Characteristics, dynamics and significance of marine snow

Rapid mass sinking of cells following diatom blooms, observed in lakes and the sea, is argued here to represent the transition from a growing to a resting stage in the life histories of these algae. Mass sinking is of survival value in those bloom diatoms that retain viability over long periods in cold, dark water but not in warm, nutrient-depleted surface water. Mechanisms for accelerating sinking speed of populations entering a resting or “seeding” mode are proposed. Previously unexplained features of diatom form and behaviour take on a new meaning in this context of diatom seeding strategies. Diatoms have physiological control over buoyancy as declining growth is accompanied by increasing sinking rates, where the frustule acts as ballast. Increased mucous secretion in conjunction with the cell protuberances characteristic of bloom diatoms leads to entanglement and aggregate formation during sinking; the “sticky” aggregates scavenge mineral and other particles during descent which further accelerates the sinking rate. Such diatom flocs will have sinking rates of ∼ 100 m d-1 or more. This is corroborated by recent observations of mass phytoplankton sedimentation to the deep sea. This mechanism would explain the origin of marine snow flocs containing diatoms in high productivity areas and also the well-known presence of a viable deep sea flora. That mortality is high in such a seeding strategy is not surprising. A number of species-specific variables pertaining to size, morphology, physiology, spore formation and frustule dissolution rate will determine the sinking behaviour and thus control positioning of resting stages in the water column or on the bottom. It is argued that sinking behaviour patterns will be environmentally selected and that some baffling aspects of diatom form and distribution can be explained in this light. Rapid diatom sedimentation is currently believed to be mediated by zooplankton faecal pellets, particularly those of copepods. This view is not supported by recently published observations. I speculate that copepod grazing actually retards rather than accelerates vertical flux, because faecal pellets tend to be recycled within the surface layer by the common herbivorous copepods. Egestion of undigested food by copepods during blooms acts as a storage mechanism, as ungrazed cells are likely to initiate mass precipitation and depletion of the surface layer in essential elements. Unique features of diatoms are discussed in the light of their possible evolution from resting spores of other algae. An evolutionary ecology of pelagic bloom diatoms is deduced from behavioural and morphological characteristics of meroplanktonic and tychopelagic forms. Other shell-bearing protistan plankters share common features with diatoms. Similar life-history patterns are likely to be present in species from all these groups. The geological significance of mass diatom sinking in rapidly affecting transfer of biogenic and mineral particles to the sea floor is pointed out.

Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance

Role of large particles in the transport of elements and organic compounds through the oceanic water column

There has been an explosion of research on marine microbial foodweb processes in the past decade. Today it is widely accepted that about 50% of the primary production in marine and fresh water is processed by bacteria each day (Williams, 1981; Cole et al., 1988). This striking finding was stimulated, as others have noted, by the introduction of convenient methods for the estimation of microbial biomass and activities in natural waters. Hobbie et al. (1977) and Watson et al. (1977) demonstrated conclusively that bacterial populations in the sea were large. By 1980, in addition to the pioneering and prescient work by Sorokin (e.g., Sorokin, 1971, 1973), reports of bacterial production measurements had begun to emerge (Sieburth et al., 1977; Karl, 1979; Larsson and Hagstrom, 1979; Fuhrman and Azam, 1980). Brock (1971) and Sieburth (1977) wrote early reviews on the subject, and Pomeroy (1974) introduced the importance of marine microbial processes to a large audience. In this chapter we review recent research on bacterial production in the ocean. The emphasis is on the open sea, but we will also discuss other marine habitats, partly because there are still few comprehensive studies of oceanic bacterial production. There is an equally large and rapidly growing literature on bacterial production in fresh waters (Cole et al., 1988; Currie, 1990) which deserves a review of its own, as well as comparison with the marine findings (Hobbie, 1988). We will not review related work in sediments, nor for the most part, related work on bacteriovores.

Oceanic Bacterial Production

Limnological surveys show that fossil pigment concentration is an accurate predictor of algal production. However, experimental and mass flux studies indicate that >90% of pigment is degraded to colourless compounds before permanent burial. To reconcile these views, this paper reviews current literature on pigment degradation and proposes a hierarchical control model for pigment deposition and fossil abundance. Over the widest range of production, pigment deposition and fossil concentration are proportional to algal standing crop. However, within a narrower range, the actual concentration of pigment in sediments is regulated by photo- and chemical oxidation. Three phases of loss exist: rapid oxidation in the water column (T1/2=days); slower post-depositional loss in surface sediments (T1/2=years); and very slow loss of double bonds in deep sediments (T1/2=centuries). Despite losses during deposition, fossil and algal abundance remain correlated through time, so long as there is no change in basin morphometry, light penetration, stratification or deepwater oxygen content. At the finest scale, food-web processes can increase the preservation of pigments from edible algae by incorporating pigments into feces that sink rapidly and bypass water column losses. As a consequence of selective loss during deposition and initial burial, carotenoid relative abundance is an unreliable measure of phytoplankton community composition. Instead, absolute concentration — scaled to the historical maximum — should be used for fossil interpretations.

A review of factors that regulate carotenoid and chlorophyll deposition and fossil pigment abundance

The fecal pellets of zooplankton are thought to be major carriers of organic matter from surface to deeper waters of the oceans. As the pellets descend, they release soluble components, partially due to breakdown by associated microorganisms. Previous laboratory work of other investigators has suggested that the surface of a fecal pellet rapidly acquires bacteria, which increase in abundance until they and their protozoan consumers disrupt the pellet membrane, spilling contents into the water. In contrast, our field collections of fecal pellets from free-floating particle interceptor traps (from the “Vertex” project off Central California in 1980 and off Mexico in 1981), suggest that microbial decomposition probably is initiated in the sea from inside the fecal pellets. Transmission and scanning electron microscopy indicate that bacterial populations are most abundant in the interior of fecal pellets obtained from the sea, but that the same pellets will acquire the surface bacterial lawn typically observed in laboratory studies if maintained aboard ship. If the fecal pellets are decomposed from the inside, then the principal agents are enteric bacteria or ingested, digestion-resistant bacteria, or both. Such bacteria may differ metabolically from those that colonize the fecal pellet surfaces. Further-more, the abundance of healthy-appearing bacteria inside the pellets suggests that their metabolic activities may produce microhabitats of reduced oxygen tension that could differ considerably from that of the pellet exteriors. Decomposition in these semi-enclosed microenvironments may proceed in a manner not yet predicted by models that attribute decomposition to well-aerated, surface-dwelling bacterial populations on fecal pellets in the sea.

Origins and microenvironments of bacteria mediating fecal pellet decomposition in the sea

Phaeodarian radiolarians were sampled from the upper 200 m along a transect through the ice-edge zone in the Weddell Sea in the austral autumn (March 1986) and at several stations in the western Antarctic Peninsula region in the austral winter (June 1987). Abundances of phaeodarians reached 3 132 m-3 and were similar to or higher than maximum abundances of polycystine radiolarians, foraminiferans, and acantharians, and similar to or less than those of the heliozoan Sticholonche sp. Phaeodarians varied in abundance and species composition both seasonally and/or geographically. In contrast to the more numerous ciliates and flagellates that were most abundant in the upper 100 m, phaeodarians were most abundant from 100 to 200 m and showed no distinct pattern related to the ice edge. Electron microscopical examination of food vacuoles showed that phaeodarians are omnivorous generalists, feeding on a variety of food ranging in size from bacteria to large protozoans in both regions and seasons. Algal cells consumed in addition to diatoms and dinoflagellates included Chlorella-like cells and members of the recently described chrysophyte order Parmales. Scales of prasinophytes were common. Phaeodarians are consumed by the non-selective particlefeeding salp Salpa thompsoni. Thus, phaeodarians link microbial food webs to macrozooplankton and increase the complexity of the Antarctic food web.

Abundance and feeding ecology of Antarctic phaeodarian radiolarians

Large (>64 µm) protozooplankton (radiolarians, thecate dinoflagellates, foraminiferans, and tintinnid ciliates) and copepod nauplii were sampled at six stations located in sea-ice-covered waters, using a multinet at five depth intervals between the surface and 1000 m depth during a late winter expedition of R.V. ‘Polarstern’ on a west-east transect across the Weddell Sea in 1989. Large (>400 µm) phaeodarian radiolarians contributed more than 98% of the carbon in the large protozooplankton fraction; large protozooplankton represented ca. 38% of the total protozooplankton carbon during late winter under the close pack ice in the upper 250 m. Large protozooplankton may therefore be an important food source for small particle-feeding zooplankton in the upper 250 m, and a modest food source down to 1000 m. Phaeodarian species distributions showed a distinct vertical pattern. Except for spumellarian and nassellarian radiolarians all other protozooplankton (foraminiferans, thecate dinoflagellates, tintinnids) were most abundant in the upper 250 m. The horizontal variation showed a western, central and eastern pattern most probably due to the differing regional hydrography. Feeding ecology of the dominant species of phaeodarians was examined using transmission electron microscopy of contents of feeding vacuoles. The 58 specimens were trophic generalists. The predominance of silica fragments and amorphous material in vacuoles and the similarity of vacuole contents of specimens from three depth zones suggest that phaeodarians in late winter may have fed on organic aggregates.

M. M. Gowing

Papers

Origins and microenvironments of bacteria mediating fecal pellet decomposition in the sea

Abundance and feeding ecology of Antarctic phaeodarian radiolarians

Late winter abundance and distribution of phaeodarian radiolarians, other large protozooplankton and copepod nauplii in the Weddell Sea, Antarctica