213
Stenohaline marine species are unable to tolerate salinities lower than about
Lalli, C. M., & Parsons,
25-30,T. andR. 2006.
they Biological
are largely excluded from oceanography: an salmon,
estuaries. Sorne fish (e.g.
eels) are transient residents of estuaries, and move freely from the sea to
introduction. 2nd Edn.rivers
Elsevier
and lakes, Butterworth-Heinemann.
or vice versa (see Section 6.6.1). Overall,Oxford. UK.
estuaries have
fewer species than adjacent aquatic environments, but abundance within
individual species as well as biomass are often markedly increased.
In general, the extent of penetration into estuaries by marine and, conversely,
freshwater species is determined by the rate and magnitude of tidal change,
rather than by the salinity gradient. That is, marine species penetrate farther
upstream, and freshwater organisms reach much closer to the sea, in estuaries
where tides are small and the salinity gradient is relatively stable. The
minimum number of species occurs in that part of the estuary where the
salinity variation is greatest. Finally, the distributions of benthic species
within estuaries are also controlled by sediment type.
QUESTION 8.5 Can you offcr any explana11on(',) a to \\ h) -..pe ic di,er-..it)
'
decline. in e-..tuarie rela11,·e to adJacent em ironment . but number<, of
indi, iduab and bioma-.. increa-..e'?
8.6 CORAL REEFS
Coral reefs are well known for their spectacular beauty (Colour Plates 34
and 35), and they are perhaps the most diverse and ecologically complex of
marine benthic communities. They are unique in being formed entirely by
the biological activity of certain corals belonging to the Phylum Cnidaria
(see Table 7.1). These tropical reefs result from massive deposits of calcium
carbonate laid down by the corals over aeons of geologic time. These are
among the oldest of marine communities, with a geological history
stretching back for more than 500 million years.
8.6.1 DISTRIBUTION ANO LIMITING FACTORS
Living coral reefs cover about 600 thousand km2 , or somewhat less than
0.2% of the global ocean area and about 15% of the shallow sea areas within
0-30 m depth. The largest reef is the Great Barrier Reef that extends along
the east coast of Australia for a distance of more than 2000 km and is as
much as 145 km wide. Reefs are located exclusively within water bounded
by the 20º C isotherms and so are virtually confined to the tropics
(Figure 3.10). Reef-building corals cannot tolerate water temperatures of less
º º º
than 18 C, and optima! growth usually occurs between 23 and 29 C,
º
although sorne corals tolerate temperatures of up to 40 C. A number of other
physiological demands further limit the distribution of reef-building corals.
They require high salinity water ranging from 32 up to 42. High light levels
are also necessary for reef-building (for reasons that will be explained
below), and this restricts corals to the euphotic zone. Even in the clear
oligotrophic water of the tropics, most reef-building species live in water
that is shallower than 25 m. The upward growth of a reef is restricted to the
level of lowest tides, as exposure to air for more than several hours kills
corals. Corals are also absent in turbid waters, as they are very sensitive to
high levels of suspended and settling sediment which can smother them and
clog their feeding mechanisms. High turbidity also affects reef-building by
decreasing the depth of light penetration. New reefs are initially formed by
214
the attachment of meroplanktonic coral larvae to a hard substrate, and for
this reason reefs always develop in association with the edges of continents
or islands.
QUESTION 8.6 Rcfcr to Figure J. 10. (al an )Oll c,plam \\h) coral red, ar1.:
gcncrall) ah,cnt on thc \\C,l rna,i-. of thc Amcríca and \frica hcl\\CCll JO
and JO ! (h) \\ hat m,ght pr1,;\Cíll recl lonnat,on off north-ea tcrn outl1
menea. north\\ard from Lhc mouth, of the Ama,on and nnoco m er-,?
8.6.2 CORAL STRUCTURE
Corals are closely related to benthic sea anemones (both are in the Class
Anthozoa) and are more distantly related to planktonic jellyfish, benthic
marine hydroids, and the freshwater Hydra. Not ali corals are reef-builders;
sorne are solitary or colonial animals that are capable of living in deeper
and/or colder water and are found throughout the world's oceans.
Reef-building stony corals are colonial animals, and each reef is formed of
billions of tiny individuals called polyps (Figure 8.8; Colour Plate 36). Each
polyp secretes a calcium carbonate exoskeleton around itself that generally
measures about 1-3 mm in diameter. Each polyp is equipped with tentacles
containing batteries of nematocysts (see Section 4.2), and these stinging cells
can be used to capture prey and for defence. The polyps can produce a large
colony by asexual division, or budding, and ali the polyps in a colony
remain connected to each other by extensions of their tissues. Corals also
reproduce sexually, producing planktonic larvae that disperse, settle, and
establish new colonies.
Individual coral colonies vary in size, but sorne are very large, weighing up
to severa! hundred tonnes. The form of a colony, whether it is branching,
massive, lobed, or folded, depends on the species and also on the physical
ten1acles
digestive --~~~ adjacent
cavlty
potyp
CJ
o D
D
L ; D
r-, CJl c=i
,--i
carbonate
skeleton
Figure 8.8 Anatomy of a coral polyp. The animal is basically a contractile sac housed in a
carbonate skeleton. The central mouth is surrounded by six, or a multiple of six, tentacles
equipped with batteries of nematocysts. The tiny zooxanthellae live in cells in the lining of
the central digestiva cavity. Each polyp secretes a protective carbonate exoskeleton consisting
of a radial arrangement of vertical plates; as it grows upward, the polyp deposits new layers
under itself.
215
environment in which the coral is located. The same species may have a very
different form when it grows in areas exposed to wave action as opposed to
calm conditions, or when it grows in shallow versus deeper waters.
8.6.3 DIVERSITY
The diversity of life on a coral reef is extraordinarily rich. Figure 8.9
illustrates only a very few dominant types of the coral-reef fauna. The Great
Barrier Reef is composed of about 350 species of hard corals, and is home
to more than 4000 species of molluscs, 1500 species of fish, and 240 species
of seabirds. In addition, there are many more species of macrobenthos, and
the numbers of micro- and meiofauna remain unknown. Representative
species of almost all phyla and classes can be found in the reef ecosystem.
Figure 8.9 A coral reef habita! illustrating sorne of the many inhabitants of this diverse
ecosystem.
1 petrel 16 snail
2 jellyfish 17 nudibranch (sea slug)
3 angelfish 18 sponges
4 lobed corals 19 colonial tunicate
5 sea whips (gorgonian corals) 20 giant clam ( Tridacna)
6 triggerfish 21 pseudochromid fish
7 sea fans (gorgonian corals) 22 starfish
8 tube anemone 23 soft corals
9 stone coral 24 cleaner shrimp
10 bryozoans 25 sea anemones
11 brain coral 26 clownfish
12 butterfly fish 27 worm tubes
13 moray eel 28 snail (cowry)
14 cleaner fish 29 sea fan (gorgonian)
15 tube corals
216
Reefs in the Indo-Pacific have a high diversity of coral species, with at least
500 reef-building species throughout the entire region. Atlantic reefs are
impoverished in comparison, with only about 75 species of reef-building
corals. The number of species in other animal groups associated with reefs is
also generally lower in the Atlantic sector than in the Indo-Pacific. The
number of mollusc species is estimated at about 5000 in the Pacific versus
1200 in the Atlantic, and there are about 2000 versus 600 fish species in
these respective reef areas. The differences in species diversity may result
from differences in the age of the oceans, and the respective geologic times
over which reefs have evolved. Geologically, the Atlantic is a more recent
ocean, and its reefs were also more severely influenced by decreased
temperatures and lowering sea levels during ice ages. Most Atlantic reefs are
only 10000-15 000 years old, these dates corresponding to the last glacial
age. In contrast, the Great Barrier Reef is about 2 million years old, and
sorne Pacific atolls date back about 60 million years.
The reef itself provides food and shelter for many plants, invertebrates, and
fish. For sessile species, the reef offers a site of attachment. Surface
irregularities in rhe reef limestone create a variety of microhabitats like
crevices and tunnels, and these contribute to the faunal diversity of the
system. Areas of rubble and sand also accumulate between coral heads, and
these sediment types require different sets of adaptations and develop
different communities from that associated with the hard-substrate reef. A
reef is also differentiated into regions distinguished by physical differences
in wave action, depth, and degree of tidal exposure. This wealth of different
habitats is a majar factor in supporting the many species of a reef.
Coral polyps usually dominate the living biomass of a reef, but other reef
organisms also contribute to the carbonate reef structure. These include the
hard, coralline red algae that grow in thin layers over the surface of the reef.
These encrusting algae precipitate CaCO 3 and play a role in cementing the
reef fragments together. Sorne green algae also secrete calcium carbonate,
other green algae do not. In addition to encrusting algae, there are benthic
algae that are erect species, and sorne that live within the spaces of the coral
framework. Seagrasses often grow in the sandy areas within or surrounding
the reef. All of these plants provide food for herbivorous species of
invertebrates and fish. However, the algae are generally inconspicuous
inhabitants of the reef, and animal life is visually dominant.
In addition to the reef-building stony corals, other types of cnidarians are
prominent reef members (see Figure 8.9 and Colour Plate 37). These include
several types of non-reef-building corals, including tire corals, pipe corals,
and soft corals. Sea whips and sea fans are also common reef inhabitants;
they are clase relatives of stony corals and have internal skeletons composed
of calcareous spicules. Other majar invertebrate groups in a reef community
include echinoderms (starfish, sea urchins, and sea cucumbers), molluscs
(limpets, snails, and clams), polychaete worms, sponges, and crustaceans
(including spiny lobsters and small shrimp ). Sorne of the invertebrates are
encrusting species, like bryozoans; sorne build calcareous tubes, like certain
polychaete worms; and sorne snails attach tube-like shells to the reef. All of
these activities serve to cement the limestone reef framework together. In the
Pacific, giant clams belonging to the genus Tridacna are also important
structural components of reefs (Figure 8.9). These molluscs contribute an
astonishing biomass to the reefs, as they grow to over 1 m in length and
may exceed 300 kg in weight.
217
Fish comprise the dominant vertebrates on a reef. Many of the reef fish are
brightly coloured and visually conspicuous. About 25% of the world's
species of marine fish are found only in reef areas. These diverse species of
fish show a high degree of feeding specialization and food selection. Sorne
are herbivores, feeding on algae or seagrasses; sorne specialize in being
plankton-feeders; and sorne are piscivorous, or are predators of benthic reef
invertebrates. Fish not only play important ecological roles in grazing or
predation, but the faeces of these abundant animals contribute an important
source of nutrients to the reef ecosystem.
The very large number of reef species, and the abundance of life on the reef,
lead to intense competition between species and between individuals for
limited resources. The high degree of food specialization observed in many
reef species is a reflection of the high species diversity of the reef, and every
available food resource is efficiently utilized. There is also intense
competition for space on the reef, and every microhabitat is occupied by
organisms adapted to their particular site. Experimental work has revealed
that the mesenterial filaments (Figure 8.8) of sorne corals contain substances
that kill polyps of adjacent colonies. Aggressive, slow-growing corals can
thus avoid being overgrown by less aggressive, but faster-growing species.
8.6.4 NUTRITION ANO PRODUCTION IN REEFS
Reef-building corals are also called hermatypic corals. They are
distinguished from non-reef-building (ahermatypic) species by having a
special symbiotic association with certain algae. Each hermatypic coral
polyp contains masses of photosynthetic dinoflagellates, called
zooxanthellae. These are a vegetative form of free-living dinoflagellates;
when cultured under laboratory conditions, they develop into motile
flagellate forms identical with planktonic dinoflagellates (see Section 3.1.2).
The zooxanthellae in all corals belong to a single genus, Symbiodinium, with
different species or strains being specific to particular coral species. The
zooxanthellae live within cells in the lining of the gut of corals, reaching
concentrations of up to 30 000 cells per mm 3 of coral tissue. Under stressful
environmental conditions, the symbiotic algae can be expelled from the
coral. Because much of the colour of corals is due to the pigmentation of the
zooxanthellae, this expulsion is referred to as 'bleaching'.
The algal-coral relationship is beneficial to both species. The coral provides
the algae with a protected environment, but it also provides certain chemical
compounds that are necessary for photosynthesis. Carbon dioxide is
produced by coral respiration, and inorganic nutrients (ammonia, nitrates,
and phosphates) are present in waste products of the coral. In return, the
algae produce oxygen and remove wastes; but most importantly, they supply
the coral with organic products of photosynthesis that are transferred from
the algae to the host. These chemical products include glucose, glycerol, and
amino acids, all compounds that are utilized by the coral polyps for
metabolism or as building blocks in the manufacture of proteins, fats, and
carbohydrates. The symbiotic algae also enhance the ability of the coral to
synthesize CaC0 3 . Rates of calcification are significantly slowed when
zooxanthellae are experimentally removed from corals, or when corals are
kept in shade or darkness. The relationship between the two independent
processes of C02 fixation by photosynthesis and C02 fixation as CaC03 is
complex and not fully understood. However, the symbiotic association with
photosynthetic dinoflagellates explains why hermatypic corals require clear,
218
lighted water. This association also leads to intense competition for space
within areas of sufficient light to support the zooxanthellae.
The coral-zooxanthellae symbiosis is maintained over time and distance
because the algae are already contained in coral larvae before they are
released from the parent polyp. This relationship is not unique on the reef,
however. Zooxanthellae are also present in other reef inhabitants, including
the majority of other cnidarians, sorne tunicates, sorne shell-less snails, and
in the giant clam Tridacna.
The symbiotic arrangement between algae and corals or other invertebrates
results in nutrients being tightly recycled within coral reefs. This intemal
nutrient cycling is of primary importance in maintaining the productivity of
the reef in oligotrophic tropical water.
Symbiotic algae do not supply all the nutritional requirements of their hosts.
All the animals harbouring zooxanthellae are mixotrophic and capable of
meeting their additional nutritional needs in other ways. Corals are true
camivores that capture zooplankton, employing their nematocysts to paralyse
the prey. Many coral species can also feed on suspended particles by
producing mucous nets or mucous filaments to entangle food that is then
drawn to the mouth by rows of cilia. Ciliary-mucus feeding extends the size
range of potential food items to include even bacteria. Corals may also
directly absorb dissolved organic matter.
The relative importance of zooxanthellae versus captured particulate food to
the nutrition of any particular coral probably depends on the particular
species, and it will be influenced by the specific chemical that is produced
and translocated from the symbiotic algae to the host. It should also be
influenced by various environmental parameters such as depth, light
intensity, abundance of zooplankton, etc.
8.6.5 PRODUCTION ESTIMATES
Primary production in the coral reef system is carried out by the benthic
algae attached to or associated with the reef, by the suspended
phytoplankton, and by the zooxanthellae living within the animals of the
reef. This ecological fractionation of primary producers makes accurate
measurements of primary productivity extremely difficult because different
techniques must be employed for each. With the exception of the
phytoplankton, it is also difficult to assess the standing stock of primary
producers. To do so requires determining the plant/animal proportions of
coral polyps and the relative contributions of various types of benthic algae
to total reef biomass. Until these have been determined, the size of the
primary producer trophic leve! remains uncertain.
Production studies of coral reefs suggest that gross primary productivity
ranges from about 1500 to 5000 g C m- 2 yc 1, values that are much higher
than those of open tropical oceans (see Section 3.5 and 3.6). In fact, they
represent sorne of the highest rates of primary production of any natural
ecosystem. However, many of the nutrients contributing to this production
are recycled (i.e. the f-ratio <0.1, see Section 5.5.1 ). Symbiosis between
primary producers and dominant animal species of the community, with
219
nutrients prevented from being washed away, is a dominant controlling
feature of the biological production, just as it is in the deep-water,
sulphide-communities which will be described in Section 8.9.
Net primary production on reefs is lower than might be expected because
respiration of the primary producers is high, with gross production to
respiration ratios (P / R) usually ranging from 1.0 to 2.5. In comparison,
healthy phytoplankton have a P / R ratio of about 10. In addition, the
coral-reef food chain is much longer than in upwelling zones (see
equation 5.2), so that respiration losses throughout the entire ecosystem are
high. This results in lowering the production of top-leve! predators relative
to the high gross primary productivity.
8.6.6 FORMATION ANO GROWTH OF REEFS
During the voyage of the Beagle in the 1830s, Charles Darwin observed that
there were three basic types of coral reefs, and he formulated an hypothesis
of reef formation that linked these types. His ideas are summarized below
and illustrated in Figure 8.10.
Reef formation is initiated with the attachment of free-swimming coral
larvae to the submerged edges of islands or continents. As the coral grows
and expands, a fringing reef is formed as a band along the coast or around
an island. This type of reef is predominant in the West Indies (Caribbean
Sea). It is also the first stage in the process of forming atolls.
If the fringing reef is attached to the edges of a volcanic island or other land
mass that is slowly sinking, while the coral continues to grow upward, a
barrier reef will eventually form. Barrier reefs are separated from the land
mass by a lagoon of open deep water. The Great Barrier Reef of Australia is
the best known of this type, but it is in fact an aggregation of many reefs.
Atolls mark the last stage in this geological process. When a volcanic island
subsides below sea leve!, the coral reef is left as a ring around a central
lagoon. Continued coral growth maintains the circular reef, but calm
conditions and hence increased sedimentation in the central lagoon prevent
development of a reef in this area. Hundreds of coral atolls are found
throughout the South Pacific Ocean, all of them located far from land but
attached to underwater seamounts (volcanic elevations rising from the
seafloor) which have subsided with age.
Darwin' s ideas on atoll formation were not substantiated until the 1950s,
when drilling programmes on coral atolls encountered volcanic rock
hundreds of metres below the surface. His hypothesis has been further
supported by the discovery of seamounts, submerged far below the sea
surface, that still have attached remnants of shallow-water corals.
QUESTION 8.8 E , luding pollution influence-.. wou ld you e pee! to tind a
difference in t tal bi logi al produ tion bel\\een a barri r reef located
off hore f a ominem and a mid- anic atoll'? plain your answ r.
The rate at which a reef develops depends on a balance between the growth
rates (budding) and calcification of the coral polyps and the rates of
destruction of the limestone framework. Corals always grow upward, toward
light, as each polyp deposits new carbonate layers under itself (Figure 8.8).
Growth of the coral skeleton is much faster in sunlight than in darkness (and
220
(a) fringing reef
volcan ic
island
sea
leve!
emergence
(b) barrier reef
lagoon
subsidence
(e) atoll central
lagoon
Figure 8.1 O The formation of coral atolls
according to Darwin's theroy of subsidence.
therefore also faster in shallower water) and, not surprisingly, the rate of
growth can be decreased if photosynthesis of the zooxanthellae is reduced by
sediment-laden water or chemicals (see Section 8.6.4). Growth rates may
also decline with age and increasing size of a colony. In general, corals are
regarded as slow-growing, with measured rates of growth usually varying
from < 1 to 10 cm yr- 1 .
However, growth rates of individual coral species do not necessarily describe
the rate of growth of an entire reef system. This is partly because different
221
species of corals have different growth rates, but also because growth and
expansion of the reef is regulated by many other factors such as predation,
competition for space with other organisms, and light intensity, to name only
a few. Further, the limestone framework is continually being destroyed by
biological activities and physical events (see below). Estimates of total reef
growth can be made from measured changes in reef topography over severa!
years, or from geological information on the thickness of reef limestone
deposits. These estimates of net vertical upward growth of reefs vary greatly,
from only a few millimetres per year, to 30 cm per 11 years under
favourable conditions.
In order to obtain better estimates of the rate at which entire reef systems
grow, it is also necessary to know something about the factors that destroy
the reef and the rate at which the limestone is broken down. Reefs are
subject to physical erosion by wave action and currents, and tropical storms
can cause extensive damage. Reefs are also subject to continua! bioerosion,
or breakdown of the calcium carbonate skeleton by reef inhabitants. Sorne
organisms associated with the reef remove part of the coral skeleton by
boring into the reef, using chemical dissolution or mechanical abrasion;
these include certain species of algae, clams, sponges, sea urchins, and
polychaete worms. Sorne animals (e.g. herbivorous limpets and snails,
parrotfish) remove pieces of the reef skeleton inadvertently during grazing.
Small coral fragments are consumed by deposit-feeders such as sea
cucumbers, and thus become further reduced in size. These destructive
activities eventually break down reef material to fine-grained carbonate sand.
Much of the fine-grained detritus is flushed away from the reef by waves
and currents, but sorne accumulates in pockets between coral heads.
8.6.7 ZONATION PATTERNS ON REEFS
Ali reefs exhibit zonation patterns resulting from a combination of bottom
topography and depth, and different degrees of wave action and exposure.
The patterns differ according to locality and type of reef, with atolls having
the most complex zonation. The major divisions are illustrated in
Figure 8.11 and discussed below, but depending on locality, the zones may
be subdivided into as many as a dozen.
The reef flat (or back-reef) is located on the sheltered side of the reef,
extending outward from the shore or coastline to the reef crest. This area is
only a few centimetres to a few metres deep, and large parts may be exposed
at low tide. The width of the reef flat varíes from a few tens to a few
thousands of metres. The substrate is formed of coral rock and loose sand.
Beds of seagrasses often develop in the sandy regions, and both encrusting
and filamentous benthic algae are common. Because it is so shallow, this
area experiences the widest variations in temperature and salinity, but it is
protected from the full force of breaking waves. The reduced water
circulation, accumulation of sediments, and periods of tidal \llilersion
combine to limit coral growth. Although living corals may be scarce except
near the seaward section, this area of many microhabitats supports a great
number of species in the reef ecosystem, with molluscs, worms, and decapod
crustaceans often dominating the visible macrofauna.
The reef crest (or alga! ridge) lies on the outer side of the reef, with its
exposed seaward margin marked by the line of breaking waves. As the name
implies, the reef crest is the highest point of the reef, and it is exposed at
222
• • •••••••••• ♦ ............ _ •• --· : •
....._... :·.\· . . ·· . ··::.-;;-.-::·
50 m
Figure 8.11 A generalized cross section of a typical Caribbean fringing reef, illustrating the
major ecological zones.
low tide. The width of this zone varíes from a few to a few tens of metres.
In sorne localities, encrusting red coralline algae are dominant; in other
reefs, brown algae predominate in this zone. Living corals are very scarce
where wave action is severe; usually only one or two robust coral species
dominate in this region.
The outermost seaward slope (also called fore-reef) extends from the low
tide mark into deep water. The upper part of this zone is broken by deep
channels in the reef face, through which water surges and debris from the
coral reef leaves. Large corals dominate here, and there are many large fish.
The maximum number of coral species tends to occur at 15-25 m, then
declines fairly rapidly with increasing depth. At 20-30 m depth, there is
little wave action and the light intensity is reduced to about 25% of that at
the surface; here, corals tend to be smaller branched forms. At 30-40 m,
sediments accumulate on the gentle slope and coral becomes patchy in
distribution. Sponges, sea whips, sea fans, and ahermatypic corals become
increasingly abundant and gradually replace hermatypic corals in deeper and
darker water. At 50 m, the slope steepens into deep water. The depth limit
for reef-building corals is about 50-60 m in the Pacific, and about 100 m in
the Caribbean; the difference is probably related to differences in light
penetration.
Mangrove swamps, also called mangals, are a common feature covering
60-75% of tropical a nd subtropical coa stlines. These forests of trees and
shrubs that are rooted in soft sediments occur in the upper intertidal zone.
They produce a marine system tha t is simila r to a sa ltma rsh in ha ving aerial
storage of pla nt bioma ss and in ha rbouring both terrestrial and marine
species. The euryha line plants making up this specia lized community are
tolerant of a wide range of sa linities and are found both in fully saline
waters and well up into estua ries, but they are restricted to protected shores
with little wave action. The distribution of mangroves overlaps with that of
