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AQUATIC Vol. 9: 69-77. 1995 Published April 28 Aquat microb Ecol

Microbial food webs and the export of biogenic in *

Louis Legendre l, Jacques Le ~evre

'GIROQ, Departernent de biologie, UniversitC Laval. Quebec. QuCbec, Canada GlK 7P4 'Unite de Recherche 'Flux de Matiere et Reponses du Vivant', Institut Universitaire Europeen de la Mer, Universite de Bretagne Occidentale, BP 809, F-29285 Brest Cedex, France

ABSTRACT: Microbial food webs, which comprise phototrophic (or ultraplankton), het- erotrophic and , are ubiquitous in marine . Members of the microbial may play various roles in the export of biogenic carbon. For example, it has been postulated that high bacterial activity may sometimes prevent a significant fraction of the production by large phytoplank- ton from reaching metazoan consumers. Phototrophit or heterotrophic small cells may be readily exported (i.e. biological CO2 pump) if incorporated into large particles, through either endo- symbiosis with larger cells, or development on material accumulated in hydrodynamic traps, or inclu- sion into , or grazing by large planktonic microphages (e.g. ) and incorporation in their sometimes fast-sinking faecal pellets. Another aspect is the export of carbonate by members of the (e.g. , ), which influences the balance of the (i.e. carbonate pump). Finally, carbon bound into refractory dissolved organic matter is chemically sequestered in the upper ocean, before being exported to depth. The activity of microbial food webs may therefore influence in several ways the export (and sequestration) of biogenic carbon in oceans.

KEY WORDS: . Plankton. Bacteria. Food web - Carbon flux

INTRODUCTION - THE MICROBIAL FOOD WEB classical textbook description of a chain from IN MARINE WATERS through and to and may in fact be only a small part of the flow of energy'. For Microorganisms are ubiquitous in the world ocean. instance, it is now widely acknowledged that, in oligo- Even in the extreme environment of the ice, het- trophic oceanic waters, phototrophic picoplankton erotrophic bacteria are present together with such pro- (cells 0.2 to 2 pm; Sieburth et al. 1978) or ultraplankton tists as and foraminifera (refs. in Legendre et al. (cells <5 to 10 pm; Sverdrup et al. 1942) generally 1992). In addition, although this is not widely recog- account for >50% of the chlorophyll a , with nized, small photosynthetically active (as small some published values >go%. Given their high pro- as

O Inter-Research 1995 Resale of full artlcle not pernutted 7 0 Aquat microb Ecol9: 69-77, 1995

ploited by ciliates. This grazing activity is accompa- ca 40% at a station in the Celtic Sea. These examples, nied by excretion of substances which are in turn used as well as other modelling exercises (e.g. Pace et al. by the bacteria, so that the system more or less oper- 1984, Fasham 1985), suggest that the microbial food ates in a closed circuit. This leaves aside the role of web can also function as a link towards metazoans. picoplanktonic photoautotrophs, which are also part of Furthermore, some large planktonic microphages the microbial food links. The 2 expressions microbial appear rather efficient at both exploiting microbial web and are found in the literature. It resources and producing resistant, fast-sinking, parti- has been proposed (e.g. Rassoulzadegan 1993) to use cles (e.g. review of Fortier et al. 1994). 'microbial loop' for designating the almost closed sys- The sink versus link views of the role of microbial tem of heterotrophic bacteria and zooflagellate graz- food webs in the ocean had to some extent developed ers, in which the latter release dissolved organic matter into a controversy, whereas some authors (Sherr & used as substrate by the former, and 'microbial food Sherr 1988) argued that the role of the microbial food web' for the more open system which also includes the web as a sink or a link for carbon is a non-issue, autotrophic pico- and nanoplankton. According to because all carbon for ingestion by metazoans must Cushing (1989), the microbial food web predominates come from the microscopic part of the food web (all in stratified waters because the exudates from photo- planktonic primary producers being microscopic). As trophic picoplankton (small eukaryotic algae and pointed out by Ducklow (1991), however, the link-sink ) are not dispersed and can therefore be approach need not be considered an either-or issue. A used by heterotrophic bacteria. number of microbial processes coexist in marine Picophytoplankton could thus be viewed as competi- waters some of which (the link aspect) will favour the tors to large cells, such as diatoms, for , while export of biogenic carbon, while others (the sink the microheterotrophs can be viewed as competitors to aspect) may delay or prevent it. This duality sets the metazoans, such as copepods and , in the utilization general framework for the present paper, in which of primary production. According to a number of some of the microbial processes that influence the empirical data (e.g. Williams 1981, Ducklow et al. export of biogenic carbon in oceans are examined 1986, Pomeroy & Deibel 1986, Smith et al. 1986) and (Fig. 1).The following discussion will only cover a few modelling exercises (e.g. Taylor & Joint 1990, Moloney of these processes, given our limited knowledge of et al. 1991), the microbial food web would thus consti- microbial food webs in the marine environment. It is tute a sink for biogenic carbon. In other words, most of recognized that, by lack of sufficient information, some the autotrophic production processed by microorgan- microbial processes that may eventually prove signifi- isms would be oxidized (respired) within the microbial cant for the export of biogenic carbon have perhaps loop in the euphotic layer (e.g.Michaels & Silver 1988) not been identified in the present paper. rather than being exported in the form of metabolic energy to higher-order consumers, or in the form of fall-out to deep waters. For example, results of SOME MICROBIAL PROCESSES INFLUENCING network analyses for 3 food webs (i.e. SE Atlantic THE EXPORT OF BIOGENIC CARBON oceanic waters, stratified column of the Agulhas Bank, and Benguela coastal ; Moloney et al. Export and sequestration of carbon in oceans: the 1991) indicate that < 1 % of the photosynthetically fixed biological CO2 pump carbon reaches >25 pm via heterotrophs <25 pm. Within the context of global climate change, 2 terms However, even if the microbial web is inefficient as a must be distinguished as to the flux of biogenic carbon carbon pathway to large heterotrophs, it is the only in oceans, i.e. export and sequestration (see Legendre available pathway when are small. The & Le Fevre 1991). On the one hand, export refers to the above-cited study by Moloney et al. (1991) shows that flux of biogenic material from surface to depth, while the proportion of the carbon which reaches hetero- on the other hand, sequestration concerns the removal trophs >25 pm directly from autotrophs may be as high of dissolved inorganic CO2 from the and as ca 90% on the Agulhas Bank and >95% in the the surface waters for periods of interest to global Benguela upwelling, while this proportion is almost nil warming (i.e. at least a few hundred years). Processes in oceanic waters. This agrees with the results of Vez- involved in carbon sequestration include: the sinking ina & Platt (1988) who found, using inverse methods to or downwards transport of biogenic dissolved and estimate fluxes in pelagic food webs, that microbial particulate carbon, followed by burial in sediments or grazers (protozoans and microzooplankton) supplied dissolution in deep waters; the long-term fixation of ca 70% of the carbon demand of the mesozooplankton carbon into calcareous material; and the binding of at a stratified station in the English Channel, and carbon into refractory dissolved organic matter. Export Legendre & Le Fevre. Export of biogenlc carbon 7 l

cloud cover) and through climate-induced variations in PRIMARY PRODUCTION the hydrodynamic forcing of biological production. If, through such effects, the net result of global warming METAZOA MICROBIAL were an enhancement of overall , this LOOP would result in a negative feedback, and climatic vari- GRAZING ations would be attenuated. The response of the bio- BACTERIA MICROFLAGELLATES - logical CO2 pump to climate change may also, how- l ever, result in positive feedback effects such as those PREDATORS \ ClLlATES/ often put forward to account for glacial-interglacial oscillations. The latter are believed to be induced by a Fig 1 Conceptual model of the flux of carbon between pri- weak astronomical forcing whose effects are amplified mary producers, metazoans and microorganisms (adapted by changes in CO2 concentration in the atmosphere. from Pomeroy & Wiebe 1988, Fig 1).The number of transfers According to a modelling exercise by Lindstrom & is variable and often unknown, for both the metazoans and the microbial food web McAyeal (1989), a threshold of about 250 ppm (vol- ume) in CO, concentration would govern the evolution of climate towards either the glacial or the interglacial and sequestration are generally not equivalent, since a quasi-stable mode. Among other mechanisms put for- large fraction of the exported biogenic carbon is some- ward to account for the self-regulation of each mode, it times rapidly respired during its downwards transit has been hypothesized that the biological CO2 pump in and recycled back to the atmosphere. For global bio- the oceans is stronger in glacial conditions, and geochenlical budgets, the really significant term is not weaker in interglacial ones (e.g. because of latitudinal the export, but the actual sequestration of carbon. shifts in the location of the areas of maximal production Close to the surface of the ocean (euphotic layer), such as major ; Sarmiento & Toggweiler solar fuels the photosynthetic incorporation of 1984). inorganic carbon into organic nlolecules by phyto- The present paper will examine the significance of plankton, a fraction of which sinks to deep waters (as microbial food webs for the biological CO2 pump. The intact cells, faecal pellets, marine snow) or is actively discussion will deal with potential influence, on the transported by vertically migrating . This export and sequestration of biogenic carbon, of 4 export pathway is known as the biologicalCO2 pump, microbial processes, i.e. the possible competition be- since the carbon supply used by the photosynthesis in tween bacteria and metazoan consumers; the export the euphotic zone is replenished by diffusion of atmos- pathways of small plankton cells, and their signifi- pheric CO2 into the oceans (and by HC03- in river cance for the sequestration of carbon; the export of car- waters). This pump and other mechanisms operate in bonate by some members of the microbial food web; such a way that a gradient of increasing CO2 concen- and finally, the production of refractory dissolved tration towards deeper waters is maintained against organic matter. the effects of turbulent mixing and diffusion (for more details, see for instance Volk & Hoffert 1985). As far as presently known, the biological CO2 pump Bacteria versus metazoan consumers is unlikely to directly increase carbon sequestration in a short-term response to the anthropogenic increase According to Pomeroy & Deibel (1986), high sec- in atmospheric CO2 concentration. This is because ondary production in cold waters may be explained by marine photosynthesis is generally not carbon-limited. low bacterial activity. At temperatures between -1 and However, new findings (Riebesell et al. 1993) indicate 2"C, as for example during the spring that, under optimal light and conditions, the bloom in Newfoundland waters, photosynthetic pro- growth of diatoms might be limited by the supply of duction is substantial but rates of bacterial growth and free CO2 in , so that a response cannot be are low (Fig. 2).Low rates of microbial uti- ruled out in some circunlstances (see Raven 1993). The lization of phytoplankton material would allow a high role of this pump in the global flux of carbon needs proportion of the autotrophic production to find its way anyway to be quantified (see JGOFS 1990), because it to metazoan consumers, i.e. benthic and planktonic does contribute to the overall balance in the exchanges . According to Pomeroy & Wiebe (1988), between the various global carbon pools (see this would explain why regions in the northern hemi- Sundquist 1985). In the long term, the biological CO2 sphere where the occurs between -1.8 pump and climate changes may interact. Biological and 2°C are also regions of resilient of con- activity in the oceans is likely to respond to climate sistently high . In warm tropical and sub- changes, both directly (e.g, effects of temperature and tropical waters, in contrast, bacterial metabolism and 7 2 Aquat microb Ecol9: 69-77, 1995

Export pathways of small plankton cells

Pathways through which the production of small plankton cells (<5 pm) is exported may contribute to uncouple the actual sequestration of carbon from the export of biogenic carbon. As explained above, not all export pathways result in sequestration. According to Legendre & Le Fevre (1991),the fraction of the original carbon production that will eventually be sequestered is largely controlled by processes. Legendre TEMPERATURE"C & Le Fevre (1989) have reviewed the various export Fig. 2. Relationship of bacterial growth (solid line) and poten- pathways from the primary producers, their hydrody- tial primary production (dotted line) to temperature, between namic control, and their significance in terms of partic- the freezing point of sea ice and +6"C, at low substrate con- ulate organic matter fall-out from the surface layer. centration (adapted from Pomeroy & Wiebe 1988, Fig. 2) These pathways include (from left to right in Fig. 3):the sinking of large intact cells: the grazing of large cells by herbivores, and production of faecal pellets as well as growth are rapid, so that the turnover time of phyto- active transport by vertically migrating organisms; the plankton production is of the order of 1 to 3 d; as a con- grazing of detrital biogenic material, accumulated in sequence, much of the carbon would not reach the hydrodynamic traps, by microphagous feeders; the in- metazoans. corporation of small cells into sinking marine snow; and This view was subsequently expanded (e.g. Pomeroy the direct grazing of ultraplankton by metazoans. & Wiebe 1993) to include the effect of substrate con- The 2 leftmost pathways in Fig. 3 do not generally centration. At high values of the latter, temperature concern the small organisms, except perhaps in the has little influence (e.g.Pomeroy et al. 1991, Wiebe et special case of endosymbiosis with larger cells. In al. 1992). In contrast, at low substrate concentrations oligotrophic waters of the Pacific Ocean, for example, usually found in seawater, minimal temperatures (e.g. the endophytic cyanobacterium Richelia intracellularis in the annual cycle) can inhibit bacterial activity even was observed to occur in >90% of the cells in 3 in temperate and warm regions. As a result, bacteria of Rhizosoleniadiatoms (Venrick 1974), and Heinbokel would often be inefficient in utilizing much of the (1986) found it in ca 80% of the cells in 2 species of spring bloom production, until excretion, defecation Herniaulus diatoms. Massive sedimentation of large and inefficient feeding by zooplankton creates micro- intact cells, at rates that may exceed 100 m d-' (refs. In zones of high substrate availability (refs. in Pomeroy & Goldman 1988), mainly takes place under bloom con- Wiebe 1993). ditions. As explained in Legendre (1990), microalgal The implication of both the original and expanded blooms largely depend on the balance between phyto- models is that metazoans and bacteria may, to a con- plankton production (resulting from hydrodynamic siderable degree, compete for the exploitation of pri- forcing) and grazing by herbivorous zooplankton. It mary production. In the view of Pomeroy & Wiebe follows that, under low grazing pressure, most of the (1988), bacteria, by channelling biogenic carbon large cells may sediment (several examples of large into the microbial food web, would be responsible for fall-out of often intact cells following a bloom a major loss, i.e. in temperate and tropical waters, are reviewed in Legendre 1990, and Legendre & microorganisms would often use (and dissipate) half or Le Fevre 1991). Active grazing by herbivores, on the more of the pnmary production. other hand, leads to sedimentation of faecal pellets. The approach discussed in the previous paragraphs faecal pellets are wrapped in a protective is essentially relevant to the possible negative role of membrane that prevents the degradation of their con- bacteria on the export of primary production towards tents during at least part of the downwards transit and metazoan consumers. Within the more general context they package fine material (including , see of biogeochemical fluxes of carbon, it may be hypothe- next section) into larger, and therefore faster-sinking, sized that, in warm waters, bacterial activity could particles. The sinking velocity of copepod faecal pel- impede and sometimes prevent the transfer of primary lets is of the same order as that of intact cells (see production towards not only metazoans but also the Legendre & Le Fevre 1991) but, because some bacter- deep waters where carbon can be sequestered. This ial degradation does take place (as well as copro- should be taken into account when assessing the sig- phagy) during their descent, they are thought to nificance of the biological CO2 pump in temperate and account for only a small faction of the carbon supply to tropical waters. deep waters (see Pilskaln & Honjo 1987). Legendre & Le Fevre: Export of biogenic carbon 7 3

MICROBIAL

GRAZING ACCUMULATION SINKING ( MICROPHAGY)v \

RECYCLED/TOTAL PRODUCTION b

Fig. 3. Model of export production (downwardsarrows) in oceans. Alternative pathways for the fluxes of materials and energy in marine are conceptually shown in the form of bifurcations. In the real world, however, alternative processestake place simultaneously, their relative importance being dependent on the prevailing conditions. At each bifurcation, part of the production may be channelled into export pathways, which does not preclude the coexistencewith recycling pathways. The length and complexity of the food webs involved in the export of biogenic carbon increase towards the right. According to Legendre & Le Fevre (1989), hydrodynamic conditions control the 5 bifurcations. Reprinted with permission from the Dahlem Workshop Report LS44,p. 51, John Wiley and Sons, Chichester

The 3 rightmost pathways in Fig. 3 directly concern the carbon that would otherwise be dissipated in the the microbial food webs (refs. in Legendre & Le Fevre microbial loop. In addition, these organisms produce 1989, 1991). Microheterotrophs (bacteria and their pro- faecal pellets that are more resistant and sink faster tozoan predators) will develop, for example, by taking than those of copepods or euphausiids (e.g. up to advantage of ageing biomass and other detrital mater- 2700 m d-l; Bruland & Silver 1981). Gelatinous organ- ial not being directly consumed by metazoans, espe- isms also are instrumental in the production of marine cially if the material is being accumulated in hydrody- snow, where small cells (which would normally not namic traps (e.g. convergent circulation associated sink at all) are aggregated together with other material with fronts, eddies, Langmuir convection cells; or such and thus made available for export to depth. Large hydrodynamic structures as the pycnocline) and, more planktonic microphages therefore also directly transfer generally in situations that do not favour the build-up some microbial carbon towards export to depth and of a full-fledged herbivore . possible sequestration. Some groups of essentially non- meta- In general, the length and complexity of food webs zoans specialise in exploiting microbial plankton. involved in the export of biogenic carbon increase to- Fortier et al. (1994) recognise 4 such groups of micro- wards the right of Fig. 3. The amount of organic mater- phages, which feed on particles at least 3.5 orders of ial respired during the downwards transit (and poten- magnitude smaller than their own size, namely salps, tially rapidly returned to the atmosphere) is largely appendicularians, doliolids and thecosome pteropods. determined by sinking velocity. Thus, rapid sedimenta- The latter produce calcareous shells, and thus con- tion of intact cells or other biogenic particles (e.g. some tribute to the processes discussed in the next section, faecal pellets) into deep waters favours the sequestra- while the former groups are gelatinous organisms. All tion of carbon. In contrast, export pathways to the right of them can feed at least on the protozoan members of of Fig. 3 involve increasingly longer downwards transit the microbial web, and some direct feeding on bacter- of the biogenic material, during which most of the car- ial size plankton is even possible (e.g. by appendicu- bon may be respired and returned to the atmosphere. larians). These microphages are in turn directly (e.g. This would result in lower sequestration relative to the larvae feeding on appendicularians) or indi- amount of biogenic carbon exported. The export path- rectly (e.g. tuna feeding on parasites such as ways, which are largely under hydrodynamic control hyperiid amphipods) prey to higher-order consumers, (Legendre & Le Fevre 1989), may thus influence the and may thus redirect to exploitable resources part of amount of carbon sequestered by the ocean. 74 Aquat microb Ecol9: 69-77, 1995

Export of carbonate by the microbial food web in 2 mid-latitude belts, i.e. near the Antarctic Conver- gence (40" to 60' S) in the southern hemisphere and The average chemical composition of marine plank- near the polar front in the northern hemisphere, and ton is given by the 'Redfield ratio' (Redfield 1958, Red- also along the continental margins (Lisitzin 1972; see field et al. 1963) C : N: P = 106 : 16 : 1 (atoms). However, also Fig. 4). Pelagic foraminifera are also abundant in some plankton organisms export an extra share of association with Antarctic sea ice (refs. in Legendre et carbon, in the form of calcareous skeletal structures al. 1992). High concentrations of suspended particulate (consisting mainly of CaC03 with small and variable carbonate along continental margins might well corre- proportions of other substances such as MgC03). spond to blooms, as observed by Holli- Members of the microbial food web with calcareous gan et al. (1983) along the continental shelf edge in the tests include photosynthetic cells (mainly coccolitho- Celtic Sea. An example of the significance of cocco- phores) and protozoans (foraminifera). Given their rel- lithophore blooms for the vertical transport of carbon- atively large size and high density, foraminifera sink ate is provided by Honjo (1982) who observed, during rapidly (up to 2500 m d-l; Takahashi & Be 1984). Coc- a bloom of the coccolithophore Umbellicosphaera sibo- coliths, on the other hand, may be carried in faecal pel- gae, a mass flux of particles of 876,mg m-' d-'. lets, and thus have a sedimentological behaviour sirni- Calcareous tests dissolve at depth, so that lar to large particles (e.g. Honjo 1980).Calcareous tests (produced, among pelagic organisms, by coccolitho- may therefore be very efficient in exporting biogenic phores and foraminiferans) is not found in sediments carbon to depth (refs. in Legendre & Le Fevre 1991). deeper than 4000 to 5000 m (in the Antarctic Ocean, and foraminiferal productivity is maximal the compensation depth is considerably shallower; see between 50" N and 50" S, in general coincidence with Legendre et al. 1992). In deep-water areas, carbonate- waters >lO°C. The highest concentrations of suspen- carbon is thus progressively released into the water ded particulate carbonate are found in surface waters column, so that its fate (i.e. rapid release to the atmos- phere versus sequestration for tens to hundreds of years in the deep waters) depends on sinking velocity and on the deep circulation. In shallow waters, on the other hand, carbonate sediments may sequester car- bon for millions of years (e.g. sediment accumulation up to several kilometres deep near the continents and on the flank of ridges, and limestone deposits from epi- continental accumulated on the continents). Concerning the of carbon, the production of plankton organisms with calcareous tests leads to paradoxical results. Limestone deposits were ultimately derived, through biological processes and complex long-term geochemical interactions (Lasaga et al. 1985), from atmospheric CO2, and carbonate cal- cination in cement factories does contribute a small fraction of the anthropogenic increase in atmospheric COz. On the other hand, the immediate effect of car- bonate precipitation is a decrease in the alkalinity of seawater, which releases dissolved CO2 in surface waters at the expense of HC03 It is generally believed that this causes a net flux of CO2 from surface waters to the atmosphere. Greater reef develop- ment in warmer conditions is, for instance, sometimes put forward as one of the positive feedback processes that contribute to the transition from glacial to inter- glacial conditions (e.g. Berger 1982). Photosynthesis, however, can be fuelled only by free CO2, not HC03-, Fig. 4. Horizontal distribution of particulate CaCO, (nmol I-') and the former may be more limiting than previously in the upper ocean (0 to 500 m), as calculated by Bishop (1989) thought (Riebesell et al. 1993). At least in some circum- in combining a map of the average 0 to 200 m ocean temper- ature together with an empirical relationship between the stances, the release of COz from carbonate precipita- mean 0 to 500 m concentration of particulate CaCO, and the tion could thus be offset by increased carbon fixation mean 0 to 200 m temperature (Raven 1993). In addition, plankton organisms with Legendre & Le Fevre: Export of biogenic carbon 75

calcareous tests generally sink faster than other carbon in oceans. Concerning export, the possible organic particles produced In surface waters, thus competition between bacteria and metazoan con- reducing the amount of carbon respired during their sumers in temperate and tropical waters may impede downward transit, and the adsorption of organic mat- and sometimes prevent primary production from ter onto calcite particles may contribute to increasing reaching both the metazoan consumers and the deep the burial of organic carbon in ocean sediments. The waters. In addition, the various pathways through production and export of biogenic carbon by calcare- which small plankton cells are exported determine the ous organisms is therefore of biogeochemical s~gnifi- magnitude of carbon export, and this is largely con- cance, even though their net contribution to the overall trolled by hydrodynamics. Also, the production of CO2 budget may depend on the time scale considered. organisms with calcareous tests in the microbial food web increases the export of biogenic carbon from sur- face waters. Finally, the production of refractory DOM Refractory dissolved organic matter may delay the export to depth of a significant fraction of the primary production. As far as sequestration is A large fraction of the concerned, channelling by bacteria of biogenic carbon (DOC) in oceans is very refractory, with a turnover time into the microbial food web, in temperate and tropical of several thousand years (e.g. Hedges 1987). Accord- areas, could reduce the flux of carbon towards the ing to Williams & Druffel (1987), most of this refractory deep waters where sequestration takes place. Seques- DOC is of marine origin. It was explained above that tration is also influenced by the export pathways, since the export of biogenic particles occurs mainly locally, these determine the length of the downwards transit and on time scales of days to months after primary pro- and thus the magnitude of respiratory carbon losses. In duction has taken place (scales of ca 10 km, and of 10-? addition, the export of carbonate by the microbial food to 10-' yr). In contrast, the transport of refractory DOM web may result, at some geological time scales, in from surface to deep waters involve basin-scale circula- reduced sequestration of carbon by the ocean. Finally tion (104 km), which extends over decades and cen- refractory DOM in surface waters may chemically turies. This led Legendre & Gosselin (1989) to conclude sequester large amounts of carbon in the upper layer of that the downwards fluxes of particulate and dissolved the ocean, before it is transferred and broken down at organic matter may be separated in space by thousands depth. The same microbial food web processes may of kilometres and in time by decades or centuries, thus therefore have quite a different impact depending on effectively uncoupling the 2 processes. whether one considers the export of carbon or its Legendre & Le Fevre (1991) have pointed out that sequestration in oceans. the refractory DOC could chemically sequester carbon Volk & Hoffert (1985) identified 3 COz pumps in the in the surface layer, for periods of interest to global oceans, one being physical and the 2 others biological. change (i.e. 100s of years), before this carbon is trans- The solubilitypump (physical) is associated with ocean ferred and released (respired) into the deep waters. circulation. This pump is especially active in areas of According to Hedges (1988), refractory DOM may be deep water formation, where cooling of the surface formed from labile compounds, by either condensation water drives a flux of CO, from the atmosphere to the of small molecular weight labile DOM, or modification ocean, and subsequent sinking of the water ensures of large molecular weight labile material (e.g. pro- sequestration of the dissolved inorganic carbon. One of teins). Toggweiler (1989) hypothesized that the refrac- the biological pumps, described above, exports car- tory organic compounds may be formed, within the bonate (the carbonate pump), and its effects on the microbial food web, by condensation reactions be- sequestration of atmospheric CO2 may be rather com- tween carbon-rich phytoplankton exudates and nitro- plex. The other (the soft tissue pump, gen-rich bacterial enzymes. Even if the conditions and identified above as the biological CO2 pump in accor- rates of production and breakdown of the refractory dance with most authors) plays an important role in DOM, through microbial activity, are still poorly carbon export and sequestration. Microbial food web known, they may be of significance for global carbon processes influence to various degrees the 2 biological fluxes in the oceans (see Kirchman et al. 1993). pumps, so that quantitative assessment of their effects is required for incorporation into models of the global biogeochemical fluxes of carbon in oceans. This task Conclusion: global significance of microbial will retain a high priority on the agenda of marine food webs in oceans microbial ecologists in the coming years.

The microbial food web processes reviewed above Acknowledgements. The authors are indebted to Dr Hugh may influence both the export and the sequestration of Ducklow and 2 other, anonymous, referees, whose criticism 76 Aquat microb Ecol9: 69-77, 1995

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