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AMER. ZOOL., 34:115-133 (1994)
Biodiversity of Coral Reefs: What are We Losing and Why?1
KENNETH P. SEBENS
Department of Zoology, University of Maryland, College Park, Maryland 20742
Coral reefs are threatened by numerous anthropogenic impacts,
some of which have already had major effects worldwide. These unique
tropical environments harbor a high diversity of corals, reef invertebrates,
fish and other animals and plants. In most taxa, the species diversity of
reef-associated organisms is poorly understood because many of the species have yet to be collected and described. High coral mortality has been
associated with natural events such as hurricanes, predator outbreaks and
periods of high temperature, but has also resulted from excess nutrients
in sewage and from specific pollutants. Reef corals and associated organisms are also threatened by the possibility of global warming which will
result in rising sea levels and periods of increased temperature stress, and
which may also bring increased storm frequency and intensity. Although
the recent extensive episodes of coral bleaching in the Caribbean and
eastern Pacific cannot be causally related to global warming at this time,
the close link between bleaching and temperature suggests that global
warming will result in severe changes in coral assemblages. Major reef
destruction has followed outbreaks of the predatory seastar Acanthaster
planci in the Pacific. Although this is considered part of a natural disturbance cycle, there are indications that altered land use patterns and reduction of predators on this seastar by human activities may have increased
the severity of outbreaks. Recreational and commercial use of reefs has
also increased, and has caused extensive damage, especially near areas of
high population density. One of the most obvious and widespread losses
to reef biota is the reduction in fish populations from intense overfishing
in most reef areas of the world. Coasts without adequately managed reefs
have suffered intense overfishing for both local and export purposes, to
the point where the positive effects offishon those reefs have been compromised. The combination of these destructive factors has altered reefs
in all localities, and many that were once considered protected by distance
and low population density are now being exploited as well. On the positive side, improved understanding of ecological processes on reefs combined with concerted conservation efforts have managed to protect some
extensive areas of reef for the future.
SYNOPSIS.
INTRODUCTION
the past few decades. Coral reefs are frequently described as the marine equivalent
Coral reefs of the world: Distribution
and diversity
of tropical rain forests, given their high spej
i L- i • * L
* J cies diversity and the similarity of certain
!-,•„
y
Ecolog,stsand coral biologists have noted s t n l c l u r i
rocesses ( C o n n e | | ^ , 7 8 J a c k .
son.99, Thepara.Se,sdono,end,here,
co r a , reefs £ most parts Jf the wortd over
i n s Z L & ^ u ^ ^ & W
beleaguered terrestrial ecosystems as
humans seek to exploit their numerous
^sources. Coral itself is used as a building
the American Society of Zoologists, 27-30 December
1992, at Vancouver, Canada.
material, reefs are destroyed by coastal
development, and reef fish are being severely
115
116
KENNETH P. SEBENS
depleted in all parts of the world (Hutchings,
1986; Russ, 1991; Wilkinson, 1993). In
some regions, fish and invertebrates, including the coral framework, are harvested
extensively for the pet and curio trades.
Meanwhile, researchers are just beginning
to understand the real diversity of reefs, the
processes that maintain and destroy them,
and the basic biology of corals themselves.
Coral reefs are distributed throughout the
world tropics, although a few coral species
reach the Arctic, the Antarctic and the deep
sea. Reef growth, the deposition and accretion of calcium carbonate skeletal material,
is limited to regions which average at least
20°C year round. The diversity of corals
(Fig. 1) and reef associated species declines
north and south of the equator, with high
latitude reefs dominated by the few hearty
coral species able to survive periodic winter
chills (Stehli and Wells, 1971;Veron, 1986).
In the Caribbean, about 80 species of reefbuilding corals are found in the southern
portion, about two thirds of those are still
common in the Florida Keys, and only 21
occur in Bermuda. In the Indo-Pacific, the
equatorial regions with large land masses
and extensive island groups support over
390 species, whereas southern Japan has
from 363 to 25 species moving northward
from 27 to 35° latitude (Veron, 19926), and
southern Australia has only 72 percent of
the northern Great Barrier Reef coral species, near the southern limit of reefs on the
eastern coast (Veron, 1986). The diversity
of other reef invertebrates and reef fish (Fig.
2) mirrors this pattern in most parts of the
world.
Another major diversity gradient occurs
moving away from high diversity centers in
the Pacific, one in the Red Sea and the other
in the Philippines, New Guinea and the surrounding region. Eastward from New
Guinea, for example, the number of coral
genera drops from over 70, to 30 in Tahiti
and French Polynesia, to a low of 15 in the
separated islands of the eastern Pacific such
as the Galapagos and the coast of Central
America (Veron, 1992a). Reef fish display
the same pattern with a high of close to 900
species in the western Pacific, to about half
that in the eastern Pacific, and a third that
number in the Atlantic (Thresher, 1991).
This diversity gradient, also present for other
reef fauna, is the result of several factors,
including the large dispersal distances limiting species colonization of islands, the
small land masses and high local extinction
probabilities, and the geological history of
the region, including the effects of numerous
large fluctuations in sea level over the past
150,000 years or more (Rosen, 1981).
Corals have been collected throughout the
world and new species have been described
FIG. 1. Worldwide distribution of hermatypic coral genera. Lines connect regions with equal numbers of genera;
there is a maximum of over 70 genera (>390 species) in northern Australia, New Guinea, the Philippines and
bordering regions. Other areas of high diversity (>50 genera) occur in the Red Sea and in the Indian Ocean.
CORAL REEF BIODIVERSITY
117
for over two hundred years. Only in the last species (described and undescribed species)
two decades, however, have there been pro- that showed almost no sign of decreasing
ductive attempts to examine the validity of even after totals of over 500 species in five
all such descriptions, and to find out how years of intensive collecting (Gosliner,
many such species are "real." The number 1993). The interstices of coral reefs provide
of described species of scleractinian corals abundant and varied habitats for cryptic
now accepted as good species has thus species; the number of undescribed polydeclined recently as researchers have rec- chaete worms, small crustaceans, bryozoognized that so-called different species ans, hydroids and other small invertebrate
described from separate island groups are species cannot even be estimated with any
in fact the same (Veron, 1986). In the Carib- degree of confidence. Shelled mollusks are,
bean, polymorphic species have recently of course, well collected and described in
been recognized as species complexes (e.g., most parts of the world and populations
Montastrea annularis, Knowlton et al, have been decimated to provide shells for
1992) thereby increasing the number of spe- sale. Their diversity often depends on the
cies known for that region. Rapid advances habitats created by corals and other reef
in molecular systematics will undoubtedly dwellers (Kohn and Leviten, 1976). Fish
alter the present species lists further. Related have received even more attention than have
anthozoan groups such as the octocorals, sea corals, however, and species rearrangeanemones and zoanthids have never ments are more common than the discovery
received the attention directed at sclerac- of many new species, yet patient underwater
tinian corals even though they are common observation and collecting continues to turn
reef inhabitants. New species and genera are up new species regularly. The taxonomic
still being discovered at a rate limited only status of coral reef fauna and flora is thus
by the time available for the few experts on extremely similar to that of diverse and
each group to collect, quantify characters, remote terrestrial habitats, including tropical rain forests, where new birds and mamand publish.
mals continue to be recognized, and hunOther invertebrate groups are incom- dreds to thousands of species of insects,
pletely described to a similar extent. A recent plants and simpler life forms await discovestimate from New Guinea produced an ery and description.
annual accumulation rate of nudibranch
The eastern Pacific is extremely depauperate and the Caribbean, with less than 80 species, reaches only one
fourth the generic diversity of the western Pacific (from Veron, 1992b).
118
KENNETH P. SEBENS
I
I
1000
800 o>
'o
a.
600 -
<D
400 -
in
200 -
ov 8
5
40 -
1
5
4
7
1
1
15
1 2
10
9
13
14
16
2
18
17
30 -
19
2
20
1
3
20 10 n
Indian
Pacific
Atlantic
FIG. 2. Coral reef fish diversity (species and families) in all coral reef locations of the world. Note the high
diversity in the western Pacific (as in Fig. 1 for corals) and the low number of species in the Atlantic and eastern
Pacific. The number of families represented shows less of a spread, suggesting that most "guilds" are represented
in each reef area, but with fewer species each (redrawn from Thresher, 1991).
119
CORAL REEF BIODIVERSITY
Coral Body Wall
Environment
Dissolved Organics,
Amino Acids
Demersal
Plankton,
Particulates,
Bacteria
2
.3?
0)
Zooxanthellae
Ammonia, Host waste
Demersal Plankton
Corals, Other Invertebrates
Zoox.
Amino Acids, etc.
Zoox.
• Host
FIG. 3. Interactions between corals, their symbiotic algae (zooxanthellae) and the environment. A section of
coral body (or tentacle) wall is represented, with three tissue layers. The gastrodermal layer contains the algae
and cells that take in and digest dissolved and paniculate food substances from the internal cavity (coelenteron).
The epidermis contains mucus gland cells and nematocysts (stinging cells). Inorganic nutrients reach the algae
by diffusion through the epidermis and mesoglea (collagenous structural layer). Organic compounds are absorbed
by active uptake, and particulates (including zooplankton) are captured by nematocysts and mucus and are then
ingested. Bacteria growing on the coral surface are sloughed off in mucus layers which are either ingested or
become food for other reef fauna. These bacteria and other microorganisms also use dissolved nutrients otherwise
available to the coral. Symbiotic algae recycle host nitrogen by using waste ammonia to form amino acids and
other compounds which are translocated to the host cell.
with algal symbionts (hermatypic) accrete
carbonate
much faster than do those withReef corals (Phylum Cnidaria: Class
out
the
algae
(ahermatypic) because algal
Anthozoa) build calcium carbonate skeletons (and are termed "scleractinian" corals), photosynthesis creates a chemical environand most derive at least some of their nutri- ment conducive to precipitation and crystion from photosynthesis by symbiotic algae tallization. Corals without symbionts must
(dinoflagellates, termed "zooxanthellae") in expend energy to lay down skeleton, and do
their gastrodermal cell layer (Fig. 3). Corals so very slowly; they therefore do not conCORAL REEF ECOLOGY
120
KENNETH P. SEBENS
pounds (energy sources) for daily metabolism, growth and reproduction; they also
recycle host wastes efficiently. Wastes contain elements (nitrogen, phosphorus, etc.)
needed as building blocks (amino acid, proteins) for algal and coral tissue growth
(reviewed by Sebens, 1987). Even with
maximum photosynthetic activity, however, corals must capture zooplankton or
other paniculate matter to gain enough
nitrogen and phosphorus to build new tissue. In deeper reef zones, photosynthesis
cannot supply all necessary energy and zooplankton or other paniculate matter must
be consumed to provide both energy and
limiting nutrients. Tropical oceanic environments are generally very low in dissolved nutrients (oligotrophic), although
coastal environments can be much richer
(D'Elia et al, 1981; Lapointe and Clark,
F = feeding/scraping mortality
1992; LaPointe et al, 1993). Limiting nutriG = growth rate enhancement
ents can also be gained by active uptake,
through the coral's body wall (Fig. 3), of
FIG. 4. Relationships between corals, macroalgae,
nutrients, and consumers. Corals prevent macroalgal
compounds dissolved in sea water (e.g.,
propagules from finding attachment sites, and may have
nitrate, nitrite, ammonia, amino acids)
allelopathic effects on algae, whereas algae shade and
although the amount available is highly
abrade corals by overgrowth of coral edges. Increasing
dissolved nutrients (e.g., N, P from sewage) increases variable. Addition of nutrients to coastal
algal growth ( + + ) and has a slower positive effect on
waters might thus seem advantageous to
coral growth (+), thus favoring algae. Herbivores
corals, and could stimulate growth. How(including omnivorous urchins and fish) remove algae
ever, such enrichment (eutrophication)
rapidly (
) and favor coral growth, except within
affects benthic algae as well, and they grow
damselfish territories where corals can be either
faster, damaging corals by shading and
destroyed, protected, or allowed to be overgrown by
abrasion and limiting coral recruitment by
algae. Corals can be removed by omnivores, especially
by urchins (-), but corals also provide structural refreducing larval contact with the rock suruges for herbivorous fish. Human exploitation of fish face.
results in high urchin densities which reduce both corals and alga. After urchin die-offs (epidemics), algae
are strongly favored by low herbivory and high nutrient
conditions. If pollutants include pesticides, hydrocarbons, metals or other toxicants, they can have a direct
negative effect on corals also.
tribute much to reef growth. Ahermatypic
corals are usually limited to dark environments on reefs, to deep water, and to high
latitudes where temperatures are low. In
addition to the scleractinian corals, reef surfaces can be dominated by octocorals, gorgonians and soft corals which usually grow
as upright "trees" and maintain flexibility
by limiting their skeleton to networks of
fused and unfused spicules.
Symbiotic algae provide shallow water
corals with more than enough carbon com-
The diversity of reef corals and associated
fauna varies along depth and habitat gradients. In general, the richest zones for coral
diversity are at or just below the zone of
strongest wave action and highest urchin
densities (reviewed by Hughes, 1989; Huston, 1985; Jackson, 1991). In very shallow
forereef and lagoonal environments, single
species often dominate large areas (e.g.,
Caribbean and Eastern Pacific). The same
is true of deep reef slopes, especially in the
Caribbean where plating species (Agaricia
spp.) dominate. The combination of high
growth rates and disturbance from storms
acts to enhance diversity in the zones affected
by wave action. This includes wave-exposed
reef flat communities of the Great Barrier
Reef and central Indo-Pacific which often
CORAL REEF BIODIVERSITY
display high diversity. Below this zone, the
cover and diversity of other invertebrates,
such as sponges and ascidians, often increase.
In the surf zone, coralline algae rather than
corals, can occupy most of the substratum.
Disturbance is best defined as any process
that clears primary substratum, including
the effects of storms, predators, or disease.
Coral predators include the Crown-ofThorns seastars {Acanthaster planci, discussed later) which clear large reef areas,
fireworms, certain snails, and a variety of
corallivorous fish. Such disturbance is as
important to coral reefs as it is to any other
community, because it opens up space and
resets a patch of substratum to an earlier
successional stage, allowing the cycle of
recovery to begin again. Without significant
disturbance, each depth zone of a reef could
theoretically become dominated by a single
coral species able to outcompete all others.
Corals compete by numerous mechanisms,
including direct overgrowth and use of
sophisticated agonistic structures such as
modified tentacles and digestive organs
(mesenterial filaments) to kill the tissue of
neighboring corals and other cnidarian species (Lang and Chornesky, review, 1988).
Any reef, at a given time, comprises a set
of "patches" of substratum at different stages
of recovery from small to large disturbances. The term "equilibrium" is frequently used to denote the climax or undisturbed community state. The actual
"equilibrium" community, however, is a
landscape of all successional stages, for a
given pattern and rate of disturbance over
time (Paine and Levin, 1981), rather than
an undisturbed "climax" with almost complete space cover by competitively dominant species. In fact, disturbance at some
optimum intermediate level allows the
greatest number of species to coexist (Connell, 1978). If there is too little disturbance,
a few species take over all the space and if
there is too much disturbance, most species
cannot recruit and grow fast enough to persist, so the community is dominated by a
few "weedy" or opportunistic species with
high rates of reproduction and recruitment,
but often with poor competitive ability.
121
encrusting invertebrates. Patches can remain
algal-dominated indefinitely when they are
within territories defended by damselfish,
which actively remove other grazers and
sometimes damage and kill coral (Lobel,
1980). The interactions between damselfish, schooling herbivorous fish and other
grazers, such as sea urchins, are complex
(Fig. 4). When fish populations are reduced,
urchin populations expand with negative
effects on coral cover because urchins
remove coral as well as algae (Hay and Taylor, 1985).
Corals usually take longer to recruit and
to cover large areas, with a few appearing
rapidly and regularly because of high larval
production and high recruitment rates. Corals reproduce by asexual fragmentation, by
brooding planula larvae, and by releasing
egg and sperm, often in bundles that burst
as they rise to the surface, where fertilization
and development to a planula stage occur.
When many species spawn over a few nights
of the year, spectacular "mass spawnings"
result (Babcock et al., 1986) and waves of
larvae can be observed from the air, moving
from one reef to another as a "surface slick."
Whether or not a reef with recently cleared
areas is in the path of such a larval mass
could determine the number and species of
new coral colonists in a given year. Anything (higher or lower temperature, altered
currents, poor water quality) that interferes
with the regulation and timing of spawning
could potentially produce a total failure of
recruitment that year, or a significant reduction in the number of recruits of particular
species.
Sufficient water movement affects the
movement of larvae, and is also critical to
coral growth because rapid flow or strong
wave action removes sediments from coral
surfaces, delivers prey organisms to coral
tentacles, and reduces the thickness of the
"boundary layer" over coral tissue surfaces
thus allowing rapid diffusion of oxygen, carbon dioxide and dissolved nutrients (Patterson et al., 1991; Sebens and Johnson,
1991). Corals in lagoons, backreef environments and deep reef zones may be severely
limited by the low flows characteristic of
Following a disturbance, open space can those habitats (Sebens and Done, 1993), thus
be colonized rapidly by algae and by some limiting the number of species that can per-
122
KENNETH P. SEBENS
linked the large scale bleaching phenomena
observed in the field to temperature as a
primary mechanism, and to increased ultraviolet light (during periods of calm clear
water) as a potential secondary factor (Glynn
et ai, 1993). As temperature increases, the
photosynthetic activity of symbiotic algae
increases as well resulting in high concentrations of oxygen inside host cells. This has
two negative effects, an increase in host metCORAL BLEACHING AND GLOBAL WARMING abolic rate because cnidarians are metabolic
In 1983 massive fields of Pocillopora conformers (reviewed in Sebens, 1987) and
damicornis and other less abundant species an increase in toxic forms of oxygen (superalong the Pacific Coast of Panama turned oxide radicals, peroxides) that can damage
white and later died (Glynn, 1988, 1991; host cell nucleic acids and interfere with
Glynn and D'Croz, 1990). This was coupled biochemical pathways (Lesser et ai, 1990).
with an extreme ENSO (El Nino Southern Following even a strong bleaching response,
Oscillation) event which raised tempera- the host contains a residual population of
tures over a broad geographic region of the algae that serve as a source population durEastern Pacific. In 1987, a similar bleaching ing the recovery period, which can take at
event was observed throughout the Carib- least a year (Goreau and MacFarlane, 1990;
bean (Williams and Bunkley-Williams, Fitt et ai, 1993; Savina, 1993). If the initial
1990; Lang et ai, 1992, reviews), involving shock is severe enough, the entire coral or
numerous species (Fig. 6), although it is not parts thereof can die, as occurred extenknown how much mortality ensued. This sively in Eastern Pacific reefs in 1983 (Glynn,
was followed by a second similar event in 1988). Coral death was also observed in
1989 and another in 1990. Although sig- mapped colonies of Agaricia on Jamaican
nificant coral reef research has been con- reefs, especially when the same coral colony
ducted in the Caribbean since the 1950s, suffered repeated bleachings (Savina, 1991).
and the bleaching phenomenon can be seen
Although significantly higher sea surface
from a small boat on a calm day, only geo- temperatures have not been demonstrated
graphically isolated bleachings had been during the three periods of bleaching for the
reported previously. In the few places where Caribbean as a whole (Atwood et ai, 1992),
quantitative observations were carried out the bleachings occurred at the warmest time
with good temperature measurements, it was of year and in years when temperatures
clear that the Caribbean bleaching events above 30°C lasted longer than usual. Temcoincided with temperatures (30-31°C) peratures measured in Jamaica were well
about two degrees above the normal annual
maxima (28-29°C). The extensive bleach- above 30°C during the three bleaching events
ings, repeated over such a short period, (Gates, 1990; Savina, 1993), and bleaching
raised concern that global warming would was particularly common in deep reef (>
30 m) corals {Agaricia lamarcki and Monsoon lead to widespread reef destruction.
tastrea annularis) where temperatures were
Bleaching occurs when symbiotic algae high but ultraviolet penetration would have
(zooxanthellae) are lost from the gastroder- been comparatively low. This does not rule
mal tissues of a host organism (corals, out the possibility that increased ultraviolet,
anemones, zoanthids, octocorals, etc.), even at low levels, could enhance bleaching
sometimes accompanied by loss of host gas- of corals not normally exposed to much
trodermal cells (Muscatine et ai, 1993). This ultraviolet light. In a recent series of detailed
phenomenon can occur as a response to high experiments, Glynn et ai (1993) tested the
temperature, low temperature, high ultra- effects of ultraviolet radiation and temperviolet light, and several other stimuli (Glynn ature on two Pacific coral species, finding
et ai, 1993; Hoegh-Guldberg et ai, 1987; that temperature alone (30 and 31°C) had
Lesser et ai, 1990). Recent studies have significant bleaching effects and that added
sist under such conditions. Habitat alterations that increase sedimentation, or reduce
flow (breakwaters, coastal modification,
eutrophication) can thus have negative
effects on coral growth and diversity. At the
other extreme, violent water motion during
storms can totally change the composition
of coral assemblages, with effects lasting
many decades (Woodley et ai, 1981).
CORAL REEF BIODIVERSITY
ultraviolet increased the effect, but that
ultraviolet alone did not cause the corals to
bleach. Partially bleached corals generally
recovered in these experiments whereas
many of the fully bleached colonies died.
Are the mass bleaching events a "signal"
that global warming has progressed to the
point where certain species face local extinction (Glynn and de Weerdt, 1991) and major
marine habitats are being degraded? It is
impossible to answer this question at present. The increase in carbon dioxide in the
atmosphere is well documented (Dickinson
and Cicerone, 1986; Gates et ai, 1992), yet
the predicted increase in mean air temperature has been harder to confirm, even
though a clear signal exists for some localities. This measurement is confounded by
the heating effect of spreading urban areas,
where many sensors are located, and by the
unreliability of old data sets. For sea surface
temperature, it is even more difficult to
demonstrate a trend, and there is no evidence at present for an increasing mean
temperature in the Caribbean over the past
decades or century. Despite the lack of firm
data, the mechanistic model (Greenhouse
Model) predicts that increasing carbon
dioxide (already substantial) will eventually
cause higher temperatures. The idea that
bleaching episodes could act as a "signal"
of global warming was tested recently by a
model where the increase in temperature
over a period of decades and the ability to
detect the "signal" (bleaching) were varied
(Ware, 1992). If, indeed, we have not missed
detecting any mass bleachings over the past
half century, and have picked up three clear
events in the late 1980s and 1990, such a
signal could theoretically be a significant
indicator of a period of slowly increasing
mean temperature and thus higher annual
maxima. This model predicts that, if warming is real, such a signal will be highly significant in approximately another two
decades.
What will happen to reefs if sea surface
temperatures actually do increase, as predicted by the Greenhouse Model? Corals
have faced periods of rapid temperature
change many times over geological history,
and some species are likely to adapt whereas
others will become more restricted in geo-
123
FIG. 5. An example of a structurally diverse Acropora
cervicornis stand typical of Caribbean reefs at mid
depths (above). This zone of reefs along the north coast
of Jamaica was destroyed by hurricanes followed by
the sea urchin die-off, leaving a pavement of A. cervicornis fragments (below) with heavy algal growth.
graphic range. From recent events, it is clear
that susceptibility to bleaching differs among
species, with some of the common species
showing no response at all so far. Some of
the most common species on Caribbean
reefs, Montastrea annularis, Agaricia
lamarcki, Porites porites, as examples, have
been severely affected. Other common species, such as Acropora cervicornis and A. palmata, have suffered high local mortality
from the "band" diseases over the past
decade at many sites in the Caribbean
124
KENNETH P. SEBENS
FIG. 6. Examples of severely bleached corals, Montastrea annularis (above) and Agaricia lainarcki (below) in
Jamaica (1988). Most colonies of the former species survived whereas a large number of the latter species died,
especially after suffering two or three bleachings.
CORAL REEF BIODIVERSITY
125
FIG. 7. A fish trap in Jamaica. Note the small mesh size and the size of fish trapped.
(Edmunds, 1991), although this is not clearly
linked to temperature as far as is known.
Continued loss of these important structural
and reef-accreting species will certainly
change the character of Caribbean reefs.
Already, Jamaica and similar localities provide a model of what the future may hold.
The combined effects of two hurricanes (Fig.
5), massive algal overgrowth, heavy overfishing, and three bleaching events have
produced reefs of severely depleted coral
cover, high algal abundance and reduced
structural heterogeneity (Hughes, 1989;
Liddell and Ohlhorst, 1993). Even stormrelated damage could become worse with
global warming, since the severity and frequency of hurricanes and other tropical
storms are expected to increase.
The bleaching events since 1987 appear
to have been worse on Caribbean reefs than
in other parts of the world. This might be
explained by the small geographic area of
the Caribbean. Also, the Caribbean is well
north of the equator and corals are probably
adapted to generally lower temperatures
including temporary periods of much colder
water along the northern limits of coral distribution. The small area and close connections between islands in the Caribbean may
also make disease effects more severe as well,
as in the case of the urchin (Diadema) dieoff which spread from the southern Caribbean throughout the region in less than a
year (Lessios, 1988). The Pacific is so large,
and some island groups so small, that it may
be hard for a substantial patch of water to
warm up sufficiently to cause bleaching.
However, just such an event happened in
Tahiti and Moorea in 1991. This bleaching
corresponded to a period of low winds, very
still water and high sea temperatures. Tahiti
is located at a site where water movement
generated by tides is minimal; without wind
forcing, water can sit and warm up substantially. The high temperatures caused by
ENSO events, by contrast, are restricted to
126
KENNETH P. SEBENS
the eastern Pacific, but affect areas far to the
north and south of the equator. Bleaching
events along the Australian coast, on the
other hand, have been linked to localized
low temperature events. Extensive events
comparable in geographic extent to those in
the Caribbean have not been observed in
the Indo-Pacific region to date.
CROWN OF THORNS AND CROWDS OF
TOURISTS
was as follows: High rainfall during storms
causes massive runoff from high islands and
decreases local salinity in surrounding
lagoonal and backreef areas. The low salinity triggers spawning by Acanthaster already
present at low population density, and the
runoff carries nutrients which enhance local
phytoplankton growth, providing better food
and growth conditions for Acanthaster larvae. The juvenile starfish that result remain
hidden within reef cavities for about three
years, at which time they are large enough
to avoid most predators and emerge onto
open reef surfaces. They then become visible to casual observers and begin to consume massive amounts of coral tissue.
Low islands and atolls lack the land surface to produce substantial runoff (and
nutrients), are less likely to experience significant local salinity reductions, and therefore never experience the outbreaks. The
critical anthropogenic factor is forest clearing on high islands, and fertilizer addition
to fields, making runoff worse and the nutrient input higher. This could increase the
probability of a large outbreak of Acanthaster. Other human activities may also
affect the severity of outbreaks, including
removal of natural predators such as "Triton shell" gastropods and certain fish
(reviewed in Birkeland and Lucas, 1990).
This theory seems to apply well to the scattered islands of the Pacific, but not to the
Great Barrier Reef of Australia where outbreaks are common and where they move
in waves from north to south as larvae produced on one reef are advected southward
to continue the march (Moran et ai, 1988).
Recent research on Acanthaster larvae indicates that abnormally high phytoplankton
concentrations are not necessary for their
survival (Olson, 1987), but does not change
the overall pattern of outbreaks identified
by Birkeland. There may be some other
aspect of low salinity or high runoff that
causes high recruitment, such as spawning
synchrony and enhanced probability of fertilization, or modified coastal circulation
patterns that retain larvae.
Should fires be allowed to burn in national
parks, or should they be controlled to preserve "climax" (incorrectly termed "equilibrium") communities? This has been a
hotly debated question for managers of terrestrial forest communities. The best marine
example of the same debate comes from the
spread of Crown of Thorns seastars (starfish) (Acanthaster planci) on coral reefs of
the Indo-Pacific. In the 1960s, researchers
in Australia observed massive outbreaks of
this predatory echinoderm, and noted
almost complete denudation of live coral in
reef areas where outbreaks occurred
(reviewed in Birkeland and Lucas, 1990).
The immediate fears were that major areas
of living coral reef would be destroyed, taking centuries to recover, and that this was
an unprecedented event somehow connected to human activity. The first fear has
been confirmed numerous times as outbreaks have been studied throughout the
Pacific, although the spatial extent of outbreaks has been limited and the recovery
from major damage can be more rapid than
originally predicted (Colgan, 1987).
Evidence that Acanthaster outbreaks are
caused by human activity is circumstantial
at present, although there is plenty of evidence that outbreaks of this species have
occurred episodically for hundreds of years
in areas where human perturbations have
been minimal (reviewed in Birkeland and
Lucas, 1990). The most persuasive explanation for outbreaks comes from Birkeland
(1982) who noted an amazing pattern of
outbreaks occurring only around high islands
in Micronesia, never on atolls. A second
correlation placed outbreaks three years after
When the first major Crown-of-Thorns
major tropical storms (typhoons), and was outbreaks occurred, recovery was predicted
even used to predict the next one correctly. to take many decades, probably more than
Birkeland's explanation for these patterns a century. Grigg and Maragos (1974) exam-
CORAL REEF BIODIVERSITY
ined lava flows of known age around the
island of Hawaii and determined that it
would take that long to develop a fully
diverse coral community following complete denudation. However, even very severe
Acanthaster outbreaks leave some corals in
their wake, especially in the shallow "surf
zone" where the sea stars have difficulty
feeding. Colgan (1987), working on reefs on
the island of Guam, found substantial
recovery of denuded reefs only 15 years after
a major outbreak. We know that many reef
corals are hundreds of years old and form
massive colonies, yet it appears that coral
reefs can develop high cover and normal
diversity in a few decades. Is this a paradox?
Probably not, just an illustration of the successional processes that occur on reefs. Colonization occurs first by rapidly growing
"opportunistic" species that cover reef rock
quickly and produce what looks like a very
healthy reef. Slower growing species are generally also slow to recruit and do, in fact,
take centuries to reach their full size and to
replace some of the earlier colonists. A goodlooking diverse reef can thus develop in a
few decades, but it is not equivalent to the
pre-disturbance "climax" condition because
it lacks the larger colonies of long-lived species.
Should reefs be managed by removing
Acanthaster? First, it is a difficult and very
expensive task to remove enough of the
seastars to actually prevent major coral
damage. Over a large geographic area, some
reefs will be severely damaged, others will
be recovering, and yet others will be undamaged for many decades and will have essentially intact coral assemblages. This pattern
has characterized Australia's Great Barrier
Reef even though several waves of Acanthaster outbreaks have gone through the reefs
in the past three decades. However, when
there is a particular reef that is of great interest to a local tourist industry, intervention
may be worthwhile. For example, if there
is an island close to a major tourist area and
it has excellent reefs, it may be worth the
effort of preventing extreme damage during
an outbreak. This is partly an economic
decision, but it has major conservation consequences. If enough people get excited by
seeing one well-preserved and heavily vis-
127
ited reef, these same people are likely to be
proponents of reef conservation in the future.
POPULATION AND POLLUTION
Coral reefs located near areas of high population density have suffered worse than
those in isolated regions with small populations, based on observations and historical information, although the data on which
to base this claim are generally unavailable
or have not been collected using comparable
methods (Wilkinson, 1993). Nonetheless,
heavy fishing pressure, harvesting of coral
and mollusks, and the effects of coastal pollution are all much higher near population
centers. The pollutants that affect reefs
include oil spills (Loya and Rinkevich,
1980), heavy metal concentrations from
industrial and mining sources, pesticides and
herbicides, high sediment loads, and
increased nutrient loading from sewage and
agricultural sources (Lapointe and Clark,
1992; LaPointe et al, 1993). Although there
are case studies of negative effects on corals
and reefs for all such pollutants, the most
widespread effects probably come from the
last category, as demonstrated for sewage
input into Kaneohe Bay in Hawaii (Banner,
1974; Smith et al., 1981), Barbados
(Tomascik and Sander, 1985) and Australia
(Bell, 1992). Increased nutrients (inorganic
and organic nitrogen and phosphorus compounds) may initially benefit corals, for
which they can be limiting to growth, but
these nutrients benefit macroalgae as well
and the latter have much higher tissue
growth rates. The result is algal overgrowth
and damage to existing corals and a reduction of surface area available for coral
recruitment (Fig. 4).
Recent studies along the Florida Keys reef
tract have demonstrated levels of certain
nutrients, chlorophyll, and turbidity in the
water column approximately three times the
usual values for reefs in less impacted areas
throughout the region (Lapointe and Clark,
1992; LaPointe et al., 1993). During the
same period, coral cover has decreased in
some localities (Dustan and Halas, 1987;
Porter and Meier, 1992), although coral
declines may also be linked to particular
disease events and high levels of human
activity on certain reefs. Eutrophication in
128
KENNETH P. SEBENS
the Florida Keys begins with sewage leaching into groundwater and moving laterally
through porous carbonate rock into the
many channels cut through the Keys. When
there is a large amount of freshwater input
after heavy rains, the water entering canals
can be severely hypoxic (<1 ppm O2), and
carries high nutrient loads.
The reefs in the Florida Keys are several
kilometers offshore, so pulses of high nutrient water must move through mangroves
and seagrass beds first, taking several days
to reach the reefs. The mangroves and
grasses act as a filter removing some nutrients, passing others through, and releasing
and transforming still others (LaPointe and
Clark, 1992). The net result is an enriched
phytoplankton standing crop and organic
detritus in the water column cutting down
light penetration and increasing the sediment load on corals and other sessile organisms. To these effects are added enhancement of algal growth and biomass, with
resultant negative effects on sessile invertebrates through overgrowth, abrasion, and
shading. High algal growth rates can support
high urchin population densities and, since
urchins are omnivores, increased rates of
urchin predation and incidental damage to
corals and other invertebrates.
FISHING THE FINAL FRONTIER
Diverse "unaltered" fish assemblages have
positive effects on corals and on reefs. Herbivorous fish remove benthic macroalgae
which compete for space with corals and
other invertebrates (Hay, 1984; Hay and
Taylor, 1985; Neudecker, 1977), and large
schools of herbivores periodically destroy
damselfish "gardens" (Robertson et al,
1976) in which algal biomass is high and
coral survival is usually poor. Schooling fish
which take shelter in coral heads can increase
the growth rate of those corals by supplying
nitrogenous waste products (Meyer et al,
1983), which can be limiting to the growth
of algae and corals in oligotrophic tropical
seas. Large predatory fish also control populations of benthic invertebrates, and of
smaller reef fish, thus potentially enhancing
diversity of both groups by limiting competitive dominants.
The physical structure of coral reefs can
enhance fish diversity by providing physical
refuges from predators, microhabitat differences, and numerous sites for recruitment.
Although the expected relationship is an
increase of fish diversity with structural
complexity, not all studies of natural reefs
have demonstrated a strong correlation
(Sale, 1991). At scales of tens to hundreds
of meters, reef fish are segregated more or
less predictably by habitat and over depth
zones (Goldman and Talbot, 1976). At
smaller scales, however, there is some evidence that only certain fish guilds subdivide
the reef by physically or biologically different microhabitats (e.g., anemones as habitat
for anemonefish, branching corals versus
mounding forms). Experimental work has
demonstrated a "lottery" effect for other
guilds; when a resident damselfish is
removed, for example, the fish that replaces
it is not necessarily of the same species, nor
is the replacement predictable (Sale, 1977).
Live coral cover appears to be important
for high fish diversity (Bell and Galzin,
1984). Simplification of reef structure
through direct damage, increased bioerosion, and reduced coral growth all lead to a
lack of branching structures, filling of holes,
and a general increase in habitat similarity.
These modifications reduce the number of
fish that can find refuge, the number of distinct habitat types, and probably the suitability of settlement sites for the larvae of
particular species. Experiments with artificial reefs have amply demonstrated the
importance of physical habitat architecture
(variety of shelter sizes) in attracting fish
and maintaining diverse assemblages,
although factors such as reef size and location may be even more critical (Bohnsack,
1991).
Two forms of intensive fishing threaten
coral reefs, their fish populations, and the
species controlled by interactions with fish.
The first is subsistence fishing in areas of
relatively high human population density.
This includes the provision of fish for fishermen's own families, for sale to other locals,
and for sale to hotels and restaurants catering to tourists. A prime example is the
intensive trap fishing (Fig. 7) and spear fishing as practiced in Haiti (Ferry and Kohler,
1987) and Jamaica (Koslow et al, 1988),
CORAL REEF BIODIVERSITY
which is carried out almost completely in
reef habitats, and results in the harvesting
of all fish and mobile invertebrates that cannot escape through chicken-wire a few centimeters in mesh size. On reefs along the
north coast of Jamaica, it is quite common
never to see a fish over about 30 cm length
in an hour of diving (also in Haiti: Ferry
and Kohler, 1987). Every community along
the coast of Jamaica practices this type of
fishing, with obvious results to the reef fish
populations (Munro et ah, 1987), and less
obvious effects on the reefs themselves.
Overfishing has definite effects on the rest
of the reef community. The epidemic
destruction of Caribbean sea urchin (Diadema antillarum) populations in 1983 (Lessios, 1988), combined with the low numbers
of herbivorous fishes remaining on Jamaican reefs, led to a particularly severe growth
of benthic algae (Hughes et ai, 1987). This
threatens the survival and recruitment of
corals and has slowed the recovery of these
reefs from hurricane damage in 1980 and
1988(LiddellandOhlhorst, 1993). Recently,
protected zones in which fishing is not
allowed have been established in areas, such
as Montego Bay, which benefit from diving
tourism. However, such areas have been in
existence only a few years and the overall
effects are not yet known. In the Florida
Keys, protection of reef fish from spear fishing had rapid positive effects on fish populations (Bohnsack, 1982).
The nearest island group to the west of
Jamaica is the Cayman Islands, just over
100 km away. This group of small islands
has a low population density, and has had
protected reefs for at least a decade. Fishing
has not had the decimating effect on these
reefs that is so evident in Jamaica, and the
Cayman Islands are one of the prime destinations for diving tourism in the Caribbean. In 1988, I had the chance to take a
university class to Jamaica and to the Cayman Islands where we sampled coral and
fish populations. The contrast was remarkable. On every dive in the Cayman Islands,
we observed numerous large grouper, snapper, and other fish rarely seen on our dives
in Jamaica. We observed that coral cover
was much higher and algal cover much lower
here than in Jamaica. This may be due partly
129
to the lesser effect of both recent hurricanes
on the Cayman Islands, but is probably also
an effect of the more "normal" fish assemblages. The same pattern was seen when
coastal fish populations were compared to
those on the Pedro Bank southwest of
Jamaica (Koslow et ai, 1988).
The second type of fishery affects even
the most remote and underpopulated reefs
of the central Pacific and the rest of the
world. This is export fishing of both reef
and offshore species for shipment to developed countries, often by airplane, soon after
they are caught. This type of fishery has
become popular in areas where, even
recently, there was no threat of local overfishing for subsistence, and where the ratio
of people to reef area was so low as to prevent significant negative impact onfishpopulations. With the strong economic incentives supplied by developed countries, every
source of harvestable fish and shellfish is
being explored and in many cases is already
overexploited (Russ, 1991; Russ and Alcala,
1989). Where once there was some hope
that distance and low human population
density would protect certain reefs, now even
those areas are at great risk.
Management of coastal fisheries is certainly the only viable way to prevent decimation of a local fish fauna and ensuing
changes to the reef communities. Such management can take the form of limits on trap
sizes, numbers and mesh size, limits to catch,
and limits to areas fished. One intriguing
proposal (Randall, 1982) holds that refuge
areas, where all fishing is prevented, can
provide a number of immediate benefits.
First, such areas will be of great interest to
diving and snorkeling tourists, who admire
the beautiful coral and invertebrates but who
spend much of their time fish-watching and
photographing fish. The tourist industry also
provides jobs for guides and boat operators,
who might alternatively add to the local
fishing pressure. Second, such refugia provide a source offish that can grow large then
migrate out into adjacent fished areas. Ferry
and Kohler (1987) stress that providing
improved fishing methods and gear for offshore fishing may reduce fishing pressure on
reefs because the fish available offshore are
larger and of greater value. However, this
130
KENNETH P. SEBENS
approach could also result in the formation
of two groups of fishermen, each exploiting
its target habitat to the maximum.
A major limitation to reef fish populations is recruitment from distant locations,
which can be highly variable in space and
time (Doherty, 1987; Doherty and Williams, 1988; Sale, 1991, review), followed
by local survival to adult size. This is
especially limiting on isolated islands hundreds of kilometers from a source of larvae.
Refugia from fishing provide areas where
these processes can be enhanced. For species with locally generated offspring, refugia
also provide a local breeding stock, and better recruitment to adjacent areas. Lobel and
Robinson (1986), for example, described a
situation where larvae produced by reef
fish on the island of Hawaii were trapped
in large offshore eddies and passively
returned to the coast to settle. Local success
and the resultant crowding of adults in refuges will again result in migration of large
fish out of the refuge area. Finally, the primary reason that protected areas (parks or
conservation areas) should be encouraged is
that this is the most conservative option in
a system where the effects of each alternative type of management are poorly understood. Many of the countries experiencing
overfishing problems also have few resources
to enforce limits and gear restrictions. Completely protected areas, spread out along a
coastline, are relatively easy to manage and
to observe. Locals benefitting from increased
tourism, including tour operators and diving concerns, can be expected to assist in
the process of discouraging illegal use of
protected areas. Therefore, the establishment of such areas is probably the quickest
and best first step any country can take to
ensure the continuation of its fishery and
the preservation of its reefs.
THE FUTURE: FAR FROM PERFECT
It is hard to be optimistic about the future
of the world's coral reefs. At present, humaninduced changes have already caused major
reef deterioration, especially near dense
population centers. The combined effects of
pollution and exploitation have altered the
species assemblages present on such reefs,
and have affected the reef framework itself
in many regions. Added to the obvious
localized effects, the effects of global warming could include local or regional loss of
species abundance and diversity due to differences in thermal tolerance, loss of species
and reef framework from increased storm
frequency or severity, and submergence of
some reefs by rising sea level. The forces
that will produce such widespread change
are already in motion and cannot be stopped
over the short term. If the present increase
in carbon dioxide has indeed caused a long
term warming trend, and if the general
aspects of the Greenhouse Theory are correct, the first results will be evident in the
next several decades. Although we can slow
the rate of increase, there is no foreseeable
way to reverse the trend in carbon dioxide
concentration in the atmosphere and in its
effects on global temperature fast enough to
avoid its effects on ecosystems.
At a practical level, there are many things
that can be done to alleviate human-induced
effects on particular reefs and reef systems.
Decreasing the input of organic and inorganic nutrients that cause eutrophication is
an obvious improvement that can happen
within a decade or even in a few years following construction of adequate treatment
facilities. Managing fisheries such that at
least some reefs in each geographic area can
attain their full complement of species and
population size structure again is another.
Prevention of physical damage to heavily
visited reefs by permitting, placing fixed
moorings, and regulating visitor density and
activity are also positive ways to reduce
impact on particular reefs.
Coral reefs, in common with other complex communities, are changing on all time
scales. In ecological time (decades, centuries) any particular reef is being disturbed
or is at some stage of recovery from a large
past disturbance (hurricane, Crown-ofThorns outbreak, over-harvesting) and can
thus be expected to change its species abundances as it follows a successional sequence,
then to change again after another disturbance. Over longer time periods (geological,
evolutionary time), reefs respond to temperature and to sea level changes, and speciation occurs as an adaptation to local conditions or as a result of physical and
CORAL REEF BIODIVERSITY
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