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The future of Coral reefs in an age of global change

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Coral reefs are the only ecosystem that is strongly defined by a geological component - most definitions require that the biological community produces its own build-up of calcium carbonate. In terms of "reef-building," the geological record reveals that coral reefs have flourished over the past few million years, particularly during interglacial periods. Based on our observations of modern-day reefs, which are limited to the past few centuries, we tend to link "coral reef health" to carbonate production; however, reef ecosystems face future global-scale environmental changes that may decrease their reef-building capacity. In contrast to past discussions of the factors which determine reef-building potential by a coral reef community, the essential question that arises from this review is: How important is reef building to a coral reef community?
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Int J Earth Sciences (Geol Rundsch) (2001) 90 : 426±437
DOI 10.1007/s005310000125
Joan A. Kleypas ´ Robert W. Buddemeier
Jean-Pierre Gattuso
The future of coral reefs in an age of global change
Received: 15 October 1999 / Accepted: 10 July 2000 / Published online: 18 October 2000
Springer-Verlag 2000
Abstract Coral reefs are the only ecosystem that is
strongly defined by a geological component ± most
definitions require that the biological community
produces its own build-up of calcium carbonate. In
terms of ªreef-building,º the geological record reveals
that coral reefs have flourished over the past few mil-
lion years, particularly during interglacial periods.
Based on our observations of modern-day reefs, which
are limited to the past few centuries, we tend to link
ªcoral reef healthº to carbonate production; however,
reef ecosystems face future global-scale environmental
changes that may decrease their reef-building capacity.
In contrast to past discussions of the factors which
determine reef-building potential by a coral reef com-
munity, the essential question that arises from this
review is: How important is reef building to a coral
reef community?
Keywords Coral reef ´ Global change ´ Calcium
carbonate ´ Saturation state ´ Temperature ´ CO
Coral reefs are threatened directly at local and
regional scales by many human activities, including
over-harvesting, deforestation, and general decline of
coastal environments due to increasing population
pressures. Over geological time, reefs have also been
affected by global scale changes in seawater chemistry,
temperature, and sea-level fluctuations. Of these
three, global changes in both seawater chemistry and
temperature will probably have the most profound
impacts on coral reefs within the next century.
In this paper we examine current definitions
applied to reefs of the past as well as to those of the
present. We then examine the implications of applying
such definitions to coral reefs of the future.
Past and present views of coral reefs
ªC'est une merveille de voir chacun de ces atollons,
environnØ d'un grand banc de pierre tout autour, n'y
ayant point d'artifice humain.º
ªIt is wonderful to see each of the atolls completely
surrounded by a great bank of stone, of no human
construction.º François Pyrard de Laval (1605) as
quoted by Darwin (1842)
Early references to reefs reveal fascination with the
reef structure. The foregoing quotation by Pyrard de
Laval reflects the natural curiosity of early explorers
about the origins of the ªgreat banks of stoneº. Such
fascination was due partly to the fact that so few
Europeans, who provided the first records of coral
reefs, had seen coral reefs before.
Humans continue to focus on the rock component
of reefs for several reasons. One is that coral reefs
pose a major threat to navigation. Indeed, the term
ªreefº was originally defined as a navigational hazard,
and ªcoral reefº was merely a navigational hazard
with corals on it. Another reason is that many of the
early reef researchers concentrated on the reef struc-
ture. Darwin (1842) was certainly preoccupied with
just how reefs formed, as was Dana (1872), and many
others of the present century (Yonge 1930; Steers
1937; Stoddart et al. 1978). Davis (1928) exemplified
the geologist's attitude in the following:
J. A. Kleypas (
Oceanography Section, National Center for Atmospheric
Research, P.O. Box 3000, Boulder, CO 80307, USA
Phone: +11-303-4971316
Fax: +11-303-4971700
R. W. Buddemeier
Kansas Geological Survey, University of Kansas, Lawrence,
KS 66047, USA
J.-P. Gattuso
Observatoire OcØanologique, ESA 7076 CNRS-UPMC, B.P. 28,
06234 Villefranche-sur-mer Cedex, France
The biology and especially the symbiosis of the
reefs are unquestionably important subjects in
themselves, but the opportunity for the establish-
ment and growth of reefs is so largely determined
by the physiographic conditions of insular and
continental coasts, over which reef-building organ-
isms have no control that those physiographic con-
ditions necessarily assume the leading role in the
problem [i.e., the ªcoral reefº problem] under dis-
Economic geologists enhanced the focus on reefs
when it became clear that ancient reef deposits were
associated with vast oil reserves (Chapman 1977).
Geologists naturally focus on reef structures because
of their prominence in the geological record, and
because they provide us with the materials necessary
for studying past environments. To non-geologists,
reefs have long been recognized for their role in
shoreline protection and for their physical complexity
which promotes high biodiversity and gross productivi-
Only in the past century has thinking about coral
reefs shifted to an ecosystem perspective, similar to
the way a rainforest is viewed. Reefs are certainly rec-
ognized as complex ecosystems with both biological
and geological features, and it is difficult to address
reef ecosystems separately from their geological
nature. Several papers in the 1970s and 1980s reflected
the struggle with defining a coral reef (Heckel 1974;
Preobrazhensky 1977; Hubbard 1985; Buddemeier and
Hopley 1988), and biologists and geologists still
appear to favor slightly different definitions: geologists
refer to reefs as ªsedimentary systemsº (James 1983),
whereas biologists focus on the organisms that build
and/or reside on reefs. Fagerstrom (1997) and Wood
(1998, 1999) provide linkages between the two by
emphasizing the importance of framework builders in
the definition of fossil reefs: an emphasis which is
based on an ecological concept of benthic organism
and community function, and which relates to the ªge-
ologicalº features of in situ production, topography,
and wave resistance (Table 1).
The bio/geo definition of coral reef is confounded
at those ªmarginal reefº areas where reef-building
communities occur and appear to function ecologically
as reefs, but have not produced a coral reef structure.
Buddemeier and Hopley (1988) addressed this dichot-
omy by implying that all coral reef communities have
the capacity to build reefs, but the surrounding envi-
ronment ultimately determines whether these com-
munities will ªturn onº or ªturn offº in terms of reef
building. Drowned reefs, or ªgive-upº reefs (a geologi-
cal term coined by Neumann and Macintyre 1985) are
one example where changing environmental con-
ditions (e.g., the decrease in light levels due to sea-
level rise) turned off carbonate production. Budde-
meier and Hopley (1988) also distinguished between
ªcoral reef,º a sedimentary structure produced by a
living coral reef community; ªcoral reef communityº,
which has the potential for reef production; and ªcoral
communityº which does not have that potential. This
convention has been adopted in recent coral reef clas-
sifications such as in ReefBase (McManus and Ver-
gara 1998), which attempts to distinguish between
coral reefs (which have underlying reef structure) and
ªnon-reef building coral communities.º
Components of a definition of ªcoral reefº
Most recent definitions of ªcoral reefº (or when
ªreefº or ªorganic reefº implies a coral reef) include
both biological and geological components, and occa-
sionally include environmental requirements (Ta-
ble 1). It is obvious that the concept has evolved from
its navigational application to a more scientific one,
but not to any single consensus definition.
Table 1 Key words found in ªcoral reefº definitions
Category Key words References
Biological features P Organic, biogenic 2±4, 6, 7, 9, 11, 17, 18, 20
(ªcoral communityº) P Interlocking coral and algal colonies (framework) 1, 4, 9, 12, 19
P Mostly ªhermatypicº corals and algae and other sessile organisms 1, 6, 9, 12, 15, 16, 17
Geological features (ªreefº) P Carbonate 2, 3, 6, 7, 16, 17, 18, 20
P In situ buildup 2, 3, 7, 15±17, 19, 20
P Topographic relief 2, 3, 7, 10, 12, 16, 18
P Wave resistant 1, 4, 6, 10, 12, 13, 17
P Cemented/consolidated 8, 9, 12, 13, 19
Environmental requirements P Marine 9, 17
P Warm (tropical) 9, 19
P Well lit 9
Other P Navigational hazard 4, 5, 8, 12, 13
1 Weyl (1970); 2 Braithwaite (1973); 3 Heckel (1974); 4 Davis
(1977); 5 Gross (1977); 6 Ross (1977); 7 Longman (1981); 8
Thurman (1981); 9 Levinton (1982); 10 Schumacher and
Zibrowius (1985); 11 Fagerstrom (1987); 12 Stowe (1987); 13
Gross (1987); 14 Scoffin (1987); 15 Buddemeier and Hopley
(1988); 16 Riding (1989); 17 Achituv and Dubinsky (1990); 18
Wright and Burchette (1996); 19 Beer (1997); 20 Wood (1999)
The most striking feature borne out by Table 1 is
the emphasis on geological terms. No other ecosystem
definition has such a strong geological component.
Certainly no terrestrial ecosystem is so heavily defined
by geology. A few other marine ecosystems do
produce rock or sediments, but the geological require-
ments are not an essential component in the definition
of that ecosystem. For example, some temperate
neritic shelf communities produce carbonate accumu-
lations at rates that rival those of coral reef systems
(Smith 1972; MignØ et al. 1998); however, the shelf
ecosystems that produce these carbonates are not
intrinsically dependent on the shelf deposits. Similarly,
deep-sea carbonate oozes are formed by planktonic
ecosystems of various carbonate-secreting organisms
(e.g., coccolithophores, pteropods). The formation of
carbonate oozes, however, is a consequence of the
planktonic community, and there is no requirement
that the calcium carbonate deposit is even formed
(and indeed it does not accumulate in waters below
the calcium carbonate compensation depth); nor do
the carbonate secretors depend on those deposits. The
component of coral reefs is somewhat analo-
gous to the amassing of woody material in old growth
forests (in the form of trees) or the build-up of peat in
peat bogs (L. Klinger, pers. commun.).
Whether a coral reef community actually builds a
reef or not depends on the balance of carbonate addi-
tion and carbonate loss. The degree of ªreefnessº is
often judged on how much accumulation has occurred,
i.e., the size of the reef; however, there are several
conceptual pitfalls underlying this view which are
identified herein.
Net CaCO
production is not simply a reflection of
how well the coral reef community produces CaCO
which can be defined (and converted to an approx-
imate potential accumulation rate) by the short-term
community calcification metabolism (Kinsey 1985;
Gattuso et al. 1999). Carbonate accumulation rep-
resents the net amount of carbonate that remains on a
particular reef (Chave et al. 1972; Stearn and Scoffin
1977), and might be represented by the following
equation, which is similar to that proposed by Eakin
Accumulation must exceed zero to meet the most
common geologically oriented definitions of a coral
reef. The local coral±algal community must be respon-
sible for most of the carbonate addition to a reef, with
some additional carbonate being added by other
organisms, or precipitated as cements. This is the ulti-
mate CaCO
production ± removing Ca
and CO
ions from the water column to secrete CaCO
erals (calcite and aragonite). On some reefs, however,
a portion of the carbonate accumulation may be
imported from elsewhere.
Physical removal of carbonate material from reefs
can be significant and sometimes associated with
biogeochemical processes. Rapid biological and
mechanical breakdown of reefs enhances the probabil-
ity that carbonate material will be exported from the
reef, and/or ultimately dissolved. Based on these reef-
controlling processes, we can thus look at export from
a carbonate budget perspective (Fig. 1). Reefs can be
classified based on the mechanisms that control their
net accumulation. Four basic reef or community types
are discussed herein, based on the dominant process
in their carbonate budgets.
Production-dominated reefs
Accumulation of biologically produced CaCO
by the
local community is the dominant process in produc-
tion-dominated reefs, and the carbonate budget
greatly exceeds 0. This is the most common type of
reef that we see presently, and it is considered the
ºnormalª reef.
Import-dominated reefs
On import-dominated reefs, much of the reef material
is not produced in situ by the coral community, but is
imported from elsewhere. The imported material may
be terrestrial or marine in origin, and may be either
carbonate or siliciclastics. Some fringing reefs owe sig-
nificant amounts of their net accumulation to
imported material. One example of these would be
the Cape Tribulation fringing reefs of Australia (Par-
tain and Hopley 1989). Here the reefs have developed
on terrigenous bars and deltaic lobes where rainforest
streams debouche into the Great Barrier Reef lagoon.
Other reefs may be developed on (or by) ridges of
storm-deposited rubble (Blanchon et al. 1997). These
reefs highlight the questions of spatial scale of def-
inition. The rubble in question normally comes from
the same reef system or a different part of the same
reef (e.g., forereef material deposited on the reef
crest), but was not produced or originally deposited in
its present location, nor by an antecedent of the reef
community presently growing on it.
Export-dominated reefs
An export-dominated reef community may have high
community calcification, but the produced material is
often removed by hydrodynamic forces (Hubbard et
al. 1991; Hubbard 1992). Hence these coral communi-
addition - CaCO
loss = Accumulation
Biological erosion ªReef growthº
Sediment import Mechanical erosion
Cementation Sediment export,
ties may be thriving as biological entities, but may not
construct or add to a geological reef, because so much
of the material is transported away. Hubbard et al.
(1990) determined that storms removed up to 50% of
reef calcification at St. Croix. In some instances,
export from one reef might become import to another;
on the same reef, material may be exported from the
highly productive shallow reef to its deeper, less pro-
ductive regions, or is relocated locally as shallow-
water storm deposits (see above). This category high-
lights the potential lack of congruence between a
reef's ecological health and function, and its geological
Bioerosion-dominated reefs
Bioerosion is a very important factor in carbonate
removal on reefs, because it causes or enhances both
physical and chemical breakdown (see review by
Hutchings 1986). In a bioerosion-dominated reef or
community, production is overwhelmed by the direct
and indirect (export) effects of bioerosion. Obviously,
this type of reef community is less likely to be pre-
served in the geological record, and they can be diffi-
cult to recognize, since framework organisms are often
reduced to sediment, and are rarely found in growth
position. There may well be bioerosional hiatuses in
the depositional record of reefs that are net construc-
tional over the long term. An example of this type of
reef would be post-1983 Galµpagos reefs. Galµpagos
corals were nearly wiped out on these reefs due to
ENSO related bleaching (Glynn 1984). Carbonate pro-
duction was therefore drastically reduced, whereas
bioerosion rates remained the same, or even increased
(Eakin 1996; Reaka-Kudla et al. 1996). Hence these
reefs experienced severe carbonate losses for several
years, until the coral community was eventually re-
Three of the foregoing process-based reef types
have geologically defined depositional structures. The
production-dominated reef would likely produce a
framework reef deposit; the bioerosion-dominated
reef would produce a detrital reef deposit; and the
import-dominated reef represents carbonate-clastic
reefs. The export-dominated reef is one which, despite
even high carbonate production, would fail to accumu-
late a reefal deposit.
Conceptually, assessing reef carbonate accumula-
tion by this approach is simple, but operationally it is
difficult. Direct measurement of net accumulation of a
living community is not practical since carbonate accu-
mulation is both spatially and temporally very heter-
ogeneous in reef environments, and because sedimen-
tary and dating techniques cannot resolve budgets at
the level of community turnover times. In lieu of such
measurements, a coral reef community that is posi-
tioned atop a late Holocene reef build-up is usually
considered a reef-building community, whereas one
that is not associated with a reef build-up is consid-
ered non-reef building.
The episodic nature of import, export and erosive
processes on coral reefs highlights an issue of tem-
poral scale. A given reef structure will probably not
be occupied continuously by the same type of (or in
some cases even by any) reef-building community on
timescales of years to decades (Aronson et al. 1998;
Done 1999). Yet, on timescales of centuries to millen-
Fig. 1 Reef types based on
the major controls on calcium
carbonate accumulation. See
text for discussion
nia, these reefs may appear to show quasi-continuous
growth with high accumulation rates (Opdyke and
Wilkinson 1993). Understanding reef-building proc-
esses can be confusing, since the temporal resolution
of geological observations tends to be coarser than the
temporal duration of real-time biological observations
(Buddemeier and Hopley 1988).
Present-day biases
ªLike obesity, a massive reef accumulation may be
the result of remaining stationary for too long under
good conditions.º Buddemeier and Kinzie (1998)
Even though reefs are often thought of as produc-
tion dominated, the foregoing statement that massive
reef accumulations represent something of a glut of
production portrays the idea that our present
vision of reefs is biased by present environmental con-
ditions. This suggestion is supported by both climatic
and geological history. Our current interglacial cli-
mate, which appears to be particularly favorable for
reef carbonate deposition and preservation, is repre-
sentative of only 10% of the past few million years
(Hay et al. 1997; Pearson and Palmer 2000). Based on
reconstructions of past CO
atmospheric concentra-
tions (Berner 1994, 1997), the currently low CO
centration is atypical for most of Earth's history.
Although there is evidence that corals control some of
the transport processes involved in calcification (see
review by Gattuso et al. 1999), both corals and reef-
building algae are classified as ªhypercalcifiers,º
organisms which have little internal control on calcifi-
cation so that the degree of their calcification tends to
reflect surrounding environmental conditions (Stanley
and Hardie 1998, 1999). These organisms therefore
form massive reef deposits when environmental con-
ditions are particularly favorable. Present-day coral
reefs, on which we base our definition, are not the
norm in reef ecosystems over geological timescales
(Wood 1999). If present-day reefs experience a drop
in CaCO
production, we can expect a decrease in net
reef accumulation. Carbonate production obviously
declines when CaCO
organisms are eliminated from
a reef, and less obviously if the coral/algal community
precipitates less CaCO
A coral reef community has the capacity for build-
ing a reef, but it is debatable whether reef building is
an obligatory function of reef communities, or merely
facultative. A common assumption is that coral reef
communities need to build reefs, because they
presently build reefs, and because we are biased by
the tendency of reefs to be preserved in the geological
record. Reef building is unquestionably an important
process, because it not only allows reefs to cope with
sea-level change (especially on atolls, where back-step-
ping would not be possible), it also creates the topo-
graphic complexity to allow for the many different
habitats that maintain reef diversity. But in many
ways coral communities function similarly to true
coral reefs (Harriott 1998, 1999), except that their car-
bonate budgets are closer to zero. In fact, if carbonate
budgets of reefs worldwide were available for compar-
ison, it is likely that non-reef coral communities are
presently more common than we think. This is
because we naturally expect to find non-reef coral
communities at higher latitudes, but we are less likely
to recognize a coral reef community as non-reef build-
ing when it occurs in the tropics. There is certainly
evidence that these exist. Many eastern Pacific reefs,
for example, are considered ªminimum examples of
coral reefsº (CortØs 1997), or non-reef coral communi-
ties (McManus and Vergara 1998).
Changing controls on coral reefs
Environmental changes are known to affect reef car-
bonate budgets. In the future, if total carbonate accu-
mulation on reefs is significantly reduced (by a
decrease in CaCO
production and/or an increase in
its removal), then production-dominated reefs will
shift to some other type of reef. The nature and mag-
nitude of this shift can be examined at the current
thresholds of reef development. The major variables
that control coral reef distribution are fairly well
understood (Kleypas 1997; Kleypas et al. 1999b), but
how these variables control carbonate accumulation is
not. Coral reef density declines rapidly at higher lati-
tudes, which is often attributed to increased competi-
tion with macroalgae, increased bioerosion rates, and
sharp reductions in reproductive ability (Hopley 1989).
Since the number of coral species declines rapidly
with increasing latitude, one might also assume that
carbonate production also declines at higher latitudes.
Although measured calcification rates on some high-
latitude coral communities are fairly high, at least dur-
ing the summer (Smith 1981; Johannes et al. 1983),
reduced carbonate production almost certainly plays a
role in the coral reef to non-reef coral community
transition at high latitude (Opdyke and Wilkinson
1993). The magnitude of this role becomes important
when one considers that biological carbonate produc-
tion is probably the carbonate budget element most
likely to change in response to future environmental
The variables that affect reef distribution operate
at different scales (Table 2). At the broadest spatial
scale, coral reefs obviously occur where warm sea-sur-
face temperatures (SST) predominate. Less obviously,
this is also where calcium carbonate saturation is the
highest, and where light availability is high and less
seasonal (Kleypas et al. 1999b). Salinity and nutrients
are certainly factors in determining reef distribution,
but both are relatively constant in the oceans, and
affect reef distribution locally to regionally, such as
near the mouths of large rivers, or at the scale of
upwelling. Human alteration of the nitrogen cycle has
greatly increased riverine transport of nitrogen to
estuaries and coastal zones (Vitousek et al. 1997;
Howarth 1998). This could have significant affects on
coastal reef ecosystems where nutrient fertilization
allows macroalgal competition for both space and
light, although the impacts of nitrogen increases on
open ocean systems are still poorly understood (Vitou-
sek et al. 1997). Storms do seem to limit certain coral
communities from developing reefs (Grigg 1998), and
some climate models predict a 10±20% increase in
maximum potential intensity of tropical cyclones
under doubled CO
conditions (Pittock 1999). How
such changes apply to the future of coral reefs is
unclear, but it is probably safe to say that future
changes in storm impacts will have only local or
regional effects. Sea-level change has the potential for
affecting reef distribution globally. Certainly there are
areas where reefs have failed to develop because
Holocene sea-level rise outpaced the rate of upward
reef growth, or where present upward growth is lim-
ited by a relatively static sea level; however, the pre-
dicted 0.4- to 0.6-m sea-level change over the next
century (Houghton et al. 1996) is two orders of mag-
nitude less than the 100+ m rise since last glacial max-
imum. This increase in sea level alone is not enough
to ªdrownº coral reefs, but the potential degradation
of water quality resulting from flooded coastlines
could certainly affect many coral reefs.
We address two major factors that may affect coral
reef distribution: temperature and calcium carbonate
saturation state. These are variables which affect reefs
at the global scale, and which correlate with their lati-
tudinal distribution. Although light is probably an im-
portant control on coral reefs, it is unlikely that solar
irradiance will change significantly as a consequence
of global change, although its relative importance as a
control on reef growth may change as both temper-
ature and saturation state change. We do not address
local to regional anthropogenic impacts, although we
recognize that direct human impacts collectively com-
prise the largest suite of threats to coral reefs.
Temperature has long been considered the main con-
trol on reef distribution. Sea-surface temperature is an
obvious variable that is easily measured, and for which
we have century-long records in many oceans. The
distribution of coral reefs and non-reef coral com-
munities (McManus and Vergara 1998) coincides well
with the 18 C monthly minimum isotherm (Fig. 2a), a
relationship which was originally pointed out by Vaug-
han (1919).
Coral reef distribution with respect to maximum
temperature is less clear. Based on the average
monthly SSTs derived from over a century of data
from ships (Fig. 2b), reefs do not appear to be limited
by average high temperatures. The increased and
widespread nature of coral bleaching events over the
past two decades is, however, convincingly correlated
with increases in maximum SST (of as little as a 1 C
increase above monthly maximum), often related to
large-scale ENSO events (Wilkinson 1998; Wilkinson
et al. 1999). Despite some evidence that corals exhibit
ªadaptive bleachingº (Buddemeier and Fautin 1993;
Rowan et al. 1997; Ware et al. 1996), over our present
scale of observation, the ability of corals to adapt to
such increases in SST has not been illustrated (Hoegh-
Goldberg 1999). Coral bleaching events have the
capacity to eliminate more than 90% of coral on a
reef (Glynn 1984; Wilkinson et al. 1999). If coral
bleaching is indeed a response to increased temper-
ature, then future increases in SST could potentially
eliminate many of those reefs where SST maxima are
increased. Note that this requires only an increase in
SST extremes, and not necessarily in SST averages. In
contrast, conventional wisdom predicts that, if reefs
are limited by low SSTs, then a general global warm-
ing will allow their colonization into higher latitudes.
Such poleward extension of coral reefs has occurred in
the past, e.g., among coral reefs of Japan (Veron
Table 2 Summary of some of the major environmental variables that determine the distribution of coral reefs. NA not applicable
Variable Scale Future change
Temperature Global Presently changing?
Saturation state Global Presently changing
Light Global±regional Not significant
Salinity Local Not significant
Nutrients Global increase in river inputs of N; local±regional (upwelling; pollution) Presently changing
Storms Local±regional ?
Sea level Global Approximately 1 m?
Coral/algal diversity Local±regional ?
Competition with algae Local±regional (scale of upwelling/runoff) ?
Substrate Local NA
Sea-level history Global NA
Calcium carbonate saturation state
Calcium carbonate saturation state (O) is defined by
the equation:
; 1
where K9
is the stoichiometric solubility product for a
particular mineral phase (cal: calcite; arag: aragonite;
hmc: high-magnesium calcite). Values of O less than
1.0 indicate undersaturation; those greater than 1.0
indicate supersaturation. In seawater, [Ca
] is approx-
imately 100 times that of [CO
] and is a near-conser-
vative element of seawater over 10
years. O is thus
largely determined by [CO
]. The K9
constants are
temperature-, salinity-, and pressure dependent. Tropi-
cal surface waters are supersaturated with respect to
all mineral phases, but the degree of saturation varies
with mineral phase: O-calc is 5±6, O-arag is 3±4, and
O-hmc is 2±3.
Calcium carbonate saturation state has only
recently been considered a control on reef growth.
This is partly due to the previous assumption that,
because the tropical oceans are supersaturated with
respect to all calcium carbonate mineral phases (cal-
cite, aragonite, high-magnesium calcite), it is not limit-
ing to calcification. Initial calculations in the 1970s
erroneously indicated that the oceans would become
undersaturated with respect to calcium carbonate by
the year 2010, and that catastrophe would befall calci-
um-carbonate-secreting organisms (Fairhall 1973;
Zimen and Altenhein 1973). Later calculations which
took into account the strongly buffered carbonate sys-
tem in seawater showed that undersaturation would
occur only with a tenfold increase in atmospheric
(Whitfield 1974; Skirrow and Whitfield 1975).
Since then, ocean-surface measurements have shown
that some ocean regions may indeed become undersat-
urated with respect to aragonite by the second half of
the 21st century (Feely et al. 1984). Yet because the
surface will remain supersaturated even under the
worst-case scenarios of the Intergovernmental Panel
on Climate Change (IPCC), there has been little con-
cern that increases in atmospheric CO
will affect
marine calcification.
Smith and Buddemeier (1992) suggested that even
in supersaturated conditions, changes in carbonate sat-
uration state could cause a decrease in calcification, a
shift toward calcite secretors, and/or a competitive
advantage for noncalcifying reef organisms. This sug-
gestion was experimentally tested in corals and coral
communities by Gattuso et al. (1998), Leclercq et al.
(2000), and Langdon et al. (2000). They illustrated
that the degree of supersaturation exerts a significant
control on calcification. A data compilation extended
that conclusion to other calcifying organisms such as
coralline algae (Gattuso et al. 1999). Kleypas et al.
(1999a) estimated how future increases in atmospheric
will alter the aragonite saturation state of shallow
tropical seas, and based on the calcification studies
cited previously, estimated how this will globally affect
reef calcification.
The oceanic carbon reservoir is an order of mag-
nitude larger than all other pools of exchangeable car-
bon combined. Ocean carbon chemistry is the culmi-
nation of processes acting over widely varying
timescales. Dissolved inorganic carbon (DIC) occurs
in three basic forms: CO
* (CO
), HCO
and CO
, and is primarily a product of weathering
(including dissolution of ocean carbonates, continental
carbonates, and silicates) acting over 10
While total DIC tends to remain constant, the relative
concentrations of its component species are subject to
Fig. 2 Distribution of coral
reefs and coral communities
superimposed on A minimum
and B maximum sea-surface
temperatures (from Levitus et
al. 1999). Solid black dots rep-
resent coral reefs, and dots
encircled in black represent
non-reef coral communities
change over much shorter periods. Under normal sea-
water conditions (pH=8.0±8.2), there is approximately
six to ten times more HCO
than CO
. When CO
dissolves in seawater, less than 1% remains as CO
most dissociates into HCO
and CO
, and the acid
formed by the dissolution of CO
in seawater lowers
the pH so that some of the CO
combines with H
to form HCO
. The concentrations of CO
*, HCO
and CO
in water can be adequately estimated given
temperature, salinity, and two of the measurable
parameters of the CO
system in water (total alkalini-
ty, DIC, pCO
, pH).
In its simplest form, the seawater-mediated inter-
action of carbon dioxide and calcium carbonate is rep-
resented by: 2 HCO
[ CO
Addition of CO
into the system enhances dissolution
of CaCO
and removal of CO
enhances its precipita-
tion (likewise, dissolution of CaCO
absorbs CO
, and
precipitation releases it). On timescales of
years, a balance between CaCO
dissolution on
land (weathering) and deposition in the ocean acts as
a stable negative feedback (called CaCO
sation) which maintains the concentration of CO
close to equilibrium values with CaCO
(Archer et al.
1997). On shorter timescales, addition of fossil fuel
perturbs the CO
concentration (Fig. 3).
Most of the present coral reef accumulation
occurred prior to the industrial revolution, when
atmospheric CO
levels were approximately 280 atm,
and SSTs were nearly the same as at present. Given
these values, one can estimate O for the surface ocean
Fig. 3 Relative concentrations of CO
, and CO
) vs pH, for average seawater with temper-
ature=28 C, salinity=35 psu, and alkalinity=2306 Eq kg
. The
lower bar represents approximate atmospheric pCO
levels (1
preindustrial; 2 twice preindustrial levels, etc.) that are needed
to effect the changes in surface seawater pH
Fig. 4 Aragonite saturation state estimates for A preindustrial
levels of atmospheric CO
(280 atm) and sea-surface temper-
atures (SSTs) equal to those of the present, and B a doubling of
and a uniform 2 C increase in SST. Solid black dots rep-
resent coral reefs, and dots encircled in black represent non-reef
coral communities. Aragonite saturation state was calculated
assuming the carbonate parameters of pCO
and total alkalinity
are known (pCO
of the surface ocean was assumed to be in
thermodynamic equilibrium with atmospheric concentration, and
alkalinity was assumed to be uniformly 2306 Eq kg
). Surface
ocean pCO
was adjusted using the air±sea pCO
differences of
Takahashi et al. (1997). Carbonate ion concentration was deter-
mined using the CO
solubility constant of Weiss (1974); the
dissociation constants of Dickson and Millero (1987); aver-
age surface temperature and salinity (Levitus 1994); and average
surface phosphate and nitrate (Levitus et al. 1993). Aragonite
saturation state was calculated using the K9
of Mucci (1983)
(Fig. 4). A conservative estimate of the preindustrial
O-arag value at the limits of Holocene coral reef
development is approximately 4.0.
Future impacts
Increased temperature and lower saturation state
Changes in temperature and CaCO
saturation state
are nearly certain to affect coral reefs over the next
few decades. The IPCC provided several projections
of atmospheric CO
changes into the next century
(Houghton et al. 1996); of which the most widely
accepted is a doubling of the pre-industrial pCO
the year 2065. Changes in SST are much more difficult
to predict, but most ocean models predict no more
than 1±2 C increase in tropical average SSTs under
doubled CO
To examine how an increase in SST might increase
coral reef expansion, the model ReefHab (Kleypas
1997) was used to estimate changes in potential reef
habitat. We assumed a uniform 2 C warming of SST
and assumed that reef growth was limited to depths
where irradiance was 200±300 mol m
. The pole-
ward shift in the 18 C isotherm resulted in a 2.5±3.5%
increase in potential reef habitat area (Fig. 5). This
value does not account for loss of habitat due to too-
warm temperatures, and assumes that reduced light at
higher latitudes is not a factor in reef development.
We contrasted this to the findings of Kleypas et al.
(1999a) who investigated how future changes in sat-
uration state will affect coral reef calcification. Under
doubled CO
conditions (and also assuming a uniform
2 C increase in SSTs), the saturation state of tropical
surface oceans will decrease approximately 30%, so
that few coral reefs will remain in waters having an
O-arag >4.0 (Fig. 5). Using compiled experimental
data on calcification vs saturation state (Gattuso et al.
1999), Kleypas et al. (1999a) determined that under
doubled CO
conditions, reef calcification rates will
decrease by 14±30% those of preindustrial levels. We
predict that this drop in reef carbonate production
will shift many reefs from net carbonate accumulation
to net carbonate loss. Here we assume that (a) in-
creases in SST will not increase calcification rates, and
(b) carbonate removal processes will remain constant.
The high latitudinal limits to reef development, at
the transition between coral reefs and coral communi-
ties, delineates that line between net accumulation
and net loss. Until there is better accounting of both
carbonate production and carbonate loss on reefs, and
how multiple factors such as temperature, light, and
saturation state affect coral calcification, we cannot
confidently estimate how many present-day reefs will
approach non-reef coral community status. We can
assume, however, that if carbonate production
decreases due to lowered saturation state, then this
line will migrate equatorward (Fig. 5), and those reefs
which already have a low surplus of carbonate produc-
tion will become non-reef coral communities.
Light, temperature and saturation state all appear
to exert control over reef formation (Kleypas 1999b).
To a first approximation the light-derived boundary
between reefs and non-reefs will remain stable, and
the saturation-state-derived boundary will move
equatorward; thus, it appears unlikely that a signifi-
cant expansion of reef area could result from warming
at higher latitudes. However, the range of coral com-
munities, as opposed to coral reefs, may remain stable
or even expand. This heightens the importance of
resolving the extent to which reef biology and geology
are interdependent.
Man's concept of a coral reef has evolved greatly over
the past few centuries, from one that focused on the
geological structure to one that highlights the inter-
dependency of biological and geological processes.
Our current definition is largely based on our observa-
Fig. 5 Comparison of areal
changes in the 18 C isotherm
vs the 4.0 ªiso-saturationº
between the preindustrial con-
ditions and those predicted for
the middle of next century
(doubled CO
and 2 C
increase in SST)
tions over the past few centuries ± a period when a
geologically and evolutionarily unusual set of environ-
mental conditions has favored reef building. The 21st
century will almost certainly experience dramatic envi-
ronmental changes. The process of predicting how
coral reefs will respond to these changes is shifting the
static address of ªcoral reefº to a more dynamic
address of ªcoral reef health.º Current definitions of
coral reef emphasize the geological component ± the
accumulation of a calcium carbonate structure. Since
carbonate production rates largely determine the cal-
cium carbonate budgets on reefs, and since carbonate
production is likely to decline in the future (either
through removal of reef builders through phenomena
such as bleaching, or through depressed calcification
rates), many coral reefs will probably shift to non-reef
coral communities. From the geological perspective,
we know that coral reef communities are important
for reef building. From the biological perspective, and
given a probable decrease in reef building in the
future, there is a strong need to fully assess how
important carbonate accumulation is to coral reef
communities over a range of environmental conditions
and timescales.
Acknowledgements This paper was first presented as a lecture
to the European Meeting of the International Society for Reef
Studies in September 1998. We thank M. Pichon for providing
both the opportunity to present this lecture, and the many help-
ful suggestions throughout its preparation. We also thank L.
Montaggioni, J. Marshall, and an anonymous reviewer for help-
ful comments.
Achituv Y, Dubinsky Z (1990) Evolution and zoogeography of
coral reefs. In: Dubinsky Z (ed) Ecosystems of the world, vol
25. Coral reefs. Elsevier, Amsterdam, pp 1±9
Aronson RB, Precht WF, Macintyre IG (1998) Extrinsic control
of species replacement on a Holocene reef in Belize: the role
of coral disease. Coral Reefs 17:223±230
Archer D, Kheshgi H, Maier-Reimer E (1997) Multiple time-
scales for neutralization of fossil fuel CO
. Geophys Res Lett
Beer T (1997) Environmental oceanography, 2nd edn. CRC
Marine Science Series, CRC Press, Boca Raton Florida
Berner RA (1994) GEOCARB II: a revised model of atmos-
pheric CO
over Phanerozoic time. Am J Sci 294:56±91
Berner RA (1997) The rise of plants and their effect on weath-
ering and atmospheric CO
. Science 276:544±546
Blanchon P, Jones B, Kalbfleisch W (1997) Anatomy of a fring-
ing reef around Grand Cayman: storm rubble, not coral
framework. J Sediment Res 67:1±16
Braithwaite CJR (1973) Reefs: just a problem of semantics?
AAPG Bull 57:1100±1116
Buddemeier RW, Fautin DG (1993) Coral bleaching as an adap-
tive mechanism: a testable hypothesis. BioScience 43:320±326
Buddemeier RW, Hopley D (1988) Turn-ons and turn-offs:
causes and mechanisms of the initiation and termination of
coral reef growth. Proc 6th Int Coral Reef Symp Townsville
Buddemeier RW, Kinzie RA III (1998) Reef science: asking all
the wrong questions in all the wrong places? Reef Encounter
(Newslett Int Soc Reef Studies) 23:29±34
Chapman RE (1977) Economic geology and fossil coral reefs.
In: Jones OA, Endean R (eds) Biology and geology of coral
reefs. Academic Press, New York, pp 107±128
Chave KE, Smith SV, Roy KJ (1972) Carbonate production by
coral reefs. Mar Geol 12:23±40
CortØs J (1997) Biology and geology of eastern Pacific coral
reefs. Coral Reefs 16:S39±S46
Dana JD (1872) Corals and coral islands. Published in 1879 by
Dodd, Mead and Co., New York
Darwin C (1842) The structure and distribution of coral reefs,
being the first part of the geology of the voyage of the
Beagle, under the Command of Capt. Fitzroy, during the
years 1832±1836, Third edition published in 1901 by D.
Appleton and Co., New York
Davis RA Jr (1977) Principles of oceanography, 2nd edn. Addis-
on-Wesley, Reading Massachusetts
Davis WM (1928) The coral reef problem. Am Geogr Soc Spec
Publ 9:1±596
Dickson AG, Millero FJ (1987) A comparison of the equilib-
rium constants for the dissociation of carbonic acid in sea-
water media. Deep-Sea Res 34:1733±1743
Done TJ (1999) Coral community adaptability to environmental
change at the scales of regions, reefs and reef zones. Am
Zool 39:66±79
Eakin CM (1996) Where have all the carbonates gone? A model
comparison of calcium carbonate budgets before and after
the 1982±1983 El Niæo at Uva Island in the eastern Pacific.
Coral Reefs 15:109±119
Fagerstrom JA (1987) The evolution of reef communities. Wiley,
New York
Fagerstrom JA (1997) Reef-building: a biological phenomenon.
Bol R Soc Es Hist Nat 92:7±13
Fairhall AW (1973) Accumulation of fossil CO
in the atmos-
phere and the sea. Nature 245:20±23
Feely RA, Byrne RH, Betzer PR, Gendron JF, Acker JG (1984)
Factors influencing the degree of saturation of the surface
and intermediate waters of the North Pacific ocean with
respect to aragonite. J Geophys Res 89:631±640
Gattuso J-P, Frankignoulle M, Bourge I, Romaine S, Budde-
meier RW (1998) Effect of calcium carbonate saturation of
seawater on coral calcification. Global Planet Change
Gattuso J-P, Allemand D, Frankignoulle M (1999) Interactions
between the carbon and carbonate cycles at organism and
community levels in coral reefs: a review on processes and
control by the carbonate chemistry. Am Zool 39:160±183
Glynn PW (1984) Widespread coral mortality and the 1982/83
El Niæo warming event. Environ Conserv 11:133±146
Grigg RW (1998) Holocene reef accretion in Hawaii: a function
of wave exposure and sea level history. Coral Reefs
Gross MG (1977) Oceanography, a view of the Earth, 2nd edn.
Prentice-Hall, Englewood Cliffs, New Jersey
Gross MG (1987) Oceanography, a view of the Earth, 4th edn.
Prentice-Hall, Englewood Cliffs, New Jersey
Harriott VJ (1998) Growth of staghorn coral
Acropora formosa
at Houtman Abrolhos, western Australia. Mar Biol
Harriott VJ (1999) Coral growth in subtropical eastern Austral-
ia. Coral Reefs 18:281±291
Hay WW, DeConto RM, Wold CN (1997) Climate: Is the past
the key to the future? Geol Rundsch 86:471±491
Heckel PH (1974) Carbonate buildups in the geological record:
a review. SEPM Spec Publ 18:90±154
Hoegh-Goldberg O (1999) Climate change, coral bleaching and
the future of the world's coral reefs. Greenpeace Report,
29 pp
Hopley D (1989) Coral reefs: zonation, zonality and gradients.
In: Bird EDF, Kelletat D (eds) Zonality of coastal geomor-
phology and ecology. Proc Sylt Symp Essener Geogr
Arbeiten Bd 18:79±123
Houghton JT, Meira Filho LG, Callander BA, Harris N, Katten-
berg A, Maskell K (1996) Climate Change 1995. The science
of climate change. Cambridge University Press, Cambridge
Howarth RW (1998) An assessment of human influences on
fluxes of nitrogen from the terrestrial landscape to the estu-
aries and continental shelves of the North Atlantic Ocean.
Nutrient Cycling Agroecosystems 52:213±223
Hubbard DK (1985) What do we mean by reef growth? Proc
3rd Int Coral Reef Congr Tahiti 6:433±438
Hubbard DK (1992) Hurricane-induced sediment transport in
open-shelf tropical systems: an example from St. Croix, U.S.
Virgin Islands. J Sediment Petrol 62:946±960
Hubbard DK, Miller AI, Scaturo D (1990) Production and
cycling of calcium carbonate in a shelf-edge reef system (St.
Croix, U.S. Virgin Islands): applications to the nature of reef
systems in the fossil record. J Sediment Petrol 60:335±360
Hubbard DK, Parsons KM, Bythell JC, Walker ND (1991) The
effects of Hurricane Hugo on the reefs and associated envi-
ronments of St. Croix, U.S. Virgin Islands: a preliminary
assessment. J Coastal Res 8:33±48
Hutchings PA (1986) Biological destruction of coral reefs. Coral
Reefs 4:239±152
James NP (1983) Facies models. Am Assoc Pet Geol Mem
Johannes RE, Wiebe WJ, Crossland CJ, Rimmer DW, Smith SV
(1983) Latitudinal limits of coral reef growth. Mar Ecol Prog
Ser 11:105±111
Kinsey DW (1985) Metabolism, calcification and carbon produc-
tion. I. Systems level studies. Proc 5th Int Coral Reef Symp
Kleypas JA (1997) Modeled estimates of global reef habitat and
carbonate production since the last glacial maximum. Paleo-
ceanography 12:533±545
Kleypas JA, Buddemeier RW, Archer D, Gattuso J-P, Langdon
C, Opdyke B (1999a) Geochemical consequences of
increased atmospheric CO
on coral reefs. Science
Kleypas JA, McManus J, Meæez LB (1999b) Environmental lim-
its to coral reef development: Where do we draw the line?
Am Zool 39:146±159
Langdon C, Takahashi T, Sweeney C, Chipman D, Goddard J,
Marubini F, Aceves H, Barnett H, Atkinson M (2000) Effect
of calcium carbonate saturation state on the rate of calcifica-
tion of an experimental coral reef. Global Biogeochem
Cycles 14:639±654
Leclercq N, Gattuso J-P, Jaubert J (2000) CO
partial pressure
controls the calcification rate of a coral community. Global
Change Biol 6:329±334
Levinton JS (1982) Marine ecology. Prentice-Hall, New Jersey,
pp 394±444
Levitus S (1994) Climatological atlas of the world ocean,
NOAA Prof Pap 13, U.S. Government Printing Office,
Washington DC, 173 pp
Levitus S, Conkright ME, Reid JL, Najjar RG, Mantyla A
(1993) Distribution of nitrate, phosphate and silicate in the
world oceans. Prog Oceanogr 31:245±273
Levitus S, Boyer T, Conkright M et al. (1999) World ocean atlas
1998. Ocean Climate Laboratory, National Oceanographic
Data Center, CD-ROM and Documentation
Longman MW (1981) A process approach to recognizing facies
of reef complexes. SEPM Spec Publ 30:9±40
McManus JW, Vergara SG (1998) Reef base: a global database
on coral reefs and their resources. Version 3.0 CD-ROM and
user's guide, ICLARM, Manila, 180 pp
MignØ A, Davoult D, Gattuso J-P (1998) Calcium carbonate
production of a dense population of the brittle star
thrix fragilis
): role in the car-
bon cycle of a temperate coastal ecosystem. Mar Ecol Prog
Ser 173:305±308
Mucci A (1983) The solubility of calcite and aragonite in sea-
water at various salinities, temperatures, and one atmosphere
total pressure. Am J Sci 283:780±799
Neumann AC, Macintyre I (1985) Reef response to sea level
rise: keep-up catch-up or give-up. Proc 5th Int Coral Reef
Congr Tahiti 3:105±110
Opdyke BN, Wilkinson BH (1993) Carbonate mineral saturation
state and cratonic limestone accumulation. Am J Sci
Partain BR, Hopley D (1989) Morphology and development of
the Cape Tribulation fringing reefs, Great Barrier Reef, Aus-
tralia, Townsville, Qld, Great Barrier Reef Marine Park
Authority, Series Technical Memorandum, ISSN 0817-6094
Pearson PN, Palmer MR (2000) Atmospheric carbon dioxide
concentrations over the past 60 million years. Nature
Pittock AB (1999) Coral reefs and environmental change: adap-
tation to what? Am Zool 39:10±29
Preobrazhensky BV (1977) Problems of studying coral-reef eco-
systems. Helgol Wiss Meeresunters 80:357±361
Reaka-Kudla ML, Feingold JS, Glynn W (1996) Experimental
studies of rapid bioerosion of coral reefs in the Galµpagos
Islands. Coral Reefs 15:101±107
Riding R (1989) Reef structure and composition. Geological
Society and Palaeontological Association Review Seminar on
Carbonate Buildups, Derbyshire College of Higher
Education, pp 2±7
Ross DA (1977) Introduction to oceanography, 2nd edn. Pren-
tice-Hall, Englewood Cliffs, New Jersey
Rowan R, Knowlton N, Baker A et al. (1997) Landscape ecol-
ogy of algal symbionts creates variation in episodes of
bleaching. Nature 388:265±269
Schuhmacher H, Zibrowius H (1985) What is hermatypic? A
redefinition of ecological groups in corals and other organ-
isms. Coral Reefs 4:1±9
Scoffin TP (1987) An introduction to carbonate sediments and
rocks. Reef growth. Blackie, Glasgow, pp 77±88
Skirrow G, Whitfield M (1975) The effect of increases in the
atmospheric carbon dioxide content on the carbonate ion
concentration of surface ocean water at 25 C. Limnol Ocea-
nogr 20:103±108
Smith SV (1972) Production of calcium carbonate on the main-
land shelf of southern California. Limnol Oceanogr 17:28±41
Smith SV (1981) The Houtman Abrolhos Islands: carbon metab-
olism of coral reefs at high latitude. Limnol Oceanogr
Smith SV, Buddemeier RW (1992) Global change and coral reef
ecosystems. Ann Rev Ecol Syst 23:89±118
Stanley SM, Hardie LA (1998) Secular oscillations in the car-
bonate mineralogy of reef-building and sediment-producing
organisms driven by tectonically forced shifts in seawater
chemistry. Palaeogeogr Palaeoclimatol Palaeoecol 144:3±19
Stanley SM, Hardie LA (1999) Hypercalcification: paleontology
links plate tectonics and geochemistry to sedimentology.
Geol Soc Am Today 9:1±7
Stearn CW, Scoffin TP (1977) Carbonate budget of a fringing
reef, Barbados. Proc 3rd Int Coral Reef Symp Miami
Steers JA (1937) The coral islands and associated features of the
Great Barrier Reef. Geogr J 89: 1±28, 119±139
Stoddart DR, McLean RF, Scoffin TP, Thom BG, Hopley D
(1978) Evolution of reefs and islands, northern Great Barrier
Reef: synthesis and interpretation. Phil Trans R Soc Lond B
Stowe K (1987) Essentials of ocean science. Wiley, New York
Takahashi T, Feely RA, Weiss RF, Wanninkhof RH, Chipman
DW, Sutherland SC, Takahashi TT (1997) Global air-sea flux
of CO
: an estimate based on measurement of sea-air pCO
difference. Proc Natl Acad Sci USA 94:8292±8299
Thurman HV (1981) Introductory oceanography. Merrill,
Columbus, Ohio
Vaughan TW (1919) Corals and the formation of coral reefs.
Annu Rep Smithsonian Inst 17:189±238
Veron JEN (1992) Environmental control of Holocene changes
to the world's most northern hermatypic coral outcrop.
Pacific Sci 46:405±425
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA,
Schindler DW, Schlesinger WH, Tilman DG (1997) Human
alteration of the global nitrogen cycle: sources and con-
sequences. Ecol Appl 7:737±750
Ware JR, Fautin DG, Buddemeier RW (1996) Patterns of coral
bleaching: modeling the adaptive bleaching hypothesis. Ecol
Model 84:199±214
Weiss RF (1974) Carbon dioxide in water and seawater: the sol-
ubility of a non-ideal gas. Mar Chem 2:203±215
Weyl PK (1970) Oceanography, an introduction to the marine
environment. Wiley, New York
Whitfield M (1974) Accumulation of fossil CO
in the atmos-
phere and in the sea. Nature 247:523±525
Wilkinson C (ed) (1998) Status of coral reefs of the World: 1998.
Australian Inst Mar Sci, Australia
Wilkinson C, LindØn O, Cesar H, Hodgson G, Rubens J, Strong
AE (1999) Ecological and socioeconomic impacts of 1998
coral mortality in the Indian Ocean: an ENSO impact and a
warning of future change? Ambio 28:188±196
Wood R (1998) Reef evolution. Oxford University Press,
Wood R (1999) The ecological evolution of reefs. Ann Rev Ecol
Syst 29:179±206
Wright, Burchette (1996) Shallow-water carbonate environ-
ments. In: Reading HG (ed) Sedimentary environments:
processes, facies and stratigraphy. Blackwell, London, pp
Yonge (1930) A year on the Great Barrier Reef. Putnam, Lon-
Zimen KE, Altenhein FK (1973) The future burden of industrial
on the atmosphere and the oceans. Z Naturforsch A
... Rugosity reflects the three-dimensional structure of a reef and improves biodiverse and abundant communities [111][112][113][114] . ...
... Branching species such as acroporids and pocilloporids are instead considered "engineering species as they grow faster and create habitats with their complex shapes which provide a quick shelter for organisms " 116 . The role of corals three dimensionality in coastal protection through the dissipation of wave energy 111,117,118 is also widely recognised and is poorly described by only analysing changes in coral cover 119 . It is therefore important to understand if and to which degree outplanted corals contribute to the enhancement of the three-dimensionality of reefs by studying their rugosity. ...
... The second model (Fig 1.9b) also describes reef growth in terms of carbonate and terrigenous sediment accumulation and removal processes, but does so through the utilisation of the concept of carbonate budgets (Kleypas et al. 2001). This model therefore details the different processes controlling reef growth by considering carbonate accumulation as the sum of imported and in situ produced carbonates, less that lost via erosive (biological, chemical and physical) and export processes (sensu Stearn et al. 1977). ...
... Therefore, to apply such an approach for the chronostratigraphic reconstruction of coral reefs it is important to consider the key processes which influence vertical reef accretion. Net reef accretion can be simply expressed as the sum of framework and sedimentological accretion, either imported or deposited in situ, minus that which is exported from a system (van Woesik and Done 1997; Kleypas et al. 2001). An important factor determining the volume of material imported to, and exported from, a coral reef is the frequency and magnitude to which it is exposed to high-energy events (e.g. ...
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Understanding how coral reefs have developed in the past is crucial for placing contemporary ecological and environmental change within appropriate reef building timescales (i.e. centennial to millennial). On Australia’s Great Barrier Reef (GBR), coral reefs situated within nearshore settings on the inner continental shelf are a particular priority. This is due to their close proximity to river point sources, and therefore susceptibility to reduced water quality as the result of extensive modification of adjacent river catchments following European settlement in the region (ca. 1850 CE). However, the extent of water quality decline and its impact on the coral reefs of the GBR’s inner-shelf remains contentious and is confounded by a paucity of long-term (> decadal) datasets. Central to the on-going debate is uncertainty related to the impact of increased sediment loads, relative to the natural movement and resuspension of terrigenous sediments, which have accumulated on the inner-shelf over the last ~6,000 years. The main aim of this thesis was to characterise and investigate the vertical development of turbid nearshore coral reefs on the central GBR. This aim was achieved through the recovery of 21 reef cores (3 - 5 m in length) from five proximal turbid nearshore reefs, currently distributed across the spectrum of reef ‘geomorphological development’ within the Paluma Shoals reef complex (PSRC). The recovered reef cores were used to establish detailed depositional and palaeoecological records for the investigation of the (1) internal development and vertical accretionary history of the PSRC; and (2) compositional variation in turbid nearshore coral and benthic foraminiferal assemblages during vertical reef accretion towards sea level. Established chronostratigraphic and palaeoecological records were further used to assess the impact of post-European settlement associated water quality change in a turbid nearshore reef setting on the central GBR. Radiocarbon dating (n = 96 dates) revealed reef initiation within the PSRC to have occurred between ~2,000 and 1,000 calibrated years before present, with subsequent reef development occurring under the persistent influence of fine-grained (< 0.063 mm) terrigenous sediments. The internal development of the PSRC was characterised by discrete reef facies comprised of a loose coral framework with an unconsolidated siliciclastic-carbonate sediment matrix. A total of 29 genera of Scleractinian coral and 86 genera of benthic foraminifera were identified from the palaeoecological inventory of the PSRC. Both coral and benthic foraminiferal assemblages were characterised by distinct assemblages of taxa pre-adapted to sediment stress (i.e. low light availability and high sedimentation). At the genus level, no discernable evidence of compositional change in either coral or benthic foraminiferal assemblages was found, relative to European settlement. Instead, variations in assemblage composition were driven by intrinsic changes in prevailing abiotic conditions under vertical reef accretion towards sea level (e.g. hydrodynamic energy, light availability, and sedimentation rate). These findings therefore highlight the importance for considering reef ‘geomorphological development’ when interpreting contemporary reef ecological status. Furthermore, this research emphasises the robust nature of turbid nearshore reefs and suggests that they may be more resilient to changes in water quality than those associated with environmental settings where local background sedimentary conditions are less extreme (e.g. towards the inner/mid-shelf boundary). To this end, this thesis presents new baseline records with which to assess contemporary ecological and environmental change within turbid nearshore settings on the central GBR.
... The physical structure of coral reefs is dependent on the dynamic balance between the production and loss of calcium carbonate (CaCO3). In this "carbonate budget", production by calcifying organisms must be higher than erosion to sustain or expand the coral reef framework (Cornwall et al., 2021;Kleypas, Buddemeier, & Gattuso, 2001). Sustaining the physical structure of reefs is vital for maintaining the abundance, diversity and ecosystem functioning of reef-associated communities (Coker, Wilson, & Pratchett, 2014;Graham & Nash, 2013) and key services to people, such as coastal protection from inundation during storms (Elliff & Silva, 2017;Reguero, Beck, Agostini, Kramer, & Hancock, 2018). ...
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Carbonate budgets dynamically balance production and loss of calcium carbonate (CaCO3) on coral reefs. To sustain or expand the coral reef framework, CaCO3 production by calcifying organisms must be higher than erosion. However, global climate change has been negatively impacting carbonate production, with bleaching events causing widespread coral mortality. While bleaching and coral mortality are well documented, the fate of coral colonies after their death, including their erosion rates, are still poorly known. We followed the fate of 143 recently dead individual coral colonies with complex growth forms (arborescent, caespitose, corymbose, digitate, and tabular), whose mortality was triggered by two consecutive bleaching events. These colonies, spread over 16 km2 of the Lizard Island reef complex, were tracked for up to 5 years, allowing detailed examination of erosion rates and post‐mortality structural persistence. We also tested how variables that are commonly used in coral reef erosion studies relate to spatial and temporal variability in the erosion rates of dead coral colonies. We revealed rapid erosion of dead coral colonies, with an average of 79.7% of dead colonies completely disintegrating within 60 months. The predicted half‐life of a dead coral colony was 40 months, with limited variation among wave exposure levels. Remarkably, we found no effect of estimated parrotfish bioerosion, wave exposure, nor coral growth form, on observed erosion rates. Our results suggest that our understanding of the erosion of dead corals may be more limited than previously thought. The rapid loss of coral colonies on our study sites calls for a re‐evaluation of the role of corals with complex growth forms in reef growth and of parrotfishes in reef erosion.
... The three major impacts of anthropogenic climate change on the oceans (i.e., warming, sea-level rise, and acidification) all directly affect the formation and development of coral reef ecosystems. Therefore, modern climate change is likely to dramatically disrupt the carbon cycle in coral reefs (Hoegh-Guldberg, 2011;Kleypas et al., 2001). Modern reefs are already experiencing impacts due to ocean warming, with temperature-driven mass bleaching events (i.e., the expulsion of algal symbionts) occurring more frequently (Hughes et al., 2017). ...
The Earth’s climate is strongly affected by the partitioning of carbon between its mobile reservoirs, primarily between the atmosphere and the ocean. The distribution between the reservoirs is being massively perturbed by human activities, primarily due to fossil fuel emissions, with a range of consequences, including ocean warming and acidification, sea-level rise and coastal erosion, and changes in ocean productivity. These changes directly impact valuable habitats in many coastal regions and threaten the important services the habitats provide to mankind. Among the most productive and diverse systems are coral reefs and vegetated habitats, including saltmarshes, seagrass meadows, and mangroves. Coral reefs are particularly vulnerable to ocean warming and acidification. Vegetated habitats are receiving heightened attention for their ability to sequester carbon, but they are being impacted by land-use change, sea-level rise, and climate change. Overall, coasts play an important, but poorly quantified, role in the global cycling of carbon. Carbon reservoirs on land and in the ocean are connected through the so-called land–ocean aquatic continuum, which includes rivers, estuaries, and the coastal ocean. Terrestrial carbon from soils and rocks enters this continuum via inland water networks and is subject to transformations and exchanges with the atmosphere and sediments during its journey along the aquatic continuum. The expansive permafrost regions, comprised of ground on land and in the seabed that has been frozen for many years, are of increasing concern because they store vast amounts of carbon that is being mobilized due to warming. Quantitative estimates of these transformations and exchanges are relatively uncertain, in large part because the systems are diverse and the fluxes are highly variable in space and time, making observation at the necessary spatial and temporal coverage challenging. But despite their uncertainty, existing estimates point to an important role of these systems in global carbon cycling.
... Given the ability of hermatypic corals to build reefs, and given the economic and ecological importance associated with reef structures 10 , symbiotic scleractinian corals have been a major focus of calcification research over the years 2,11 . Whereas, ahermatypic non-symbiotic scleractinian corals have not been extensively studied and to date they remain under-represented especially in terms of molecular data 12 . ...
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In hermatypic scleractinian corals, photosynthetic fixation of CO 2 and the production of CaCO 3 are intimately linked due to their symbiotic relationship with dinoflagellates of the Symbiodiniaceae family. This makes it difficult to study ion transport mechanisms involved in the different pathways. In contrast, most ahermatypic scleractinian corals do not share this symbiotic relationship and thus offer an advantage when studying the ion transport mechanisms involved in the calcification process. Despite this advantage, non-symbiotic scleractinian corals have been systematically neglected in calcification studies, resulting in a lack of data especially at the molecular level. Here, we combined a tissue micro-dissection technique and RNA-sequencing to identify calcification-related ion transporters, and other candidates, in the ahermatypic non-symbiotic scleractinian coral Tubastraea spp. Our results show that Tubastraea spp. possesses several calcification-related candidates previously identified in symbiotic scleractinian corals (such as SLC4-γ, AMT-1like, CARP, etc.). Furthermore, we identify and describe a role in scleractinian calcification for several ion transporter candidates (such as SLC13, -16, -23, etc.) identified for the first time in this study. Taken together, our results provide not only insights about the molecular mechanisms underlying non-symbiotic scleractinian calcification, but also valuable tools for the development of biotechnological solutions to better control the extreme invasiveness of corals belonging to this particular genus.
... Scleractinian corals are the primary reef-builders of the coral reef structures that sustain ecosystem services ranging from shoreline protection, fisheries provisioning, cultural significance, and tourism revenue for billions of people worldwide (Kleypas et al. 2001;Perry and Alvarez-Filip 2019;Woodhead et al. 2019). However, global coral cover has declined precipitously in recent decades under local and global environmental change (Gardner et al. 2003;Bruno and Selig 2007;De'ath et al. 2012) with the 3 rd global coral bleaching event from 2014 to 2017 further jeopardizing coral dominated reef states and associated maintenance of coral reef structures . ...
The 2014–2017 global coral bleaching event caused widespread coral mortality; however, its impact on the capacity for coral reefs to maintain calcium carbonate structures has not been determined. Here, we quantified remotely sensed maximum heat stress during the 2014–2017 bleaching event, census‐based net carbonate budgets from benthic imagery and fish survey data, and net reef calcification from salinity normalized seawater total alkalinity anomalies collected from 2017–2019 for 56 Pacific coral reef sites (Mariana Islands, Northwestern Hawaiian Islands, Pacific Remote Island Areas, and American Samoa). We incorporated the census‐based and chemistry‐based metrics to determine a calcification vulnerability index for each site to maintain calcium carbonate balance to provide accessible information to managers and policy makers. Most coral reef sites likely experienced ecologically severe (79%, n = 44) or significant (9%, n = 7) heat stress during the 2014–2017 coral bleaching event. Census‐based net carbonate budgets (mean ± 95% = 2.1 ± 0.6 kg CaCO3 m−2 yr−1) were positive for 77% of sites (n = 43), neutral for 16% of sites (n = 9), and negative for 7% of sites (n = 4). Chemistry‐based relative net reef calcification (mean ± 95% = 22 ± 10 μmol kg−1) was positive for 84% of sites (n = 47), neutral for 11% of sites (n = 6), and negative for 5% of sites (n = 3). The calcification vulnerability index suggested the Pacific Ocean reef sites surveyed were of minimal (68%, n = 38) to moderate (32%, n = 18) concern for maintaining calcium carbonate balance following the bleaching event. This suggests that many reefs maintained positive calcium carbonate balance, but that a large number of reefs may be approaching a potential threshold for maintaining their calcium carbonate balance under the climate crisis.
Coral reefs are critically important to the economic development of most tropical countries. However, they have faced multi-stressors from natural and anthropogenic disturbances, particularly from coastal development, tourism, overfishing, and coral bleaching. Consequently, the loss of vulnerable species from coral communities is occurring at an accelerating rate. Many coral species are particularly at risk. Coral reef recovery following severe disturbances depends on several complicated factors, including resistance and tolerance to stresses, recruitment rate, reef connectivity, and local stressors. Maintaining reef framework is also very important, particularly bioerosion rate at a degraded reef. As global climate change potentially causes more frequent and severe coral bleaching events, identifying and conserving coral reef refugia is critically important. Most coral reefs are in a type of marine protected areas that intensively require scientific data for management. The achievements of passive and active coral reef restoration projects in the Western Pacific are necessarily considered for the improvement of coral reef management plans. In this chapter, we synthesize important information on coral reef biodiversity decline and extinction risk; coral reef recovery after disturbances; coral reef resilience; coral reef connectivity; coral reef bioerosion; coral reef refugia under global change; marine protected area networks; and passive and active restoration of degraded coral reefs.KeywordsCoral ecologyBiodiversityExtinction riskRecoveryResilienceConnectivityBioerosionRefugiaClimate changeMarine protected areaRestoration
Ancient coral reefs are rich archives of historical process and vital baselines for future development. Coring gives a window into the growth of ancient coral reefs and the fossil coral community's response to paleoenvironment. Well NK-1 drilled from Meiji Reef is the longest scientific core with the highest recovery in the South China Sea. This study focused on the upper section of the Well NK-1 accumulated during the Holocene. From 8200 yr BP, Holocene reef initiated on the substrates of Pleistocene limestone and stopped accreting vertically at 4800 yr BP. It consisted of an initiation and fast reef growth (5.6 mm yr⁻¹) from 8200 yr BP to 7300 yr BP, a shift to slow reef growth (2.0 mm yr⁻¹) between 7300 yr BP and 5400 yr BP, a return to a rapid reef growth (8.8 mm yr⁻¹) from 5400 yr BP to 4800 yr BP, and finally a cessation of upward accretion and a reinforced lateral progradation since 4800 yr BP. A total of 11 coral genera and 16 Acropora species were identified from the Holocene segment of the core. The diversity of coral communities had an impact on reef growth. Coral communities with less genera and absolute predominance of branching Acropora were corresponded with a rapid vertical accumulation of reef framework with higher accretion rate. Acropora corals with rapid growth and dispersion by fragmentation were principal reef-builders during the Holocene, with A.valida being the most prevalent coral species. The highest Acropora species richness occurred at the geological era of 5400–5300 yr BP when reef accumulated with the fastest upward accretion rate of 23.1 mm yr⁻¹. This intricate and detailed pattern presented a new and novel model for the development of Holocene reef, indicating that the coral community and key reef builders were crucial to reef growth. These findings are extremely helpful for understanding the current ecological state of modern coral reefs as well as their potential response to global climate change.
The ability of coral populations to recover from disturbance depends on larval dispersion and recruitment. While ocean warming and acidification effects on adult corals are well documented, information on early life stages is comparatively scarce. Here, we investigate whether ocean warming and acidification can affect the larval and juvenile development of the Mediterranean azooxanthellate coral Astroides calycularis. Larvae and juveniles were raised for 9 months at ambient (23 °C) and warm (26 °C) temperatures and ambient (8.0) and low pH (7.7, on the total scale). The timing of the larvae metamorphosis, growth of the juvenile polyp, and skeletal characteristics of the 9-month-old polyps were monitored. Settlement and metamorphosis were more successful and hastened under a warm temperature. In contrast, low pH delayed the metamorphosis and affected growth of the recruits by reducing the calcified area of attachment to the substrate, as well as by diminishing the skeleton volume and the number of septa. However, skeleton density was higher under low pH and ambient temperature. The warm temperature and low pH treatment had a negative impact on the survival, settlement, and growth of recruits. This study provides evidence of the threat that represents ocean warming and acidification for the larval recruitment and the growth of recruits of A. calycularis.
St. Martin's Island (Bangladesh), a biodiversity hotspot in the northeastern Bay of Bengal, continues to be misunderstood by many scientists. There seems to be continued confusion surrounding the geologic history of St. Martin's Island and its intertidal and subtidal geomorphology. St. Martin's Island is a sedimentary continental island surrounded by a rocky reef covered by numerous intertidal and subtidal boulder fields. The rocky reef and its boulder fields support numerous scleractinian coral assemblages, but as a result of marginal environmental condition coral reefs are absent. We argue that since there are no coral reefs present on St. Martin's Island the total economic valuation that Rani et al. (2020) assigned to the island's coral reef ecosystem is an economic valuation of the whole island itself, and that the island is protected by a sedimentary rocky reef and not a coral reef.
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Early in the morning of Sepetember 18 1989 Hurricane Hugo exceeded 150 mph with gusts exceeding 170 mph. On the north coast, wave heights ranged from 3-7 m; larger waves occurred on the south shore. Beach erosion was generally less than expected, but did reach 20 m in extreme cases. The pattern of reef destruction was controlled by 1) water depth, 2) the character of the pre-storm bottom communities, and 3) the orientation of the shoreline and reefs. Many of these areas were swept clean of nearly all loose sediment. This storm-induced flushing may be a positive factor in the long-term development of these reefs. -from Authors
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The year 1998, was the warmest year since the start of temperature recordings some 150 years ago. Similarly, the 1990s have been the warmest decade recorded. In addition, 1998 saw the strongest El Nino ever recorded. As a consequence of this, very high water temperatures were observed in many parts of the oceans, particularly in the tropical Indian Ocean, often with temperatures of 3°to 5°C above normal. Many corals in this region bleached and subsequently died, probably due to the high water temperatures in combination with meteorological and climatic factors. Massive mortality occurred on the reefs of Sri Lanka, Maldives, India, Kenya, Tanzania, and Seychelles with mortalities of up to 90% in many shallow areas. Reefs in other parts of the Indian Ocean, or in waters below 20 m, coral mortality was typically 50%. Hence, coral death during 1998 was unprecedented in severity. The secondary socioeconomic effects of coral bleaching for coastal communities of the Indian Ocean are likely to be long lasting and severe. In addition to potential decreases in fish stocks and negative effects on tourism, erosion may become an acute problem, particularly in the Maldives and Seychelles. If the observed global trends in temperature rises continue, there will be an increased probability of a recurrence of the phenomenon observed in 1998 on the coral reefs of the Indian Ocean, as well as in other parts of the tropical oceans in coming years. Coral reefs of the Indian Ocean may prove to be an important signal of the potential effects of global climate change, and we should heed that warning.
Conference Paper
Projected global increases In temperature, sea level, storminess and atmospheric carbon dioxide (CO2) are likely to cause changes in reef coral communities which the present human generation will view as deleterious. It is likely coral community trajectories will be influenced as much by the reduction in intervals between extreme events as the projected increases in means of environmental parameters such as temperature, atmospheric CO2, and sea-level, Depressed calcification rates in corals caused by reduced aragonite saturation state of water may increase vulnerability of corals to storms. Moreover, reduction in intervals between storms and other extreme events causing mass mortality in corals (coral predators, diseases, bleaching) are likely to more frequently "set back" reef coral communities to early successional stages or alternate states characterized by non-calcifying benthos (plants, soft corals, sponges). The greater the area and the longer the duration of dominance of putative '"coral/coralline algae" zones of coral reefs by non-calcifying stages, the less will be the reef's capacity to accrete limestone bulk locked up in the big skeletal units of late successional stages (i.e., very large old corals). Averaged over decades to centuries, the effects of such changes on the coral community's carrying capacity for other biota such as fish are unpredictable. A "shifting steady-state mosaic" null model may provide a useful conceptual tool for defining a baseline and tracking changes from that baseline through time.
Marine organic reefs are biological-paleobiological features; they are not sedimentologic-stratigraphic features resulting from locally over-thickened accumulations of sediment. The positive topographic relief of reefs is due to the relatively rapid upward growth, skeletal strength/rigidity and high packing density of the clonal (or gregarious) organisms comprising the reef framework. In modern, tropical reefs, these features reach their acme at the relatively narrow, shallow water crest marking the interface between the backreef lagoon or reef fiat and the forereef or seaward slope. In ancient reefs, sediment commonly comprises a much greater volume of the reef than the framework. However, it is the organisms, preserved either in their original growth positions or in situ, that distinguish reefs from accumulations of transported skeletal debris on level-bottom substrates. Both modern and ancient reef communities have characteristic taxonomic compositions, diversities and guild structures. It is the relative skeletal volume (or areal coverage) of members of the constructor, baffler and binder guilds that controls the reef-building process and in ancient reefs becomes the basis for their classification as framestones, bafflestones and boundstones, respectively.
... dioxide in the atmosphere and Chamberlin2 suggested a variety of geological processes that could affect atmospheric carbon dioxide concentra- tions ... established values for surface ocean pH and alkalinity, it is possible to calculate aqueous CO2 and atmospheric pCO2. ...
Hurricane Hugo passed directly over St. Croix on 17 September 1989. Sustained winds in excess of 110 knots (gusts to 165 knots) and waves 6-7m in height accompanied the storm. Along the north coast, wave height was lower (c3-4m) due to the leeward position of the shelf. In the deeper reefs at Cane Bay and Salt River, damage was confined primarly to the soft-bodied benthic community (eg sponges, gorgonians); coral damage was much less severe, largely because of the buffering effects of the water column. The greatest change observed after the storm was wholesale flushing of sand from shelf-edge areas. In Salt River submarine canyon, a minimum of 2 million kg of sediment were flushed into deeper water. -from Author