salp/krill interactions in the southern ocean:spatial

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

Salp/krill interactions in the Southern Ocean: spatialsegregation 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 Africab 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.

Resume

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’Oc!ean Austral sont synth!etis!ees dans cette !etude. Le krill et les

salpes pr!esentent une distribution qui se traduit en g!en!eral par une forte s!egr!egation spatiale, "a toutes les !echelles

d’espaces. Ceci semble #etre le r!esultat d’une s!eparation claire des niches !ecologiques de ces deux esp"eces cl!es du r!eseau

trophique antarctique. Le krill et les salpes sont observ!es dans des masses d’eau diff!erentes qui sont s!epar!ees par des

fronti"eres primaires et secondaires. A petite !echelle (o100 km), soit le krill antarctique et les salpes sont habituellement

localis!ee dans des parcelles d’eaux sp!ecifiques, ou alors ils sont s!epar!es verticalement. Les vitesses de broutage du krill et

des salpes, estim!ees en utilisant la technique de fluorescence in situ, sont parmi les plus !elev!ees rencontr!ees au sein du

r!eseau trophique p!elagique antarctique. Bien que le krill et les salpes peuvent parfois consommer l’ensemble de la

production primaire journali"ere, l’impact de leur activit!e de broutage est g!en!eralement mod!er!e (p50% de la production

primaire). Les cons!equences !ecologiques r!egionales d’ann!ees caract!eris!ees par des fortes densit!es 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 0 9 6 7 - 0 6 4 5 ( 0 2 ) 0 0 0 1 7 - 6

dramatiques. Si la tendance au r!echauffement, qui est observ!ee autour de la P!eninsule Antarctique et dans l’Oc!ean

Austral, continue, les salpes pourraient jouer un r #ole plus important dans la structuration des !ecosyst"emes marins

antarctiques. A cela serait probablement associ!e une diminution dramatique de la productivit!e 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 m!ecanismes physiologiques effectifs qui pourraient offrir une certaine protection vis "a

vis d’une invasion par les salpes.

1. Introduction

The Antarctic krill, Euphausia superba, and thetunicate, Salpa thompsoni, are among the mostimportant filter-feeding metazoans of the SouthernOcean, ranking only after copepods in terms oftotal dry pelagic biomass (Pages, 1997; Voronina,1998). These two species are also recognized asmicrophages of key importance, as they are able toefficiently re-package small particles into large fastsinking feces, thereby playing a major role inchanneling biogenic carbon from surface watersinto the long-living pools and to the ocean’sinterior and seafloor (Huntley et al., 1989; Fortieret al., 1994; Schnack-Schiel and Mujica, 1994;Pakhomov et al., 1997; Le F"evre et al., 1998;Perissinotto and Pakhomov, 1998a). As a conse-quence, the ecological role of these two key speciesin the Antarctic pelagic food web has recentlyreceived much attention (e.g., Nishikawa et al.,1995; Siegel and Loeb, 1995; Siegel and Harm,1996; Dubischar and Bathmann, 1997; Loeb et al.,1997; Kawaguchi et al., 1998; Perissinotto andPakhomov, 1998b; Ross et al., 1998). It has beensuggested that krill and salps may be in directcompetition with one another in certain areas ofthe Antarctic Peninsula (Loeb et al., 1997) and inthe Lazarev and Cooperation Seas (Perissinottoand Pakhomov, 1998a, b). It also was tentativelypostulated that if the increase in seawater tem-perature, already observed in the Antarctic Penin-sula region, continues (Zwally, 1991; Rott et al.,1996), salps may spread into the high Antarcticregions, with important implications for theregional carbon flux and the Antarctic food webstructure (Perissinotto and Pakhomov, 1998a, b).

In the Southern Ocean, S. thompsoni is generallyrestricted to the warmer water masses (Voronina,1984; Nast, 1986; Siegel et al., 1992; Pakhomov,

1993a; Park and Wormuth, 1993; Kawamura et al.,1994; Nishikawa et al., 1995). With the exceptionof only few areas, such as Antarctic Peninsularegion, spatial exclusion between Antarctic krilland salps has been widely documented (Pakhomovet al., 1994a; Hosie, 1994; Voronina, 1998). Studieson the community structure of zooplanktonconducted in the vicinity of the Greenwichmeridian have indicated that Antarctic krill andsalps may overlap in their distribution south of theAntarctic Polar Front (Fransz and Gonzalez,1997; Pakhomov et al., 2000). Feeding studiesconducted in this region provided evidence thatthese species may at times consume the entire dailyprimary production (Dubischar and Bathmann,1997; Perissinotto et al., 1997; Perissinotto andPakhomov, 1998a; Froneman et al., 2000). Unlikefor case of krill, for which there are numerous dataon its feeding ecology, there are still large gaps inour understanding of the biology and the ecologi-cal role of salps in the Southern Ocean (Le F"evreet al., 1998). The aims of this paper are tosummarize studies on the trophic ecophysiologyof Antarctic krill and of the tunicate S. thompsoni,with particular emphasis to the tunicates, and todiscuss the phenomenon of krill/salp spatialseparation.

2. Materials and methods

Data on ingestion rates of Antarctic krill, E.

superba, and of the tunicate, S. thompsoni,estimated using the gut fluorescence techniquewere obtained mainly during the three expeditionsto the southern part of the Atlantic sector of theSouthern Ocean: (a) the second cruise of the SouthAfrican Antarctic Marine Ecosystem Study(SAAMES II) conducted aboard the mv SA

E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–19071882

Agulhas along the Greenwich Meridian (WOCESR2 line) in January 1993 (Perissinotto et al., 1997;Froneman et al., 2000; Pakhomov et al., 2000); (b)the SAAMES IV aboard the mv SA Agulhas in theLazarev Sea during December 1994–January 1995(Froneman et al., 1997; Perissinotto and Pakho-mov, 1998a, b); (c) the joint Scandinavian/SouthAfrican Antarctic Research Expedition aboard themv SA Agulhas along the 61E meridian between491S and 601300S (Pakhomov, 2002; Pakhomovand Froneman, 2002a, b).

In addition, numerous published and unpub-lished sources (mentioned throughout the text) onkrill and salps ingestion rates, abundances, bio-mass and distribution in the Southern Ocean wereused for this synthesis. To convert wet weight intocarbon weight, the following conversion factorswere used: (a) S. thompsoni dry weight wasassumed to be 4% of wet weight, and carbonweight was assumed to be 4.3% of dry weight(Ikeda and Mitchell, 1982; Ikeda and Bruce, 1986;Hagen, 1988; Huntley et al., 1989; Donnelly et al.,1994); (b) E. superba dry weight was assumed to be22% of wet weight, and carbon weight assumed tobe 45% of dry weight (Ikeda and Mitchell, 1982;Ikeda and Bruce, 1986; Torres et al., 1994). Toconvert chlorophyll values into carbon values astandard chlorophyll/carbon ratio of 50 wasapplied (Booth et al., 1993).

3. Euphausia superba and Salpa thompsoni:densities and distribution

3.1. Krill/salp densities: importance in the Antarctic

pelagic ecosystem

There is a great deal of uncertainty in estimatingtotal stocks of Antarctic krill and salps in theSouthern Ocean due to their extremely patchydistribution (e.g., Miller and Hampton, 1989;Voronina, 1998). The most recent revision ofAntarctic krill biomass estimates obtained usingscientific and commercial trawls was presented byVoronina (1998, Tables 2–4). After converting wetweight into carbon, the average biomass of E.

superba throughout the Southern Ocean rangesfrom 400 to 37800 mg C m�2 (mean 595071110 mg

C m�2) and from 1 to 1200 mg C m�2 (mean2207320 mg C m�2) in the regions of dense andlow krill concentrations, respectively (Voronina,1998).

Although Southern Ocean tunicates have notbeen targeted specifically, over the past twodecades a substantial amount of data on S.

thompsoni density has been accumulated in differ-ent sectors of the Southern Ocean (Table 1). Insummary, these data indicate extreme variability insalp densities across the Southern Ocean (Table 1).Nevertheless, throughout much of the area southof 401S, S. thompsoni densities remain moderate,on average varying between o0.1 and 30 mgC m�2, or between o0.1 and 30 ind m�2. However,S. thompsoni densities in the Antarctic Peninsularegion, particularly in the Bransfield Strait andaround Elephant Island, were found to beconsistently elevated (Table 1). Furthermore, thesecondary frontal systems that demarcate low andhigh latitude water masses around the AntarcticContinent, e.g., Weddell–Scotia Confluence,Warm Counter Weddell Current in the LazarevSea, the northern part of the Ross Sea, alsoshowed enhanced densities of S. thompsoni.Foxton (1966) first mentioned this phenomenon,e.g., an increased biomass of S. thompsoni at thenorthern limit of Antarctic krill distribution. In theregions of high salp densities, average concentra-tions generally ranged from 22 to 1115 mg C m�2

and from 20 to 800 ind m�2, with a maximumbiomass level of 2.5 g C m�2 observed in thenorthern Ross Sea (Voronina et al., 1993) andabundance of ca 6000 ind m�2 off the Adelie Coast(Chiba et al., 1998). The mean S. thompsoni

biomass, estimated using average values presentedin Table 1, is 72.17189 mg C m�2 (N ¼ 54).

For comparison, mean copepod biomass in theSouthern Ocean is estimated at E1161 mg C m�2.This value was obtained from Voronina (1998) byassuming that dry weight is equivalent to 15% ofwet weight and that carbon weight accounts for43% of dry weight (Ikeda and Mitchell, 1982;Ikeda and Bruce, 1986; Donnelly et al., 1994).

From the above comparative biomass estimatesof the three large Antarctic metazoan filter-feedergroups, it is obvious that the tunicates do not playa major role in terms of total carbon biomass.

E.A. Pakhomov et al. / Deep-Sea Research II 49 (2002) 1881–1907 1883

Table 1

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

Location Date Sampling

depth (m)

Biomass

(mgC m�2)

Abundance

(ind m�2)

Source

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 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–

591.1

nd nd Torres et al. (1984)

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

Bransfield Strait

Dec 1983–Jan 1984 0–200 23.8 0.04–207.7nd nd Witek et al. (1985)

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


Table 1 (continued)


depth (m)

Biomass

(mgC m�2)

Abundance

(ind m�2)

Source


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

Sea

Feb–Mar 1983 0–300 13.2 nd 12.3 nd Boysen-Ennen and

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: STCFAPF Dec 1979–Jan 1980 surface 0.004 nd o0.01 nd Pakhomov and McQuaid

(1996)

AS: APFF60–651S Dec 1979–Jan 1980 surface 0.03 nd 0.2 nd

AS: 01, 46–691S Jan 1993 0–300 5.97 0–45.1 41.4 0–222.6 Pakhomov et al. (2000)

AS: 61E, 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

(PBR)

Feb–Mar 1985 0–52 6.2 nd 2.15 nd Pakhomov (1991)

Dec 1985–Jan 1986 0–59 0.1 nd 0.3 nd Pakhomov (1991)



Dec 1987–Mar 1988 0–150 7.9 nd 7.2 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 651S Jan–Feb 1991 0–200 0 0 0 0 Hosie 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)


Similar results could be obtained using estimatesof the total stock for these filter-feeders in theSouthern Ocean provided by Voronina (1998).Voronina (1998) showed that in terms of freshmass, salps are the main contributors to total stockin the Southern Ocean, followed by copepods andAntarctic krill (Fig. 1). However, in terms of dryand carbon mass, copepods were identified as themost important and salps the least important(Fig. 1). The main argument of Voronina is thatAntarctic krill is neither first in total metazoanbiomass nor in production, as in both cases it issecond to the herbivorous copepods (Voronina,1998). Unlike for Antarctic copepods and krill,there are no annual production estimates for S.

thompsoni available in the literature. However, it isknown, that salps exhibit the fastest individualgrowth rates among metazoans (Heron, 1972;Heron and Benham, 1984). Although salp abun-dance maxima are short-lived, the P/B coefficientof a one-year life cycle would likely exceed one(Fraser, 1962; Foxton, 1966) and reach 3 (N.M.Voronina, personal communication). As a conse-quence, salp contribution to total filter-feederproduction should be substantial, probably rank-ing second only to that of copepods. As salps playan increasingly important role in the Antarcticecosystem, studies on the production of S.

thompsoni are urgently required.

3.2. Krill/salp distribution

3.2.1. Large-scale distribution

Despite uncertainties in the small-scale distribu-tion of Antarctic krill, the large-scale distributionof this species is relatively well documented (Millerand Hampton, 1989; Knox, 1994; Voronina,

1998). One of the most important features of themacro-scale distribution of Antarctic krill is thetypical increase in density in two different zones ofthe Southern Ocean (Makarov and Spiridonov,1993). The southern circumpolar belt of high krilldensity is restricted to the Antarctic CoastalCurrent (East Wind Drift), north of the shelf edgeand above the upper part of the continental slope.The northern belt of high krill density is associatedwith the secondary frontal zones (Maslennikov,1980, 1995), where waters of high latitudes aremixed with waters of the Antarctic Circumpolar

Table 1 (continued)


depth (m)

Biomass

(mgC m�2)

Abundance

(ind m�2)

Source


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 m�3.

0%

20%

40%

60%

80%

100%

Wet

mas

s

Dry

mas

s

Car

bon

mas

s

Pro

duct

ion

Fae

cal

pelle

tpr

oduc

tion

Con

trib

utio

n

copepods Antarctic krill salps

Fig. 1. Comparative role of major metazoan filter-feeders in the

Southern Ocean. Wet and dry masses are taken from Voronina

(1998). Carbon mass calculated from dry mass assuming that

carbon accounts for 4.3%, 43% and 45% dry weight of salps,

copepods and krill, respectively (see Sections 2 and 3.1). Annual

production of copepods and krill is taken from Voronina

(1998), while production of salps was calculated assuming a P/B

coefficient of 1 (see Section 3.1 for explanation). Faecal pellet

production was calculated as follows: for copepods assuming

average daily ration of 10% of body carbon and assimilation

efficiency of 70%; for Antarctic krill assuming average egestion

rate of 8.143mg C mgDW�1 d�1 (Table 3); for S. thompsoni

assuming egestion rate of 10.2% of carbon mass per day

(Huntley et al., 1989).


Current. Apart from the Weddell Sea, where thenorthern belt is strongest, this area is not ascontinuous as the southern one, but it can bedistinctly identified around the Antarctic Con-tinent in the Bellingshausen, Lazarev, Riiser-Larsen, Cosmonaut, Cooperation and DumontD’Urvile Seas (e.g., Makarov and Sysoeva, 1983;Williams et al., 1983, 1986; Iganake et al., 1984;Hampton, 1985; Miller, 1986, 1987; Shirakiharaet al., 1986; Bibik et al., 1988; Miquel, 1991;Pakhomov, 1993a, b).

Unlike its southern counterpart, the northernbelt of high krill density exhibits an asymmetricalpattern in distribution (Marr, 1962; Mackintosh,1973). For instance, in the Atlantic sector, watersof high krill biomass are associated with the northbranch of the Weddell Gyre (Weddell–ScotiaConfluence), which deflects southward east ofBouvet Island (Marr, 1962; Maslennikov, 1980).Accordingly krill, which are found in the Atlanticsector as far north as 511S, are not generallyrecorded north of 59–601S in eastern Antarctica(Marr, 1962; Miller and Hampton, 1989).

A detailed map showing the spatial distributionof S. thompsoni in the Southern Ocean was firstprovided by Foxton (1966) who used a compre-hensive collection of Discovery expeditions con-ducted between 1925 and 1951 (Fig. 2). On thebasis of Foxton’s (1966) data, the northern limit ofS. thompsoni distribution appears to coincide withthe mean position of the Subtropical Convergence,while the southern limit is generally shaped by theice-edge (Foxton, 1966). At that stage, a belt ofelevated densities of S. thompsoni was restricted tothe region between 45 and 601S (Fig. 2). It isevident that S. thompsoni was absent or found invery low numbers in the waters of high latitudes,particularly in waters of Weddell Sea origin(Foxton, 1966). These data were subsequentlysupported by the addition of a data set collectedbetween 1956 and 1958 by Russian expeditionsaboard the RV Ob’ (Fig. 2, see Voronina, 1998 fordetails).

After comparing the zooplankton densitiesrecorded during the BIOMASS expeditions withthose from the Discovery results, Kawamura(1986) stated ‘‘that behavior of salp populationshould be considered very important in total

Antarctic zooplankton biomass’’. Following anincrease in the occurrence of dense salp concentra-tions around the Antarctic Peninsula and SouthGeorgia, the author tentatively hypothesized thatthe increase in population size of salps over thevast range of the Southern Ocean over the pastseveral decades may have been in response to thechange in the Antarctic marine ecosystem (Kawa-mura, 1987). As the number of publicationsdocumenting mass salp occurrences in differentregions of the high Antarctic recently has in-creased dramatically (e.g., Huntley et al., 1989;Park and Wormuth, 1993; Voronina et al., 1993;Pakhomov et al., 1994a; Nishikawa et al., 1995;Loeb et al., 1997; Perissinotto and Pakhomov,1998a, b; Chiba et al., 1998, 1999), we have tried tore-construct a similar map of S. thompsoni

distribution using all data available (publishedand unpublished) from 1980 till 1998 (Fig. 3). Thestriking difference between the recent map andthat presented by Foxton in 1966 is that S.

thompsoni is now regularly found at high latitudes,including the southern parts of the Bellingshausen,Weddell and Lazarev seas, and the belt of its denseconcentrations extends further south to E651S(Fig. 3). In our opinion, this increase in distribu-tion may underline dramatic changes in theAntarctic marine environment.

Warming trend over the past 40 years has beendemonstrated for the Antarctic Peninsula region(Gloersen and Campbell, 1991; Zwally, 1991; Rottet al., 1996). This is linked to an increase in theaverage percentage of open water in the form ofleads and polynyas, to the disintegration of ice-shelves, and to a decrease in areal and seasonalextent of sea-ice cover (Doake and Vaughan, 1991;Gammie, 1995; Vaughan and Doake, 1996;Hewitt, 1997). Furthermore, the warming trendhas shown some correlation with an increase insalp occurrence and with a decrease in krill stock(Loeb et al., 1997; Naganobu et al., 1999). There isevidence for the warming in the Arctic region andoff the Antarctic Peninsula (Johannessen et al.,1995; Vaughan and Doake, 1996) as well as atsome sub-Antarctic islands (Smith and Steen-kamp, 1990; Smith, 1991). Most recently, warmingof the World Ocean, including the SouthernOcean, has been demonstrated (Levitus et al.


2000). Although the warming signals are notmonotonic, they were found to be consistent ineach ocean basin (de la Mare, 1997; Levitus et al.,2000). Therefore, since S. thompsoni is considereda warm-water species, data presented in Fig. 3 mayindicate that large-scale warming of high Antarcticregions is in progress. If the hypothesis is correct(still remains to be proven), the change in salpdistribution may have very important implicationsfor the high Antarctic ecosystem. The occurrenceof salps in high latitudes may change the regionalcarbon flux (Perissinotto and Pakhomov,

1998a, b). More importantly, an increase in salpabundance may be coupled with a dramatic fall inkrill stock and productivity due to a decrease inthe spatial extension of the krill biotope (Pakho-mov, 2002), which in turn will affect the Antarcticmarine food web and krill resource management(Loeb et al., 1997). In light of this, it is worthnoting that the most recent Antarctic krill stockestimates, ca 61� 106–155� 106 tonnes (Nicolet al., 2000a), are about half of those previouslyestimated, ca 100� 106–600� 106 tonnes (Rossand Quetin, 1986). This, however, may be linked

WEDDELL SEA

ROSSSEA

01800150 W

012

0W

090

W0

60W

030 W 00

0150 E

0120

E0

90E

060

E

030 E

AC

STC 040 S

12345

080 S

060 S

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 m�2 for

Russian data).


to the development of better or more accurateassessment techniques/models.

3.2.2. Meso-scale distribution

Hempel (1985) described three major zooplank-ton associations south of the Antarctic PolarFront (APF). These are: (1) ice-free oceanic West

Wind Drift assemblage, where copepods, salps andsmall euphausiids dominate; (2) the seasonal pack-ice assemblage, where Antarctic krill is the mostimportant species; and (3) the permanent pack-iceassemblage. Meso-scale community structure stu-dies conducted in different sectors of the SouthernOcean provided many of the data to support

WEDDELL SEA

ROSSSEA

01800150 W

012

0W

090

W0

60W

030 W 00

0150 E

0120

E0

90E

060

E

030 E

060 S

AC

STC040 S

080 S

12345

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 m�2 (or gWW m�2).

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).


Hempel’s subdivision. These clearly showed thatAntarctic krill and S. thompsoni are dominantspecies in different zooplankton assemblages,which belong to specific water masses or modifica-tions (Brinton, 1984; Nast, 1986; Huntley et al.,1989; Lancraft et al., 1989; Makarov and Solyan-kin, 1990; Siegel and Piatkowski, 1990; Siegel et al.,1992; Pakhomov, 1993a, b; Pakhomov et al.,1994a, 2000; Hosie, 1994; Nishikawa et al., 1995;Chiba et al., 1998; Minkina et al., 1999). There isgrowing evidence in the literature to suggest thatthe ice-edge may represent a natural boundarybetween the distribution of S. thompsoni and thatof Antarctic krill (Foxton, 1966; Brinton, 1984;Torres et al., 1984; Ainley et al., 1988; Siegel et al.,1992). The importance of the frontal zone asso-ciated with the winter northern limit of theseasonal pack ice, Antarctic Ice Boundary Front(AIBF, after Klyausov, 1993), has recently beenrecognized (Grachev, 1991; Pakhomov andMcQuaid, 1996; Pakhomov and Froneman,2002a). From an oceanographic point of view,the AIBF coincides with the disappearance of thesubsurface cold-water layer that separates the highlatitude waters from the warmer water massesaffected by the ACC (Klyausov, 1993; Pakhomovet al., 2000). Ecologically, the AIBF represents thenorthern limit of Antarctic krill distribution andthe southern limit of the mass development ofsmall gastropods of the genus Limacina (Grachev,1991). The front also coincides with the sharpdecline in S. thompsoni populations to the south(Pakhomov, 1989, 1993a; Pakhomov andMcQuaid, 1996; Pakhomov et al., 2000).

High-resolution studies, conducted in the Atlan-tic sector of the Southern Ocean along the Green-wich and the 61E meridians, have shown that thespatial overlap in distribution of Antarctic krilland S. thompsoni is minimal and occurs onlywithin the AIBF region (Fig. 4). There are,however, records showing that S. thompsoni mayoccur as far south as 681S in the Lazarev Sea(Pakhomov et al., 1994a; Perissinotto and Pakho-mov, 1998a, b) and also may be found in thesouthern parts of Bellingshausen, Weddell, Cos-monaut and Cooperation seas and off the AdelieLand (Fig. 3; Boysen-Ennen et al., 1991; Pakho-mov, 1991; Siegel and Harm, 1996; Chiba et al.,

1998; Nicol et al., 2000b). It is evident that on suchoccasions S. thompsoni populations are restrictedto the warm water intrusions or layers (Fig. 5;Boysen-Ennen and Piatkowski, 1988; Makarovand Solyankin, 1990; Pakhomov, 1991, 1993a;Pakhomov et al., 1994a). This is confirmed by thesignificant positive correlation observed betweenintegrated average seawater temperature and S.

thompsoni densities in the Lazarev Sea (Pakhomovet al., 1994a; Pakhomov and Perissinotto, unpub-lished), in the Cosmonaut Sea (Pakhomov, 1991)and in the Prydz Bay region (Hosie et al., 1997).Casareto and Nemoto (1986) were the first tosuggest that at the higher latitudes S. thompsoni

exist close to its thermo-physiological limits. Thiswas recently confirmed by Chiba et al. (1999) usinga data set collected off Adelie Land. It was

0

0.06

0.05

0.04

0.03

0.02

0.01

48 50 52 54 56 58 60 62 64 66

Latitude (˚South)

0

1.8

1.5

1.2

0.9

0.6

0.3

Euphausia superba Salpa thompsoni

1997/98AIBF

0

0.1

0.2

0.3

0.4

46 48 50 52 54 56 58 60 62 64 66 68 70

Latitude (South)

Kril

l abu

ndan

ce (

ind.

m-3

)

0

0.3

0.6

0.9

1.2

1.5Euphausia superba Salpa thompsoni

1993AIBF

Kril

l abu

ndan

ce (

ind.

m-3

)

Sal

p ab

unda

nce

(ind.

m-3

)S

alp

abun

danc

e (in

d.m

-3)

Fig. 4. Horizontal distribution pattern of E. superba and S.

thompsoni along the Greenwich Meridian during January 1993

(top, data extracted from Pakhomov et al., 2000) and along the

61E meridian during December 1997–January 1998 (bottom,

data extracted from Pakhomov, 2002) in the top 300 m layer.

AIBF: Antarctic Ice Boundary Front after Klyausov (1993).


observed that no solitary forms were found in thehigh latitudes and that aggregate forms werealways small in size, thus suggesting that S.

thompsoni aggregates were transported into thearea, rather than being the result of asexualreproduction in situ (Boysen-Ennen et al., 1991;Siegel and Harm, 1996; Chiba et al., 1999). Thetesting of this hypothesis certainly requires moreresearch. Unlike that of S. thompsoni, the distribu-tion of Antarctic krill is restricted to highAntarctic waters masses and its life cycle is closelylinked to the seasonal sea-ice biotope (Knox, 1994;Loeb et al., 1997).

Analyzing the macro-scale contrasting distribu-tion of Antarctic krill and S. thompsoni, Kawa-mura et al. (1994) suggested that this could not beexplained by either behavioral functions of organ-isms, such as swarm formation, or ecologicalregimes, such as competitive exclusion. Theyhypothesized that the marked inverse distributionof salps and krill might be related to the watermass structure in the areas investigated. Thisseems to be confirmed by data presented in this

study, which show that Antarctic krill and S.

thompsoni are spatially separated through most ofthe Southern Ocean (Nicol et al., 2000b). Never-theless, in the Atlantic sector, particularly in thewaters off the Antarctic Peninsula and aroundSouth Shetland Islands, Antarctic krill and salpsshow some degree of overlap in their summermacro-scale distribution (e.g., Witek et al., 1985;Piatkowski, 1987; Loeb et al., 1997; Ross et al.,1998). This is hardly surprising as this region is oneof the most complex areas of the Southern Ocean,where water masses of different origin are oftenmixed together (Maslennikov and Solyankin,1979; Maslennikov, 1980; Sahrhage, 1988). Recentanalysis of long-term data sets on krill biomass,krill spawning and recruitment, salp biomass andsea-ice cover in the vicinity of the Elephant Islandhas revealed significant correlation between theseparameters (Loeb et al., 1997). It has beenpostulated that winters characterized by poorsea-ice cover would promote extensive salp bloomsand poor krill spawning during the followingsummer and, as a consequence, poor krill

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 m�2.


recruitment the following year. A long-termwarming trend was suggested to be responsiblefor the increased occurrence of ‘salp’ years aroundElephant Island (Loeb et al., 1997). Significantcorrelations have been obtained between lowAntarctic krill biomass and unusually high sea-water temperatures in the vicinity of the AntarcticPeninsula (Priddle et al., 1988; Loeb et al., 1997),to the extent that during some years salps (mainlyS. thompsoni) dominated total zooplankton (Mu-jica and Asencio, 1985; Witek et al., 1985; Nast,1986; Huntley et al., 1989; Siegel and Loeb, 1995;Loeb et al., 1997; Minkina et al., 1999). None-theless, despite this large-scale overlapping pat-tern, during fine-scale surveys conducted off theAntarctic Peninsula, particularly around ElephantIsland, a pronounced spatial, horizontal or verticalseparation between krill and salps has beendemonstrated in a number of studies (e.g., Nast,1986; Piatkowski, 1989; Park and Wormuth, 1993;Brinton, 1984; Maklygin and Pakhomov, 1993;Pakhomov, 1993a, b; Nishikawa et al., 1995; Rosset al., 1998; Minkina et al., 1999).

4. Krill/salp feeding dynamics

4.1. Euphausia superba: ingestion and egestion

rates

Despite the numerous attempts to estimate dailyconsumption rates in Antarctic krill (see Table 2),ingestion rates obtained using the gut fluorescencetechnique are not numerous. In situ measuredphytoplankton consumption by Antarctic krillvaries between 0.06 and 0.62 mg (pigm) ind�1 d�1,for specimens o25 mm in length, and between 0.3and 96.9 mg (pigm) ind�1 d�1 in specimens>30 mm (Drits and Semenova, 1989; Daly, 1990;Drits and Pasternak, 1993; Pakhomov et al., 1997;Perissinotto et al., 1997; Pakhomov and Frone-man, 2002b). The daily carbon rations obtainedusing the gut fluorescence method are generally inthe lower range (o5% of body carbon) ofestimates calculated employing other techniques(Table 2). When the high metabolic activity ofAntarctic krill is combined with the energetic costsfor growth, molting and reproduction, krill carbon

uptake ranges between 5% and 15% of bodycarbon (Table 2). This daily ration can be obtainedfrom phytoplankton only on occasions whenchlorophyll-a concentrations are in excess of3 mg l�1 (Table 2). It is now recognized thatAntarctic krill exhibits omnivory and carnivorythroughout most of the year and can be regardedas a truly herbivore only during the period ofspring/early summer phytoplankton blooms (Mill-er and Hampton, 1989; Perissinotto et al., 1997).As a purely phytoplankton diet often does notcover even its basic metabolic demands (e.g.,Pakhomov et al., 1997; Perissinotto et al., 1997),Antarctic krill complement its diet with hetero-trophic carbon by consuming on average up to80% of total carbon in the form of micro- andmesozooplankton (Perissinotto et al., 2000).

Grazing rates of Antarctic krill, as a function offood concentration, show different types ofresponse depending on krill physiological state,season, quality and quantity of food (Kato et al.,1982; Schnack, 1985a, b; Helbling et al., 1992). Anon-saturating linear response was obtained withchlorophyll-a concentrations of up to 20 mg l�1

(Price et al., 1988; Ross et al., 1998). A saturationtype of model has also been described on severaloccasions, particularly in experiments where het-erotrophic food is offered, with upper foodconcentration thresholds of 6–8 mg C l�1 (Samy-shev and Lushov, 1983; Krylov, 1989; Ross et al.,1998).

Egestion rates of Antarctic krill range consider-ably, between 0.3 and 55 mg C mg dry wt�1 d�1

(Table 3), and appear to correlate with the ambientchlorophyll-a concentration (Clarke et al., 1988) aswell as with the krill mass (Table 3).

4.2. Salpa thompsoni: feeding dynamics

One of the goals of this revision is to derivesimple predictive models of individual ingestionand egestion rates for S. thompsoni in the SouthernOcean. As predictor variables, salp body lengthand mass were used. Salps are believed to have anon-saturation feeding response to food concen-tration, as they are probably unable to regulatetheir filtration rates (Perissinotto and Pakhomov,1998a, b). Indeed, a positive trend between S.


Table 2

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

Daily ingestion

rate (mg

C ind�1 d�1)

% of body C Length, stage Conditions, food, method Sources

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

after Clarke and Morris (1983)

Antezana et al. (1982)

0.18–0.22 2.9–3.9 19–35 mm In vitro filtration rates with a

culture of Dunaliella

Kato et al. (1982)

1.47–1.92 1.1–1.5 35–55 mm In vitro filtration rates with a

culture of Dunaliella

Kato et al. (1982)

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

2.0

16–50 mm Radiocarbon method, phytoplankton

cultures and detritus as food

Samyshev and Lushov (1983)

3.6–5.04 2.3–10.0 40–50 mm In vitro filtration and ingestion

rates with net phytoplankton, furcilia

of E. superba and infusoria as food

Boyd et al. (1984)

0.38–2.05 2.6–17.1 30–35 mm In vitro ingestion rates with net

phytoplankton as food

Schnack (1985a, b)



Schnack (1985a, b)



Schnack (1985a, b)

9.5–17.9 17–28 40–50 mm Faecal pellet evacuation rates using

net phytoplankton as food

Clarke et al. (1988)

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

and Artemia nauplii as food

Krylov (1989)

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)

0.022–0.024 mean 4.4 furcilia 4–5 In situ and in vitro filtration rates,


Huntley and Brinton (1991)

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

thompsoni aggregates as food

Kawaguchi and Takahashi

(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)


thompsoni ingestion rates and ambient phyto-plankton concentration has been documented inthe chlorophyll-a range of 0.2–1.2 mg l�1 (Pakho-mov and Froneman, 2002b). A linear functionalresponse of ingestion rates versus food concentra-tion may apply only to a relatively narrow range ofparticle concentrations, as it has been shown thatat higher concentrations salp feeding can bedisrupted (Harbison et al., 1986; Zeldis et al.,1995; Perissinotto and Pakhomov, 1997). Theupper concentration threshold for S. thompsoni isnot clearly defined. However, in the Lazarev Sea2–5 cm long aggregates of S. thompsoni are unableto graze at particle concentrations >1 mg l�1

(Perissinotto and Pakhomov, 1997).To date, there are only seven literature sources

dealing with estimates of gut pigment content,filtration, ingestion and egestion rates of S.

thompsoni in the Atlantic sector of the SouthernOcean (Reinke, 1987; Drits and Semenova, 1989;Huntley et al., 1989; Drits and Pasternak, 1993;Dubischar and Bathmann, 1997; Perissinotto andPakhomov, 1998a, b; Pakhomov, 2002). Poolingthese data, a significant linear relationship betweenlog-transformed salp length and gut pigmentcontent is obtained (Fig. 6). As expected, clearancerates of S. thompsoni increase with body length(Fig. 7). Although derived from several authors,the ingestion rates of S. thompsoni are remarkablysimilar and consistent. Changes in ingestion ratesas a function of salp length are best represented bya power function. However, the global data set isbest fitted by a polynomial function, or by a linearfunction when log-transformed (Fig. 8). Whenconverted to carbon units, S. thompsoni ingestionrates increase linearly with the carbon mass of thesalp body (Fig. 9). Interestingly, daily rations of S.

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 wt�1 d�1) 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)

y = 1.7291x + 0.6089

R2 = 0.8381, N = 470

0

1

2

3

4

5

0.5 1 1.5 2 2.5

Log salp length (mm)

Log

pigm

ent c

onte

nt (

ng(p

igm

).in

d.-1

)

Fig. 6. Gut pigment content of S. thompsoni as a function of

body length. Data were extracted mainly from Dubischar and

Bathmann (1997), Perissinotto and Pakhomov (1998a, b), and

Pakhomov and Froneman (2002b).

y = 1.8603x - 1.4266

R2 = 0.8439N = 16

0

0.5

1

1.5

2

2.5

0.5 1 1.5 2 2.5


Log

clea

ranc

e ra

te (

I.ind

.-1 d

-1)

Fig. 7. Clearance rates of S. thompsoni as a function of body

length. Data extracted from Reinke (1987); Drits and Semenova

(1989); Huntley et al. (1989), Drits and Pasternak (1993),

Dubischar and Bathmann (1997), Perissinotto and Pakhomov

(1998a, b), and Pakhomov, 2002).


thompsoni do not show a distinct trend, either withincreasing body length or with body carbon mass(Fig. 10).

Overall, in situ individual ingestion and clear-ance rates of S. thompsoni are the highest of anyother primary consumer in the Antarctic pelagiccommunity (e.g., Drits and Semenova, 1989; Dritsand Pasternak, 1993; Froneman et al., 1997;Perissinotto and Pakhomov, 1998a, b; Pakhomov,2002; Pakhomov and Froneman, 2002a, b). Inges-tion rates of S. thompsoni estimated with in vitroincubations are up to one order of magnitudelower than in situ consumption rates (Fig. 11).Therefore, in vitro estimated consumption ratesare most likely erroneous due to such things assmall volume, stress during capture, short adapta-tion time, particularly when large specimens areincubated.

Unlike for Antarctic krill, there is little informa-tion available on egestion rates of S. thompsoni. Ina single experiment conducted near the AntarcticPeninsula during austral summer 1983/84, a21 mm blastozoid of S. thompsoni egested 10.2%of body carbon and 6.6% of body nitrogen perday, which accounted for 40.7% and 48.8% of thecarbon and nitrogen ingested, respectively (Hunt-ley et al., 1989). During the summer season 1997/98, in the region south of the APF and along 61E,daily egestion rates of S. thompsoni ranged from187.8 ng (pigm) ind�1 d�1 (or 9.4 mg C ind�1 d�1) in10 mm salps, to 3.57 mg (pigm) ind�1 d�1 (or178.6 mg C ind�1 d�1) in 55 mm salps (Fig. 12).Although in situ egestion rates on averageaccounted for 36% (range 22–56%) of the in situpigment consumption, they were equivalent toonly 0.9–3.5% of body carbon (Pakhomov, 2002).

4.3. Krill/salp particle selectivity

As non-selective filter-feeders, salps are able toretain efficiently particles within a wide size range,

y = 2.8795x2.3194

R2 = 0.9427N = 15

y = 13.06x2 - 34.304x - 1719.2

R2 = 0.9861, N = 32

0

20

40

60

80

140

120

100

0 20 40 60 80 100 120

Salp total length (mm)

Inge

stio

n ra

te (

µg(p

igm

).in

d-1.d

-1)

Pakhomov, in press Dubischar & Bathmann, 1997

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

Huntley et al., 1989 Drits & Pasternak, 1993

y = 2.0948x + 0.7424

R2 = 0.821, N = 32

2

3

4

5

6

0.7 0.9 1.1 1.3 1.5 1.7 1.9 2.1


Log

inge

stio

n ra

te (

ng(p

igm

).in

d-1.d

-1)

(a)

(b)

Fig. 8. A summary of daily ingestion rates of S. thompsoni as a

function of body length.

y = 0.2167x - 118.91

R2 = 0.953, N = 32

0

7000

6000

5000

4000

3000

2000

1000

0 5000 10000 15000 20000 25000 30000 35000

Salp carbon body weight (µg)

Inge

stio

n ra

te (

µgC

.ind.

-1.d

-1)

y=1.9913x - 0.3605

R2 = 0.7978, N = 32

1

1.5

2

2.5

3

3.5

4

0.5 1 1.5 2 2.5

Log Salp length (mm)

Log

IR (

mic

rogr

am C

.ind.

-1.d

-1)

Fig. 9. Carbon daily ingestion rates of S. thompsoni as a

function of carbon body mass and body length.


ranging from 1 to 1000 mm (Drits and Semenova,1989; Fortier et al., 1994), while Antarctic krillconsumes mainly food particles >10–o50 mm(Meyer and El-Sayed, 1983; Drits and Semenova,1989; Maciejewska, 1993; Opalinski et al., 1997).

4.4. Krill/salp grazing impact: implications for

vertical carbon flux

Table 4 summarizes estimates of grazing impactfor Antarctic krill and S. thompsoni obtained usinga variety of techniques. With the exception of twoestimates obtained by Dubischar and Bathmann(1997) and by Perissinotto and Pakhomov(1998a, b), the highest impacts are derived fromindirect estimates of the energetic requirements ofkrill and salps, under the assumption that allcarbon demands are met through an herbivorousdiet (Table 4). This is incorrect since bothAntarctic krill and S. thompsoni are known toconsume a substantial proportion of heterotrophicmaterial (Foxton, 1966; Hopkins, 1985; Hopkinsand Torres, 1989; Hopkins et al., 1993; Lancraftet al., 1991; Perissinotto et al., 1997, 2000).Overall, the grazing impact of both krill and salpsis moderate through most of the Southern Ocean,and even in areas where they co-occur they usuallydo not make sufficient impact to control phyto-plankton growth (Pakhomov, 2002; Pakhomovand Froneman, 2002b). This, however, might bean underestimate as Chla/carbon ratio of 50 wasemployed in most of these studies.

Regarding the contribution of krill and salps tothe vertical carbon flux, data suggest that it isindeed extremely variable, reflecting the naturalpatchiness of food and of both species. Based ondirect (fecal pellet production) and indirect (graz-ing impact and assimilation efficiency) data,Antarctic krill may account on average for a

0

10

20

30

40

50

0 20 40 60 80 100 120

Salp body length (mm)

Dai

ly ra

tion

(% b

ody

carb

on)

N = 32

0

10

20

30

40

50

0 5000 10000 15000 20000 25000 30000 35000

Salp carbon body weight (microgram)

Dai

ly ra

tion

(% b

ody

carb

on)

N = 32

Fig. 10. Carbon daily rations as percentage of body carbon of

S. thompsoni as a function of body length and body carbon

weight.

0

10000

20000

30000

40000

50000

60000

70000

30 40 70

Salp length (mm)

Inge

stio

n ra

te (

ng(p

igm

).in

d.-1

d-1)

in situ in vitro

Fig. 11. Comparison between in situ and in vitro estimated

ingestion rates of S. thompsoni. Data extracted from Dubischar

and Bathmann (1997) and Pakhomov (2002).

y = 1.6328x + 0.6634

R2 = 0.8901

1

2

3

4

1.81.71.61.51.41.31.21.110.9


Log

eges

tion

rate

(ng(

pigm

).in

d.-1

d-1)

Fig. 12. Egestion rates of S. thompsoni as a function of body

length. Data extracted from Pakhomov (2002).


vertical flux of feces ranging from 0.01 to 15.6 mgC m�2 d�1 (Pakhomov et al., 1997; Ross et al.,1998; Pakhomov, 2002). While swarming, Antarc-

tic krill are able to contribute a vertical flux ofbetween 44.9 mg C m�2 d�1 and 1.3 gC m�2 d�1

(Clarke et al., 1988; Pakhomov et al., 1997). The

Table 4

Summary of grazing impact estimates of Antarctic krill and Salpa thompsoni

Geographical location Season Daily grazing impact Source

% Chla

stock

% daily PP

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.


above values are in the range of those obtainedfrom sediment trap collections in different regionsof the high Antarctic, where krill feces were foundto contribute up to 80% of total particle carbonflux in the top 200–300 m (Schnack, 1985a, b; vonBodungen, 1986; N .othig and von Bodungen, 1989;Bathmann et al., 1991; Gonzalez, 1992).

Although the salp contribution to the verticalcarbon flux in the Southern Ocean has yet to bemeasured through sediment trap collections, S.

thompsoni feces potentially may account for0.1–88 mg C m�2 d�1 (Huntley et al., 1989; Peri-ssinotto and Pakhomov, 1998a, b; Ross et al.,1998; Pakhomov, 2002). It is estimated thattogether Antarctic krill and S. thompsoni may re-package and remove up to 20% of phytoplanktonproduction per day from the euphotic zone(Pakhomov, 2002). As S. thompsoni has lower(Pakhomov, 2002) or similar (Huntley et al., 1989)carbon mass specific egestion rates than Antarctickrill (Fig. 13), maximum salp contribution to thevertical flux in carbon units should be substantiallylower, due to the differences in carbon densitiesbetween the two species (see Section 3.1).

Antarctic krill is known to channel a largefraction of ingested material into a long-lived (e.g.,food web transport) carbon pool (sensu Fortieret al., 1994), while salps are more important insequestering biogenic carbon, by producing large,fast sinking feces (Le F"evre et al., 1998). Indeed,Antarctic krill is a well known food source fornumerous Antarctic top predators, includingsquid, demersal and mesopelagic fish, flying birdsand penguins, seals and whales (Knox, 1994).Antarctic top predators are thought to consumebetween 166� 106 and 450� 106 tonnes of Ant-arctic krill annually (Lubimova and Shust, 1980;Laws, 1985; Miller and Hampton, 1989). Salp-mediated export to the top predators is much lessknown. It has been suggested that the export maybe both direct and indirect (Le F"evre et al., 1998).Data gathered from literature sources, show that asubstantial number of Antarctic zooplanktonspecies (13), including Antarctic krill, 8 birdspecies and 24 species of fish may consume salpsin energetically meaningful amounts (Table 5). It isbecoming obvious that salps are not a trophic cul-

de-sac in the Antarctic ecosystem and may actually

play a more important role in the ecosystembudget than previously believed.

5. Krill/salp interactions: competitive exclusion or

biotopical separation?

The increasing interest developed towards krilland salp interactions in the Southern Ocean overthe past few decades has led to the formulation ofseveral hypotheses to explain their spatial separa-tion (Nishikawa et al., 1995). Firstly, it has beensuggested that salps may prey (filter out) on eggsand early larval stages of Antarctic krill, thusaffecting krill recruitment (Huntley et al., 1989).This hypothesis was based on the occurrence ofkrill debris and larvae in food boluses of S.

thompsoni (Foxton, 1966; Hopkins, 1985; Hopkinsand Torres, 1989; Hopkins et al., 1993; Lancraftet al., 1991). However, due to the verticalsegregation of Antarctic krill eggs/early stagesand salps, direct consumption appears to benegligible (Perissinotto and Pakhomov, 1998b).Even if salps prey upon early developmental stagesof Antarctic krill, the effect will only be noticeablein later years and, as a consequence, cannotexplain the spatial segregation of salps and adultkrill during a particular season.

Secondly, salps may produce distasteful meta-bolic products, which may drive krill away(Fraser, 1962). This hypothesis cannot be dis-carded although it has never been tested. In

Fig. 13. Mass specific egestion rates of E. superba and S.

thompsoni as a function of body carbon mass. Data extracted

from Table 3 and from Pakhomov (2002).


Table 5

Predators of Salpa thompsoni in the Southern Ocean

Predator name Consumption rate Source

Crustaceans

Euphasuia superba 0.5 salp. krill�1 d�1 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

melanophris)

nd Foxton (1966)

Gray-headed Albatross (Diomedea

chrysostoma)

nd Foxton (1966)

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

oceanicus)

1.8% of FBW Ainley et al. (1991)

White-chinned Petrel (Procellaria

aequinoctialis)

10–15 FO; 0.3–1.5% of PN Catard et al. (2000)

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)


contrast, recent observations have shown thatAntarctic krill is actually attracted to S. thompsoni

extracts and is able to prey successfully on salpswith a meaningful rate of up to 0.5 salps per krillper day, or E8.7% of body carbon per day (Table2; Kawaguchi and Takahashi, 1996).

Thirdly, Antarctic krill may be excluded fromthe areas of high salp densities because salps mayoutcompete other zooplankton, including krill, forfood (Fraser, 1962; Perissinotto and Pakhomov,1998b). Salps are indeed efficient at retainingparticles within a wide size range, while Antarctickrill prey selectively on specific food particles(Section 4.3). Although it is almost impossible toverify the above hypothesis in the marine environ-ment (Le F"evre et al., 1998), there is indirectevidence that competition between salps andAntarctic krill for food is negligible. No directinteractions between the proportion of green krill(intensively feeding krill) and salp density has beenobserved around the Antarctic Peninsula regionusing a comprehensive data set collected duringthe Japanese krill fishing operations (Kawaguchiet al., 1998). The authors also noticed a clearspatial and temporal mismatch between salps andgreen krill and linked this to the appearance ofwarmer waters in the region (Kawaguchi et al.,1998).

Competitive removal of food may be the majorseparating force of krill and salp concentrations(Perissinotto and Pakhomov, 1998b) when they

are found together spatially and temporally, whichdoes not seem to be the case on most occasions(Kawaguchi et al., 1998). Recently, it has beenhypothesized that food availability prior to theinteraction, rather than direct food competitionbetween different herbivores, may be responsiblefor competitive exclusion (Chiba et al., 1998). Ifthis applies to Antarctic krill and salps, it meansthat in the high Antarctic region we alwaysobserve the end result of the competition ratherthan the process itself, even despite extensiveseasonal coverage. We are of the opinion thatdirect competition for food may indeed be valid inthe long-term (Loeb et al., 1997), while this wouldnot explain the short-term inverse distributionbetween krill and salps (Chiba et al., 1998).Finally, most recently an approach comparingthe carbon budgets of major metazoan herbivoresin the Southern Ocean has been used (Le F"evreet al., 1998). According to these calculations,resource thresholds at which herbivores are ableto fulfill their basic metabolic requirements are3.5–30 mg C l�1 for S. thompsoni, 105 mg C l�1 forcopepods and 125 mg C l�1 for Antarctic krill (LeF"evre et al., 1998). This clearly implies that salpsmay survive successfully at low food concentra-tions compared, for example, to Antarctic krill.Interestingly, the empirical upper threshold of>1 mg chlorophyll-a l�1, at which salp cloggingmay occur (Perissinotto and Pakhomov, 1997),would be equal to 7100 mg C l�1, after converting

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.


to carbon and adding a heterotrophic component(following Le F"evre et al., 1998). Therefore, ifsalps would be able to maintain low foodconcentration, this may prevent development ofcopepods and Antarctic krill (Chiba et al., 1998;Perissinotto and Pakhomov, 1998a, b). It is likely,however, that once a phytoplankton bloom devel-ops within the Marginal Ice Zone, salps woulddisappear to the advantage of other zooplanktonsuch as krill and copepods, which are moreadapted to operate in the presence of high particleconcentrations (Nishikawa et al., 1995; Perissinot-to and Pakhomov, 1998b).

Finally, the spatial separation between krill andsalp populations may be due to the advection ofdifferent water masses in the region (Kawamuraet al., 1994; Kawaguchi et al., 1998). Thishypothesis has already been discussed above(Section 3.2.2) and seems to explain the limitedspatial overlap observed in krill/salp distributionoutside the Antarctic Peninsula region (see alsoNicol et al., 2000b). Although a small-scalesynchronized pattern between salp density andelevated sea-surface temperatures has been noticedaround the Antarctic Peninsula in number ofstudies (e.g., Nast, 1986; Piatkowski, 1989; Nishi-kawa et al., 1995; Minkina et al., 1999), thedistribution patterns of both Antarctic krill and S.

thompsoni are still to be studied in detail there,with particular emphasis to environmental vari-ables characterizing this area.

It appears that Antarctic krill and S. thompsoni

are adapted to be successful in biotopes withdifferent environmental conditions (Table 6, afterLe F"evre et al., 1998). These biotopes broadlycharacterize the open-ocean and coastal environ-ments, e.g., spatially separated realms (Nicol et al.,

2000b). However, in the regions of complex andvariable oceanography (e.g., off Antarctic Penin-sula, within the Marginal Ice Zone and polynyas)spatial separation, particularly in the macro-scale,becomes unclear. As a consequence, in suchregions krill and salp may theoretically co-existover short periods of time (Le F"evre et al., 1998).Nevertheless, the physiological constrains may beof crucial importance in keeping Antarctic krilland S. thompsoni separated in the long-term.Therefore, the environmental warming may leadto the increase in degree of spatial and temporaloverlap between these two large metazoans of theSouthern Ocean (see also Section 3.2.2). Theregional ecological consequences of the salp years,as discussed above, may be dramatic, suggestingthat if the warming trend will continue in the highAntarctic, salps would probably play more pro-minent role in the trophic structure of theAntarctic marine ecosystem. This could be coupledwith the dramatic decrease in krill productivitylargely due to decrease in the spatial extension ofthe krill biotope and inter-specific salp/krill inter-actions. High Antarctic regions, particularly theMarginal Ice Zone, however, have effectiveprotective mechanisms against salp invasions,e.g., low temperatures (reproduction constrains,Chiba et al., 1999) and high particle concentra-tions associated with the ice retreat (Perissinottoand Pakhomov, 1997).

Acknowledgements

This synthesis was completed with the financialsupport of the South African Department ofEnvironmental Affairs and Tourism (Pretoria)

Table 6

Environmental conditions under which salps and krill are expected to succeed (after Le F"evre 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


and the South African National Research Foun-dation (Pretoria).

References

Ainley, D.G., Fraser, W.R., Daly, K.L., 1988. Effects of pack

ice on the composition of micronektonic communities in the

Weddell Sea. In: Sahrhage, D. (Ed.), Antarctic Ocean and

Resources Variability. Springer, Berlin, Heidelberg, pp.

140–146.

Ainley, D.G., Fraser, W.R., Smith Jr, W.O., Hopkins, T.L.,

Torres, J.J., 1991. The structure of upper level pelagic food

webs in the antarctic: effect of phytoplankton distribution.

Journal of Marine Systems 2, 111–122.

Alcaraz, M., Saiz, E., Fernandez, J.A., Trepat, I., Figueiras, F.,

Calbet, A., Bautista, B., 1998. Antarctic zooplankton

metabolism: carbon requirements and ammonium excretion

of salps and crustacean zooplankton in the vicinity of the

Bransfield strait during January 1994. Journal of Marine

Systems 17, 347–359.

AMLR 1993/94 Field Season Report. Objectives, accomplish-

ments and tentative conclusions. 1994. Southwest Fisheries

Science Center. Atlantic Ecosystem Research Group.

Administrative report LJ-94-13.

Antezana, T., Ray, K., Melo, C., 1982. Trophic behavior of

Euphausia superba Dana in laboratory conditions. Polar

Biology 1, 77–82.

Bathmann, U., Fischer, G., M .uller, P.J., Gerdes, D., 1991.

Short-term variations in particular matter sedimentation off

Kapp Norvegia, Weddell Sea, Antarctica: relation to water

mass advection, ice cover, plankton biomass and feeding

activity. Polar Biology 11, 185–195.

Bibik, V.A., Maslennikov, V.V., Pelevin, A.S., Polonsky, V.E.,

Solyankin, E.V., 1988. The current system and the distribu-

tion of waters of different modifications in the Cooperation

and Cosmonaut Seas. In: Makarov, R.R. (Ed.), Interdisci-

plinary Investigations of Pelagic Ecosystem in the Coopera-

tion and Cosmonaut Seas. VNIRO Publishers, Moscow, pp.

16–43.(in Russian)

Booth, B.C., Lewin, J., Postel, J.R., 1993. Temporal variations

in the structure of autotrophic and heterotrophic commu-

nities in the subarctic pacific. Progress in Ocenography 32,

57–99.

Boyd, C.M., Heyraud, M., Boyd, C.N., 1984. Feeding of the

Antarctic krill Euphausia superba. Journal of Crustacean

Biology 4, 123–141.

Boysen-Ennen, E., Piatkowski, U., 1988. Meso- and macro-

zooplankton communities in the Weddell Sea, Antarctica.

Polar Biology 9, 17–35.

Boysen-Ennen, E., Hagen, W., Hubold, G., Piatkowski, U.,

1991. Zooplankton biomass in the ice-covered Weddell Sea,

Antarctica. Marine Biology 111, 227–235.

Brinton, B., 1984. Observations of plankton organisms

obtained by Bongo nets during the November–December

1983 ice-edge investigations. Antarctic Journal of the

United States 19 (5), 113–115.

Casareto, B.E., Nemoto, T., 1986. Salps of the Southern Ocean

(Australian sector) during the 1983–84 summer, with special

reference to the species Salpa thompsoni. Memories of

National Institute of Polar Research 40, 221–239.

Catard, A., Weimerskirch, H., Cherel, Y., 2000. Exploitation of

distant Antarctic waters and close shelf-break waters by

white-chinned petrels rearing chicks. Marine Ecology

Progress Series 194, 249–261.

Chechun, I.S., 1984. Feeding and trophic relationships of

some fish from the sub-Antarctic waters of the Indian

Ocean. Proceedings of the Zoological Institute, USSR

Academy of Sciences, Leningrad, Vol. 127, pp. 38–68 (in

Russian).

Chekunova, V.I., Rynkova, T.I., 1974. Energy requirements of

the Antarctic crustacea Euphausia superba Dana. Oceanol-

ogy 14, 434–440.

Chiba, S., Horimoto, N., Saton, R., Yamaguchi, Y., Ishimaru,

T., 1998. Macrozooplankton distribution around the

Antarctic Divergence off Wilkes Land in the 1996 austral

summer: with reference to high abundance of Salpa

thompsoni.. Proceedings of the NIPR Symposium on Polar

Biology 11, 33–50.

Chiba, S., Ishimaru, T., Hosie, G.W., Wright, S.W., 1999.

Population structure change of Salpa thompsoni from

austral mid-summer to autumn. Polar Biology 22, 341–349.

Clarke, A., Morris, D.J., 1983. Towards an energy budget for

krill: the physiology and biochemistry of Euphausia superba

Dana. Polar Biology 2, 69–86.

Clarke, A., Quetin, L.B., Ross, R.M., 1988. Laboratory and

field estimates of the rate of faecal pellet production by

Antarctic krill, Euphausia superba. Marine Biology 98,

557–563.

Daly, K.L., 1990. Overwintering development, growth and

feeding of larval Euphausia superba in the Antarctic

marginal ice zone. Limnology and Oceanography 35,

1564–1576.

De la Mare, W.K., 1997. Abrupt mid-twentieth-century decline

in Antarctic sea-ice extent from whaling records. Nature

389, 57–60.

Doake, C.S.M., Vaughan, D.G., 1991. Rapid disintegration of

the Word Ice Shelf in response to atmospheric warming.

Nature 350, 328–330.

Donnelly, J., Torres, J.J., Hopkins, T.L., Lancraft, T.M., 1994.

Chemical composition of Antarctic zooplankton during

austral fall and winter. Polar Biology 14, 171–183.

Drits, A.V., Pasternak, A.F., 1993. Feeding of dominant species

of the Antarctic herbivorous zooplankton. In: Voronina,

N.M. (Ed.), Pelagic Ecosystems of the Southern Ocean.

Nauka Press, Moscow, pp. 250–259.(in Russian)

Drits, A.V., Semenova, T.N., 1989. Trophic characteristics of

major planktonic phytphages from South Shetland Islands

region during early spring. In: Ponomareva, L.A. (Ed.),

Complex Investigations of the Pelagic Zone of the Southern

Ocean. Shirshov Institute Oceanology Publishers, Moscow,

pp. 66–78.(in Russian)


Dubischar, C.D., Bathmann, U.V., 1997. Grazing impact of

copepods and salps on phytoplankton in the Atlantic sector

of the Southern Ocean. Deep-Sea Research II 44, 415–433.

Duhamel, G., 1981. Caract!eristiques biologiques des principales

esp"eces de poissons do plateau continental des #ıles

Kerguelen. Cybium 5, 19–33.

Duhamel, G., Hureau, J.C., 1985. The role of zooplankton in

the diets of certain sub-Antarctic marine fish. In: Siegfried,

W.G., Condy, P.R., Laws, R.M. (Eds.), Antarctic Nutrient

Cycles and Food Webs. Springer, Berlin, Heidelberg, pp.

420–429.

Duhamel, G., Pletikosic, M., 1983. Donn!ees biologiques sur les

Nototheniidae des #ıles Crozet. Cybium 7, 43–57.

Fortier, L., Le F"evre, J., Legendre, L., 1994. Export of biogenic

carbon to fish and to the deep ocean: the role of large

planktonic microphages. Journal of Plankton Research 16,

809–839.

Foxton, P., 1966. The distribution and life history of Salpa

thompsoni Foxton with observations on a related species

S.gerlachei Foxton. Discovery Reports 34, 1–116.

Fransz, H.G., Gonzalez, S.R., 1997. Latitudinal metazoan

plankton zones in the Antarctic Circumpolar Current along

61W during austral spring 1992. Deep-Sea Research II 44,

395–414.

Fraser, J.H., 1962. The role of ctenophores and salps in

zooplankton production and standing crop. Rapports et

Proces-Verbaux des Reunions Conseil Perm International

Exploration de la Mer 153, 121–123.

Froneman, P.W., Pakhomov, E.A., Perissinotto, R.,

Laubscher, R.K., McQuaid, C.D., 1997. Dynamics of the

plankton communities during seasonal ice melt in the

Lazarev Sea in austral summer 1994–1995. Marine Ecology


Froneman, P.W., Pakhomov, E.A., Perissinotto, R., McQuaid,

C.D., 2000. Zooplankton structure and grazing in the

Atlantic sector of the Southern Ocean in late austral

summer 1993. Part 2. Biochemical zonation. Deep-Sea

Research I 47, 1687–1702.

Gammie, F., 1995. Breakaway iceberg due to warming. Nature

374, 108.

Gloersen, P., Campbell, W.J., 1991. Recent variations in Arctic

and Antarctic Sea-Ice Covers. Nature 352, 33–36.

Godlewska, M., 1989. Energy flow through the main phyto-

phagous species in the Bransfield Strait and Drake Passage

during SIBEX 1983/1984. Proceedings of the 21st European

Marine Biology Symposium, Gdansk, 14–19 September

1986, Wroclaw, etc., pp. 291–296.

Gonzalez, H.E., 1992. The distribution and abundance of krill

faecal material and oval pellets in the Scotia and Weddell

Seas (Antarctica) and their role in particle flux. Polar

Biology 12, 81–91.

Grachev, D.G., 1991. Frontal zone influences on the distribu-

tion of different zooplankton groups in the central part of

the Indian sector of the Southern Ocean. In: Samolova,

M.S., Shumkova, S.O. (Eds.), Ecology of Commercial

Marine Hydrobionts. TINRO Press, Vladivostok, pp.


Hagen, W., 1988. On the significance of lipids in Antarctic

zooplankton. Berichte zur Polarforschung 49, 1–129.

Hampton, I., 1985. Abundance, distribution and behaviour of

Euphausia superba in the Southern Ocean between 151 and

301E during FIBEX. In: Siegfried, W.R., Condy, P.R.,

Laws, R.M. (Eds.), Antarctic Nutrient Cycles and Food

Webs. Springer, Berlin, pp. 294–303.

Harbison, G.R., McAlister, V.L., Gilmer, R.W., 1986. The

response of the salp, Pegea confoederata, to high levels of

particulate material: starvation in the midst of plenty.

Limnology and Oceanography 31, 371–382.

Helbling, E.W., Sala, L.O., Loeb, V., 1992. AMLR program:

feeding of krill around Elephant Island, AntarcticaFphy-

toplankton biomass in digestive tracts and rates of

clearance. Antarctic Journal of the United States 27 (5),

217–218.

Hempel, G., 1985. On the biology of polar seas, particularly the

Southern Ocean. In: Gray, J.S., Christiansen, M.E. (Eds.),

Marine Biology of Polar Regions and Effects of Stress on

Marine Organisms. Wiley, Chichester, pp. 3–33.

Heron, A.C., 1972. Population ecology of a colonizing species:

the pelagic tunicate Thalia democratica: I. Individual growth

rates and generation time. Oecologia 10, 269–293.

Heron, A.C., Benham, E.E., 1984. Individual growth rates of

salps in three populations. Journal of Plankton Research 6,

811–828.

Hewitt, R.P., 1997. Areal and seasonal extent of sea-ice cover

off the northwestern side of the Antarctic Peninsula: 1979 to

1996. CCAMLR Science 4, 65–73.

Holm-Hansen, O., Huntley, M., 1984. Feeding requirements of

krill in relation to food sources. Journal of Crustacean

Biology 4, 156–178.

Hopkins, T.L., 1985. Food web of an Antarctic midwater

ecosystem. Marine Biology 89, 197–212.

Hopkins, T.L., Torres, J.J., 1989. Midwater food web in the

vicinity of marginal ice zone in the western Weddell Sea.

Deep-Sea Research I 36, 543–560.

Hopkins, T.L., Ainley, D.G., Torres, J.J., Lancraft, T.M., 1993.

Trophic structure in open waters of the marginal ice zone in

the Scotia-Weddell confluence region during spring (1983).

Polar Biology 13, 389–397.

Hosie, G.W., 1994. The macrozooplankton communities

in the Prydz Bay region, Antarctica. In: El-Sayed, S.Z.

(Ed.), Southern Ocean Ecology. The BIOMASS

Perspective. Cambridge University Press, Cambridge, pp.

93–123.

Hosie, G.W., Cochran, T.G., 1994. Mesoscale distribution

patterns of macrozooplankton communities in Prydz Bay,

AntarcticaFJanuary to February 1991. Marine Ecology


Hosie, C.W., Schultz, M.B., Kitchener, J.A., Cochtan, T.G.,

Richards, K., 2000. Macrozooplankton community struc-

ture off East Antarctica (80–1501E) during the austral

summer of 1995/1996. Deep-Sea Research II 47, 2437–2463.

Hosie, G.W., Cochran, T.G., Pauly, T., Beaumont, K.L.,

Wright, S.W., Kitchener, J.A., 1997. Zooplankton commu-

nity structure of Prydz bay, Antarctica, January–February


1993. Proceedings of the NIPR Symposium on Polar

Biology 10, 90–133.

Huntley, M., Brinton, E., 1991. Mesoscale variation in growth

and early development of Euphausia superba Dana in the

Western Bransfield Strait region. Deep-Sea Research I 38,

1213–1240.

Huntley, M., Nordhausen, W., Lopez, M.D.G., 1994. Ele-

mental composition. metabolic activity and growth of

Antarctic krill Euphausia superba during winter. Marine

Ecology Progres Series 107, 23–40.

Huntley, M.E., Sykes, P.F., Marin, V., 1989. Biometry and

trophodynamics of Salpa thompsoni Foxton (Tunicata:

Thaliacea) near the Antarctic Peninsula in Austral summer,

1983–1984. Polar Biology 10, 59–70.

Iganake, D., Matsuura, E., Kurita, Y., 1984. Stock and

quantitative distribution of the Antarctic krill (Euphausia

superba Dana) in the Antarctic Ocean south of Australia in

January and February 1984. Transactions of Tokyo

University of Fisheries 6, 139–147.

Ikeda, T., Bruce, B., 1986. Metabolic activity and elemental

composition of krill and other zooplankton from Prydz Bay,

Antarctica, during early summer (November–December).

Marine Biology 92, 545–555.

Ikeda, T., Mitchell, A.W., 1982. Oxygen uptake, ammonia

excretion and phosphate excretion by krill and other

Antarctic zooplankton in relation to their body size and

chemical composition. Marine Biology 71, 283–298.

Johannessen, O.M., Miles, M., Bjorgo, E., 1995. The arctic’s

shrinking sea ice. Nature 376, 126–127.

Kato, M., Segawa, S., Tanoue, E., Murano, M., 1982. Filtering

and ingestion rates of the Antarctic krill, Euphausia superba

Dana. Transactions of Tokyo University of Fisheries 5,

167–175.

Kawaguchi, S., Takahashi, Y., 1996. Antarctic krill

(Euphausia superba Dana) eat salps. Polar Biology 16,

479–481.

Kawaguchi, S., Ichii, T., Naganobu, M., de la Mare, W.K.,

1998. Do krill and salps compete? Contrary evidence from

the krill fisheries. CCAMLR Science 5, 205–216.

Kawamura, A., 1986. Has marine Antarctic ecosystem chan-

ged?FA tentative comparison of present and past macro-

zooplankton abundances. Memories of National Institute of

Polar Research 40, 197–211.

Kawamura, A., 1987. Two series of macrozooplankton catches

with the H70 V net in the Indian sector of the Antarctic

Ocean. Proceedings of the NIPR Symposium on Polar

Biology 1, 84–89.

Kawamura, A., Michimori, K., Moto, J., 1994. Marked

inverse distribution of salps to other macrozooplankton

in waters adjacent to the South Shetland Islands.

Proceedings of the NIPR Symposium on Polar Biology 7,

70–81.

Klyausov, A.V., 1993. On the frontal zone near the northern

boundary of sea ice area distribution in the Southern Ocean.

Oceanology 33, 824–832.

Knox, G.A., 1994. The biology of the Southern Ocean.

Cambridge University Press, Cambridge.

Kozlov, A.N., Tarverdieva, M.I., 1989. Feeding of different

species of Myctophidae in different parts of the Southern

Ocean. Journal of Ichthyology 23 (3), 160–167.

Krylov, P.I., 1989. Carnivore feeding of Euphausia superba

Dana. In: Ponomareva, L.A. (Ed.), Complex Investigations

of the Pelagic Zone of the Southern Ocean. Shirshov

Institute Oceanology Publishers, Moscow, pp. 94–105.(in

Russian)

Lancraft, T.M., Hopkins, T.L., Torres, J.J., Donnelly, J., 1991.

Oceanic micronektonic/macrozooplanktonic community

structure and feeding in ice covered Antarctic waters during

the winter (AMERIEZ 1988). Polar Biology 11, 157–167.

Lancraft, T.M., Torres, J.J., Hopkins, T.L., 1989. Micronekton

and macrozooplankton in the open waters near Antarctic

ice edge zones (AMERIEZ 1983 and 1986). Polar Biology 9,

225–233.

Laws, R.M., 1985. The ecology of the Southern Ocean.

American Scientist 1, 36–40.

Le F"evre, J., Legendre, L., Rivkin, R.B., 1998. Fluxes of

biogenic carbon in the Southern Ocean: roles of large

microphagous zooplankton. Journal of Marine Systems 17,

325–345.

Levitus, S., Antonov, J.I., Boyer, T.P., Stephens, C., 2000.

Warming of the World Ocean. Science 287, 2225–2229.

Loeb, V., Siegel, V., Holm-Hansen, O., Hewitt, R., Fraser, W.,

Trivelpiece, W., Trivelpiece, S., 1997. Effects of sea-ice

extent and krill or salp dominance on the Antarctic food

web. Nature 387, 897–900.

Lubimova, T.G., Shust, K.V., 1980. Assessment of Antarctic

krill consumption by main groups of consuments. In:

Lubimova, T.G. (Ed.), Biological Resources of Antarctic

Krill (Collected papers). VNIRO Publishers, Moscow, pp.


Maciejewska, K., 1993. Feeding of Antarctic krill Euphausia

superba in Weddell Sea. Polish Polar Research 14, 52–54.

Mackintosh, N.A., 1973. Distribution of postlarval krill in the

Antarctic. Discovery Reports 36, 95–156.

Makarov, R.R., Solyankin, E.V., 1990. Abundant copepods

and regional reculiarities of their seasonal development in

the east area of the Weddell Gyre. In: Solyankin, E.V. (Ed.),

Investigations of the Weddell Gyre. Oceanographic condi-

tions and peculiarities of the development of plankton

communities. VNIRO Publishers, Moscow, pp. 140–167.

(in Russian)

Makarov, R.R., Spiridonov, V.V., 1993. Life cycle and

distribution of the Antarctic krill. Some results of the

studies and problems. In: Voronina, N.M. (Ed.), Pelagic

Ecosystems of the Southern Ocean. Moscow, Nauka Press,

pp. 158–168.(in Russian)

Makarov, R.R., Sysoeva, M.V., 1983. Biological condition and

distribution of Euphausia superba Dana in the Lazarev Sea

and adjacent waters. In: Antarctic krill. The distribution

pattern and environment (Collected papers). Legkaja i

pishevaja promyshlennost Press, Moscow, pp. 110–117

(in Russian).

Maklygin, L.G., Pakhomov, E.A., 1993. Vertical distribution

and diurnal migrations of Antarctic macrozooplankton


(February–March 1989, Atlantic sector of the Southern

Ocean). In: Klekowski, R.Z., Opalinski, K.W. (Eds.), The

Second Polish–Soviet Antarctic Symposium. Polish Acad-

emy of Sciences, Institute Ecology Publishing Office,

Dziekan !ow Lesny, pp. 145–150.

Marr, J.W.S., 1962. The natural history and geography of

the Antarctic krill (Euphausia superba Dana). Discovery

Reports 33, 33–464.

Maruyama, T., Toyoda, H., Suzuki, S., 1982. Preliminary

report on the biomass of macroplankton and micronekton

collected with a Bongo net during the Umitaka Maru

FIBEX cruise. Transactions of Tokyo University of Fish-

eries 5, 145–153.

Maslennikov, V.V., 1980. Modern concepts on the large-scale

circulation of Antarctic waters and routes of mass drift of

krill. In: Makarov, R.R. (Ed.), Biological resources of the

Antarctic krill. VNIRO Publishers, Moscow, pp. 8–27.

(in Russian)

Maslennikov, V.V., 1995. The Antarctic water modifications

with regard to their influence on distribution of some

planktonic and fish species. The Antarctic 33, 43–54

(in Russian).

Maslennikov, V.V., Solyankin, Y.V., 1979. Interannual dis-

placements of the zone of interaction of Weddell Sea waters

with the Antarctic Circumpolar Current. The Antarctic 18,

118–122 (in Russian).

Meyer, M.A., El-Sayed, S.Z., 1983. Grazing of Euphausia

superba Dana on natural phytoplankton populations. Polar

Biology 1, 193–197.

Miller, D.G.M., 1986. Results from biological investigations of

krill (Euphausia superba) in the southern Indian Ocean

during SIBEX I. Memories of National Institute of Polar

Research Tokyo 40, 117–139.

Miller, D.G.M., 1987. The South African SIBEX II Cruise to

the Prydz Bay region, 1985: cruise description and

preliminary review of results. South African Journal of

Antarctic Research 17, 105–111.

Miller, D.G.M., Hampton, I., 1989. Biology and ecology of the

Antarctic krill (Euphausia superba Dana): a review. BIO-

MASS Scientific Series 9, 1–166.

Miller, D.G.M., Hampton, I., Henry, J., Abrams, R.W.,

Cooper, J., 1985. The relationship between krill food

requirements and phytoplankton production in a sector of

the southern Indian Ocean. In: Siegfried, W.G., Condy,

P.R., Laws, R.M. (Eds.), Antarctic nutrient cycles and food

webs. Springer, Berlin, Heidelberg, pp. 362–371.

Minkina, N.I., Samyshev, E.Z., Chmyr V. D., Seregin, S.A.,

1999. The relative evaluation of assimilation of primary

production by krill, salps and bacterioplankton in Atlantic

sector of Antarctic (ASA) under the conditions of mass

development of gelatinous animals. In: Abstracts of the

Second International Symposium on Krill (23–27 August

1999), Santa Cruz, USA, pp. 33–34.

Miquel, J.C., 1991. Distribution and abundance of post-larval

krill (Euphausia superba Dana) near Prydz Bay in summer

with reference to environmental conditions. Antarctic

Science 3, 279–292.

Mujica, A.R., Asencio, V.V., 1985. Fish larvae, euphausiids and

community structure of zooplankton in the Bransfield Strait

(SIBEX-Phase I) 1984. Ser Cient INACH Vol. 33, pp.

131–154.

Naganobu, M., Kutsuwada, K., Sasai, Y., Taguchi, S., Siegel,

V., 1999. Relationships between Antarctic krill (Euphausia

superba) variability and westerly fluctuations and ozone

depletion in the Antarctic Peninsula area. Journal of

Geophysical Research 104 (C9), 20651–20665.

Nast, F., 1986. Changes in krill abundance and in other

zooplankton relative to the Weddell–Scotia Confluence

around Elephant Island in November 1983, November

1984 and March 1985. Archiv fuer Fischereiwissenschaft 37,

73–94.

Nicol, S., Constable, A.J., Pauly, T., 2000a. Estimates of

circumpolar abundance of Antarctic krill based on recent

acoustic density measurements. CCAMLR Science 7, 87–99.

Nicol, S., Pauly, T., Bindoff, N.L., Wright, S., Thlele, D.,

Hosie, G.W., Strutton, P.G., Woehler, E., 2000b. Ocean

circulation off east Antarctica affects ecosystem structure

and sea-ice extent. Nature 406, 504–507.

Nishikawa, J., Naganobu, M., Ichii, T., Ishii, H., Terazaki, M.,

Kawaguchi, K., 1995. Distribution of salps near the South

Shetland Islands during austral summer, 1990–1991 with

special reference to krill distribution. Polar Biology 15,

31–39.

Nordhausen, W., Huntley, M., 1990. RACER: carbon egestion

rates of Euphausia superba.. Antarctic Journal of the United

States 25 (5), 161–162.

N .othig, E.-M., von Bodungen, B., 1989. Occurrence and

vertical flux of faecal pellets of probably protozoan origin

in the southeastern Weddell Sea (Antarctica). Marine

Ecology Progress Series 56, 281–289.

Opalinski, K.W., Maciejewska, K., Georgieva, L.V., 1997.

Notes on food selection in the Antarctic krill, Euphausia

superba. Polar Biology 17, 350–357.

Pages, F., 1997. The gelatinous zooplankton in the pelagic

system of the Southern Ocean: a review. Annales de

l’Institut Oceanographique 73, 139–158.

Pakhomov, E.A., 1989. Macroplankton distribution in the

central part of the Indian sector of Antarctica during

summer of 1984–1986. The Antarctic 28, 145–158

(in Russian).

Pakhomov, E.A., 1991. Antarctic macroplankton and the

nutrition of coastal fishes. Ph.D. thesis, P.P. Shirshov

Institute of Oceanology, Russian Academy of Sciences,

Moscow, pp. 1–263 (in Russian).

Pakhomov, E.A., 1993a. The faunistic complexes of macro-

plankton in the Cooperation Sea (Antarctica). Antarctica

32, 94–110 (in Russian).

Pakhomov, E.A., 1993b. Vertical distribution and diel migra-

tions of Antarctic macroplankton. In: Voronina, N.M.

(Ed.), Pelagic Ecosystems of the Southern Ocean. Nauka

Press, Moscow, pp. 146–150.(in Russian)

Pakhomov, E.A., 1993c. Feeding habitats and estimate of

ration of gray notothenia, Notothenia squamifrons squami-

frons Norman, on the Ob and Lena tablemounts (Indian


Ocean sector of Antarctica). Journal of Ichthyology 33 (9),

57–71.

Pakhomov, E.A., 1995. Composition and distribution of

macrozooplankton around the Antarctic islands of Kergue-

len. Hydrobiological Journal (Kiev) 31 (3), 21–32.

Pakhomov, E.A., 2002. Salp/krill interactions in the eastern

Atlantic sector of the Southern Ocean. Deep-Sea Research

II, in press.

Pakhomov, E.A., Froneman, P.W., 2000. Composition and

spatial variability of macroplankton and micronekton

within the Antarctic Polar Frontal Zone of the Indian Ocean

during austral autumn 1997. Polar Biology 23, 429–436.

Pakhomov, E.A., Froneman, P.W., 2002a, Mesozooplankton

dynamics in the eastern Atlantic sector of the Southern

Ocean during the austral summer 1997/1998.1. Community

structure. Deep-Sea Research II, in press.

Pakhomov, E.A., Froneman, P.W., 2002b. Mesozooplankton

dynamics in the eastern Atlantic sector of the Southern

Ocean during the austral summer 1997/1998. 1. Grazing

impact. Deep-Sea Research II, in press.

Pakhomov, E.A., McQuaid, C.D., 1996. Distribution of surface

zooplankton and seabirds across the Southern Ocean. Polar

Biology 16, 271–286.

Pakhomov, E.A., Grachev, D.G., Trotsenko, B.G., 1994a.

Distribution and composition of macroplankton commu-

nities in the Lazarev Sea (Antarctic). Oceanology 33,

635–642.

Pakhomov, E.A., Perissinotto, R., McQuaid, C.D., 1994b.

Comparative structure of the macrozooplankton/micronek-

ton communities of the Subtropical and Antarctic Polar

Fronts. Marine Ecology Progress Series 111, 155–169.

Pakhomov, E.A., Perissinotto, R., McQuaid, C.D., 1996. Prey

composition and daily rations of myctophid fishes in the

Southern Ocean. Marine Ecology Progress Series 134, 1–14.

Pakhomov, E.A., Perissinotto, R., Froneman, P.W., McQuaid,

C.D., 1997. Energetics and feeding dynamics of Euphausia

superba in the South Georgia region during the summer of

1994. Journal of Plankton Research 19, 399–423.

Pakhomov, E.A., Perissinotto, R., McQuaid, C.D., Froneman,

P.W., 2000. Zooplankton structure and grazing in the

Atlantic sector of the Southern Ocean in late summer 1993.

Part 1. Ecological zonation. Deep-Sea Research I 47,

1663–1686.

Park, C., Wormuth, J.H., 1993. Distribution of Antarctic

zooplankton around Elephant Island during the austral

summers of 1988, 1989, and 1990. Polar Biology 13,

215–225.

Perissinotto, R., Pakhomov, E.A., 1997. Feeding association of

the copepod Rhincalanus gigas with the tunicate Salpa

thompsoni in the Southern Ocean. Marine Biology 127,

479–483.

Perissinotto, R., Pakhomov, E.A., 1998a. Contribution of salps

to carbon flux of marginal ice zone of the Lazarev Sea,

Southern Ocean. Marine Biology 131, 25–32.

Perissinotto, R., Pakhomov, E.A., 1998b. The trophic role of

the tunicate Salpa thompsoni in the Antarctic marine

ecosystem. Journal of Marine Systems 17, 361–374.

Perissinotto, R., Gurney, L., Pakhomov, E.A., 2000. Contribu-

tion of heterotrophic material to diet and energy budget of

Antarctic krill Euphausia superba. Marine Biology 136,

129–135.

Perissinotto, R., Pakhomov, E.A., McQuaid, C.D., Froneman,

P.W., 1997. In situ grazing rates and daily ration of the

Antarctic krill Euphausia superba feeding on phytoplankton

at the Antarctic Polar Front and the Marginal Ice Zone.

Marine Ecology Progress Series 160, 77–91.

Permitin, Yu.E., Tarverdieva, M.I., 1972. The food of some

Antarctic fish in the South Georgia area. Journal of

Ichthyology 12 (1), 104–114.

Permitin, Yu.E., Tarverdieva, M.I., 1978. Feeding of Antarctic

cods (Nototheniidae) and ice-fishes (Channichthyidae) near

the South Orkney Islands. Biologiya Morya 2, 75–81

(in Russian).

Piatkowski, U., 1985. Maps of the geographical distribution of

macrozooplankton in the Atlantic sector of the Southern

Ocean. Berichte zur Polarforschung 22, 1–55.

Piatkowski, U., 1987. Zoogeographische Undersuchungen und

Gemeinschaftanalysen an antarktischem Makroplankton.

Berichte zur Polarforschung 34, 1–150.

Piatkowski, U., 1989. Macroplankton communities in Antarctic

surface waters: spatial changes related to hydrography.


Piatkowski, U., Rodhouse, P.G., White, M.G., Bone, D.G.,

Symon, C., 1994. Nekton community of the Scotia Sea as

sampled by the RMT 25 during Austral summer. Marine

Ecology Progress Series 112, 13–28.

Phleger, C.F., Nelson, M.M., Mooney, B., Nichols, P.D., 2000.

Lipids of Antarctic salps and their commensal hyperiid

amphipods. Polar Biology 23, 329–337.

Ponomareva, L.A., Kuznetsova, I.A., 1989. Feeding and

rations of Euphausia superba in the south part of the Scotia

Sea. In: Ponomareva, L.A. (Ed.), Complex Investigations of

the Pelagic Zone of the Southern Ocean. Shirshov Institute

Oceanology Publishers, Moscow, pp. 86–93.(in Russian)

Price, H.J., Boyd, K.R., Boyd, C.M., 1988. Omnivorous feeding

behaviour of the Antarctic krill Euphausia superba. Marine

Biology 97, 67–77.

Priddle, J., Croxall, J.P., Everson, I., Heywood, R.B., Murphy,

E.J., Prince, P.A., Sear, C.B., 1988. Large-scale fluctuations

in distribution and abundance of krillFa discussion of

possible causes. In: Sahrhage, D. (Ed.), Antarctic Ocean and

resources variability. Springer, Berlin, pp. 169–182.

Reinke, M., 1987. Zur Nahrungs- und Bewegungsphysiologie

von Salpa thompsoni und Salpa fusiformis. Berichte zur

Polarforschung 36, 1–89.

Ross, R.M., Quetin, L.B., 1986. How productive are Antarctic

krill. Bioscience 36, 264–269.

Ross, R.M., Quetin, L.B., Haberman, K.L., 1998. Interannual

and seasonal variability in short-term grazing impact of

Euphausia superba in nearshore and offshore waters west of

the Antarctic Peninsula. Journal of Marine Systems 17,

261–273.

Rott, H., Skvarca, P., Nagler, T., 1996. Rapid collapse of

northern Larsen Ice Shelf, Antarctica. Science 271, 788–792.


Sahrhage, D., 1988. Some indications for environmental and

krill resources variability in the Southern Ocean. In:

Sahrhage, D. (Ed.), Antarctic Ocean and Resources

Variability. Springer, Berlin, Heidelberg, pp. 33–40.

Samyshev, E.Z., 1985. Distribution and production of

the Antarctic krill. In: Vinogradov, M.E., Flint, M.V.

(Eds.), Biological basis for the fishery utilization of open

regions of the Ocean. Nauka Press, Moscow, pp. 40–49.(in

Russian)

Samyshev, E.Z., 1991. Antarctic krill and the structure of the

plankton community in its area of occurrence. Moscow,

Nauka Press.(in Russian)

Samyshev, E.Z., Lushov, A.I., 1983. Feeding and its compo-

nents of the Antarctic krill. Oceanology 23, 1018–1022.

Schnack, S.B., 1985a. Feeding by Euphausia superba and

copepod species in response to varying concentrations of

phytoplankton. In: Siegfried, W.R., Condy, P.R., Laws,

R.M. (Eds.), Antarctic Nutrient Cycles and Food Webs.

Springer, Berlin, Heidelberg, pp. 311–323.

Schnack, S.B., 1985b. A note on the sedimentation of

particulate matter in Antarctic waters during summer.

Meeresforschung 30, 306–315.

Schnack-Schiel, S.B., Mujica, A., 1994. The zooplankton of the

Antarctic Peninsula region. In: El-Sayed, S.Z. (Ed.), South-

ern Ocean Ecology: the BIOMASS Perspective. Cambridge

University Press, Cambridge, pp. 79–92.

Shandikov, G.A., 1986. Biological characteristics of

Nototheniops tchizh (Balushkin) (Nototheniidae) from the

Ob and Lena seamounts, Indian sector of the Southern

Ocean. Proceedings of the Zoological Institute, USSR

Academy of Sciences, Leningrad, Vol. 153, pp. 91–109 (in

Russian).

Shirakihara, K., Nakayama, K., Komaki, Y., 1986. Acoustic

estimation of krill biomass in R.V. Kaiyo Maru SIBEX I

survey area (Indian sector of the Southern Ocean).

Memories of National Institute of Polar Research Tokyo

40, 140–152.

Siegel, V., Harm, U., 1996. The composition, abundance,

biomass and diversity of the epipelagic zooplankton

communities of the southern Bellingshausen Sea (Antarctic)

with special reference to krill and salps. Archives of

Fisheries and Marine Research 44, 115–139.

Siegel, V., Loeb, V., 1995. Recruitment of Antarctic krill

Euphausia superba and possible causes for its variability.


Siegel, V., Piatkowski, U., 1990. Variability in the macro-

zooplankton community off the Antarctic Peninsula. Polar

Biology 10, 373–386.

Siegel, V., Skibowski, A., Harm, U., 1992. Community

structure of the epipelagic zooplankton community under

the sea-ice of the northern Weddell Sea. Polar Biology 12,

15–24.

Smith, V.R., 1991. Climate change and its ecological con-

sequences at Marion and Prince Edward Islands. South

African Journal of Antarctic Research 21, 223–224.

Smith, V.R., Steenkamp, M., 1990. Climatic change and its

ecological implications at a subantarctic island. Oecologia

85, 14–24.

Sushin, V.A., Zhigalova, N.N., Krasovsky, I.V., Semenova,

S.N., Fedulov, P.P., Yakovlev, V.N., 1985. Planktonic

communities in the Antarctic part of Atlantic. In: Vino-

gradov, M.E., Flint, M.V. (Eds.), Biological basis for the

fishery utilization of open regions of the Ocean. Nauka

Press, Moscow, pp. 29–39.(in Russian)

Tarverdieva, M.I., 1972. Daily ration and feeding pattern of

marble notothenia Notothenia rossi marmorata Fischer and

toothfish Dissostichus eleginoides Smitt (family Notothenii-

dae) in the region of South Gerogia. Journal of Ichthyology

12 (4), 748–756.

Torres, J.J., Lancraft, T.M., Weigle, B.L., Hopkins, T.L.,

Robinson, B.H., 1984. Distribution and abundance of fishes

and salps in relation to the marginal ice zone of the Scotia

Sea, November and December 1983. Antarctic Journal of

the United States 19 (5), 117–119.

Torres, J.J., Donnelly, J., Hopkins, T.L., Lancraft, T.M.,

Aarset, A.V., Ainley, D.G., 1994. Proximate composition

and overwintering strategies of Antarctic micronektonic

crustacea. Marine Ecology Progress Series 113, 221–232.

Vaughan, D.G., Doake, C.S.M., 1996. Recent atmospheric

warming and retreat of ice shelves on the Antarctic

Peninsula. Nature 379, 328–331.

Von Bodungen, B., 1986. Phytoplankton growth and krill

grazing during spring in the Bransfield Strait, Antarctica-

Fimplications from sediment trap collections. Polar

Biology 6, 153–160.

Voronina, N.M., 1984. Pelagic Ecosystems of the Southern

Ocean. Nauka Press, Moscow.(in Russian)

Voronina, N.M., 1998. Comparative abundance and distribu-

tion of major filter-feeders in the Antarctic pelagic zone.

Journal of Marine Systems 17, 375–390.

Voronina, N.M., Levin, L.A., Zadorina, L.A., Sazhin, A.F.,

1993. Planktonic community in the Pacific sector of the

Antarctic in February–March, 1992. Oceanology 33 (6),

882–889 (in Russian).

Williams, R., Kirkwood, J.M., O’Sullivan, D., 1983. FIBEX

cruise zooplankton data. ANARE Research Notes 7, 1–163.

Williams, R., Kirkwood, J.M., O’Sullivan, D., 1986. ADBEX I

cruise zooplankton data. ANARE Research Notes 31,

1–107.

Witek, Z., Kittel, W., Czykieta, H., Zmijewska, M.I., Presler,

E., 1985. Macrozooplankton in the southern Drake Passage

and in the Bransfield Strait during BIOMASS-SIBEX

(December 1983–January 1984). Polish Polar Research 6,

95–115.

Zeldis, J.R., Davis, C.S., James, M.R., Ballara, S.L., Booth,

W.E., Chang, F.H., 1995. Salp grazing: effects on phyto-

plankton abundance, vertical distribution and taxonomic

composition in a coastal habitat. Marine Ecology Progress

Series 126, 267–283.

Zwally, H.J., 1991. Breakup of Antarctic ice. Nature 350, 274.


salp/krill interactions in the southern ocean:spatial

Documents