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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 . 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 kotschyanum has 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 onkodes cover 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 onkodes and other ridge-forming algae, such as Lithophyllum kotschyanum,
grow particularly well where waves beat most powerfully and currents are
strong; they flourish where seaweed-eating herbivores are most abundant.
Indeed, grazing is essential to their survival. P. onkodes grows 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 .

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.

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 setosum and D. savignii
in the Pacific and D. antillarum in the Atlantic, and the large, short-spined
Tripneustes gratilla rasp 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 Acmaea testudinalis was
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. circumscriptum without 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 Spirorbis and 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 outbreaks 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
antillarum in 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.

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 AE 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 kotschyanum and Porolithon
onkodes form ridges growing upwards to the level of low spring tide, and
seawards, extending the reef front. Other species such as Sporolithon erythaeum
and Hydrolithon reinboldii cement 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 (Acropora sp), fire coral (Millepora
dicho toma) and Stylophora pistillata grow rapidly over the reef.

Along the reefs of the Gulf of Aqaba, brown stands of fire coral grow
at right angles to the current. 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, Halimeda or 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. onkodes covers 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. onkodes and 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.

* * *

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, PSB 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.

* * *

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. Archeolithophyllum was the most widespread 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 gastropod 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.

Brian Maudsley is a biology teacher and freelance writer, who has studied
coraline algae and phosphate pollution in the Gulf of Aqaba.