100.0 nd nd Maruyama et al. (1982) Feb 1981 0–250 5.7 0–24.9 nd nd Maruyama et al. (1982)

PS:APF–AD Jan–Feb 1981 surface 0.21 nd 0.22 nd Pakhomov and McQuaid (1996) Wilkes Land Jan–Feb 1996 0–200 8.15 0.2–44.5 nd Max 5975 Chiba et al. (1998) East Antarctica Jan–Feb 1996 0–200 28.2 0–904 19.7 0–714 Hosie et al. (2000) 1886 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907

Table 1 (continued)

Location Date Sampling Biomass Abundance Source depth (m) (mgC mÀ2) (ind mÀ2)

Mean Range Mean Range

Ross Sea, 671S Feb–Mar 1992 0–200 1115 522–2547 nd nd Voronina et al. (1993) Bellingshausen Sea Feb–Mar 1994 0–200 0.2 nd nd 0–10.2 Siegel and Harm (1996)

ACC, Antarctic Circumpolar Current waters; WW, Weddell Sea waters; WCWC, Warm Counter Weddell Current; APF, Antarctic Polar Front; STC, Subtropical Convergence; AD, Antarctic Divergence; OC, Oceanic Community; TC, Transitional Community; NC, Neritic Community; WSC, Weddell–Scotia Confluence; AS, Atlantic sector; nd, no data; *Fabundance expressed as ind 1000 mÀ3.

Similar results could be obtained using estimates 100% of the total stock for these filter-feeders in the 80% Southern Ocean provided by Voronina (1998). 60%

Voronina (1998) showed that in terms of fresh 40% mass, salps are the main contributors to total stock Contribution 20% in the Southern Ocean, followed by copepods and 0% Antarctic krill (Fig. 1). However, in terms of dry

and carbon mass, copepods were identified as the mass Carbon pellet Faecal Dry mass Wet mass

most important and salps the least important production Production (Fig. 1). The main argument of Voronina is that copepods Antarctic krill salps Antarctic krill is neither first in total metazoan Fig. 1. Comparative role of major metazoan filter-feeders in the biomass nor in production, as in both cases it is Southern Ocean. Wet and dry masses are taken from Voronina second to the herbivorous copepods (Voronina, (1998). Carbon mass calculated from dry mass assuming that 1998). Unlike for Antarctic copepods and krill, carbon accounts for 4.3%, 43% and 45% dry weight of salps, S. copepods and krill, respectively (see Sections 2 and 3.1). Annual there are no annual production estimates for production of copepods and krill is taken from Voronina thompsoni available in the literature. However, it is (1998), while production of salps was calculated assuming a P/B known, that salps exhibit the fastest individual coefficient of 1 (see Section 3.1 for explanation). Faecal pellet growth rates among metazoans (Heron, 1972; production was calculated as follows:for copepods assuming Heron and Benham, 1984). Although salp abun- average daily ration of 10% of body carbon and assimilation efficiency of 70%; for Antarctic krill assuming average egestion dance maxima are short-lived, the P/B coefficient À1 À1 rate of 8.143 mg C mgDW d (Table 3); for S. thompsoni of a one-year life cycle would likely exceed one assuming egestion rate of 10.2% of carbon mass per day (Fraser, 1962; Foxton, 1966) and reach 3 (N.M. (Huntley et al., 1989). Voronina, personal communication). As a conse- quence, salp contribution to total filter-feeder production should be substantial, probably rank- ing second only to that of copepods. As salps play 1998). One of the most important features of the an increasingly important role in the Antarctic macro-scale distribution of Antarctic krill is the ecosystem, studies on the production of S. typical increase in density in two different zones of thompsoni are urgently required. the Southern Ocean (Makarov and Spiridonov, 1993). The southern circumpolar belt of high krill 3.2. Krill/salp distribution density is restricted to the Antarctic Coastal Current (East Wind Drift), north of the shelf edge 3.2.1. Large-scale distribution and above the upper part of the continental slope. Despite uncertainties in the small-scale distribu- The northern belt of high krill density is associated tion of Antarctic krill, the large-scale distribution with the secondary frontal zones (Maslennikov, of this species is relatively well documented (Miller 1980, 1995), where waters of high latitudes are and Hampton, 1989; Knox, 1994; Voronina, mixed with waters of the Antarctic Circumpolar E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1887

Current. Apart from the Weddell Sea, where the Antarctic zooplankton biomass’’. Following an northern belt is strongest, this area is not as increase in the occurrence of dense salp concentra- continuous as the southern one, but it can be tions around the Antarctic Peninsula and South distinctly identified around the Antarctic Con- Georgia, the author tentatively hypothesized that tinent in the Bellingshausen, Lazarev, Riiser- the increase in population size of salps over the Larsen, Cosmonaut, Cooperation and Dumont vast range of the Southern Ocean over the past D’Urvile Seas (e.g., Makarov and Sysoeva, 1983; several decades may have been in response to the Williams et al., 1983, 1986; Iganake et al., 1984; change in the Antarctic marine ecosystem (Kawa- Hampton, 1985; Miller, 1986, 1987; Shirakihara mura, 1987). As the number of publications et al., 1986; Bibik et al., 1988; Miquel, 1991; documenting mass salp occurrences in different Pakhomov, 1993a, b). regions of the high Antarctic recently has in- Unlike its southern counterpart, the northern creased dramatically (e.g., Huntley et al., 1989; belt of high krill density exhibits an asymmetrical Park and Wormuth, 1993; Voronina et al., 1993; pattern in distribution (Marr, 1962; Mackintosh, Pakhomov et al., 1994a; Nishikawa et al., 1995; 1973). For instance, in the Atlantic sector, waters Loeb et al., 1997; Perissinotto and Pakhomov, of high krill biomass are associated with the north 1998a, b; Chiba et al., 1998, 1999), we have tried to branch of the Weddell Gyre (Weddell–Scotia re-construct a similar map of S. thompsoni Confluence), which deflects southward east of distribution using all data available (published Bouvet Island (Marr, 1962; Maslennikov, 1980). and unpublished) from 1980 till 1998 (Fig. 3). The Accordingly krill, which are found in the Atlantic striking difference between the recent map and sector as far north as 511S, are not generally that presented by Foxton in 1966 is that S. recorded north of 59–601S in eastern Antarctica thompsoni is now regularly found at high latitudes, (Marr, 1962; Miller and Hampton, 1989). including the southern parts of the Bellingshausen, A detailed map showing the spatial distribution Weddell and Lazarev seas, and the belt of its dense of S. thompsoni in the Southern Ocean was first concentrations extends further south to E651S provided by Foxton (1966) who used a compre- (Fig. 3). In our opinion, this increase in distribu- hensive collection of Discovery expeditions con- tion may underline dramatic changes in the ducted between 1925 and 1951 (Fig. 2). On the Antarctic marine environment. basis of Foxton’s (1966) data, the northern limit of Warming trend over the past 40 years has been S. thompsoni distribution appears to coincide with demonstrated for the Antarctic Peninsula region the mean position of the Subtropical Convergence, (Gloersen and Campbell, 1991; Zwally, 1991; Rott while the southern limit is generally shaped by the et al., 1996). This is linked to an increase in the ice-edge (Foxton, 1966). At that stage, a belt of average percentage of open water in the form of elevated densities of S. thompsoni was restricted to leads and polynyas, to the disintegration of ice- the region between 45 and 601S (Fig. 2). It is shelves, and to a decrease in areal and seasonal evident that S. thompsoni was absent or found in extent of sea-ice cover (Doake and Vaughan, 1991; very low numbers in the waters of high latitudes, Gammie, 1995; Vaughan and Doake, 1996; particularly in waters of Weddell Sea origin Hewitt, 1997). Furthermore, the warming trend (Foxton, 1966). These data were subsequently has shown some correlation with an increase in supported by the addition of a data set collected salp occurrence and with a decrease in krill stock between 1956 and 1958 by Russian expeditions (Loeb et al., 1997; Naganobu et al., 1999). There is aboard the RV Ob’ (Fig. 2, see Voronina, 1998 for evidence for the warming in the Arctic region and details). off the Antarctic Peninsula (Johannessen et al., After comparing the zooplankton densities 1995; Vaughan and Doake, 1996) as well as at recorded during the BIOMASS expeditions with some sub-Antarctic islands (Smith and Steen- those from the Discovery results, Kawamura kamp, 1990; Smith, 1991). Most recently, warming (1986) stated ‘‘that behavior of salp population of the World Ocean, including the Southern should be considered very important in total Ocean, has been demonstrated (Levitus et al. 1888 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907

300 W 00 300 E

STC 400 S

AC 0E 60 0 0 60 W

600 S

WEDDELL SEA 800 S 0E 90 0 0 90 W

ROSS SEA 2 E 120 0 0 120 W

1 2 3 4 5

1500 W 1800 1500 E

Fig. 2. Horizontal distribution of S. thompsoni in the Southern Ocean after Foxton (1966) with addition of data sets collected during Russian expeditions onboard the RV Ob’ in March–May 1956, February–March 1957 and March–May 1958 (after Voronina, 1998). 1, negative; 2, 1–100 (o1); 3, 101–1000 (1–10); 4, 1001–10000 (11–100); 5, >10000 (>100) individuals per 20 min tow (gWW mÀ2 for Russian data).

2000). Although the warming signals are not 1998a, b). More importantly, an increase in salp monotonic, they were found to be consistent in abundance may be coupled with a dramatic fall in each ocean basin (de la Mare, 1997; Levitus et al., krill stock and productivity due to a decrease in 2000). Therefore, since S. thompsoni is considered the spatial extension of the krill biotope (Pakho- a warm-water species, data presented in Fig. 3 may mov, 2002), which in turn will affect the Antarctic indicate that large-scale warming of high Antarctic marine food web and krill resource management regions is in progress. If the hypothesis is correct (Loeb et al., 1997). In light of this, it is worth (still remains to be proven), the change in salp noting that the most recent Antarctic krill stock distribution may have very important implications estimates, ca 61 106–155 106 tonnes (Nicol for the high Antarctic ecosystem. The occurrence et al., 2000a), are about half of those previously of salps in high latitudes may change the regional estimated, ca 100 106–600 106 tonnes (Ross carbon flux (Perissinotto and Pakhomov, and Quetin, 1986). This, however, may be linked E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1889

300 W 00 300 E

STC 400 S

AC 0E 60 0 0 60 W

600 S

WEDDELL SEA 800 S 0E 90 0 0 90 W

ROSS SEA 2 E 120 0 0 120 W

1 2 3 4 5

1500 W 1800 1500 E

Fig. 3. Horizontal distribution of S. thompsoni in the Southern Ocean using published and unpublished literature sources covering period from 1980 till 1998. 1, negative; 2, 1–10 (o1); 3, 11–100 (1–10); 4, 101–1000 (11–100); 5, >1000 (>100) ind mÀ2 (or gWW mÀ2). Sources used:unpublished data of the Southern Ocean Group, Rhodes University (South Africa) along the transect between the Prince Edward Islands and Madagascar, Pakhomov, unpublished along 451,501 and 801E transects; published:Boysen-Ennen and Piatkowski (1988), Boysen-Ennen et al. (1991), Brinton (1984), Casareto and Nemoto (1986), Chiba et al. (1998), Huntley et al. (1989) Makarov and Solyankin (1990), Maklygin and Pakhomov (1993), Maruyama et al. (1982), Nast (1986), Nishikawa et al. (1995), Pakhomov (1989, 1991, 1993a, b, 1995, 2002), Pakhomov and Froneman (2000, 2002a), Pakhomov and McQuaid (1996) Pakhomov et al. (1994a, b, 2000), Park and Wormuth (1993) Perissinotto and Pakhomov (1998a, b) Piatkowski (1985, 1987) Piatkowski et al. (1994), Ross et al. (1998), Siegel and Harm (1996), Voronina (1998), and Voronina et al. (1993).

to the development of better or more accurate Wind Drift assemblage, where copepods, salps and assessment techniques/models. small euphausiids dominate; (2) the seasonal pack- ice assemblage, where Antarctic krill is the most 3.2.2. Meso-scale distribution important species; and (3) the permanent pack-ice Hempel (1985) described three major zooplank- assemblage. Meso-scale community structure stu- ton associations south of the Antarctic Polar dies conducted in different sectors of the Southern Front (APF). These are:(1) ice-free oceanic West Ocean provided many of the data to support 1890 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907

0.4 1.5 Hempel’s subdivision. These clearly showed that Euphausia superba Salpa thompsoni Antarctic krill and S. thompsoni are dominant ) ) AIBF -3 -3 1.2 species in different zooplankton assemblages, 0.3 1993 which belong to specific water masses or modifica- 0.9 tions (Brinton, 1984; Nast, 1986; Huntley et al., 0.2

1989; Lancraft et al., 1989; Makarov and Solyan- 0.6 kin, 1990; Siegel and Piatkowski, 1990; Siegel et al., 0.1 0.3

1992; Pakhomov, 1993a, b; Pakhomov et al., Krill abundance (ind.m Salp abundance (ind.m 1994a, 2000; Hosie, 1994; Nishikawa et al., 1995; Chiba et al., 1998; Minkina et al., 1999). There is 0 0 46 48 50 52 54 56 58 60 62 64 66 68 70 growing evidence in the literature to suggest that Latitude (South) the ice-edge may represent a natural boundary 0.06 1.8 between the distribution of S. thompsoni and that Euphausia superba Salpa thompsoni ) of Antarctic krill (Foxton, 1966; Brinton, 1984; ) 0.05 AIBF 1.5 -3 Torres et al., 1984; Ainley et al., 1988; Siegel et al., -3 1997/98 1992). The importance of the frontal zone asso- 0.04 1.2 ciated with the winter northern limit of the 0.03 0.9 seasonal pack ice, Antarctic Ice Boundary Front (AIBF, after Klyausov, 1993), has recently been 0.02 0.6 Krill abundance (ind.m recognized (Grachev, 1991; Pakhomov and 0.01 0.3 Salp abundance (ind.m McQuaid, 1996; Pakhomov and Froneman, 2002a). From an oceanographic point of view, 0 0 48 50 52 54 56 58 60 62 64 66 the AIBF coincides with the disappearance of the Latitude (ûSouth) subsurface cold-water layer that separates the high Fig. 4. Horizontal distribution pattern of E. superba and S. latitude waters from the warmer water masses thompsoni along the Greenwich Meridian during January 1993 affected by the ACC (Klyausov, 1993; Pakhomov (top, data extracted from Pakhomov et al., 2000) and along the et al., 2000). Ecologically, the AIBF represents the 61E meridian during December 1997–January 1998 (bottom, northern limit of Antarctic krill distribution and data extracted from Pakhomov, 2002) in the top 300 m layer. the southern limit of the mass development of AIBF:Antarctic Ice Boundary Front after Klyausov (1993). small gastropods of the genus Limacina (Grachev, 1991). The front also coincides with the sharp decline in S. thompsoni populations to the south 1998; Nicol et al., 2000b). It is evident that on such (Pakhomov, 1989, 1993a; Pakhomov and occasions S. thompsoni populations are restricted McQuaid, 1996; Pakhomov et al., 2000). to the warm water intrusions or layers (Fig. 5; High-resolution studies, conducted in the Atlan- Boysen-Ennen and Piatkowski, 1988; Makarov tic sector of the Southern Ocean along the Green- and Solyankin, 1990; Pakhomov, 1991, 1993a; wich and the 61E meridians, have shown that the Pakhomov et al., 1994a). This is confirmed by the spatial overlap in distribution of Antarctic krill significant positive correlation observed between and S. thompsoni is minimal and occurs only integrated average seawater temperature and S. within the AIBF region (Fig. 4). There are, thompsoni densities in the Lazarev Sea (Pakhomov however, records showing that S. thompsoni may et al., 1994a; Pakhomov and Perissinotto, unpub- occur as far south as 681S in the Lazarev Sea lished), in the Cosmonaut Sea (Pakhomov, 1991) (Pakhomov et al., 1994a; Perissinotto and Pakho- and in the Prydz Bay region (Hosie et al., 1997). mov, 1998a, b) and also may be found in the Casareto and Nemoto (1986) were the first to southern parts of Bellingshausen, Weddell, Cos- suggest that at the higher latitudes S. thompsoni monaut and Cooperation seas and off the Adelie exist close to its thermo-physiological limits. This Land (Fig. 3; Boysen-Ennen et al., 1991; Pakho- was recently confirmed by Chiba et al. (1999) using mov, 1991; Siegel and Harm, 1996; Chiba et al., a data set collected off Adelie Land. It was E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1891

Fig. 5. Vertical distribution of temperature and S. thompsoni along 601E and 751E (Indian sector) during summer seasons of 1985 and 1986. Seawater temperature was measured down to 1500 m, while salps were sampled down to 500 m at depth strata:0–25, 25–50, 50– 100, 100–200 and 200–500 m every degree of latitude. Redrawn from Pakhomov (1991). 1, negative; 2, 1–10; 3, 11–100; 4, 101–1000; 5, >1000 ind mÀ2. observed that no solitary forms were found in the study, which show that Antarctic krill and S. high latitudes and that aggregate forms were thompsoni are spatially separated through most of always small in size, thus suggesting that S. the Southern Ocean (Nicol et al., 2000b). Never- thompsoni aggregates were transported into the theless, in the Atlantic sector, particularly in the area, rather than being the result of asexual waters off the Antarctic Peninsula and around reproduction in situ (Boysen-Ennen et al., 1991; South Shetland Islands, Antarctic krill and salps Siegel and Harm, 1996; Chiba et al., 1999). The show some degree of overlap in their summer testing of this hypothesis certainly requires more macro-scale distribution (e.g., Witek et al., 1985; research. Unlike that of S. thompsoni, the distribu- Piatkowski, 1987; Loeb et al., 1997; Ross et al., tion of Antarctic krill is restricted to high 1998). This is hardly surprising as this region is one Antarctic waters masses and its life cycle is closely of the most complex areas of the Southern Ocean, linked to the seasonal sea-ice biotope (Knox, 1994; where water masses of different origin are often Loeb et al., 1997). mixed together (Maslennikov and Solyankin, Analyzing the macro-scale contrasting distribu- 1979; Maslennikov, 1980; Sahrhage, 1988). Recent tion of Antarctic krill and S. thompsoni, Kawa- analysis of long-term data sets on krill biomass, mura et al. (1994) suggested that this could not be krill spawning and recruitment, salp biomass and explained by either behavioral functions of organ- sea-ice cover in the vicinity of the Elephant Island isms, such as swarm formation, or ecological has revealed significant correlation between these regimes, such as competitive exclusion. They parameters (Loeb et al., 1997). It has been hypothesized that the marked inverse distribution postulated that winters characterized by poor of salps and krill might be related to the water sea-ice cover would promote extensive salp blooms mass structure in the areas investigated. This and poor krill spawning during the following seems to be confirmed by data presented in this summer and, as a consequence, poor krill 1892 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 recruitment the following year. A long-term uptake ranges between 5% and 15% of body warming trend was suggested to be responsible carbon (Table 2). This daily ration can be obtained for the increased occurrence of ‘salp’ years around from phytoplankton only on occasions when Elephant Island (Loeb et al., 1997). Significant chlorophyll-a concentrations are in excess of correlations have been obtained between low 3 mglÀ1 (Table 2). It is now recognized that Antarctic krill biomass and unusually high sea- Antarctic krill exhibits omnivory and carnivory water temperatures in the vicinity of the Antarctic throughout most of the year and can be regarded Peninsula (Priddle et al., 1988; Loeb et al., 1997), as a truly herbivore only during the period of to the extent that during some years salps (mainly spring/early summer phytoplankton blooms (Mill- S. thompsoni) dominated total zooplankton (Mu- er and Hampton, 1989; Perissinotto et al., 1997). jica and Asencio, 1985; Witek et al., 1985; Nast, As a purely phytoplankton diet often does not 1986; Huntley et al., 1989; Siegel and Loeb, 1995; cover even its basic metabolic demands (e.g., Loeb et al., 1997; Minkina et al., 1999). None- Pakhomov et al., 1997; Perissinotto et al., 1997), theless, despite this large-scale overlapping pat- Antarctic krill complement its diet with hetero- tern, during fine-scale surveys conducted off the trophic carbon by consuming on average up to Antarctic Peninsula, particularly around Elephant 80% of total carbon in the form of micro- and Island, a pronounced spatial, horizontal or vertical mesozooplankton (Perissinotto et al., 2000). separation between krill and salps has been Grazing rates of Antarctic krill, as a function of demonstrated in a number of studies (e.g., Nast, food concentration, show different types of 1986; Piatkowski, 1989; Park and Wormuth, 1993; response depending on krill physiological state, Brinton, 1984; Maklygin and Pakhomov, 1993; season, quality and quantity of food (Kato et al., Pakhomov, 1993a, b; Nishikawa et al., 1995; Ross 1982; Schnack, 1985a, b; Helbling et al., 1992). A et al., 1998; Minkina et al., 1999). non-saturating linear response was obtained with chlorophyll-a concentrations of up to 20 mglÀ1 (Price et al., 1988; Ross et al., 1998). A saturation 4. Krill/salp feeding dynamics type of model has also been described on several occasions, particularly in experiments where het- 4.1. Euphausia superba: ingestion and egestion erotrophic food is offered, with upper food rates concentration thresholds of 6–8 mg C lÀ1 (Samy- shev and Lushov, 1983; Krylov, 1989; Ross et al., Despite the numerous attempts to estimate daily 1998). consumption rates in Antarctic krill (see Table 2), Egestion rates of Antarctic krill range consider- ingestion rates obtained using the gut fluorescence ably, between 0.3 and 55 mg C mg dry wtÀ1 dÀ1 technique are not numerous. In situ measured (Table 3), and appear to correlate with the ambient phytoplankton consumption by Antarctic krill chlorophyll-a concentration (Clarke et al., 1988) as varies between 0.06 and 0.62 mg (pigm) indÀ1 dÀ1, well as with the krill mass (Table 3). for specimens o25 mm in length, and between 0.3 and 96.9 mg (pigm) indÀ1 dÀ1 in specimens 4.2. Salpa thompsoni: feeding dynamics >30 mm (Drits and Semenova, 1989; Daly, 1990; Drits and Pasternak, 1993; Pakhomov et al., 1997; One of the goals of this revision is to derive Perissinotto et al., 1997; Pakhomov and Frone- simple predictive models of individual ingestion man, 2002b). The daily carbon rations obtained and egestion rates for S. thompsoni in the Southern using the gut fluorescence method are generally in Ocean. As predictor variables, salp body length the lower range (o5% of body carbon) of and mass were used. Salps are believed to have a estimates calculated employing other techniques non-saturation feeding response to food concen- (Table 2). When the high metabolic activity of tration, as they are probably unable to regulate Antarctic krill is combined with the energetic costs their filtration rates (Perissinotto and Pakhomov, for growth, molting and reproduction, krill carbon 1998a, b). Indeed, a positive trend between S. E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1893

Table 2 Estimates of the daily ration in the Antarctic krill, Euphausia superba

Daily ingestion % of body C Length, stage Conditions, food, method Sources rate (mg C indÀ1 dÀ1)

0.28–5.38 3.97–11.9 18–53 mm Energy budget Chekunova and Rynkova (1974) 0.02–1.92 0.02–1.66 30–50 mm Ingestion rates and energy budget Antezana et al. (1982) after Clarke and Morris (1983) 0.18–0.22 2.9–3.9 19–35 mm In vitro filtration rates with a Kato et al. (1982) culture of Dunaliella 1.47–1.92 1.1–1.5 35–55 mm In vitro filtration rates with a Kato et al. (1982) culture of Dunaliella 4.77–5.72 5.0–6.0 40–50 mm Energy budget Clarke and Morris (1983) 0.43–1.04 0.86–5.63, mean 16–50 mm Radiocarbon method, phytoplankton Samyshev and Lushov (1983) 2.0 cultures and detritus as food 3.6–5.04 2.3–10.0 40–50 mm In vitro filtration and ingestion Boyd et al. (1984) rates with net phytoplankton, furcilia of E. superba and infusoria as food 0.38–2.05 2.6–17.1 30–35 mm In vitro ingestion rates with net Schnack (1985a, b) phytoplankton as food 0.42–1.37 0.8–2.4 40–45 mm In vitro ingestion rates with net Schnack (1985a, b) phytoplankton as food 0.74–2.6 0.9–3.2 50–55 mm In vitro ingestion rates with net Schnack (1985a, b) phytoplankton as food 9.5–17.9 17–28 40–50 mm Faecal pellet evacuation rates using Clarke et al. (1988) net phytoplankton as food 7.64 8.5 20–30 mm Energy budget Price et al. (1988) 0.41–5.07 0.53–5.81 40–55 mm Filtration rates using zooplankton Krylov (1989) and Artemia nauplii as food 1.1–4.4 0.75–3.09 40–55 mm In situ gut pigment contents Ponomareva and Kuznetsova (1989) 8.1–14.4 5.0–7.3 40–55 mm In vitro gut pigment contents Ponomareva and Kuznetsova (1989) 0.18–0.6, max 9.4 0.31–5.76 40–55 mm Gut evacuation and ingestion rates Drits and Semenova (1989)

0.003–0.067 2–52, mean 10 furcilia 3–6 Gut evacuation rates Daly (1990) 0.006–0.026 mean 19.7 calyptopis 1–2 In situ and in vitro filtration rates, Huntley and Brinton (1991) net phytoplankton as food 0.022–0.024 mean 4.4 furcilia 4–5 In situ and in vitro filtration rates, Huntley and Brinton (1991) net phytoplankton as food 0.011 0.05 38–55 mm Gut evacuation and ingestion rates Drits and Pasternak (1993) 6.72–9.12 0.8–3.67 20–40 mm Estimated by model Huntley et al. (1994) 6.12 8.66 47.3 mm In vitro ingestion rates with Salpa Kawaguchi and Takahashi thompsoni aggregates as food (1996) 0.23–0.93 0.43–1.7 38–43 mm In situ gut pigment contents Pakhomov et al. (1997) 2.73 4.99 38–43 mm In situ egestion rates Pakhomov et al. (1997) 0.05–4.45 0.15–1.68, max 13 35–50 mm In situ gut pigment contents Perissinotto et al. (1997) 0.026–0.031 0.5–0.6 o25 mm In situ gut pigment contents Pakhomov and Froneman (2002b) 0.079 0.55 25–35 mm In situ gut pigment contents Pakhomov and Froneman (2002b) 0.178 0.38 35–50 mm In situ gut pigment contents Pakhomov and Froneman (2002b) 1894 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907

Table 3 Antarctic krill Euphausia superba egestion rates. Carbon content of faecal pellets was assumed to account in average for 11% of their dry mass (Pakhomov et al., 1997)

Mean krill mass (mg dry wt) Egestion rate (mg C mg dry wtÀ1 dÀ1) Source

243.6720.0 mean 0.287, max 2.258 Antezana et al. (1982) 144.0 4.583–43.083 Clarke et al. (1988) 154.9723.2 mean 0.298, max 0.393 Ponomareva and Kuznetsova (1989) 45.3716.6 mean 10.0, max 55.0 Nordhausen and Huntley (1990) 137.0731.4 mean 7.131 Pakhomov et al. (1997)

thompsoni ingestion rates and ambient phyto- )

-1 5 plankton concentration has been documented in À1 the chlorophyll-a range of 0.2–1.2 mgl (Pakho- 4 mov and Froneman, 2002b). A linear functional response of ingestion rates versus food concentra- 3 tion may apply only to a relatively narrow range of particle concentrations, as it has been shown that 2 at higher concentrations salp feeding can be y = 1.7291x + 0.6089 1 disrupted (Harbison et al., 1986; Zeldis et al., R2 = 0.8381, N = 470

1995; Perissinotto and Pakhomov, 1997). The 0 upper concentration threshold for S. thompsoni is 0.5 1 1.5 2 2.5 Log pigment content (ng(pigm).ind. not clearly defined. However, in the Lazarev Sea Log salp length (mm) 2–5 cm long aggregates of S. thompsoni are unable À1 Fig. 6. Gut pigment content of S. thompsoni as a function of to graze at particle concentrations >1 mgl body length. Data were extracted mainly from Dubischar and (Perissinotto and Pakhomov, 1997). Bathmann (1997), Perissinotto and Pakhomov (1998a, b), and To date, there are only seven literature sources Pakhomov and Froneman (2002b). dealing with estimates of gut pigment content, filtration, ingestion and egestion rates of S. thompsoni in the Atlantic sector of the Southern Ocean (Reinke, 1987; Drits and Semenova, 1989; 2.5 )

Huntley et al., 1989; Drits and Pasternak, 1993; -1 y = 1.8603x - 1.4266

d 2

Dubischar and Bathmann, 1997; Perissinotto and -1 2 R = 0.8439 Pakhomov, 1998a, b; Pakhomov, 2002). Pooling N = 16 these data, a significant linear relationship between 1.5 log-transformed salp length and gut pigment content is obtained (Fig. 6). As expected, clearance 1 rates of S. thompsoni increase with body length

(Fig. 7). Although derived from several authors, 0.5 the ingestion rates of S. thompsoni are remarkably similar and consistent. Changes in ingestion rates Log clearance rate (I.ind. 0 as a function of salp length are best represented by 0.5 1 1.5 2 2.5 a power function. However, the global data set is Log salp length (mm) best fitted by a polynomial function, or by a linear function when log-transformed (Fig. 8). When Fig. 7. Clearance rates of S. thompsoni as a function of body length. Data extracted from Reinke (1987); Drits and Semenova converted to carbon units, S. thompsoni ingestion (1989); Huntley et al. (1989), Drits and Pasternak (1993), rates increase linearly with the carbon mass of the Dubischar and Bathmann (1997), Perissinotto and Pakhomov salp body (Fig. 9). Interestingly, daily rations of S. (1998a, b), and Pakhomov, 2002). E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1895

) 7000 -1 140 ) -1 .d

(a) .d -1 2 6000 y = 0.2167x - 118.91

y = 13.06x - 34.304x - 1719.2 -1 120 2 2 R = 0.953, N = 32 R = 0.9861, N = 32 5000 100 gC.ind.

µ 4000 80 g(pigm).ind

µ 3000 60 2.3194 2000 40 y = 2.8795x 2 R = 0.9427 1000 20 N = 15 Ingestion rate ( 0 0

Ingestion rate ( 0 5000 10000 15000 20000 25000 30000 35000 0 20 40 60 80 100 120 µ Salp total length (mm) Salp carbon body weight ( g)

Pakhomov, in press Dubischar & Bathmann, 1997 ) 4 -1

Perissinotto & Pakhomov, 1998a,b Drits & Semenova, 1989 .d

-1 3.5 Huntley et al., 1989 Drits & Pasternak, 1993 3 )

-1 6 .d (b) 2.5 -1 y = 2.0948x + 0.7424 2 2 y=1.9913x - 0.3605 5 R = 0.821, N = 32 2 1.5 R = 0.7978, N = 32 Log IR (microgram C.ind. 4 1 0.5 1 1.5 2 2.5 Log Salp length (mm) 3 Fig. 9. Carbon daily ingestion rates of S. thompsoni as a

2 function of carbon body mass and body length. 0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1 Log ingestion rate (ng(pigm).ind Log salp length (mm) Fig. 8. A summary of daily ingestion rates of S. thompsoni as a Unlike for Antarctic krill, there is little informa- function of body length. tion available on egestion rates of S. thompsoni.In a single experiment conducted near the Antarctic Peninsula during austral summer 1983/84, a 21 mm blastozoid of S. thompsoni egested 10.2% thompsoni do not show a distinct trend, either with of body carbon and 6.6% of body nitrogen per increasing body length or with body carbon mass day, which accounted for 40.7% and 48.8% of the (Fig. 10). carbon and nitrogen ingested, respectively (Hunt- Overall, in situ individual ingestion and clear- ley et al., 1989). During the summer season 1997/ ance rates of S. thompsoni are the highest of any 98, in the region south of the APF and along 61E, other primary consumer in the Antarctic pelagic daily egestion rates of S. thompsoni ranged from community (e.g., Drits and Semenova, 1989; Drits 187.8 ng (pigm) indÀ1 dÀ1 (or 9.4 mg C indÀ1 dÀ1)in and Pasternak, 1993; Froneman et al., 1997; 10 mm salps, to 3.57 mg (pigm) indÀ1 dÀ1 (or Perissinotto and Pakhomov, 1998a, b; Pakhomov, 178.6 mg C indÀ1 dÀ1) in 55 mm salps (Fig. 12). 2002; Pakhomov and Froneman, 2002a, b). Inges- Although in situ egestion rates on average tion rates of S. thompsoni estimated with in vitro accounted for 36% (range 22–56%) of the in situ incubations are up to one order of magnitude pigment consumption, they were equivalent to lower than in situ consumption rates (Fig. 11). only 0.9–3.5% of body carbon (Pakhomov, 2002). Therefore, in vitro estimated consumption rates are most likely erroneous due to such things as 4.3. Krill/salp particle selectivity small volume, stress during capture, short adapta- tion time, particularly when large specimens are As non-selective filter-feeders, salps are able to incubated. retain efficiently particles within a wide size range, 1896 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907

50 4 N = 32 40 ) -1 d

-1 3 30

20 2 Log egestion rate

10 (ng(pigm).ind. y = 1.6328x + 0.6634 R2 = 0.8901

Daily ration (% body carbon) 0 1 0 20406080100120 0.9 1 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 Salp body length (mm) Log salp length (mm) 50 Fig. 12. Egestion rates of S. thompsoni as a function of body N = 32 length. Data extracted from Pakhomov (2002). 40

30

20 4.4. Krill/salp grazing impact: implications for vertical carbon flux 10

Daily ration (% body carbon) 0 Table 4 summarizes estimates of grazing impact 0 5000 10000 15000 20000 25000 30000 35000 for Antarctic krill and S. thompsoni obtained using Salp carbon body weight (microgram) a variety of techniques. With the exception of two Fig. 10. Carbon daily rations as percentage of body carbon of estimates obtained by Dubischar and Bathmann S. thompsoni as a function of body length and body carbon (1997) and by Perissinotto and Pakhomov weight. (1998a, b), the highest impacts are derived from indirect estimates of the energetic requirements of )

-1 70000 krill and salps, under the assumption that all d

-1 in situ in vitro carbon demands are met through an herbivorous 60000 diet (Table 4). This is incorrect since both 50000 Antarctic krill and S. thompsoni are known to 40000 consume a substantial proportion of heterotrophic material (Foxton, 1966; Hopkins, 1985; Hopkins 30000 and Torres, 1989; Hopkins et al., 1993; Lancraft 20000 et al., 1991; Perissinotto et al., 1997, 2000). 10000 Overall, the grazing impact of both krill and salps is moderate through most of the Southern Ocean, 0 Ingestion rate (ng(pigm).ind. 30 40 70 and even in areas where they co-occur they usually Salp length (mm) do not make sufficient impact to control phyto- plankton growth (Pakhomov, 2002; Pakhomov Fig. 11. Comparison between in situ and in vitro estimated and Froneman, 2002b). This, however, might be ingestion rates of S. thompsoni. Data extracted from Dubischar and Bathmann (1997) and Pakhomov (2002). an underestimate as Chla/carbon ratio of 50 was employed in most of these studies. Regarding the contribution of krill and salps to the vertical carbon flux, data suggest that it is ranging from 1 to 1000 mm (Drits and Semenova, indeed extremely variable, reflecting the natural 1989; Fortier et al., 1994), while Antarctic krill patchiness of food and of both species. Based on consumes mainly food particles >10–o50 mm direct (fecal pellet production) and indirect (graz- (Meyer and El-Sayed, 1983; Drits and Semenova, ing impact and assimilation efficiency) data, 1989; Maciejewska, 1993; Opalinski et al., 1997). Antarctic krill may account on average for a E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1897

Table 4 Summary of grazing impact estimates of Antarctic krill and Salpa thompsoni

Geographical location Season Daily grazing impact Source

% Chla % daily PP stock

Euphausia superba Elephant Island Summer nd 60–81 Holm-Hansen and Huntley (1984) Summer 1989 nd 0.1–6.7 Drits and Pasternak (1993), Pakhomov (1991) Autumn 1998 nd 33 Minkina et al. (1999)

Scotia Sea Summer nd 2.2–4.4 Holm-Hansen and Huntley (1984) Summer 1984 nd 1.2 Samyshev (1991)

Bouvet Island region Winter 1982 nd o12 Sushin et al. (1985) South Georgia Summer 1994 0.4–1.9 9.6–59.2 Pakhomov et al. (1997) Greewich Meridian, APF–MIZ Summer 1993 o0.1–2.7 o0.1–50.8 Perissinotto et al. (1997) 61E, 56–651S Summer 1997/98 o0.1–6.9 o0.1–22.7 Pakhomov (2002)

Bransfield Strait Spring nd 45 von Bodungen (1986) Summer 1983/84 nd p1 Godlewska (1989)

South Shetland Islands Spring 1985 p0.2 0.1–5.5 Drits and Semenova (1989) Antarctic Peninsula Summers 1993–95 nd p23, max 421 Ross et al. (1998) Weddell Sea Summer 1989 nd o0.1–23.4 Pakhomov (1991) Southern Indian Ocean Summer 1981 nd E3 Miller et al. (1985) Prydz Bay Region Summers 1980–84 nd 10–84.5, max 190 Samyshev (1985, 1991)

Salpa thompsoni Elephant Island Summer 1994 nd 19 Loeb et al. (1997) Autumn 1998 nd 261 Minkina et al. (1999)

South Shetland Islands Spring 1985 1.5 44 Drits and Semenova (1989) Summer 1990/91 nd 9 Nishikawa et al. (1995) Bransfield Strait Summer 1989 nd 14.5–39 Drits and Pasternak (1993), Pakhomov (1991) Summer 1994 nd E5 Alcaraz et al. (1998)

Antarctic Peninsula Summer 1989/90 nd 1–10, max E100 Huntley et al. (1989) Summers 1993–95 nd p37 Ross et al. (1998)

Atlantic Sector, southern ACC Spring 1992 nd >100 Dubischar and Bathmann (1997) 61E, 49–591S Summer 1997/98 1–19.3 3.1–63.3 Pakhomov (2002) Lazarev Sea Summer 1994/95 o0.1–21.4 o1–109 Perissinotto and Pakhomov (1998a, b) Weddell Sea Summer 1989 nd p2.5 Pakhomov (1991) nd:Not determined. vertical flux of feces ranging from 0.01 to 15.6 mg tic krill are able to contribute a vertical flux of CmÀ2 dÀ1 (Pakhomov et al., 1997; Ross et al., between 44.9 mg C mÀ2 dÀ1 and 1.3 gC mÀ2 dÀ1 1998; Pakhomov, 2002). While swarming, Antarc- (Clarke et al., 1988; Pakhomov et al., 1997). The 1898 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 above values are in the range of those obtained from sediment trap collections in different regions of the high Antarctic, where krill feces were found to contribute up to 80% of total particle carbon flux in the top 200–300 m (Schnack, 1985a, b; von Bodungen, 1986; Nothig. and von Bodungen, 1989; Bathmann et al., 1991; Gonzalez, 1992). Although the salp contribution to the vertical carbon flux in the Southern Ocean has yet to be measured through sediment trap collections, S. thompsoni feces potentially may account for À2 À1 0.1–88 mg C m d (Huntley et al., 1989; Peri- Fig. 13. Mass specific egestion rates of E. superba and S. ssinotto and Pakhomov, 1998a, b; Ross et al., thompsoni as a function of body carbon mass. Data extracted 1998; Pakhomov, 2002). It is estimated that from Table 3 and from Pakhomov (2002). together Antarctic krill and S. thompsoni may re- package and remove up to 20% of phytoplankton production per day from the euphotic zone play a more important role in the ecosystem (Pakhomov, 2002). As S. thompsoni has lower budget than previously believed. (Pakhomov, 2002) or similar (Huntley et al., 1989) carbon mass specific egestion rates than Antarctic krill (Fig. 13), maximum salp contribution to the 5. Krill/salp interactions: competitive exclusion or vertical flux in carbon units should be substantially biotopical separation? lower, due to the differences in carbon densities between the two species (see Section 3.1). The increasing interest developed towards krill Antarctic krill is known to channel a large and salp interactions in the Southern Ocean over fraction of ingested material into a long-lived (e.g., the past few decades has led to the formulation of food web transport) carbon pool (sensu Fortier several hypotheses to explain their spatial separa- et al., 1994), while salps are more important in tion (Nishikawa et al., 1995). Firstly, it has been sequestering biogenic carbon, by producing large, suggested that salps may prey (filter out) on eggs fast sinking feces (Le Fevre" et al., 1998). Indeed, and early larval stages of Antarctic krill, thus Antarctic krill is a well known food source for affecting krill recruitment (Huntley et al., 1989). numerous Antarctic top predators, including This hypothesis was based on the occurrence of squid, demersal and mesopelagic fish, flying birds krill debris and larvae in food boluses of S. and penguins, seals and whales (Knox, 1994). thompsoni (Foxton, 1966; Hopkins, 1985; Hopkins Antarctic top predators are thought to consume and Torres, 1989; Hopkins et al., 1993; Lancraft between 166 106 and 450 106 tonnes of Ant- et al., 1991). However, due to the vertical arctic krill annually (Lubimova and Shust, 1980; segregation of Antarctic krill eggs/early stages Laws, 1985; Miller and Hampton, 1989). Salp- and salps, direct consumption appears to be mediated export to the top predators is much less negligible (Perissinotto and Pakhomov, 1998b). known. It has been suggested that the export may Even if salps prey upon early developmental stages be both direct and indirect (Le Fevre" et al., 1998). of Antarctic krill, the effect will only be noticeable Data gathered from literature sources, show that a in later years and, as a consequence, cannot substantial number of Antarctic zooplankton explain the spatial segregation of salps and adult species (13), including Antarctic krill, 8 bird krill during a particular season. species and 24 species of fish may consume salps Secondly, salps may produce distasteful meta- in energetically meaningful amounts (Table 5). It is bolic products, which may drive krill away becoming obvious that salps are not a trophic cul- (Fraser, 1962). This hypothesis cannot be dis- de-sac in the Antarctic ecosystem and may actually carded although it has never been tested. In E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1899

Table 5 Predators of Salpa thompsoni in the Southern Ocean

Predator name Consumption rate Source

Crustaceans Euphasuia superba 0.5 salp. krillÀ1 dÀ1 Kawaguchi and Takahashi (1996) Vibilia antarctica nd Phleger et al. (2000), Lancraft et al. (1991) Cyllopus licasii 19.4–30.7% FO Hopkins and Torres (1989) Cyllopus magellanicus nd Phleger et al. (2000) Themisto gaudichaudi 47.1% FO Hopkins (1985) Cyphocaris richardi 5.1% FO Hopkins (1985) Epimeriella macronyx 4.5% FO Hopkins (1985) Eusirus microps 12.5% FO Hopkins (1985) Orchomene plebs 28% FO Hopkins (1985) Orchomene rossi 22.7% FO Hopkins (1985) Parandania boecki 12.5% FO Hopkins (1985) Antarctomysis ohlinii 1.0% FO Hopkins (1985)

Polychetes Tomopteris carpenteri 10% FO Hopkins (1985)

Birds Black-browed Albatross (Diomedea nd Foxton (1966) melanophris) Gray-headed Albatross (Diomedea nd Foxton (1966) chrysostoma) Antarctic Fulmar (Fulmarus antarcticus) 5% of FBW Ainley et al. (1991) Blue Petrel (Halobaena coerulea) 2.7% of FBW Ainley et al. (1991) Cape Petrel (Daption capense) 1–14.9% of FBW Ainley et al. (1991) Antarctic Prion (Pachiptila vittata) 3.2% of FBW Ainley et al. (1991) Wilson’s Storm Petrel (Oceanites 1.8% of FBW Ainley et al. (1991) oceanicus) White-chinned Petrel (Procellaria 10–15 FO; 0.3–1.5% of PN Catard et al. (2000) aequinoctialis)

Demersal fish Gobionotothen gibberifrons 0.2–4.3% of PN Permitin and Tarverdieva (1972) Gobionotothen gibberifrons 10% FO Permitin and Tarverdieva (1978) Lepidonotothen nudifrons 1.4% of PN Permitin and Tarverdieva (1972) Lepidonotothen squamifrons 2.7–39.5% of PN Duhamel (1981), Duhamel and Pletikosic (1983), Duhamel and Hureau (1985) Lepidonotothen squamifrons 25.3–30.6% of FBW Pakhomov (1993c) Lepidonotothen squamifrons 8.2–40% FO, 4–19% FBW Chechun (1984) Lepidonothoten larseni 15% FO Permitin and Tarverdieva (1978) Nototheniops tchizh 23–88% FO, 21–84% FBW Shandikov (1986) Notothenia rossii rossii 4.4–18.4% of PN Duhamel (1981), Duhamel and Hureau (1985) Notothenia rossii marmorata 1.5–2% FO, 1.3% FBW Tarverdieva (1972) Notothenia rossii rossii 13–40% FO, 4–20% FBW Chechun (1984) Dissostichus eleginoides 1–6.3% FO, 0.3–2.3% FBW Chechun (1984) Channichthys rhinoceratus 5.7% FO, 0.4% FBW Chechun (1984) Trematomus eulepidotus 0.8% of FBW Pakhomov (1991) Trematomus lepidorchinus 3.7% FO; 3.7% of FBW Pakhomov (1991) Trematomus hansoni 11.2% FO; 2.1% of FBW Pakhomov (1991) Trematomus scotti 4.2% FO; 0.8% of FBW Pakhomov (1991) Trematomus centronotus 10.1% FO; 1.9% of FBW Pakhomov (1991) Trematomus bernacchii 54.4% FO; 32.8% of FBW Pakhomov (1991) 1900 E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907

Table 5 (continued)

Predator name Consumption rate Source

Gymnodraco acuticeps 1.0% FO; 0.01% of FBW Pakhomov (1991) Dissostichus mawsoni 0.5% FO; 0.1% of FBW Pakhomov (1991) Lepidonotothen kempi 15.9% FO; 5.4% of FBW Pakhomov (1991) Cygnodraco mawsoni 0.3% FO; 0.1% of FBW Pakhomov (1991) Histiodraco velifer 14.3% FO; 1.4% of FBW Pakhomov (1991)

Mesopelagic fish Bathylagus antarcticus 11.4% FO; 1–14% of PN Hopkins and Torres (1989), Lancraft et al. (1991) Electrona antarctica 0.5–22.2% FO; 0.1–1% of FBW Hopkins (1985), Hopkins and Torres (1989), Pakhomov et al. (1996) Electrona carlsbergi 0–14% FO, 0–7.4% FBW Kozlov and Tarverdieva (1989) Gymnoscopelus opisthopterus 11.1% of FBW Pakhomov et al. (1996) Gymnoscopelus braueri 7.7% FO Lancraft et al. (1991)

FO, Frequency of occurrence in stomachs; FBW, Food bolus weight; PN, prey numbers; nd, Not determined. contrast, recent observations have shown that are found together spatially and temporally, which Antarctic krill is actually attracted to S. thompsoni does not seem to be the case on most occasions extracts and is able to prey successfully on salps (Kawaguchi et al., 1998). Recently, it has been with a meaningful rate of up to 0.5 salps per krill hypothesized that food availability prior to the per day, or E8.7% of body carbon per day (Table interaction, rather than direct food competition 2; Kawaguchi and Takahashi, 1996). between different herbivores, may be responsible Thirdly, Antarctic krill may be excluded from for competitive exclusion (Chiba et al., 1998). If the areas of high salp densities because salps may this applies to Antarctic krill and salps, it means outcompete other zooplankton, including krill, for that in the high Antarctic region we always food (Fraser, 1962; Perissinotto and Pakhomov, observe the end result of the competition rather 1998b). Salps are indeed efficient at retaining than the process itself, even despite extensive particles within a wide size range, while Antarctic seasonal coverage. We are of the opinion that krill prey selectively on specific food particles direct competition for food may indeed be valid in (Section 4.3). Although it is almost impossible to the long-term (Loeb et al., 1997), while this would verify the above hypothesis in the marine environ- not explain the short-term inverse distribution ment (Le Fevre" et al., 1998), there is indirect between krill and salps (Chiba et al., 1998). evidence that competition between salps and Finally, most recently an approach comparing Antarctic krill for food is negligible. No direct the carbon budgets of major metazoan herbivores interactions between the proportion of green krill in the Southern Ocean has been used (Le Fevre" (intensively feeding krill) and salp density has been et al., 1998). According to these calculations, observed around the Antarctic Peninsula region resource thresholds at which herbivores are able using a comprehensive data set collected during to fulfill their basic metabolic requirements are the Japanese krill fishing operations (Kawaguchi 3.5–30 mgClÀ1 for S. thompsoni, 105 mgClÀ1 for et al., 1998). The authors also noticed a clear copepods and 125 mgClÀ1 for Antarctic krill (Le spatial and temporal mismatch between salps and Fevre" et al., 1998). This clearly implies that salps green krill and linked this to the appearance of may survive successfully at low food concentra- warmer waters in the region (Kawaguchi et al., tions compared, for example, to Antarctic krill. 1998). Interestingly, the empirical upper threshold of Competitive removal of food may be the major >1 mg chlorophyll-a lÀ1, at which salp clogging separating force of krill and salp concentrations may occur (Perissinotto and Pakhomov, 1997), (Perissinotto and Pakhomov, 1998b) when they would be equal to 7100 mgClÀ1, after converting E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1901

Table 6 Environmental conditions under which salps and krill are expected to succeed (after Le Fevre" et al. (1998) with additions)

Conditions Salps Krill

Food concentration Low High Food distribution Homogeneous Patchy Hydrodynamic conditions Dynamic Stable Type of algae Small, flagellates Large, diatoms Other food items Bacteria, microzooplankton, small mesozooplankton Micro- to macro-zooplankton

to carbon and adding a heterotrophic component 2000b). However, in the regions of complex and (following Le Fevre" et al., 1998). Therefore, if variable oceanography (e.g., off Antarctic Penin- salps would be able to maintain low food sula, within the Marginal Ice Zone and polynyas) concentration, this may prevent development of spatial separation, particularly in the macro-scale, copepods and Antarctic krill (Chiba et al., 1998; becomes unclear. As a consequence, in such Perissinotto and Pakhomov, 1998a, b). It is likely, regions krill and salp may theoretically co-exist however, that once a phytoplankton bloom devel- over short periods of time (Le Fevre" et al., 1998). ops within the Marginal Ice Zone, salps would Nevertheless, the physiological constrains may be disappear to the advantage of other zooplankton of crucial importance in keeping Antarctic krill such as krill and copepods, which are more and S. thompsoni separated in the long-term. adapted to operate in the presence of high particle Therefore, the environmental warming may lead concentrations (Nishikawa et al., 1995; Perissinot- to the increase in degree of spatial and temporal to and Pakhomov, 1998b). overlap between these two large metazoans of the Finally, the spatial separation between krill and Southern Ocean (see also Section 3.2.2). The salp populations may be due to the advection of regional ecological consequences of the salp years, different water masses in the region (Kawamura as discussed above, may be dramatic, suggesting et al., 1994; Kawaguchi et al., 1998). This that if the warming trend will continue in the high hypothesis has already been discussed above Antarctic, salps would probably play more pro- (Section 3.2.2) and seems to explain the limited minent role in the trophic structure of the spatial overlap observed in krill/salp distribution Antarctic marine ecosystem. This could be coupled outside the Antarctic Peninsula region (see also with the dramatic decrease in krill productivity Nicol et al., 2000b). Although a small-scale largely due to decrease in the spatial extension of synchronized pattern between salp density and the krill biotope and inter-specific salp/krill inter- elevated sea-surface temperatures has been noticed actions. High Antarctic regions, particularly the around the Antarctic Peninsula in number of Marginal Ice Zone, however, have effective studies (e.g., Nast, 1986; Piatkowski, 1989; Nishi- protective mechanisms against salp invasions, kawa et al., 1995; Minkina et al., 1999), the e.g., low temperatures (reproduction constrains, distribution patterns of both Antarctic krill and S. Chiba et al., 1999) and high particle concentra- thompsoni are still to be studied in detail there, tions associated with the ice retreat (Perissinotto with particular emphasis to environmental vari- and Pakhomov, 1997). ables characterizing this area. It appears that Antarctic krill and S. thompsoni are adapted to be successful in biotopes with Acknowledgements different environmental conditions (Table 6, after Le Fevre" et al., 1998). 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