Victor Smetacek

Architecture and material properties of diatom shells provide effective mechanical protection

Diatoms are the major contributors to phytoplankton blooms in lakes and in the sea and hence are central in aquatic ecosystems and the global carbon cycle. All free-living diatoms differ from other phytoplankton groups in having silicified cell walls in the form of two ‘shells’ (the frustule) of manifold shape and intricate architecture whose function and role, if any, in contributing to the evolutionary success of diatoms is under debate. We explored the defence potential of the frustules as armour against predators by measuring their strength. Real and virtual loading tests (using calibrated glass microneedles and finite element analysis) were performed on centric and pennate diatom cells. Here we show that the frustules are remarkably strong by virtue of their architecture and the material properties of the diatom silica. We conclude that diatom frustules have evolved as mechanical protection for the cells because exceptional force is required to break them. The evolutionary arms race between diatoms and their specialized predators will have had considerable influence in structuring pelagic food webs and biogeochemical cycles.

Carbon dioxide limitation of marine phytoplankton growth rates

THE supply of dissolved inorganic carbon (DIC) is not considered to limit oceanic primary productivity1, as its concentration in sea water exceeds that of other plant macronutrients such as nitrate and phosphate by two and three orders of magnitude, respectively. But the bulk of oceanic new production2 and a major fraction of vertical carbon flux is mediated by a few diatom genera whose ability to use DIG components other than CO2, which comprises < 1% of total DIC3, is unknown4. Here we show that under optimal light and nutrient conditions, diatom growth rate can in fact be limited by the supply of CO2. The doubling in surface water pCO2 levels since the last glaciation from 180 to 355 p.p.m.5,6 could therefore have stimulated marine productivity, thereby increasing oceanic carbon sequestration by the biological pump.

Polar ocean ecosystems in a changing world

Polar organisms have adapted their seasonal cycles to the dynamic interface between ice and water. This interface ranges from the micrometre-sized brine channels within sea ice to the planetary-scale advance and retreat of sea ice. Polar marine ecosystems are particularly sensitive to climate change because small temperature differences can have large effects on the extent and thickness of sea ice. Little is known about the interactions between large, long-lived organisms and their planktonic food supply. Disentangling the effects of human exploitation of upper trophic levels from basin-wide, decade-scale climate cycles to identify long-term, global trends is a daunting challenge facing polar bio-oceanography.

Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom

The growth cycle in nutrient-rich, aquatic environments starts with a diatom bloom that ends in mass sinking of ungrazed cells and phytodetritus. The low grazing pressure on these blooms has been attributed to the inability of overwintering copepod populations to track them temporally. We tested an alternative explanation: that dominant diatom species impair the reproductive success of their grazers. We compared larval development of a common overwintering copepod fed on a ubiquitous, early-blooming diatom species with its development when fed on a typical post-bloom dinoflagellate. Development was arrested in all larvae in which both mothers and their larvae were fed the diatom diet. Mortality remained high even if larvae were switched to the dinoflagellate diet. Aldehydes, cleaved from a fatty acid precursor by enzymes activated within seconds after crushing of the cell, elicit the teratogenic effect. This insidious mechanism, which does not deter the herbivore from feeding but impairs its recruitment, will restrain the cohort size of the next generation of early-rising overwinterers. Such a transgenerational plant–herbivore interaction could explain the recurringly inefficient use of a predictable, potentially valuable food resource—the spring diatom bloom—by marine zooplankton.

Primary production and sedimentation during spring in the Antarctic Peninsula region

Phytoplankton biomass and composition, primary productivity (in situ simulated and in vitro incubations) and sedimentation rates (measured with free-drifting sediment traps suspended at 100 m depth) were recorded in the Bransfield Strait area of the Antarctic Peninsula during November to December 1980. Three distinct and persistent zones were encountered: low biomass comprising flagellates and diatoms in the Drake Passage and Scotia Sea (zone I): high to moderate biomass of Phaeocystis and diatoms in the northern and central Bransfield Strait (zone II); and moderate biomass (Thalassiosira spp. in the process of forming resting spores) in the vertically homogeneous water on the northern Antarctic Peninsula shelf (zone III). Nutrient concentrations were high throughout; zooplankton grazing relative to phytoplankton biomass and production was heavy in zone I but negligible in the other 2 zones. Rates of primary production in zones I, II, and III averaged 230, 1660 and 830 mg C m−2 d−1, respectively. Assimilation numbers were low throughout (< 1 mg Chl a)−1 h−1) and growth physiology of the zonal phytoplankton assemblages was basically similar. Sedimentation rates recorded by 2 traps in zone II were low (97 and 138 mg C m−2 d−1) and higher (546 mg C m−2 d−1) in a third trap which collected mostly euphausiid faeces. Sedimentation was heaviest in zone III (450 to 1400 mg C m−2 d−1) where collections of the 3 traps deployed were dominated by intact diatom frustules (Thalassiosira spp.). Spore formation and heavy sedimentation of diatoms thus also occurs at the end of Antarctic blooms in spite of high ambient nutrients. As approximately two-thirds of the diatoms in traps were resting spores, we suggest that sinking of cells represents a seeding strategy which ensures regional persistence of neritic assemblages. Species-specific differences in seeding strategies may well be important in determining spatial and temporal patterns of Antarctic phytoplankton abundance. This aspect of phytoplankton biology is likely to have far-reaching implications, not previously considered, for the structure of Antarctic food webs.

The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles

This review examines the links between pelagic ecology and ocean biogeochemistry with an emphasis on the role of the Southern Ocean in global cycling of carbon and silica. The structure and functioning of pelagic ecosystems is determined by the relationship between growth and mortality of its species populations. Whereas the key role of iron supply in conditioning the growth environment of land-remote oceans is now emerging, the factors shaping the mortality environment are still poorly understood. This paper addresses the role of grazing as a selective force operating on the structure and functioning of pelagic ecosystems within the larger conceptual framework of evolutionary ecology. That mortality due to grazing decreases with increasing cell size is widely taken for granted. We examine the impact of this principle across the range of size classes occupied by Southern Ocean plankton and show that relatively few species play crucial roles in the trophic structure and biogeochemical cycles of the Southern Ocean. Under iron-sufficient conditions, high growth rates of weakly silicified diatoms and Phaeocystis result in build-up of blooms that fuel “the food chain of the giants” (diatoms-krill-whales) and drive the carbon pump. In contrast, high grazing pressure of small copepods and salps on the regenerating microbial communities characteristic of the iron-limited Southern Ocean results in accumulation of large, heavily silicified diatoms that drive the silicon pump. The hypotheses we derive from field observations can be tested with in situ iron fertilization experiments.

Spring development of phytoplankton biomass and composition in major water masses of the Atlantic sector of the Southern Ocean

Abstract The distribution and composition of phytoplankton stocks in relation to water masses were studied during the SO-JGOFS cruise of R.V. Polarstern in the Atlantic sector of the Southern Ocean in October/November 1992. The cruise comprised one west-to-east transect along the ice edge from 49°W to 6°W and several meridional transects along 6°W that extended from the closed pack ice of the Weddell Sea, across the southern Antarctic Circumpolar Current (ACC) and into the Polar Frontal Zone. Chlorophyll (chi a concentrations, temperature and salinity were recorded continuously in surface water during the transects. Vertical distribution and species composition of microplankton were assessed microscopically in discrete water samples collected at stations. Contrary to expectations, no significant enhancement of phytoplankton biomass was found in the vicinity of the retreating ice cover. Melt-water-influenced zones were indicated by low salinity but also by abundance of characteristic sea-ice species such as Nitzschia closterium and N. prolongatoides, but chlorophyll concentrations averaged only 0.3 mg chi a m−3 and barely increased during the spring. Values were even lower and remained constant in the southern ACC (ca 0.2 mg chi a m−3). In contrast, large phytoplankton blooms developed during the 6 weeks of investigation in the region of the Polar Front (PFr), from 0.7 to > 4 mg chi a m−3. Three distinct blooms extended below 70 m depth, each dominated by a different diatom species (Fragilariopsis kerguelensis, Corethron inerme and C. criophilum). We speculate that the large phytoplankton stocks below 40 m depth are a result of subduction of surface layers as sinking and in situ growth can be ruled out. The factors leading to the accumulation of high phytoplankton stocks in the PFr (up to 270 mg chi m−2), but not in the meltwater zones or in the front between ACC and Weddell Gyre, are not clear, but higher iron concentrations in the former region seem to have played a role.

Deep carbon export from a Southern Ocean iron-fertilized diatom bloom

Fertilization of the ocean by adding iron compounds has induced diatom-dominated phytoplankton blooms accompanied by considerable carbon dioxide drawdown in the ocean surface layer. However, because the fate of bloom biomass could not be adequately resolved in these experiments, the timescales of carbon sequestration from the atmosphere are uncertain. Here we report the results of a five-week experiment carried out in the closed core of a vertically coherent, mesoscale eddy of the Antarctic Circumpolar Current, during which we tracked sinking particles from the surface to the deep-sea floor. A large diatom bloom peaked in the fourth week after fertilization. This was followed by mass mortality of several diatom species that formed rapidly sinking, mucilaginous aggregates of entangled cells and chains. Taken together, multiple lines of evidence—although each with important uncertainties—lead us to conclude that at least half the bloom biomass sank far below a depth of 1,000 metres and that a substantial portion is likely to have reached the sea floor. Thus, iron-fertilized diatom blooms may sequester carbon for timescales of centuries in ocean bottom water and for longer in the sediments.

Seasonal and Regional Variation in the Pelagial and its Relationship to the Life History Cycle of Krill

The earlier concept of Antarctic pelagic seasonality has changed drastically. We now know that the characteristic pelagic community resembles the oligotrophic communities of warm, nutrient-depleted waters. Results of recent sediment trap moorings show that the Antarctic oceanic pelagial behaves as a highly efficient retention system as losses due to sinking particles are exceptionally low. We show that the distinction into “new” and “regenerating” type pelagic systems only applies to restricted regions experiencing sizeable blooms where spring sedimentation pulses have been recorded. Apparently, community biomass is built up by channelling of nitrate into the recycling pool whereby balance between auto- and heterotrophs must be maintained, presumably within time scales of weeks. Interannual variability is likely to be much less pronounced in this type of buffered pelagic system.

A watery arms race.

Imagine yourself in a light forest looking upwards, seeing in your mind’s eye only the chlorophyll-bearing cells of the canopy floating in mid-air, free from the attachment of leaves, twigs, branches and trunks. Now forget the forest and the trees, and see only blurred clouds of tiny green cells obscuring the blue sky beyond. You are looking at a phytoplankton bloom of a density typical of lakes and coastal oceans. Forests and algal blooms fix about the same amount of carbon — a few grams per square metre per day — because both are based on essentially the same photosynthetic machinery, fuelled by chlorophyll a in chloroplasts, the descendants of free-living cyanobacteria that have since evolved into plant organelles by endosymbiosis. Chloroplasts provide their host cells with food in return for resources and protection. The land was colonized by one type of chloroplast/host cell, and the evolution of its various life-supporting systems is, from a human perspective, a straightforward success story: from algal slime to tropical rainforest. Indeed, the sole function of land plants, as considered in the thought experiment above, is to provide the chloroplasts with water and nutrients and give them access to light. Competition for resources and resource space has shaped the evolution of form and function in terrestrial vegetation. Can one apply the same evolutionary criteria to the other main plant life-form on our planet — the free-floating plankton of the pelagic realm? The phytoplankton bloom is suspended in a soup of resources, circulated by the wind within the sunlit surface layer. Its chloroplasts are provisioned by this viscous medium and do not require life-supporting hosts. Moreover, a striking feature of pelagic systems is the recurrent pattern of annual species succession. This is different from succession in land plants because the various stages, dominated by characteristic phytoplankton species, last for only a few weeks. There may be competition between species at the same stage for light and nutrients, but hardly at all between species of different stages. Apparently, space-holding plankton has not evolved. So what other forces shape plankton cells, and are they the same as those that drive succession? Photosynthesis in plankton is spread across about ten different divisions, as separate from one another as land plants are from animals. Many of the lineages have species that function as algae (‘plants’) or as ingestors of particles (‘animals’); many species do both. Generally, species with chloroplasts look no different to their relatives without them — cell shape does not reflect the mode of nutrition. Properties of the host cell, including shape, must do more than improve the photosynthetic efficiency of chloroplasts. Indeed, the enormous diversity of lineages and shapes present in unicellular plankton has defied explanation. Although adoption by a host must have imposed many changes on the chloroplast, one main function of host cells is to protect chloroplasts against attack. The many mechanical and chemical defence systems evolved by land plants have elicited an equally heterogeneous arsenal of attack systems among their enemies, ranging from viruses to fungi, insects to elephants. Defence systems need to be deployed at the level of the leaf and are therefore not reflected in gross morphology, but they can be expensive. Hence there are fast-growing and slow-growing plants, all fuelled by chloroplasts, but differing in the degree of investment in defence. The range of defence systems in plankton is only now coming to light. The size range of phytoplankton spans three orders of magnitude, but that of its predators spans five orders, from micron-scale flagellates to shrimp-sized krill. Pathogens (viruses and bacteria) pose a further challenge. Most predators and pathogens feed or infect selectively. Smaller predators hunt individual cells, whereas larger ones use feeding currents, mucous nets or elaborate filters to collect them en masse. Captured cells are pierced, ingested, engulfed or crushed, but have evolved specific defence measures. They can escape by swimming or by mechanical protection; mineral or tough organic cell walls ward off piercers or crushers. In adapting to deterring predators, cells have increased in size, formed large chains and colonies, or grown spines. Noxious chemicals also provide defence. Obviously, none of these defence mechanisms conferred by host cells provides universal protection to chloroplasts. Most phytoplankton cells are eventually eaten or succumb to pathogens. Rapid fluctuation in population size favours survival fitness, more cycles and hence more adaptation to attack. If the carbon fixed by planktonic chloroplasts is invested mainly in this biological ‘arms race’, then planktonic evolution is ruled by protection and not by competition. The many different shapes and life cycles reflect responses to specific attack systems. Suppose that competition for light rather than protection were the driving force in shaping pelagic ecosystems. Faced with a single, optimal solution, algae could well have evolved more efficient photosynthetic machinery. Improved energy use would favour production of hydrocarbons as both a buoyancy aid and a reserve substance. The ocean surface would then be covered with oily scum that would, as well as changing the planetary heat budget, severely reduce evaporation and hence rainfall on the continents, where life as we know it could not then have evolved. Luckily for us, this did not happen, and we have our blue, white and brown planet with its smudges of green, instead of dark green (or even black) oceans and bare, brown continents. ■ Victor Smetacek is at the Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany.