Seeing is Believing: Diatoms and the Ocean Carbon Cycle Revisited.

Terrestrial ecologists and biogeochemists are in direct contact with their objects of study via sense organs evolved in those environments; they hence share a common awareness because they can all see the whole elephant, as in the ancient Indian parable. Pelagic ecologists and biogeochemists on the other hand are the blind men groping different parts of the elephant - the protist-dominated biome of the planet - in attempts to understand its structure and functioning in terms of organism life cycles and the biogenic elements of which they are made. The pelagial is an alien world for us that we can only sense through instruments of our making: the propensity for bias is enormous. Throughout my career I have been acutely aware of this fundamental problem faced by protist ecologists. In this essay I would like to convey an impression of the subjective driving forces that led me to the conclusions I reached on the relationships between ocean ecology and biogeochemistry in the light of evolution by natural selection. Key personal encounters with sinking diatom blooms are recounted to illustrate how my convictions grew that led me to challenge mainstream thinking of the time.

Green and golden seaweed tides on the rise.

Sudden beaching of huge seaweed masses smother the coastline and form rotting piles on the shore. The number of reports of these events in previously unaffected areas has increased worldwide in recent years. These 'seaweed tides' can harm tourism-based economies, smother aquaculture operations or disrupt traditional artisanal fisheries. Coastal eutrophication is the obvious, ultimate explanation for the increase in seaweed biomass, but the proximate processes that are responsible for individual beaching events are complex and require dedicated study to develop effective mitigation strategies. Harvesting the macroalgae, a valuable raw material, before they beach could well be developed into an effective solution.

Thick-shelled, grazer-protected diatoms decouple ocean carbon and silicon cycles in the iron-limited Antarctic Circumpolar Current.

Diatoms of the iron-replete continental margins and North Atlantic are key exporters of organic carbon. In contrast, diatoms of the iron-limited Antarctic Circumpolar Current sequester silicon, but comparatively little carbon, in the underlying deep ocean and sediments. Because the Southern Ocean is the major hub of oceanic nutrient distribution, selective silicon sequestration there limits diatom blooms elsewhere and consequently the biotic carbon sequestration potential of the entire ocean. We investigated this paradox in an in situ iron fertilization experiment by comparing accumulation and sinking of diatom populations inside and outside the iron-fertilized patch over 5 wk. A bloom comprising various thin- and thick-shelled diatom species developed inside the patch despite the presence of large grazer populations. After the third week, most of the thinner-shelled diatom species underwent mass mortality, formed large, mucous aggregates, and sank out en masse (carbon sinkers). In contrast, thicker-shelled species, in particular Fragilariopsis kerguelensis, persisted in the surface layers, sank mainly empty shells continuously, and reduced silicate concentrations to similar levels both inside and outside the patch (silica sinkers). These patterns imply that thick-shelled, hence grazer-protected, diatom species evolved in response to heavy copepod grazing pressure in the presence of an abundant silicate supply. The ecology of these silica-sinking species decouples silicon and carbon cycles in the iron-limited Southern Ocean, whereas carbon-sinking species, when stimulated by iron fertilization, export more carbon per silicon. Our results suggest that large-scale iron fertilization of the silicate-rich Southern Ocean will not change silicon sequestration but will add carbon to the sinking silica flux.

Making sense of ocean biota: how evolution and biodiversity of land organisms differ from that of the plankton.

The oceans cover 70% of the planet's surface, and their planktonic inhabitants generate about half the global primary production, thereby playing a key role in modulating planetary climate via the carbon cycle. The ocean biota have been under scientific scrutiny for well over a century, and yet our understanding of the processes driving natural selection in the pelagic environment - the open water inhabited by drifting plankton and free-swimming nekton - is still quite vague. Because of the fundamental differences in the physical environment, pelagic ecosystems function differently from the familiar terrestrial ecosystems of which we are a part. Natural selection creates biodiversity but understanding how this quality control of random mutations operates in the oceans - which traits are selected for under what circumstances and by which environmental factors, whether bottom-up or top-down - is currently a major challenge. Rapid advances in genomics are providing information, particularly in the prokaryotic realm, pertaining not only to the biodiversity inventory but also functional groups. This essay is dedicated to the poorly understood tribes of planktonic protists (unicellular eukaryotes) that feed the ocean's animals and continue to run the elemental cycles of our planet. It is an attempt at developing a conceptually coherent framework to understand the course of evolution by natural selection in the plankton and contrast it with the better-known terrestrial realm. I argue that organism interactions, in particular co-evolution between predators and prey (the arms race), play a central role in driving evolution in the pelagic realm. Understanding the evolutionary forces shaping ocean biota is a prerequisite for harnessing plankton for human purposes and also for protecting the oceanic ecosystems currently under severe stress from anthropogenic pressures.

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.

Mineralization of the metre-long biosilica structures of glass sponges is templated on hydroxylated collagen.

The minerals involved in the formation of metazoan skeletons principally comprise glassy silica, calcium phosphate or carbonate. Because of their ancient heritage, glass sponges (Hexactinellida) may shed light on fundamental questions such as molecular evolution, the unique chemistry and formation of the first skeletal silica-based structures, and the origin of multicellular animals. We have studied anchoring spicules from the metre-long stalk of the glass rope sponge (Hyalonema sieboldi; Porifera, Class Hexactinellida), which are remarkable for their size, durability, flexibility and optical properties. Using slow-alkali etching of biosilica, we isolated the organic fraction, which was revealed to be dominated by a hydroxylated fibrillar collagen that contains an unusual [Gly-3Hyp-4Hyp] motif. We speculate that this motif is predisposed for silica precipitation, and provides a novel template for biosilicification in nature.

Iron defecation by sperm whales stimulates carbon export in the Southern Ocean.

The iron-limited Southern Ocean plays an important role in regulating atmospheric CO(2) levels. Marine mammal respiration has been proposed to decrease the efficiency of the Southern Ocean biological pump by returning photosynthetically fixed carbon to the atmosphere. Here, we show that by consuming prey at depth and defecating iron-rich liquid faeces into the photic zone, sperm whales (Physeter macrocephalus) instead stimulate new primary production and carbon export to the deep ocean. We estimate that Southern Ocean sperm whales defecate 50 tonnes of iron into the photic zone each year. Molar ratios of C(export):Fe(added) determined during natural ocean fertilization events are used to estimate the amount of carbon exported to the deep ocean in response to the iron defecated by sperm whales. We find that Southern Ocean sperm whales stimulate the export of 4 × 10(5) tonnes of carbon per year to the deep ocean and respire only 2 × 10(5) tonnes of carbon per year. By enhancing new primary production, the populations of 12 000 sperm whales in the Southern Ocean act as a carbon sink, removing 2 × 10(5) tonnes more carbon from the atmosphere than they add during respiration. The ability of the Southern Ocean to act as a carbon sink may have been diminished by large-scale removal of sperm whales during industrial whaling.

Recalibrating sleep: is recalibration and readjustment of sense organs and brain-body connections the core function of sleep?

Sleep is an enigma because we all know what it means and does to us, yet a scientific explanation for why animals including humans need to sleep is still lacking. However, the enigma can be resolved if the animal body is regarded as a purposeful machine whose moving parts are coordinated with spatial information provided by a disparate array of sense organs. The performance of all complex machines deteriorates with time due to inevitable instrument drift of the individual sensors combined with wear and tear of the moving parts which result in declining precision and coordination. Peak performance is restored by servicing the machine, which involves calibrating the sensors against baselines and standards, then with one another, and finally readjusting the connections between instruments and moving parts. It follows that the animal body and its sensors will also require regular calibration of sense organs and readjustment of brain-body connections which will need to be carried out while the animal is not in functional but in calibration mode. I suggest that this is the core function of sleep. This recalibration hypothesis of sleep can be tested subjectively. We all know from personal experience that sleep is needed to recover from tiredness that sets in towards the end of a long day. This tiredness, which is quite distinct from mental or muscular exhaustion caused by strenuous exertion, manifests itself in deteriorating general performance: the sense organs lose precision, movements become clumsy and the mind struggles to maintain focus. We can all agree that sleep sharpens the sense organs and restores agility to mind and body. I now propose that the sense of freshness and buoyancy after a good night's sleep is the feeling of recalibrated sensory and motor systems. The hypothesis can be tested rigorously by examining available data on sleep cycles and stages against this background. For instance, REM and deep sleep cycles can be interpreted as successive, separate calibration runs of the vestibulo-ocular reflex and the sensory-motor systems, respectively, amongst other functions running in parallel, such as dreaming. Because the split-second connections between sensory information and emotional responses will also require calibration, some aspects of dreaming could be interpreted in this light. Much of the baffling behaviour and patterns of brain activity of sleeping animals and humans make sense in the framework of this technological paradigm since different animal lineages will have evolved different techniques to achieve calibration.

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.

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.