Fluxes of biogenic carbon in the Southern Ocean: roles of large microphagous zooplankton1

Journal of Marine Systems 17 Ž1998. 325–345

Fluxes of biogenic carbon in the Southern Ocean: roles of large microphagous zooplankton 1 Jacques Le Fevre ` a

a,)

, Louis Legendre b, Richard B. Rivkin

c,2

Unite´ Mixte de Recherche CNRS No. 6539, Bioflux, UniÕersite´ de Bretagne Occidentale, Institut UniÕersitaire Europeen ´ de la Mer, Place Nicolas Copernic, Technopole ˆ Brest-Iroise, F-29280 Plouzane, ´ France b Departement de biologie, UniÕersite´ LaÕal, Quebec, Quebec, Canada G1K 7P4 ´ c Ocean Sciences Centre, Memorial UniÕersity of Newfoundland, St. John’s, Newfoundland, Canada A1C 5S7 Received 15 September 1995; accepted 15 April 1997

Abstract The Southern Ocean is an extreme environment, where waters are permanently cold, a seasonal ice cover extends over large areas, and the solar energy available for photosynthesis is severely restricted, either by vertical mixing to considerable depths or, especially south of the Antarctic Circle, by prolonged seasonal periods of low or no irradiance. Such conditions would normally lead to low productivity and a water column dominated by recycling processes involving microbial components of pelagic communities but this does not seem to be the case in the Southern Ocean, where there is efficient export to large apex predators and deep waters. This paper investigates the role of large microphagous zooplankton Žsalps, krill, and some large copepods. in the partitioning of biogenic carbon among the pools of short- and long-lived organic carbon and sequestered biogenic carbon. Large microphagous zooplankton are able to ingest microbial-sized particles and thus repackage small, non-sinking particles into both metazoan biomass and large, rapidly sinking faeces. Given the wide spatio-temporal extent of microbial trophic pathways in the Southern Ocean, large zooplankton that are omnivorous or able to ingest small food particles have a competitive advantage over herbivorous zooplankton. Krill efficiently transfer carbon to a wide array of apex predators and their faecal pellets are exported to depth during occasional brief sedimentation episodes in spring time. Salps may be a significant link towards some fish Ždirectly. and other apex predators Žindirectly. and, at some locations Žespecially in offshore waters. and time, they may account for most of the downward flux of biogenic carbon. Large copepods are a trophic link towards fish and at least one whale species, and their grazing activity generally impedes the export of organic particles to depth. As a result, biogenic carbon is channelled mainly towards apex predators and episodically into the deep ocean. Without these original interactions, Antarctic waters might well be dominated by microbial components and recycling processes instead of active export from the generally small primary producers towards large apex predators.

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Corresponding author. Tel.: q33-2-9849-8653; Fax: q33-2-9849-8645; E-mail: [email protected] Contribution to programme Antares ŽJGOFS-France., and to the programmes of GIROQ ŽGroupe interuniversitaire de recherches oceanographiques du Quebec ´ ´ . and the Ocean Sciences Centre, Memorial University of Newfoundland. 2 Authors listed in alphabetical order. 1

0924-7963r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. PII: S 0 9 2 4 - 7 9 6 3 Ž 9 8 . 0 0 0 4 7 - 5

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J. Le FeÕre ` et al.r Journal of Marine Systems 17 (1998) 325–345

Resume ´ ´ L’Ocean ou` les eaux sont en permanence froides, ou` les glaces recouvrent ´ Austral est un environnement extreme, ˆ saisonnierement de vastes zones, et ou` l’energie solaire disponible pour la photosynthese restreinte, soit par ` ´ ` est severement ´ ` melange vertical jusqu’a` des profondeurs considerables, soit par de longues periodes saisonnieres ´ ´ ´ ` d’irradiance faible ou nulle, en particulier au sud du cercle antarctique. De telles conditions devraient normalement se traduire par une faible productivite´ et une colonne d’eau dominee ´ par des processus de recyclage impliquant les composants microbiens des communautes Mais tel n’est pas le cas dans l’Ocean ´ pelagiques. ´ ´ Austral, ou` a lieu une exportation efficace vers des predateurs terminaux de grande taille et vers les eaux profondes. Le present article etudie le role ´ ´ ´ ˆ de grands organismes . dans la partition du carbone biogene zooplanctoniques microphages Žles salpes, le krill et certains copepodes ´ ` entre les stocks a` longue et courte duree ´ de vie et le stock sequestre. ´ Les grands organismes zooplanctoniques microphages sont capables d’ingerer de la matiere pas vers de la ´ des proies de taille microbienne et transferent ` ` de petites particules qui ne sedimentent ´ ´ biomasse de metazoaires, et vers de grandes particules fecales a` sedimentation rapide. Etant donnee ´ ´ ´ ´ l’importance spatio-temporelle des voies trophiques microbiennes dans l’Ocean ´ Austral, les organismes zooplanctoniques omnivores ou capables d’ingerer sur les herbivores. Le krill transfere ´ de petites particules alimentaires ont un avantage competitif ´ ` efficacement le carbone vers une large gamme de predateurs terminaux et ses pelotes fecales sont exportees ´ ´ ´ en profondeur lors de brefs episodes printaniers de sedimentation. Les salpes peuvent constituer un lien significatif vers certains poissons ´ ´ Ždirectement. et d’autres predateurs Žindirectement.; elles peuvent etre ´ ˆ responsables de l’essentiel du flux vertical de carbone . et a` certains moments. Les grands copepodes biogene, sont un ` au moins localement Žen particulier dans les eaux oceaniques ´ ´ lien trophique vers les poissons et vers une espece ` de baleine, au moins. Leur activite´ de broutage tend en revanche a` reduire ´ le flux vertical de particules organiques. En consequence, le carbone biogene ´ ` est principalemement dirige´ vers les predateurs ´ terminaux et episodiquement vers les eaux profondes. Au lieu d’etre ´ ˆ le siege ` d’un transfert actif depuis les producteurs primaires, generalement de petite taille, vers de grands predateurs terminaux, les eaux antarctiques pourraient bien, sans ces ´ ´ ´ interactions originales, etre ˆ dominees ´ par les organismes microbiens et les processus de recyclage. q 1998 Elsevier Science B.V. All rights reserved. Keywords: biogenic carbon; microphagous zooplankton; krill; sedimentation; copepods; apex predators; salps

1. Introduction: export of biogenic carbon in oceans The Southern Ocean is an extreme environment, where waters are permanently cold, a seasonal ice cover extends over large areas, and the solar energy available for photosynthesis is severely restricted, either by vertical mixing to considerable depths or, especially south of the Antarctic Circle, by prolonged seasonal periods of low or no irradiance. Such conditions would normally lead to low productivity and a water column dominated by recycling processes involving microbial components of pelagic communities. However, waters that surround Antarctica support large abundances of apex predators such as whales, seals and birds, and extensive biogenic deposits are found over vast bottom areas. The present paper addresses this apparent paradox by considering some unique biological and ecological characteristics of key large zooplankton taxa. One important characteristic of these large zooplankton is mi-

crophagy, i.e., their ability to ingest microbial-sized particles. Large microphagous zooplankton repackage small, non-sinking particles into both metazoan biomass and large, rapidly sinking faeces. Microphagy thus results in the efficient transfer of biogenic carbon to apex predators andror the deep ocean. In oceans, biogenic carbon resulting from primary production may be remineralized Ži.e., respired. in situ or exported. The term ‘export’ encompasses here the channelling of primary production toward both large animals and deep waters. Food-web export to large and long-lived animals is through grazing and predation on smaller organisms. Export towards deep waters is mainly through the production of fast-sinking particles Žaggregated ungrazed algae, faecal pellets, organic debris, and carcasses.. Other mechanisms include vertical migrations of zooplankton ŽLonghurst et al., 1990., downward mixing of dissolved organic carbon ŽDOC. produced by phytoplankton and heterotrophs ŽCarlson et al., 1994;

J. Le FeÕre ` et al.r Journal of Marine Systems 17 (1998) 325–345

Michaels et al., 1994., and microbial and metazoan metabolism in deep waters ŽChildress and Mickel, 1985; Cho and Azam, 1988; Siebenaller and Somero, 1989.. Another major transport of carbon from surface to deep waters is in the form of dissolved inorganic carbon ŽDIC. in sinking dense water Že.g., Antarctic Bottom Water and North Atlantic Deep Water.. Carbon in deep waters Ž) ca. 1000 m. or sediments is sequestered, i.e., prevented from returning to the atmosphere for centuries or even millenia. The three potential fates of biogenic carbon which are described above Ži.e., in situ remineralization, export to food webs, and sequestration. correspond to the three pools of biogenic carbon proposed by Ž1992.. These pools are Legendre and Le Fevre ` defined on the basis of the turnover time of biogenic carbon, i.e., the time elapsed between the photosynthetic uptake of carbon by phytoplankton and the return of this carbon as CO 2 to the surface waters or the atmosphere. The pools are: short-lived organic carbon Ž- 10y2 years s 3 to 4 days., long-lived organic carbon Ž10y2 year to 10 2 years., and sequestered biogenic carbon Ž) 10 2 years.. Short-lived organic carbon consists of organisms with high turnover rates, as well as labile dissolved organic compounds, and it mainly transits through the microbial food web. Long-lived organic carbon comprises renewable marine resources Že.g., fish, marine mammals. and also microbial heterotrophs involved in the breakdown of organic matter derived from large heterotrophs. Sequestered biogenic carbon includes organic remains buried in sediments Že.g., petroleum., inorganic deposits of biological origin Žmainly carbonates., refractory dissolved organic matter, and dissolved CO 2 in deep waters resulting from the oxidation Žrespiration. of organic compounds. Climate changes at various time scales, including the possible ongoing global warming, may be related to Žor mediated by. variations in the pool of sequestered carbon. The trophic structure of the pelagic community has a profound influence on the magnitude and temporal patterns of biogenic carbon export. Ž1. In a herbivorous food web Žor chain., large phytoplankton Ž) 2 to 5 mm. are grazed by mesozooplankton, which are themselves prey to larger organisms. This is traditionally exemplified by copepods grazing on diatoms and sustaining, directly or indirectly, fish

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production. Until recently, it was thought that this link underlies all important fisheries Že.g., Ryther, 1969; Cushing, 1989.. Ž2. In the microbial loop, heterotrophic bacteria are grazed by flagellates, which are in turn prey to ciliates; flagellated and ciliated protozoa release dissolved organic compounds which are used by bacteria. The cycling within the microbial loop is finite because organic carbon is remineralized by all organisms involved, so that maintenance of the loop requires a source of DOC. In the Southern Ocean, this source is mostly autochthonous, i.e., local primary production. When solar irradiance is too low to allow photosynthesis, the water column is dominated by the microbial loop, but there may be some predation on protozoa by larger organisms, so that the loop may not be completely closed. Ž3. When solar irradiance is high enough to permit photosynthesis, the microbial loop may change to the microbial food web Žin the literature, the microbial loop and web are often confused; see the work of Rassoulzadegan Ž1993... The microbial food web is similar to the microbial loop, except that protozoa graze on both small phytoplankton Ž- 5 mm. and heterotrophic bacteria and that remineralized dissolved inorganic and organic nutrients are used by both small phytoplankton and bacteria. Because of the input of primary production, the microbial food web can export biogenic carbon to larger organisms via mesozooplankton feeding on microzooplankton. Ž4. Although the herbivorous and microbial trophic modes are often perceived as exclusive of each other, Legendre and Rassoulzadegan Ž1995. proposed that they can co-occur in pelagic ecosystems. This trophic configuration is called the multivorous food web. As an example, there is growing evidence that many copepods can switch their diet from phytoplankton to microzooplankton, which allows them to exploit both the herbivorous and the microbial food webs Že.g., Gifford, 1993; Ohman and Runge, 1994; Cowles and Fessenden, 1995.. The microphagous link is an important special case of the multivorous food web, where large organisms directly feed on microbial sized particles which are orders of magnitude smaller than themselves, thus by-passing several potential steps that exist in the other trophic pathways. Fortier et al. Ž1994. have shown that large planktonic microphages are especially efficient at channelling towards the long-lived

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carbon pool Že.g., fish, marine mammals and birds., and even the sequestered carbon pool, part of the biogenic carbon that would have otherwise been shorter-lived. The present paper investigates how the environment and patterns of production in Antarctic waters affect the trophic interactions of key zooplankton taxa, and especially the role of large zooplankton in the partitioning of biogenic carbon among the pools of short- and long-lived organic carbon and sequestered biogenic carbon. Our general hypothesis is that the trophic pathways encountered in the Southern Ocean are governed by the unique physical characteristics of this environment, and by the resultant patterns of autotrophic and heterotrophic biomass and production. 2. Environmental characteristics of the Southern Ocean 2.1. Physical–biological interactions Water temperatures in the Seasonal Ice Zone ŽSIZ. are cold Žtypically y2 to q28C. whereas those in the Permanent Open Ocean Zone ŽPOOZ. are higher Že.g., q2 to q48C, south of Kerguelen Islands; see the work of Pondaven et al. Žthis volume... Depending on the latitude, sea-ice begins to form in autumn and continues to grow through late spring. During the phase of active ice growth, the ions in sea water are excluded from the crystal lattice, and salts are concentrated in liquid brine. Some of the latter is retained in the ice, but most of it is ejected into the underlying water column. Temperature controls the volume of brine in ice, and consequently the free space available for habitation. In newly formed ice, most of the volume is occupied by small brine channels Ži.e., 10 mm to 1 mm.. As the ice ages, thickens and cools, the brine drains and the channels enlarge Žfrom millimeters to decimeters.. Hence, the porosity of the ice and the connectivity and size of the pores change with temperature Že.g., Perovich and Gow, 1991.. These pores and channels provide habitats for heterotrophic bacteria, protozoa and small animals. In spring, because the ice matrix offers a solid substratum where microalgae are maintained at high solar irradiance, they can accumulate to very high biomasses Že.g., Horner et al., 1992; Palmisano

and Garrison, 1993.. Clearly, the seasonal change in the temperature-dependent pore size contributes to the structuring of the sea-ice community ŽEicken, 1992.. First, it determines the trophic relationships within the ice by providing refuges for small grazers, such as protozoa, which have access to the sub-millimetre pores whilst large grazers, such as copepods, krill and amphipods are restricted to larger, millimetre to decimetre channels. Second, it influences the development and succession of communities by controlling the nutrient budget ŽClarke and Ackley, 1984; Cota et al., 1987; Garrison et al., 1990.. In late spring, the absorption of solar radiation by the dense layer of algae in the ice bottom, the concomitant increase in temperature, and resultant melting of the ice bottom cause the release of algae from the ice. Later in the season, as the desalinated ice melts, the freshening of the surface layer vertically stabilizes the upper water column. The combined effects of increased vertical stability and downwelling irradiance results in a mixing depth which is shallower than the critical depth ŽSverdrup, 1953., hence phytoplankton often grow rapidly at receding ice edges ŽSmetacek and Passow, 1990; Nelson and Smith, 1991.. Although light, nutrients and temperature interact to influence the development of algal populations in all polar regions, the growth of ice and planktonic algae is generally limited by light. The unique annual cycle in solar radiation constrains the cycles of primary production Že.g., Palmisano et al., 1987; Rivkin, 1991; Sakshaug and Slagstad, 1991.. South of the Antarctic Circle, up to 4 months of continuous darkness are separated from as many months of continuous light by a transition period of rapidly changing photoperiod Žca. 20 min dayy1 at McMurdo Sound, 788S, which is the southernmost extent of seasonally open water.. In the SIZ, the ocean is ice-covered for most of the year. Attenuation of light by snow, ice and the algal community at the base of the ice results in very low irradiances Žtypically - 0.1% of the incident insolation. at the ice–water interface and in the sub-ice water column ŽGrenfell and Maykut, 1977; Maykut, 1985; Grenfell, 1991.. The open water regions, between the SIZ and the Polar Front Žca. 50 to 608S. are not influenced by melt water stabilization and, because of strong circumpolar winds, they are typically well mixed down to 50 to 75 m in

J. Le FeÕre ` et al.r Journal of Marine Systems 17 (1998) 325–345

summer ŽFoster and Middleton, 1984. and ) 100 m in winter ŽMuench et al., 1990.. The combined deep mixing, low sun angle and short photoperiod results in low average downwelling irradiances. 2.2. Primary and bacterial production Because of the extreme seasonal cycle in solar radiation, the presence of a seasonal ice cover, and deep winter mixing in areas without ice cover, primary production in most of the Southern Ocean is low to nil for up to 6 months of the year. Large sectors are thus dominated for long periods by microbial heterotrophic pathways. When and where primary production takes place, it is often low and dominated by small cells ŽBrockel, 1981; Weber and ¨ El-Sayed, 1987., i.e., in the under-ice water column ŽRivkin, 1991., in deeply mixed spring and autumn waters ŽKopczynska, 1992; Kivi and Kuosa, 1994; Jochem et al., 1995., and in the stratified summer water column ŽVillafane et al., 1991; Bak et al., 1992.. Large algae Žmostly diatoms. frequently dominate within the sea-ice ŽPalmisano and Garrison, 1993., at receding ice edges ŽSmith and Nelson, 1985; Nelson and Smith, 1986; Wilson et al., 1986., and in offshore frontal areas ŽHolm-Hansen et al., 1977; Hattori and Fukuchi, 1989; Laubscher et al., 1993.. In some near-shore and ice edge zones, there also are massive accumulations of the colonial form of Phaeocystis. Although these blooms are frequently short-lived, they significantly contribute to the total annual primary production. For example, based upon recent reviews by Smith Ž1987, 1991., approximately 50% of the annual primary production in the Southern Ocean Ž12.3 = 10 14 g C. is associated with phytoplankton in the marginal ice zone ŽMIZ.. Legendre et al. Ž1992. estimated the total annual production, in the area south of 608S, to be ca. 2.9 = 10 14 g C, with G 60% occurring in ice edge blooms, ca. 15–20% in the water column under ice cover, and G 20% within the sea-ice. Although diatom blooms are thought to occur primarily in shallow coastal waters or under land-fast ice Že.g., Smetacek et al., 1990., this view appears too restrictive. Fig. 1, which is a composite of all CZCS images recorded in the Southern Ocean from 1978 to 1986, shows the time-integrated chlorophyll distribution in the Southern Ocean. The numbers on

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Fig. 1 denote the following areas of high chlorophyll concentration: Ž1. a nearly circumpolar maximum, absent only from the eastern Pacific Sector, follows the Subtropical Convergence, Ž2. a weaker maximum is associated with the Polar Front, mainly in the Atlantic Sector: at this latitude, the mixed layer is too deep in the Pacific Sector to allow much phytoplankton growth, Ž3. higher biomasses are found in the Scotia–Weddell confluence, which is a complex hydrodynamic region with several frontal systems, Ž4. a band of high chlorophyll concentrations in the Pacific Sector may denote open-ocean ice-edge blooms ŽD. Nelson, personal communication., Ž5. in the Bellingshausen Sea, blooms likely occur in frontal regions, whose structure is associated with an extension or bend of the Polar Front ŽTurner and Owens, 1995., Ž6. coastal ice-edge blooms are found in the Ross Sea and Ž7. the eastern Weddell Sea and Ž8. near-shore blooms also take place around the Antarctic Continent. The relative and absolute quantity of biogenic silicon in sediment is not an unequivocal proxy for diatom production: biogenic silica may be better preserved in the Southern Ocean than in other regions, and the downward fluxes of biogenic carbon and silica may be somewhat uncoupled Že.g., Crawford, 1995.. However, a huge circumpolar belt of highly siliceous sediments is found in the Southern Ocean, and the accumulation rate of biogenic silica was evaluated by Treguer et al. Ž1995. to be 4.75 ´ Tmol Si yeary1 in Antarctic deep waters compared to 0.2 Tmol Si yeary1 at continental margins. This suggests efficient vertical export of biogenic matter through direct sinking of diatoms, which is consistent with the widespread occurrence, offshore, of high chlorophyll concentrations as shown by Fig. 1. In addition, diatoms and large blooms of Phaeocystis, which are advected from offshore towards the ice ŽDayton and Oliver, 1977; Barry, 1988; Barry and Dayton, 1988. or result from local growth Že.g., in the Ross Sea, triggered by increased irradiance under the thinning ice cover; D. Nelson, personal communication. can sink as intact cells under or near the land-fast ice ŽDayton and Oliver, 1977; Barry, 1988; Bathmann et al., 1991.. Overall, because the Southern Ocean is largely undersampled, and the frequency of cloud cover decreases the reliability of remote sensing, offshore blooms may often go unno-

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Fig. 1. Chlorophyll a concentrations in the Southern Ocean. Composite image of all CZCS data acquired between November 1978 and June 1986 Žca. 66 000 individual 2-min scenes.. Black areas: no data. Numbers 1 to 8 refer to features identified in the text. Image courtesy of NASArGoddard Space Flight Center.

ticed. Crawford Ž1995. fortuitously observed, in the Polar Front, mass sedimentation of empty frustules at the end of a diatom bloom. It follows that the downward flux of algal material in the deep ocean, offshore, is probably significant.

When light limits algal growth which, in many areas, may be for most of the year, the Southern Ocean is dominated by the microbial loop in winter and the microbial food web in summer. Exceptions to this are algal blooms at ice-edges or in offshore

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fronts. Furthermore, even at retreating ice edges, early grazing by overwintering krill can prevent large phytoplankton from blooming, resulting in a water column which is dominated by the microbial web ŽLancelot et al., 1993a.. Given the wide spatio-temporal extent of microbial trophic pathways in the Southern Ocean, large zooplankton that are omnivorous or able to ingest small food particles would have a competitive advantage over herbivorous zooplankton.

3. Key pelagic grazers in the Southern Ocean: large copepods, krill and salps Pelagic trophic pathways in the Southern Ocean have been the subject of several reviews. For example, Hempel Ž1987. recognized three major Antarctic pelagic systems. These are the following. Ž1. In the seasonal and highly productive pack-ice zone, krill Ž Euphausia superba. dominate. This crustacean is an important link between large phytoplankton and warm-blooded vertebrates. Ž2. In ice-free and low productive ocean waters, herbivorous copepods, salps Žprimarily Salpa thompsoni . and euphausiids other than krill Že.g., E. Õallentini . dominate. Ž3. In the zone of cold ice shelf water, which is well developed in the shallow parts of the inner Weddell and Ross Seas, pack-ice is present for most of the year. Hence, primary production is generally low with a brief but intense peak. The pelagic fish Pleuragramma antarcticum may play an important role, much of the primary production is directly transferred to the benthos, and various herbivores are closely linked with the sea-ice. Smetacek et al. Ž1990. applied the conceptual model of Peinert et al. Ž1989., that describes downward particle fluxes, to classify pelagic ecosystems of the Southern Ocean as systems which either ‘retain’ or ‘lose’ organic material. According to Peinert et al. Ž1989., retention occurs in ecosystems where grazing is dominated by copepods, because most of the faecal material is recycled in the upper water column Žsee Section 5.. In contrast, loss from surface waters Ži.e., vertical export. occurs when aggregated intact cells andror phytodetritus sink. This generally takes place when nutrients are exhausted or when phytoplankton blooms are grazed by large zooplank-

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ton which produce large, rapidly sinking faecal pellets, such as euphausiids or salps. Because of their high sinking velocities, these faecal pellets are not degraded in the upper water column. Smetacek et al. Ž1990. proposed that retention-type systems are dominated by intense copepod grazing and subsequent disintegration of faecal pellets within the surface mixed layer Že.g., in the Weddell Sea throughout the year and in the Bransfield Strait during summer.. In contrast, loss-type systems are characterized by a downward flux of faecal pellets typically produced by krill as brief pulses during spring. According to the authors, a third type of systems, dominated by sinking of intact diatoms, would only occur in shallow coastal waters or under land-fast ice. However, as discussed in Section 2.2, there are other areas of the Southern Ocean where intact algae may significantly contribute to the downward flux of biogenic material. Thus, considering that the third type of systems is limited to shallow coastal waters and land-fast ice may be too restrictive. According to the above scheme, the downward fluxes of biogenic carbon in the Southern Ocean mostly consist of fresh algal cells Žmainly large diatoms. from ungrazed blooms and faecal material produced by large zooplankton. Phytoplankton blooms occur at the edge of the seasonal pack ice as it melts and retreats during the austral spring and summer. In some regions Že.g., Ross Sea; Smith and Nelson, 1986; Nelson and Treguer, 1992., phytoplankton biomasses as high as ´ 20 mg Chl a my3 extend several hundred kilometers seaward from the retreating ice edge. In other areas, such as the Weddell Sea, concentrations - 10 mg Chl a my3 are more typical ŽLancelot et al., 1993b.. Lancelot et al. Ž1993a. proposed that these two contrasted situations may reflect different trophic roles played by krill. Ž1. When overwintering krill are abundant Že.g., in the Weddell Sea. they may consume ice algae, hence there is only a relatively small amount of seeding of the upper water column by these algae as the ice-edge melts and recedes. When this occurs, the ice-edge assemblage is dominated by nanoflagellates rather than diatoms. In this case, a microbial food web develops which tracks primary production and prevents phytoplankton from reaching high concentrations. These microbial grazers are in turn ingested by metazoan grazers. Ž2. In

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areas where overwintering krill are absent or scarce Že.g., Ross Sea., surface waters at the time of ice melt are seeded by large quantities of sea-ice algae, which results in intense blooms dominated by diatoms, or sometimes Phaeocystis. The main grazers of large phytoplankton are copepods. Ž3. Lancelot et al. Ž1993a. recognized a third trophic system in ice-free areas in which algal biomass is regulated by episodic passage of krill swarms that track algal blooms and thus heavily graze on nanophytoplankton, protozoa, large diatoms and copepods. As a result the biomass of plankton is very low. A common view in the above schemes is that the major planktonic grazers in the various subsystems of the Southern Ocean are krill, salps and copepods. In Antarctic waters, the trophic role of some large copepods is similar to that of euphausiids and salps ŽSection 4.. Although the three groups share some similar trophic characteristics, they display a number of distinct adaptive strategies. These characteristics are examined in the following sections with respect to the environmental and production characteristics of the Southern Ocean and their influence on the fluxes of biogenic carbon.

4. Trophic characteristics and environmental adaptations of copepods, krill and salps 4.1. Feeding modes and distribution In a review on the role of large planktonic microphages in exporting biogenic carbon, Fortier et al. Ž1994. concluded that, in general, microphagous pathways are dominated by large mucous-web feeders Žsalps, doliolids, appendicularians and pteropods.. In the Southern Ocean, salps Žmainly S. thompsoni, up to ) 100 mm. are indeed among the major large microphages. An exception to the general pattern, however, occurs in polar waters where, in addition to mucous-web feeders, some crustaceans are facultative microphages. In open Antarctic waters, both krill and some large copepods can feed upon microbial components of the food webs ŽSchnack, 1985.. Three of these copepod species Ž Calanus propinquus, Calanoides acutus, Rhincalanus gigas . are very large Žup to 10 mm. and a fourth Ž Metridia gerlachei . is somewhat

smaller, and thus a less spectacular microphage. Under favourable conditions, the first three species feed efficiently on high biomass of large phytoplankton Žmainly diatoms., while M. gerlachei is more omnivorous ŽSchnack, 1985.. In winter, some species Ž Cal. acutus . migrate to deep waters and enter into diapause, while others Ž C. propinquus. continue feeding under the sea-ice in more or less the same way as krill ŽSchnack-Schiel and Hagen, 1994.. Since microbial trophic pathways are prevalent in the Southern Ocean over a large proportion of the year, microphagy is a crucial feeding strategy, even for diapausing species. C. propinquus, Cal. acutus, R. gigas, and to a lesser extent M. gerlachei, are prominent members of the copepod community in Southern Ocean Že.g., Schnack et al., 1985; Hopkins and Torres, 1989; Siegel et al., 1992., although small species in the genus Oithona can dominate in numbers Že.g., Hopkins and Torres, 1989. and perhaps strongly contribute to production ŽFransz and Gonzalez, 1995.. The ecology of krill in the Southern Ocean has been extensively reviewed Že.g., Hempel, 1987; Miller and Hampton, 1989; Smetacek et al., 1990.. Their versatile feeding behaviour allows krill to opportunistically feed during all seasons and in most environments. Consequently, krill are widely distributed in Antarctic waters. During summer, compact mobile swarms forage the widely dispersed phytoplankton blooms in offshore frontal zones and near retreating ice edges ŽSection 2.2.. However, the main habitat of krill is the seasonal pack ice zone Že.g., Hempel, 1987; Section 3.. This habitat provides both food supply and refuge from predators. Later in the season, stabilization of the upper water column caused by the melting of sea-ice provides conditions favourable for the rapid growth of phytoplankton. In the scheme of Smetacek et al. Ž1990., krill feed on ice algae during winter in regions north of the Antarctic Circle where there is sufficient light to sustain year-round photosynthesis. This is because algal concentration in the water column beneath the sea-ice is far below the feeding threshold of krill. However, since krill are microphagous, they may also ingest small heterotrophic prey in both the sea-ice and the water column. In contrast, south of the Antarctic Circle, the low or nil solar radiation during several months precludes herbivorous feeding

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for much of the year, so that overwintering krill would ingest small heterotrophic flagellates Že.g., choanoflagellates. thus exploiting the under-ice microbial loop Že.g., Marchant and Nash, 1986; Marchant, 1990.. Alternatively, under some circumstances, adult krill may fast for up to several months, with a resulting shrinkage of their bodies and gonads Žas observed in aquaria by Ikeda and Dixon Ž1982... The ability of some large crustacean zooplankton from polar waters to efficiently feed on small particles may be due to a combination of morphological adaptations Že.g., the finest setae of the Antarctic krill can retain particles down to 1 mm; Kils, 1983; however, this does not mean that the smallest particles actually filtered by the animal are that small. and low seawater temperature. As discussed by Legendre et al. Ž1996., the dynamic viscosity of seawater is ca. 2.5 times greater at y28C than at 258C. The dominance of viscous forces in cold seawater may facilitate the ingestion of very small particles by some macrozooplankton. It also enables filter feeders to influence water movement around themselves for much larger distances relative to their sizes than when turbulent forces dominate. Higher viscosity of seawater in polar regions may, in addition, account for the relatively high clearance rates of bacterivorous flagellates and their efficient control of bacterial biomasses and the reports of many large bacterivorous ciliates ŽGarrison, 1991; Garrison and Gowing, 1993.. A fundamental characteristic of salp biology is unregulated filtration of all particles that enter the branchial cavity. This may lead to fatal clogging of the oesophagus at particle concentrations that are typical of neritic waters and may in part explain why salps are often restricted to oligotrophic offshore waters and generally absent from areas with high phytoplankton concentrations. Another striking characteristic is their ability to rapidly increase their numbers through asexual multiplication, from very low background levels Žoften undetectable. to very high abundances. Fortier et al. Ž1994. hypothesized that salps swarm in response to sudden increases of phytoplankton productivity. This results in a rapid increase in community clearance rates, which in turn reduces and maintains particle concentration below the clogging threshold. According to the above hypothesis, salp swarming would be a response to

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disruption of normal feeding conditions, whereas low background concentrations would be the normal state encountered by salp populations under optimal food conditions. In the Southern Ocean, high concentrations of salps are most often reported from the warmer waters north of ca. 658S Že.g., Van der Spoel and Heyman, 1983.. According to Perissinotto and Pakhomov Ž1998., S. thompsoni is generally restricted to the warmer water masses Žlayers.. Siegel et al. Ž1992. observed, in the region of the Weddell–Scotia Confluence, a gradient in salp abundance from dominant or sub-dominant in open waters to undetectable in ice-covered waters. Salps, however, seem to be widely distributed in Antarctic waters. They are commonly found between 65 and 708S in the Indian and Pacific sectors of the Southern Ocean Že.g., Foxton, 1961; Casareto and Nemoto, 1986, 1987.. Harbison Ž1988. observed high concentrations of S. thompsoni at the ice edge in McMurdo Sound Ž788S. and Boysen-Ennen et al. Ž1991. found large abundances Ž500–1600 mg 1000 my3 , dry weight. of the same species near the ice edge and in the under-ice water column of the Weddell Sea. The water was in both cases near the freezing point Žy1.88C., so that low temperature obviously does not preclude salps. The waters south of 658S are frequently covered by seasonal pack ice and are often undersampled for taxa other than krill. The difficulty in deploying plankton-collecting equipment in ice-covered waters aggravates the problem. The bias is all the more critical for salps because their abundance is generally low and patchy. This sampling bias may, in part, explain the reported scarcity of salps at the highest latitudes. 4.2. From microphagy to omniÕory and carniÕory Microphagy probably does not have the same significance for large copepods, krill and salps in the Southern Ocean. Salps filter large volumes of water through a continuously secreted mucous net, which retains all particles ) ca. 4 mm with 100% efficiency and smaller particles with lower efficiency. They are thus obligate microphages, and they presumably exploit small food particles in the Southern Ocean year round. In contrast, krill can use different feeding modes according to the nature and concen-

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tration of food particles Žsee the works of Kils Ž1983., Hempel Ž1987. and Smetacek et al., 1990.. The normal feeding mode is filtration through the large basket formed by the thoracopods. When particle concentration is high, filtration is by active pumping whereas, at low concentration, the animal swims with the basket wide open, filtering as it moves. Other modes include scraping and ‘sucking’ of algae from the undersurface of the ice, capture of copepods, and perhaps cannibalism on smaller individuals. Thus, for krill, microphagy is one among several feeding modes, and it is probably most significant in the under-ice water column during the aphotic winter when only heterotrophic microbial prey are available ŽMarchant and Nash, 1986.. In open waters, as mentioned above, the feeding modes of large copepods are similar to those of krill ŽSchnack, 1985.. Copepods, however, are less efficient than krill at exploiting the under-ice environment in winter, where at least one species Ž Cal. acutus . cannot continue feeding ŽSchnack-Schiel and Hagen, 1994.. They also are less efficient than salps at microphagy. Microphagy is not the exclusive feeding mode for any of the above grazers. Krill feed on algae and actively ingest micro- and mesozooplankton. Their diet is often dominated by non-chlorophyllous prey Že.g., Price et al., 1988; Hopkins and Torres, 1989; Hopkins et al., 1993a,b.. In addition carnivory appears to be an important feeding mode, especially in the water column under the sea-ice ŽHopkins and Torres, 1989.. Motile organisms are often captured by large raptorial feeders, such as krill, but they may be able to avoid or escape from the filtration current of salps. The maximum size of particles entering the pharyngeal cavity of salps is constrained by the mouth diameter, but actual ingestion only occurs if the items present in the cavity stick to the mucous net and are transported to the digestive track. Crustaceans ) ca. 10 mm that often visit salps are there to exploit the salp food supply, if not the salp itself Žsee Section 5.1., and this sets a limit on what could be considered salp prey. Thus, the feeding regime of salps includes microphagy, herbivory Žon small and large phytoplankton., and omnivory on microzooplankton and perhaps small metazoans. The large copepods dealt with in this paper are herbivorous, omnivorous on heterotrophic protists and occasion-

ally carnivorous, especially under the pack ice ŽHopkins and Torres, 1989.. Large copepods, krill and salps, in the Southern Ocean, can feed on a wide size and compositional range of particles ŽTable 1.. Large Antarctic copepods, E. superba and S. thompsoni can all efficiently feed on particles as small as 3–5 mm. However, there appears to be a major difference in the maximum size of ingested prey. Krill can effectively capture and ingest prey as large as at least 20 mm. In contrast, the upper size limit of particles ingested by Antarctic salps is not well known, but it probably does not exceed 3–9 mm Žsee above.. Maximum prey size of large copepods is smaller than that of krill and salps, i.e., 1–2 mm. The trophic indices for the three groups, as defined in the caption to Table 1, are: krill ) salps ) copepods. This suggests that krill can both more readily exploit larger prey, via carnivory, and ingest a greater diversity of prey than either salps or copepods. The ability of krill to opportunistically forage across a wide taxonomic and size range allows them to exploit the food items which are seasonally available. This ability is not found in lower latitude oceans or in other pelagic grazers. Although the range of food items ingested by salps is smaller than that of large Antarctic microphagous crustaceans, their unique and highly efficient filtration mechanism permits ingestion of microbial food at much lower concentrations than other large microphages. We propose that the diversity of feeding modes of krill, salps and, to a lesser degree, some large copepods explains the success of these organism in Antarctic waters. Carnivory, which is a more important feeding mode for krill than salps or copepods, permits krill to capture highly nutritious prey when the abundances of smaller autotrophic and heterotrophic prey are very low, and hence exploit the under-ice water column. In contrast, microphagy is probably more significant for salps than for krill, since the latter likely rely on microphagy only when larger food items are scarce, e.g., in the under-ice water column during winter. The ability of salps to systematically exploit microbial food accounts for their ubiquity. Microphagy provides the large Antarctic copepods with flexibility, that permits them to co-exist with the other two groups, both in open waters, where salps are at an advantage under olig-

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335

Table 1 Range in size and taxonomic composition of representative food items ingested by salps, krill and large copepods from Antarctic waters Consumer size Žmm. a Minimum prey size Žmm. Representative small prey

Maximum prey size Žmm. Representative large prey

Trophic index n

Salps

Krill

Large copepods

38 b - 5e PICO, PNAN, HNAN, DIAT, DINO g – i 3–9 h,i,l TIN, MT, PL, OT, IE, RAD h,i,l

60 c 3f PNAN, HNAN, PNAN, HNAN, DIAT, DINO f,h – k 3–20 h,i,k TIN, MT, PL, OT, COP, CLI, RAD, HAh,i,l,m 2.5

10 d 3f PNAN, HNAN, DIAT, DINO f,i,l

1.8

1–2 i TIN, ON j

1.5

Trophic index ŽTI. of the ingested ration is the number of consumer steps above primary production. It was computed as the product of the trophic level of prey Ž1.0 s phytoplankton; 2.0 s protozoans; 2.5 s herbivorous metazoans; 3.0 s carnivorous metazoans. and the percent occurrence of that prey in the gut of the consumer. TI of consumers: 1.0 s ingest phytoplankton; 2.0 s ingest protozoans; 2.5 s ingest herbivorous metazoans; 3.0 s ingest carnivorous metazoans. CLI, Clione sp.; COP, copepods; DIAT, diatoms; DINO, dinoflagellates; HA, hyperiid amphipods; HNAN, heterotrophic nanoflagellates; IE, invertebrate eggs; MT, M. gerlachei; ON, Oncaea sp.; OT, Oithona sp.; PICO, photosynthetic picoplankton; PL, Pelegobia longicirrata; PNAN, photosynthetic nanoflagellates; RAD, foraminiferans, radiolarians and heliozoans; TIN, tintinnids. a Fortier et al. Ž1994.. b S. fusiformis Žalso the approximate size of S. thompsoni blastozoids, which made up the bulk of the population studied by Perissinotto and Pakhomov Ž1998.; oozoids may be larger, up to ca. 12 cm.. c E. superba. d R. gigas. e Value for S. fusiformis, to which S. thompsoni is morphologically similar, from the work of Silver and Bruland Ž1981.. f Schnack Ž1985.. g Harbison and McAlister Ž1979. and Caron et al. Ž1989.. h Hopkins Ž1985.. i Hopkins and Torres Ž1989.. j Marchant and Nash Ž1986.. k Hopkins Ž1987.. l Hopkins et al. Ž1993a,b.. m Price et al. Ž1988.. n Rau et al. Ž1991..

otrophic conditions, and in the under-ice environment which in many areas is dominated by krill.

5. Export towards apex predators and deep waters 5.1. Food-web transfers It is generally believed that the main trophic pathway sustaining major fish stocks flows through copepods feeding on diatoms Že.g., Cushing, 1989.. Copepods indeed occupy such a niche in the Southern Ocean. However, in addition to fish as a trophic link, other important apex predators are marine mammals and birds. While most baleen whales feed

on krill, the Sei Whale Ž Balaenoptera borealis ., exploits large calanoid copepods ŽKawamura, 1980., including C. propinquus, Cal. acutus and R. gigas in the Southern Ocean. Penguins essentially feed on large plankton Žkrill and other euphausiids, hyperiid amphipods.; among sea birds, only small flying species such as Salvin’s Prion Ž Pachyptila salÕini . ingest significant quantities of copepods ŽRidoux, 1994.. Since the early study of Barkley Ž1940., which described Antarctic krill as mainly herbivorous, this species is often considered as the key link in a three-step food chain between large diatoms and apex predators. The coupling of E. superba to apex predators has been recently reviewed ŽMurphy, 1995.. The Antarctic three-step food chain is homol-

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ogous to the simple herbivorous chain described by Ryther Ž1969. in temperate waters, where copepods fill a similar niche, between large phytoplankton and commercial fish, as krill in the Antarctic. These food-chain concepts were developed before it was recognized that small algae dominate autotrophic biomass and production and that most of this production is processed through microbial instead of herbivorous pathways ŽPomeroy, 1974; Azam et al., 1983; Riegman et al., 1993.. High production by large algae is episodic in both space and time, so that the herbivorous food chain through krill or copepods is a transient link between primary production and apex predators. Perhaps the most unique aspect of the trophic role of krill the Southern Ocean is their ability to feed across a wider range of sizes and taxa than other planktonic organisms there, or other planktonic crustaceans in temperate or tropical oceans. Salp-mediated export to apex predators in the Southern Ocean may be direct or indirect. For example, near the MIZ in the southern Scotia Sea, the fish Bathylagus antarcticus, Electrona antarctica, Gymnoscopelus braueri, Notolepis coatsi Žsize range: 3.5 to 14 cm; Hopkins et al., 1993a. appear to directly feed on salps. Fortier et al. Ž1994. pointed out that the real food targeted by predators may be the phytoplankton and microzooplankton accumulated on the filtering apparatus of salps, rather than their body tissue Ž96% water and ca. 1% organic matter for S. thompsoni; Huntley et al., 1989.. The copepod R. gigas, which is part of the diet of apex predators Žsee above., has been occasionally observed to exploit this resource by feeding inside the branchial cavity of S. thompsoni ŽPerissinotto and Pakhomov, 1997.. More classically, several hyperiid amphipods are facultative or obligate symbionts of salps and exploit the food collected by their host, and, at least occasionally, the host itself. In Gerlache Strait, Hopkins Ž1985. reported salp remains in the guts of several such amphipods Žsize range: 10–55 mm., which are in turn ingested by apex predators. 5.2. Contribution to the Õertical flux The sinking of copepod faecal pellets does not appear to contribute to the downward flux of biogenic particles out of the euphotic zone. This is

because of generally low sinking rates, typically - 100 m dayy1 at average sea-water temperatures Že.g., Honjo and Roman, 1978.. Sinking velocities are lower at the low sea-water temperatures of the Southern Ocean, because of higher sea-water density and viscosity. Moreover, copepods can ingest their own faecal pellets Žcoprophagy. and mechanically break them into smaller, slower-sinking particles Žcoprorhexy.. This further retards the vertical export of copepod faecal pellets. Consequently, only a negligible fraction of copepod faecal material leaves the upper 100 m Že.g., Bathmann et al., 1987; Lampitt et al., 1990; Ayukai and Hattori, 1992.. In the Southern Ocean as elsewhere, grazing by copepods contributes to the termination of phytoplankton blooms; however, for the reasons discussed above, much of the grazed material is retained and recycled in the upper mixed layer, and not exported to depth. Krill are reported to contribute significantly to the downward flux of biogenic carbon in the Southern Ocean ŽSection 3.. Indeed, the exoskeletons of krill are relatively fast-sinking ŽF 1000 m dayy1 ; Nicol and Stolp, 1989.. In contrast, the importance and contribution of their faecal pellets to the vertical export from the surface layer remains equivocal. Cadee ´ et al. Ž1992. reported sinking velocities of faecal pellets and strings from E. superba to vary from 50 to 800 m dayy1 , depending on their size Žlarger faecal strings sink faster., packing index and diet. For example, krill feeding on diatoms generally produced faster-sinking pellets than when krill ingested flagellates. These authors ŽCadee ´ et al., 1992. also suggested that laboratory-based observations of faecal pellet ‘potential’ sinking rates may overestimate those determined from sediment traps. Although these sinking rates are generally faster than those of copepod faecal pellets, the analyses of sediment trap contents ŽGonzalez, 1992. showed that ´ krill faecal strings in the Weddell and Scotia Seas were most abundant Ž130 mg my3 , dry weight, on the average. in the upper 50 m, and decreased exponentially with depth down to 0.6 mg my3 in the 500–1000 m layer. Only the largest faecal strings were collected in the deep traps. As noted for copepods, a large fraction of this material was recycled in the upper water column, perhaps due to coprophagy and coprorhexy. Despite the repackaging of small prey into larger faecal pellets, it is likely that krill

J. Le FeÕre ` et al.r Journal of Marine Systems 17 (1998) 325–345

channel a large fraction of their ingested material to the long-lived Ži.e., food web export. rather than the sequestered carbon pool. Indeed, although episodic and large sedimentation events of krill faeces have occasionally been reported Že.g., von Bodungen et al., 1987; Bathmann et al., 1991., they are variable in space Žgiven the horizontal heterogeneity in the distributions of krill and their food. and time. They may, in addition, occur in conditions such that direct settling of cells from a diatom bloom is a competing process Žsee the work of Bathmann et al. Ž1991... Despite the uncertainties pointed out in Section 4.1, salps in the Southern Ocean appear to be more abundant in offshore ice-free waters where small phytoplankton often dominate. Because of their low sinking rates, these small phytoplankton are not normally exported. Hence, salps can efficiently ingest and repackage non- or slowly sinking small particles Žsuch as phytoplankton and heterotrophic nanoflagellates. into large and dense faecal pellets that are both resistant to bacterial degradation and are among the fastest-sinking from all zooplankters Žup to 2700 m dayy1 ; see the work of Fortier et al. Ž1994... These pellets often reach the deep waters in almost intact state, thus contributing to the downward transport and potential sequestration of biogenic carbon. This appears to be general in oceanic waters. At some locations and times, in Antarctic waters, salps may account for most of the downward flux of biogenic carbon, as was apparently the case in the Bransfield Strait in March 1984, where S. thompsoni egested up to 67 mg C my2 dayy1 ŽHuntley et al., 1989..

6. Interactions among copepods, krill and salps There have been reports of mutual exclusion between copepods and krill Že.g., Hempel, 1987., and krill and salps in Antarctic Waters Že.g., Piatkowski, 1985; Nishikawa et al., 1995.. In the northern Weddell Sea, Siegel et al. Ž1992. found that the large copepods were overwhelmingly dominant by numbers in open waters and that their abundance decreased sharply towards the closed ice pack. Salp wet weight was greater than that of copepods in open waters. However, since there are large differences in the water content for the two taxa, the patterns in

337

carbon biomass may have differed from those of wet weight. Salps were very scarce in ice-covered waters, where krill became overwhelmingly dominant, in terms of both numbers Ž33% of total meso- and macroplankton. and biomass Ž91%.. As already mentioned in Section 4.1, high abundances of salps have also been observed near the ice edge and sometimes in the under-ice water column. It is unclear if the reported gradients reflect selectivity of the sampling gears, differential responses of organisms to environmental characteristics, or competitive exclusion. For example, studies in Antarctic waters have addressed the apparent mutual exclusion of salps and krill Že.g., Huntley et al., 1989; Nishikawa et al., 1995.. The latter study examined four possible mechanisms for the exclusion of krill from areas of high salp abundances, i.e., removal of krill food by salps, predation by salps on krill eggs and larvae, production of distasteful compounds by salp metabolism, and differential advection of water masses containing krill and salps, respectively. The authors rejected the possibility of krill exclusion by food removal, and considered instead direct predation by salps on small krill individuals, eggs or larvae, already suggested by Huntley et al. Ž1989.. However, ingestion by salps of significant numbers of krill larvae is questionable ŽSection 4.2.. In any case, this could not explain the absence of adult krill, which are known to forage for food in open waters as compact swarms during summer ŽSection 4.1.. This example shows the difficulty of approaching the interaction between taxa from the perspective of mutual exclusion, because this hypothesis is almost impossible to falsify in the natural marine environment. An alternative approach is comparing carbon budgets for salps, krill and large copepods. The ratio of carbon assimilated to carbon respired is: Ca Cr

CCR= AE s R

w POCx

Ž 1.

where: wPOCx is the ambient particulate organic carbon concentration Žmg ly1 ., CCR is the carbonspecific clearance rate, i.e., the volume swept clear per unit carbon biomass, per unit time Žl mgy1 dayy1 ., AE is the assimilation efficiency, i.e., the ratio of carbon assimilated to carbon ingested and R

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is the amount of carbon respired per unit carbon biomass, per unit time Žmg mgy1 dayy1 .. Sustained survival requires that the amount of carbon assimilated be at least equal to the amount respired, i.e., C arC r G 1. Hence, according to Eq. Ž1., the minimum wPOCx should be:

w POCx min s Rr Ž CCR= AE.

Ž 2.

Table 2 compares wPOCx min values for representative species in the three groups of organisms, as calculated from average carbon biomasses and rates of clearance and respiration from the literature, and from very conservative assimilation ratios. In the case of S. thompsoni, however, because reported clearance rates vary by ) 10-fold, we present the results for both average Žca. 15 l indy1 dayy1 . and reported maximum Ž130 l indy1 dayy1 . clearance rates. Fig. 2 models the ratio of assimilation to respiration over a range of POC concentrations. The slopes decrease as the relative importance of respiratory losses increases, and the thresholds wPOCxmin are visualized by the intercepts between the curves and the horizontal for C arC r s 1. Krill and copepods will fulfil their respiratory requirements at minimum wPOCx of 125 and 105 mg C ly1 , respectively. For salps, this minimum threshold ranges from 3.5 to 30 mg C ly1 , depending on the clearance rate.

It might be tempting to use known carbon to chlorophyll ratios to convert wPOCx values into phytoplankton biomass. This would be inappropriate, because all three taxonomic groups consume both algal and non-chlorophyllous prey, including protozooplankton. In the Southern Ocean, during some seasons and at some locations, microheterotrophic biomass indeed greatly exceeds that of phytoplankton. The empirical threshold of 1 mg Chl ly1 reported by Perissinotto and Pakhomov Ž1998. as the upper limit of food concentration that salps can tolerate would, according to traditional conversion factors, correspond to a wPOCx of ca. 50 mg ly1 . Taking into account microheterotrophic biomass and small detritus would, however, increase the value to perhaps 100 mg ly1 . The above results imply that salps, because of their low basal metabolic requirement, can tolerate, and develop populations in, periods when the abundance of food is too low for either copepods or krill to meet their respiratory requirements. This is consistent with the observation of Hopkins Ž1985. that, in Crocker Passage during autumn, S. thompsoni continued to successfully feed despite the low concentrations of phytoplankton whereas E. superba could not. The above values also indicate that, assuming that food is uniformly distributed, the average mini-

Table 2 Comparison of feeding and metabolic characteristics of S. thompsoni Žfor two clearance rates., E. superba and C. propinquus S. thompsoni Biomass Ž B; mg C indy1 . Clearance rate ŽCR; l indy1 dayy1 . Carbon-specific CR ŽCCRs CRrB; l mgy1 C dayy1 . Respirationa Ž R; mg C mgy1 C dayy1 . Assimilation efficiency ŽAE; %. Resource thresholdb ŽwPOCx min ; mg C ly1 . a

6.4c 130d 20 35c 50e 3.5

6.4c 15f 2.34 35c 50e 30

E. superba

C. propinquus

88.3g,h 50i 0.57 50i 70j 125

0.45i 0.45i 1.0 90g 85k 105

Oxygen was converted to carbon assuming a respiratory quotient RQ s 1. Minimum ambient particulate organic carbon concentration needed to meet respiratory requirements, calculated according to Eq. Ž2.. See also Fig. 2. c Reinke Ž1987. d Maximum reported rate ŽPerissinotto and Pakhomov, 1998.. e In S. fusiformis ŽAndersen, 1985.. f Average rate ŽReinke, 1987.. g Ikeda and Mitchell Ž1982.. h Voss Ž1982.. i Schnack Ž1985.. j Ross Ž1982. and Price et al. Ž1988.. k Omori and Ikeda Ž1984.. b

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Fig. 2. Ratio of carbon assimilation to carbon respiration, C arC r , as a function of ambient POC concentration, calculated using Eq. Ž1. and values given in Table 2 for S. thompsoni Žmaximum and average clearance rates., E. superba and C. propinquus, respectively. Minimum ambient POC concentrations required for sustained survival ŽC arC r s 1: dashed line. are wPOCx min s 3.5 to 30, 125 and 105 mg C ly1 , for S. thompsoni, E. superba and C. propinquus, respectively.

mum concentration of food needed to sustain respiration is at least four times, and possibly 40 times, higher for krill than for salps. The case of large copepods would be similar to that of krill, but not as extreme. Krill are active feeders that can acquire food in large aggregates Že.g., patches of ice algae, other animals., contrary to salps which are limited to a smaller range of particles Žsee Section 4.2.. It follows that krill will thrive at either high particle concentrations Že.g., at some receding ice edges. or in patchy environments Že.g., undersurface of the ice.. In contrast, salps do not benefit from patchy

conditions and they generally cannot tolerate high particle concentrations. Patchy conditions are encountered under low wind mixing, whereas uniform distributions are favoured by active hydrodynamics. Table 3 summarizes the conditions under which salps and krill are expected to thrive. The under-ice environment, well south of the MIZ, and polynyas could be areas where the two groups co-exist ŽHarbison, 1988; Boysen-Ennen et al., 1991., because particle concentrations there are lower than in the MIZ, yet the environment is heterogeneous as a result of leads and the complex ice–water interface.

Table 3 Conditions under which salps and krill are expected to succeed

Food concentration Food distribution Hydrodynamic conditions Type of algae a Other food items a

Salps

Krill

Low Homogeneous Dynamic Small, flagellates Bacteria, microzooplankton

High Patchy Stable Large, diatoms Mesozooplankton

Type of algae that generally corresponds to the stated hydrodynamic conditions.

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7. Conclusion The three major physical characteristics of the Southern Ocean are: permanently cold temperatures, the presence of a seasonal ice cover, and extreme seasonal cycle of underwater irradiance, especially south of the Antarctic Circle. In waters other than those surrounding Antarctica, such conditions are generally associated with low productivity or otherwise unfavourable conditions for growth. However, the waters surrounding Antarctica support large abundances of apex predators such as whales, seals and birds. In this paper, we developed the conceptual linkages between the physical characteristics of the Southern Ocean and the export fluxes of biogenic carbon, by invoking the special regime of primary

production and some unique biological and ecological characteristics of key taxa of large zooplankton. Our ideas are schematized in Fig. 3. Interaction between the seasonal ice cover and cycle of underwater irradiance constrains the temporal and spatial patterns, size distribution and magnitude of algal production. Because of the prevalence of small algal cells and generally low primary production, microbial trophic levels dominate the pelagic communities over large areas of the Southern Ocean, for most of the year. Low temperatures and ice cover are crucial in structuring the zooplankton communities. First, the cold temperature may be partly responsible for the ability of large crustaceans Žkrill and some copepods. to feed on particles orders of magnitude smaller than themselves Žmicrophagy..

Fig. 3. The three main physical factors that shape Antarctic pelagic marine ecosystems are: permanently cold water, extreme seasonal cycle of solar radiation and presence of a seasonal ice cover. Low water temperature facilitates the grazing of small particles by some large planktonic crustaceans Žlarge copepods and krill; microphagy.. Null submarine irradiance Žseasonal or because of thick ice–snow cover. prevents photosynthesis, hence the dominant production pathway is the microbial loop. Low irradiance favours the photosynthetic activity of small Ž- 2–5 m. vs. large phytoplankton. Blooms of large phytoplankton Ž) 2–5 m. occur in association with offshore fronts and at retreating ice edges in the MIZ. The 1st-year ice provides a substratum for ice algae and a refuge for krill. Because of microphagy, krill, salps and some large copepods can survive and even thrive in Antarctic waters dominated by small plankton. In addition, krill Žand some large copepods. take advantage of large algae, when these are abundant in and near the sea ice and also in offshore fronts. All large microphages channel, to various degrees, biogenic carbon towards apex predators. Large algae and the fast-sinking faeces of salps and krill are the main components of the deep flux of organic particles in the Southern Ocean.

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This biological characteristic seems to occur exclusively in polar waters, and it has been reported for both the North and South Hemispheres. Second, the seasonal ice cover is an essential component of the ecology of krill, as it provides highly concentrated food as well as habitat and refuge. As a consequence of the physical characteristics and patterns of primary production of Antarctic waters, salps, krill, and some large copepods influence in unique ways the fluxes of biogenic carbon in the Southern Ocean. The three taxa share a means of survival which is their ability to ingest the small particles that are typical of the ambient production regime, and they can all potentially transfer biogenic carbon from the microbial components Žthat generally correspond to the short-lived pool of biogenic carbon. to apex predators Žlong-lived pool. or the deep waters Žleading to sequestration.. Krill are very efficient at transferring biogenic carbon to a wide array of apex predators Že.g., crabeater seals, rorquals, penguins. and their faecal pellets are episodically exported to depth. Thus, krill are the key link in Antarctic food webs and they contribute to exporting some biogenic material to depth. Salps may be a significant link towards some fish Ždirectly. and other apex predators Žindirectly. and they could potentially contribute to most of the downward carbon flux, especially in offshore waters. However, there are still large gaps in the information on the biology of this group in the Southern Ocean and on its ecological role there. Finally, large copepods are a trophic link towards fish, at least one whale species and a few sea birds, but their faecal pellets do not contribute to the downward flux of biogenic carbon. Actually, their grazing activity generally impedes the export of organic particles to depth. Fig. 4 summarizes the trophic characteristics of the three taxa of large zooplankton microphages, within the context of the fundamental niche defined by Hutchinson Ž1957, 1965.. In the fundamental niche, each axis corresponds to one environmental variable that is critical for a species to exist, and it specifies the limiting conditions within which the species can exist indefinitely. In the present case, the two axes correspond to trophic characteristics, so that the figure can be thought of as the trophic sub-niche. The two axes specify the POC concentra-

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Fig. 4. Summary trophic characteristics of the three large zooplankton microphages in Antarctic waters. Ratios of consumer to prey sizes were computed from Table 1 Žnote that the ordinate is logarithmic.. Minimun wPOCx values for each taxon are from Fig. 2 Žthe two estimates for salps correspond to high and average clearance rates, respectively; Table 2.. The maximum value of 100 mg ly1 for salps is roughly estimated according to Section 6; maximum values for large copepods and krill, if any, are outside the range of wPOCx displayed in the figure. The diagonal Žshaded. band defines a ‘ridge’ of high contribution to export; in the upper left-hand part, the contribution to export is mainly towards deep waters whereas, in the lower right-hand part, it is mostly towards the food web. Interpretation of the wPOCx axis, at the bottom of the figure, is consistent with Table 3.

tions and range of prey sizes within which each of the three taxa can exist indefinitely. Outside its sub-niche, a given taxon is either absent or transiently present. There is no implication that all combinations of environmental characteristics actually occur in nature, e.g., high ratios of consumer to prey sizes are unlikely at high POC concentrations because, when large prey are available, krill or large copepods do not usually resort to microphagy. Fig. 4 shows that, even when only considering trophic characteristics, the three taxa occupy distinct niches in Antarctic waters. Fig. 4 also stresses the fact that the three taxa span several orders of magnitude in consumer to prey sizes, which explains their success in the Southern Ocean, as discussed above. Finally, a ‘ridge’ of high contribution to export was drawn into the trophic subspace, in an attempt to relate the export properties of the three taxa to their trophic

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characteristics. It is interesting to note that, in the upper left-hand part of the ridge, the contribution to export is mainly towards deep waters whereas, in the lower right-hand part, it mostly occurs towards the food web. In the Southern Ocean, the interaction between physical environmental factors, their effects on primary production and their consequences on the biology and ecology of key zooplankton clearly influence the magnitude and timing of the fluxes of biogenic carbon. Biogenic carbon is channelled mainly towards apex predators and episodically into the deep ocean. The ability of the major zooplankton taxa, in the Southern Ocean, to ingest and repackage microbial-sized, non-sinking particles into both metazoan biomass and large, rapidly sinking faeces appears to be unique to this environment. This shunt from small food particles to large grazers permits efficient transfer of energy to apex predators. Without these original interactions, Antarctic waters might well be dominated by microbial components and recycling processes instead of active export from the generally small primary producers towards large apex predators.

Acknowledgements CNRS support to UMR 6539 Žformerly URA 1513. and to the Southern Ocean JGOFS Symposium, Brest, August 1995, as well as research grants from the Natural Sciences and Engineering Research Council of Canada to L.L. and R.R. were instrumental in the completion of the work. We thank K. Crocker and D. Deibel for helpful discussions. Criticism by U. Bathmann and two anonymous referees led to significant improvement of the manuscript.

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