¿ìè¶ÌÊÓƵ

The relentless progress of the icebreaker through the polar pack ice, accompanied by a cacophony of cracking ice, makes it easy to forget that you are at sea. Frozen expanses stretch to the horizon, with avenues of ice boulders several metres high overlooking snow-covered terraces. But these are not monochrome wastelands devoid of life. Underneath the frozen surface is a coffee-coloured interior, coloured by the hardy microorganisms that survive in a maze of tiny channels within the sea ice.

Most of the ice-dwellers are single-celled algae but bacteria, fungi, protozoans and larger animals such as amphipods, copepods and marine flatworms also live there. These communities, first documented by whalers in the 18th century, were once regarded as a biological curiosity. ¿ìè¶ÌÊÓƵs still do not fully understand how they survive. They do know, however, that sea-ice biology plays an important part in Antarctic and Arctic ecology, and may have a role in the destruction of the ozone layer in spring. ‘Sea ice is no longer thought of as something that gets in the way of ships, but as a habitat for a vast range of organisms and an important influence on the world’s climate,’ says Cornelius Sullivan, Director of the Office of Polar Programs at the National Science Foundation in Virginia.

BREAKING THE ICE

Since the early 1980s, research in polar regions has been revolutionised by the use of icebreakers as research ships capable of operating deep in the ice fields during winter. The first icebreaker devoted solely to polar research was the German ship Polarstern, launched in 1983. Before then, limited sea ice research was done from land-based stations and from ships able to penetrate only the outer margins of the pack ice. Over the past four years the US, Britain and Australia have launched their own icebreakers complete with state-of-the-art laboratories.

Superficially, sea ice looks like a homogeneous frozen mass, but it contains a variety of habitats. At the upper surface, where temperatures drop to -20 °C, almost all the water freezes and the ice is packed solid. But further down the ice sheet are pockets and channels filled with concentrated brine, and these range in size from a few hundred micrometres to several centimetres across. Their structure and size depend on the temperature of the ice. At the bottom of the floe, where the sea permeates, the ice is even more pitted. The compact surface layer buffers the interior and bottom of the floe from extremes of temperature, but during polar winters this maze of channels is an extremely gloomy home for algae that rely on light for their existence.

The ice is colonised as it forms in the autumn. Freezing winds sweep off the polar continent causing millimetre-sized ice crystals to form in the open sea. The crystals mix with plankton on and near the surface, and although some organisms are able to swim away, most are caught up in the ice as it rises through the top few metres of water. The plankton-laden crystals accumulate on the surface in slicks which freeze to form ice pancakes – circular discs of ice several centimetres thick. The pancakes become more rigid as water trapped between the ice crystals freezes into an intricate lattice. Within a couple of weeks, waves lift the pancakes on top of each other to create a surface strong enough to support humans.

During the first few days, the variety of life in the pancakes is similar to that in the sea. But ice is a hostile environment and all but the hardiest creatures quickly die. As the seawater freezes, the ice crystals grow, crushing larger animals and plants when tunnels in the lattice become smaller. The ice itself is pure water and sea salt concentrates in the remaining liquid which collects in the system of channels. Within two to three weeks, these salty passages become home to those species able to cope with the transition from the open ocean to an environment which is very salty with temperatures well below zero. Researchers have identified well over a hundred species of algae living in polar sea ice.

WORKING ON THIN ICE

Studying how these communities survive is a challenge in its own right for all of us who work on these ice breakers. When the ice is forming and not yet strong enough to support a human, collecting ice cores can be a precarious task, with researchers suspended just above the surface in a chair lowered from their ship. Later on, they explore the ice on snow mobiles or are airlifted by helicopter to sites up to 30 kilometres from the ship. It is a dangerous environment. The thickness of the ice is unpredictable, and varies greatly. Once, on an expedition in the Weddell Sea in the Antarctic, one of our snow mobiles plunged through thin ice into the sea. The driver and passengers managed to scramble clear, but we lost over $10 000 worth of equipment.

Most of this field work is geared towards collecting ice cores. By examining the ice structure and organisms within them, and by simulating this harsh environment in our own laboratories, we are just starting to piece together some of the survival mechanisms that ice-dwellers use. The major problems they face are threefold and vary according to which ice layer an organism inhabits. In winter, the surface freezes almost solid, leaving salt to accumulate in the tiny amounts of water still present. Concentrations can exceed 250 grams per litre – seawater contains an average of 35 grams per litre – making this layer virtually uninhabitable. In the middle layer, the major barriers to survival are low temperatures, high salinity and poor light. For organisms living at the bottom of the ice floe, adapting to very poor light is the crucial challenge.

Our experiments have shown that several common ice algae grow, albeit slowly, at -5.5 °C. Some can endure -8 °C. How can this be when most algae from warmer waters cannot survive temperatures below freezing? A few species, including some dinoflagellates, cope by forming into cysts – robust, thick-walled dormant cells able to withstand the attack of ice. When the ice melts, the cysts germinate, producing normal cells. Other species, including diatoms, the most common species found in sea ice, ‘hibernate’ to survive the onset of winter. At very low temperatures, their metabolic rates seem to slow. By growing the organisms in seawater spiked with radioactive carbon, we measured the amount of carbon they take in during photosynthesis and release in respiration. In a simulation of the sea-ice environment with respiration rates where so low we could hardly measure them.

In recent years, evidence has been growing that several species found in sea ice make natural antifreezes. Proteins released by pennate diatoms into the surrounding water may keep their immediate environment liquid. Many species have been shown to contain large concentrations of organic solutes which could act as internal anti-freezes, preventing the extreme cold from damaging their membranes and organelles.

But these antifreezes are better known for their ability to help algae withstand extreme salinity. In the middle of the floe, organisms face an environment which is between two and four times more salty than the open sea. The problem here is dehydration. By the process of osmosis, water tends to move out of the cell until the concentration of inorganic ions in cellular fluid is balanced with that in the surrounding water. To prevent this potentially lethal water loss, the algae take up inorganic ions such as potassium. In addition, the organic substances they produce – the amino acid proline and dimethylsulphoniopropionate (DMSP), for example – help restore osmotic balance. For the moment, no one understands the whole story. When they do, it could help in developing crops that are frost-resistant and able to withstand high levels of salt.

Lack of nutrients is the second problem faced by organisms living in the middle layer of ice. In the first weeks after the sea ice forms, there is a burst of growth. This tails off, however, as essential nutrients become scarce. Nitrates, phosphates and silicates are in particularly short supply, and further growth through photosynthesis is slow because light decreases with the depth of the floe. At the bottom, organisms have a constant input of nutrients from the sea, but shortage of light is severe. The question of how ice-dwelling algae cope with poor light is another that has intrigued scientists working at the poles.

Sullivan and his former team at the Hancock Institute of the University of Southern California have dominated research in this area, showing that sea-ice algae vary the amount and type of light-harvesting pigments they contain in response to poor light. They tend to produce more of their primary pigment, chlorophyll a, in low light and less in strong light conditions. Furthermore, diatoms have a variety of photo-synthetic pigments which enable them to produce energy from light of a wide band of wavelengths. In poor light, this variety is maintained, but the balance is shifted in favour of the pigments best able to use the changing spectrum of light as it passes through the ice. In highly shaded sea-ice habitats, for example, levels of the pigment fucoxanthin are raised.

LIGHTING UP

In research published this year, Sullivan, together with James Raymond from the University of South Alabama and Arthur DeVries from the University of Illinois, have suggested that the protein-based antifreezes unique to ice diatoms may also help to increase the amount of light available to algae living deep within sea ice. They argue that when these substances are released into the environment, they roughen the surfaces of ice crystals, increasing scattering of light and allowing it to penetrate further into the floe.

Several groups have attempted to measure the amount of plant material produced in sea ice by photosynthesis. Known as primary production, this gives an indication of algae’s overall importance as a food source in the polar ecosystem. But most of the information is restricted to a few well-studied sites. Seasonal variations in levels of photosynthesis and the highly patchy distribution of communities makes generalising about the polar regions extremely unreliable. The best guesses, however, suggest that the annual amount of primary production in sea ice is at least 5 per cent of the total in these areas.

As yet our knowledge of food webs in sea ice is very sketchy. We are only starting to build up a picture of the predator and prey relationships that combine to form the various food chains in this environment. We do not, for example, know how much movement there is between different levels within floes or how important this is for predation. In some sea-ice communities, algae appear to dominate. Other studies, however, have revealed large numbers of the organisms that eat algae, indicating an active food web. Bacteria which feed on dissolved organic material are also abundant in some sea-ice cores. During the winter, bacterial production rates reach up to 15 per cent of primary production by algae. With zooplankton grazing on bacteria, this represents an important part of the food web.

The bottom of the floe is where ice-dwellers interact with the wider polar ecosystem. Not only are nutrients available to the organisms in this layer, but they end up as a source of food for free-swimming creatures. Krill are the most important predators – though they are not found in the Arctic. As the plankton they normally feed on become scarce at the start of winter, krill collect in cracks and crevices on the bottom of the ice. Analysis of their stomach contents shows that ice organisms provide almost all of krill’s diet during the winter.

The rate at which krill feed is phenomenal. According to research done by Peter Marschall at the Alfred Wegener Institute for Polar Marine Research in Bremerhaven, an individual animal in the laboratory will devour the algae growing on a 20-centimetre square glass plate in about five minutes. Such voracious grazing results in a huge stock of krill, perhaps as much as 1.35 billions tons – the total world human biomass is only about 0.28 billion tons. Krill are eaten by predators such as penguins, seals and the whales of the southern oceans, completing a complex food chain that starts with sea-ice algae and reaches all the way to the largest mammals.

The dominance of krill in the southern oceans is just one of several differences between sea-ice habitats at the two poles. Most Antarctic sea ice exists for only a year, growing less than 2 metres thick. In the spring, when the temperature of the sea rises, the margins of the ice sheet melt and fragment, and the majority of the ice disappears. But the Arctic is surrounded by the landmasses of Russia, Canada and Greenland, which restrict the flow of sea ice into more southerly, warmer waters. Arctic ice floes can survive many years, joining up again in winter and growing several metres thick.

The girdle of ice around Antarctica, which in winter extends 20 million square kilometres – about the size of Europe – shrinks back to just 4 million square kilometres in summer. At the Arctic, sea ice covers 14 million square kilometres in winter, and around half remains through the summer. When surface ice melts in the Arctic summer, ponds of almost pure water form. These becomes brackish when mixed with sea spray and support an unusual mix of marine, estuarine and fresh-water plankton, carried over the ice by sea birds or from rivers.

Most of the organisms found in Antarctic sea ice undergo an annual cycle as the ice melts and refreezes. In the Arctic, habitats can remain frozen for years. Researchers are still not sure why Antarctic sea ice has such huge communities living in its middle layer compared with ice in the Arctic, or why algae seem to flourish more readily at the bottom of the Arctic ice floes.

At both poles, spring brings ideal conditions for algal growth. The days grow longer, and with the sun higher in the sky, rising temperatures melt the ice. Heavy spring snowfalls submerge the floe and nutrient-rich waters pour into it. During this time, dense algal growth, with concentrations as high as 300 micrograms of chlorophyll per litre have been recorded – normal summertime concentrations in the Southern Ocean reach no more than about 1 microgram per litre. With concentrations so high, the ice can turn dark brown, almost black, resulting in further melting as the dark surface absorbs heat. Melting floes often have a honeycomb structure with large holes where the parts of the ice that were filled with organisms have melted first.

In the Antarctic, more than 80 per cent of sea ice melts in the spring. As organisms are released back into the sea, there is an explosion of feeding activity. According to Peter Wadhams at the Scott Polar Research Institute in Cambridge: ‘At this time of year huge algal blooms fill the sea at the edge of receding ice floes and it is likely that sea ice organisms seed these blooms.’ The strongest evidence for this comes from comparisons of the variety of diatom communities in ice and in water and from the discovery of blooms composed of species normally associated with sea ice.

As they return to the sea, pennate diatoms release bromoform gas. Bromoform breaks down into a highly reactive form of bromine that destroys the ozone layer. William Sturges, from the University of Colorado estimates that the amount of bromine released by algae could be as high as those of industrial emissions – around 0.16 million kilograms a year. Ice-dwelling organisms also add to the atmospheric sulphur associated with acid rain. When they make the transition back from a highly saline environment to one where salt concentrations are normal, they pump ions and organic compounds out of their cells. These substances include DMSP which is converted into dimethylsulphide (DMS) in the sea and decomposes in the atmosphere to give sulphate particles. Acid rain is one consequence, but DMS emissions also have a positive effect. Clouds forming around the sulphate particles reflect sunlight, reducing the impact of global warming (see ‘Can algae cool the planet?’, ¿ìè¶ÌÊÓƵ, 21 August 1993).

There is still much to be learnt about sea ice and its inhabitants. Sullivan has high hopes for some new sensor technology and a planned launch by NASA. Sensors able to detect the abundance of living organisms throughout an ice core will soon be available. These are designed to be frozen into the ice, and will provide estimates of how growth rates vary from season to season by measuring changes in light absorption. NASA’s polar-orbiting satellite known as SeaWiFS (Sea-viewing wide field-of-view sensor), which is due to be launched later this year, will provide invaluable information. We eagerly await infrared images showing how plant life changes in the surface waters around polar ice fields during the annual cycle.

David Thomas and Gerhard Dieckmann are marine biologists based in Germany. Thomas is at the University of Oldenburg and Dieckmann at the Alfred Wegener Institute for Polar Marine Research, Bremerhaven.