Bill Wood/NHPA
The photographs are scanned from the original article in New Scientist 28thApril 1990
Defenders of the reef
Jewel-like corals and brightly coloured fish attract biologists to the study of reefs. But a sorely neglected group of organisms, the coralline algae, may be more crucial to the survival of the reef than any of their more spectacular neighbours
Brian Maudsley
ANIMAL, vegetable or mineral? Confusion has always surrounded coralline algae, the hard, lime-encrusted red seaweeds. In the days when naturalists believed that corals, sponges and bryozoans were plants, these curious, crusty algae were lumped in the same category. And when biologists discovered that corals and sponges were not plants after all, they moved coralline algae into the animal kingdom with them.
Despite their somewhat dubious status as a taxonomic afterthought, the coralline algae deserve far more attention than they get. They are the mainstay of many of the world's coral reefs: if the coralline algae are damaged, the physical structure of the reef may crumble. Left to themselves, coral reefs usually adapt to natural variations in their environment. Even the damage wrought by a hurricane can be repaired. But, as is so often the case, human interference can upset the equilibrium, setting off a domino effect with each organism affecting dozens of others. The damage is often irreversible. Only when ecologists understand the biology of the algae and their relationships with other organisms, will they be in a position to predict what will happen when reefs are damaged or polluted.
Unlike most algae, which are either finely filamentous or leathery and strap-like, coralline algae are solid and hard. Their crustiness is caused by crystals of magnesium calcite, a form of calcium carbonate, embedded in the walls of the algal cells (see Box 1). Most coralline algae form cement-like crusts over rocks and reefs in permanent rock pools and below the lowest level of the spring tide. Some go a step further, growing into rhodoliths, pink or purple "living" rocks that roll gently about on the seabed. Some rhodoliths reach 30 centimetres in diameter and may be eight centuries old. Unlike corals, coralline algae are not confined to the tropics but can form massive ridges far into polar waters.
Coralline algae are a considerable challenge to taxonomists. Not only do they lack distinctive surface features, they also change shape and colour. For example, Lithophyllum kotschyanumhas fine branches in sheltered places but where the sea is rough the tips of the branches become rounded and massive. Another species, Porolithon onkodes, is pale grey where there is plenty of sunlight, but purple in the shade. Often the only way to identify a species is to look at its structure under a microscope, but the rock-like surface makes sectioning difficult without removing the calcium crystals first by soaking them in acid. Researchers have to learn specialised techniques just to put a name to their specimens, and so the coralline algae have been a much-neglected group. Ecologists also virtually ignored coralline algae until recently. Many modern studies of the ecology of reefs simply refer to the corallines as "lithothamnia", a general catch-all. Knowledge of the ecology of corallines is sketchier than their taxonomy, yet they play a key role in the growth and development of tropical reefs. Without a rich and varied flora of coralline algae, modern reefs would be at best fragmented, and at worst confined to sheltered bays.
Coralline algae are often the dominant organism on the surface of "coral" reefs. In the Gulf of Aqaba, a thin arm of the Red Sea, the grey, rounded protuberances of Porolithon onkodescover more than a third of the reef crest. This alga also grows at high densities in many other places, including the Pacific islands.
Because coralline algae survive best in places subjected to great environmental stress, they protect coral reefs against the full brunt of storms and currents. Porolithon onkodesand other ridge-forming algae, such as Lithophyllum kotschyanum, grow particularly well where wales beat most powerfully, and currents are strong; they flourish where seaweed-eating herbivores are most abundant. Indeed, grazing is essential to their survival. P. onkodesgrows in full tropical sunlight under a few centimetres of water; other species grow in what seems impossibly dim light where most algae would be unable to photosynthesise. Walter Adey, of the National Museum of Natural History in Washington, maintains that coralline algae from the Arctic need only a little light for three-quarters of each day for a month and they can survive the rest of the year in the dark. Adey's colleague, Mark Littler, has found a species growing at a depth of almost 300 metres, where the light is imperceptible to human eyes; he estimates that the light at this depth is 0.0005 per cent of that at the surface.
A hard crust is a considerable advantage for an alga. Not only does it protect the plant from the wear and tear of waves and currents, it also makes it unpalatable to animals that might otherwise feed on it. As well as being hard to eat, coralline algae are not very nutritious, so there is little point in trying to eat them. The rise in ecological importance of coralline algae in the past corresponded with the increase in herbivores during the Cretaceous period, from about 135 million years ago (see Box 2).
Bill Wood/Planet Earth Pictures
Red rocks: encrusting red algae (left) help to build reefs. More decorative forms provide shelter
Calcification places severe constraints on coralline algae as well as on would-be grazers. The process of laying down crystals requires energy that might otherwise be used to produce organic materials. As a result, growth is very slow. Some encrusting species grow only about 5 millimetres thicker each year. Species that live in cold water grow even more slowly. The danger for algae that grow so slowly on tropical reefs is that other organisms might grow over them. Once the algae are shaded, photosynthesis becomes impossible and they soon die.
Coralline algae have overcome these difficulties in several ways. They often live in environments where other algae cannot compete. Strong waves, dim light and an abundance of herbivores partial to algae all prevent the growth of most large seaweeds, such as wracks and kelps. Microalgae, which form an almost invisible algal turf, coat all unoccupied spaces on the reef. In contrast to the coralline algae, microalgae grow so fast that they are replenished as quickly as they are grazed; the annual production of this thin layer is enormous, beating any terrestrial field of grass. Algal turf is an important competitor of coralline algae in shallow water, because it has the potential to overgrow and smother them within a very short time. Yet
this happens only when the corallines are damaged or weakened, for example by sediment, undergrazing or destructive overgrazing by parrot fish, which can take great chunks out of the hardest coral rock with their horny teeth.
Bill Wood/NHPA
Parrot fish and other grazers encourage the growth of coralline algae
One reason that other algae rarely grow on top of corallines is because they shed their outer layer, sloughing off any would-be colonist. The surface layer of the plant, the epithallium, is continuously renewed from below by the actively dividing cells of the meristem. As the epithallium is pushed upwards, the cells degenerate and are cut off from below. They loosen and easily fall off. When algal spores or small animals settle on the surface of coralline algae, the unstable surface layer peels away, together with the settlers. Grazing is a far more important process in clearing colonists from the surface of coralline algae. Tropical reefs abound with grazers, such as limpets, parrot fish and surgeon fish, but the most important are the sea urchins. The common jewelled "hat-pin" urchins, Diadema setosumand D. savigniiin the Pacific and D. antillarumin the Atlantic, and the large, short-spined Tripneustes gratillarasp over every inch of the reef, day and night, with their hard, powerful teeth. Urchins graze mostly on the nutritious algal turf and small creatures associated with it. When they eat coralline algae, their teeth do not penetrate far, removing just the disposable epithallium and any organisms attached to it. Vital growth and reproductive cells are well protected beneath the surface. Corallines are only occasionally damaged by overgrazing when there are massive population explosions of urchins.
In some cases, the feeding relationship is very close and there is one case of a grazer having a symbiotic relationship with a coralline alga. Adey noticed that in the Gulf of Maine the limpet Acrnaea testudinaliswas always associated with a particular coralline alga, Clathromorphum circumscriptum. Later, Robert Steneck, also of the National Museum of Natural History in Washington, showed that the association is a truly symbiotic one in which both partners are adapted to one another to their mutual advantage. The limpet prefers feeding on that coralline above all other algae; its teeth are short but massive and designed for deep grazing of tough substrates. For its part, the coralline alga has lost the ability to slough off the surface layer and has a multilayered, uncalcified epithallium. The limpet can feed exclusively on C. circumscriptumwithout doing it any damage. The smooth surface of the coralline alga also allows the limpet to hold on tightly by suction if it is threatened or in rough conditions. The limpet does not wear away home depressions like most other limpets, and it has no competition from other species of grazers.
Researchers have found instances of hierarchical commensalism on tropical reefs, in which organisms depend upon chains of others but without any of them gaining any benefit or doing any harm. For example, in a community of urchins, limpets, coralline algae and coral, the urchins are necessary to keep the numbers of large algae down so the limpets can graze over the smooth coralline algae, keeping it healthy. Some coral larvae seem to need a coralline surface to settle on. Recently, Daniel and Aileen Morse of the Marine Biotechnology Center of the University of California, showed that the larvae of abalones settle and metamorphose into adult shellfish only on coralline algae. They settle in response to a chemical, a peptide, on the surface of the alga.
Several types of reef-building organisms show a preference for coralline algae when they settle; these include the tubeworm Spirorbisand some corals. Some "lettuce corals", for example, respond to a polysaccharide present in the cell walls of certain species of coralline algae. This type of controlled settlement is also important for the predatory crown-of-thorns starfish, Acanthaster planci. Periodic out-breaks of these coral-eating starfish have devastated hundreds of kilometres of the Great Barrier Reef off the east coast of Australia. The free-floating larvae of the crown-of-thorns settle only on coralline algae, probably only on Porolithon onkodes, which they eat for the first year of their lives until moving on to corals. The presence or absence of particular species of coralline algae has a big effect on the type of organisms that join the reef community.
Changes in the populations of urchins can also have far-reaching effects. In 1983, between 95 and 99 per cent of the population of the urchin Diadema antillarumin the Caribbean died, probably from some disease. Don Levitan, from the University of Delaware, reported a 30-fold increase in the amount of algae covering reefs in six months; even three years later, there was still five times the usual covering of algae. Levitan did not record the effect on coralline algae, but we can assume that they declined when covered by large fleshy algae. Changes in the structure of the community probably lasted many years.
Ken Lucas Planet Earth Pictures
Deceptively tough: the stony fronds of this coralline alga are a defence against rough seas and hard teeth
Crustose coralline algae are not only a significant factor in the development of reefs because they provide a substrate for coral larvae, they also make up much of the bulk of many reefs. At the turn of century, a researcher called A.E. Finckh drilled cores from reefs on the Funafuti Atoll in the Pacific. Finckh found that for most of its history, the bulk of the reef was crustose coralline algae, followed, in order of importance, by Halimeda(a calcified green alga), microscopic foraminifera (shelled protozoans) then, finally, corals. Deep drillings into other Pacific atolls and reefs confirm this general pattern. Some marine biologists suggest that the term "coral reef" is misleading and that "biotic reef" is more accurate. Crustose corallines such as Lithophyllum kotschyanumand Porolithon onkodes form ridges growing upwards to the level of low spring tide, and seawards, extending the reef front. Other species such as Sporolithon erythaeumand Hydrolithon reinboldiicement loose rocks and rubble in the reef's crevices, consolidating the reef and preventing the formation of channels in the reef, which might hasten erosion. The contribution of corals is that of hard-core. Branching corals such as stag's horn (Acroporasp), fire coral (Millepora dichotoma) and Stylophora pistillatagrow rapidly over the reef. Along the reefs of the Gulf of Aqaba, brown stands of fire coral grow at right angles to the current.
Y. M. Chamberlain
Calcite crystals in the cell wall ofLithophyllum
Box 1: Growth of a suit of stony armour
MANY algae encase their cells with calcium carbonate in the form of aragonite crystals, laid down in a rather irregular manner. Coralline algae, however, seem to calcify in a totally different manner; the crystals are in the hexagonal calcite form and they are laid down very regularly. The simplest method of precipitating calcium carbonate is to reduce the acidity of a concentrated solution of the ions. Tropical seas are saturated with calcium carbonate. As carbon dioxide is removed from sea water, calcium carbonate tends to precipitate out as the cells become slightly alkaline. Once crystal nuclei form, the crystals continue to grow as long as the surrounding water remains saturated with the right ions. If the mechanism was as simple as this however, all tropical algae would become calcified and there could be no fine control over the process. Calcification takes place not only in tropical waters but also in colder seas, which are not saturated with calcium carbonate. This suggests that some other process is at work and has led to much speculation. Examination of the structure of the cell wall of coralline algae shows that there is an intimate relationship between the calcite crystals and the cellulose fibres. Michael Borowitzka, of Murdoch University in Western Australia, proposes an "organic matrix theory", in which cellulose (or an organic complex including cellulose) acts as a centre for concentrating the raw materials of calcification. This centre may form a nucleus for crystal formation. The presence of calcite supports this idea. In Canada, P.S.B. Digby of McGill University in Montreal favours a "bicarbonate usage theory", based on biochemical or electrochemical events inside the cells. The rate of calcification depends on light: the more light there is, the faster the rate of calcification. In essence, Digby suggests that electrons produced during photosynthesis react with hydrogen carbonate ions to form carbonate ions. These ions then move out of the cytoplasm (being replaced by an inward flow of hydrogen carbonate ions) into the cell wall where they partly hydrolyse. Hydrolysis causes an increase in pH at the place where calcium ions from the sea, and carbonate ions from the cytoplasm, have reached saturation, and so precipitation occurs. A further requirement is for the hydrogen ions to diffuse outward, probably through the tips of the algal filaments, which, unlike the rest of the plant, remain uncalcified. Although the nature of the mechanism remains unclear, it probably involves a combination of both these processes, or processes similar to them. ❑
D. W. J. Bosence
Rock of algae: the remains of a coralline reef on the coast of Malta
Box 2: Evolution of a modern coral reef
TROPICAL reefs have existed for more than 500 million years. Because lands that once lay in the tropics have drifted with time, ancient reefs are often found in regions that are temperate today. The oldest Australian reefs began to develop only about 18 million years ago, as Australia gradually drifted northwards into the western Pacific. In more recent times, changes in sea level have affected reefs; 15 000 years ago, the sea was 120 metres lower than it is today. Only in the past 5000 years has the sea been around its present level. Modern reefs began to develop at this time. Coralline algae form excellent fossils and are one of the few groups of algae to have a well-documented fossil history. Palaeozoic reefs (dating from 570 to 225 million years ago) were rich in species of calcareous algae as well as corals. The main algae were calcifying green algae, blue-green algae and solenopores (which have been extinct since the beginning of the Cenozoic era, roughly 64 million years ago). Solenopores were red algae with large calcified cells. During the Devonian period (about 410 million years ago), another red calcareous algal group appeared which closely resembled the modern corallines. Archeolithophyllumwas the most wide-spread of these "ancestral corallines"; it was thin and leafy and lived in an environment similar to a shallow reef. Some suggest that true corallines evolved from a solenopore and that, despite a lack of fossil evidence, they later evolved to form the true corallines. Solenopores dominated the reefs until late in the Jurassic period (about 140 million years ago) when the first true coralline algae appeared. They became dominant during the Cretaceous period (135 million to 64 million years ago, the time when flowering plants appeared and the dinosaurs faded away) and have grown in importance since then. One reason why coralline algae might have become so successful is that they developed the ability to fuse adjoining cells. This was*a breakthrough that allowed them to grow sideways very rapidly to form
crusts; and also gave them the ability to grow in many forms and to recover from deep wounds. The coralline algae also have very small cells and, as a result, they are densely calcified and resist grazing successfully. Through evolution, they have tended to change from delicate leafy forms to thicker crusts as the number of herbivorous gastro-pod molluscs, echinoderms and fish increased. Intensive grazing may have driven the solenopores to extinction, leaving a gap on the reef for corallines. To the present day the corallines are the only algae that thrive on being eaten. Some even require it. ❑
During stormy weather pieces break off and lodge at the base of the reef. Within a year these are cemented together by masses of pink and purple corallines, which grow in the weak light percolating down through the rubble. The almost solid mass that forms is then capped by P. onkodes. In some parts of the world, much of the "filling in" material is provided by skeletons of the green alga, Halimedaor the sediments formed from the shells of foraminiferans. Any spaces left in the bulk of the reef are soon filled up by a physical process known as cryptocrystallisation, in which materials are precipitated out of the water onto the cavity walls. The production of organic materials by organisms on the reef may somehow encourage mineralisation. If the balance of species in the reef community is upset, there might be repercussions deep within the reef. Likewise, cementation by coralline algae is vital to the formation of a durable reef. And, again, if the balance of the community is upset, the corallines will be disturbed and might no longer fulfil this function. Disturbance of any part of the web can have catastrophic effects and eventually destroy the reef. The best documented examples of what can happen involve pollution. The effect on coralline algae is rarely mentioned in studies of polluted reefs. Researchers tend to concentrate instead on the corals. The reefs in the Gulf of Aqaba show the sort of changes that pollution can bring. For more than a decade, hundreds of tonnes of phosphate dust have been blowing from the dock at Aqaba into the sea during loading from conveyor belts. The dust settles on reefs as far as 2 kilometres downwind. Until recently there was also a sewage outflow nearby. Phosphate dust is insoluble and tends to lie on the seabed, accumulating in particular in the shallow area behind the reef. On an unpolluted reef, P. onkodescovers more than 30 per cent of the reef, while algal turf covers about 10 per cent. On a polluted reef, the proportions are reversed as the slow-growing corallines cannot grow fast enough to avoid being smothered by sediment. The reef at Aqaba is a narrow fringing reef. Near the loading dock it is dissected by wide gullies, while farther away it is continuous. The reef platform seems to be in the early stages of
degeneration. It is probable that the destruction of P. onkodesand other cementing corallines is responsible for the chain of events leading to this decay. Calcification in some corallines is slowed by high concentrations of phosphate, which seem to prevent crystals from forming. At the same time, sediments smother them, and thick mats of algal turf grow over them. Even many of the healthier corallines are penetrated by green, filamentous algae that bore into calcified structures and damage them. For some unexplained reason, the population of urchins is smaller here than in unpolluted areas. Without urchins to graze the reef, and with the extra supply of nutrients, epiphytes flourish and prevent coral larvae from settling.
A slow crumbling death
Gradual pollution can be just as destructive as catastrophic events, such as hurricanes. Researchers from the Netherlands Institute for Sea Research studied a reef next to an oil refinery on the Caribbean island of Aruba. After more than six decades of chronic pollution by oil and detergents, a long stretch of reef downstream from the refinery is showing serious deterioration. The dwindling covering of crustose coralline algae may have contributed to the destruction of the reef. Researchers at Tel Aviv University, Israel, have shown that corals subject to chronic oil pollution do not regenerate to repair damage to the reef. Perhaps the most infamous case of pollution damaging a reef involved the sewage flowing into Kanehoe Bay, on the Hawaiian island of Oahu. During the 1950s and 1960s, the population around the bay grew steadily. By 1970 many of the reefs were blanketed with a common green alga, Dictyosphaeria cavernosa, which flourished in the presence of such vast concentrations of nutrients. Many corals were dead and coral heads broke off easily.
Such damage is not uncommon. Almost any reef near human settlement or near the mouths of silt-laden rivers will suffer. Eventually, the reef organisms are worn down, they lose condition and become vulnerable to boring algae and sponges. Once these penetrate the reef, it begins to crumble. Overfishing can also damage reefs. Last year, biologists from the Friend's World College and the Fisheries Research Institute in Kenya discovered that areas that are heavily fished become heavily populated by the sea urchin Echinometra mathaei. This urchin burrows into the reef to create a safe place to live and then feeds by scouring organisms from the sides of its burrow. The scouring prevents the growth of algae, including cementing coralline algae, while the burrows weaken the structure of the reef. Worldwide this could be a bigger problem than pollution, which is more localised. Bar the occasional shipwreck on northern reefs, coralline algae have never had much obvious effect on human affairs and so they have received little attention. Now, it is clear that they are central to the health of reefs in all the world's oceans. Reefs are nurseries for vast numbers of fish and one of the richest of the Earth's ecosystems. More practically, they are the first line of defence against the sea for many small ocean islands. The loss of reefs leaves coral islands exposed to the powerful erosive force of the waves, threatening newly developing tourist industries and ancient settlements alike. As the sea rises in response to the greenhouse effect, this defence will become still more crucial. Reefs are also strikingly beautiful. Understanding their biology and vulnerability is the best way to ensure that they stay that way.
Brian Maudsley is a biology teacher and freelance writer, who has studied coralline algae and phosphate pollution in the Gulf of Aqaba.