Coral Reefs Under Rapid Climate Change and
Ocean Acidification

et al.
O. Hoegh-Guldberg,
Science
, 1737 (2007);
318
DOI: 10.1126/science.1152509
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REVIEW
ing a mean temperature of 25°C during the past
420,000 years (Fig. 1B). The results show a tight
Coral Reefs Under Rapid Climate
cluster of points that oscillate (temperature ±3°C;
carbonate-ion concentration ±35 mmol kg-1) be-
tween warmer interglacial periods that had lower
Change and Ocean Acidification
carbonate concentrations to cooler glacial pe-
riods with higher carbonate concentrations. The
overall range of values calculated for seawater
O. Hoegh-Guldberg,1* P. J. Mumby,2 A. J. Hooten,3 R. S. Steneck,4 P. Greenfield,5 E. Gomez,6
pH is ±0.1 units (10, 11). Critically, where coral
C. D. Harvell,7 P. F. Sale,8 A. J. Edwards,9 K. Caldeira,10 N. Knowlton,11 C. M. Eakin,12
reefs occur, carbonate-ion concentrations over
R. Iglesias-Prieto,13 N. Muthiga,14 R. H. Bradbury,15 A. Dubi,16 M. E. Hatziolos17
the past 420,000 years have not fallen below
240 mmol kg-1. The trends in the Vostok ice
Atmospheric carbon dioxide concentration is expected to exceed 500 parts per million and global
core data have been verified by the EPICA study
temperatures to rise by at least 2°C by 2050 to 2100, values that significantly exceed those of at
(6), which involves a similar range of temperatures
least the past 420,000 years during which most extant marine organisms evolved. Under conditions
and [CO2]atm values and hence extends the con-
expected in the 21st century, global warming and ocean acidification will compromise carbonate
clusions derived from the Vostok record to at least
accretion, with corals becoming increasingly rare on reef systems. The result will be less diverse reef
740,000 years before the present (yr B.P.). Con-
communities and carbonate reef structures that fail to be maintained. Climate change also exacerbates
ditions today ([CO2]atm ~380 ppm) are significantly
local stresses from declining water quality and overexploitation of key species, driving reefs increasingly
shifted to the right of the cluster points represent-
toward the tipping point for functional collapse. This review presents future scenarios for coral reefs that
ing the past 420,000 years. Sea temperatures are
predict increasingly serious consequences for reef-associated fisheries, tourism, coastal protection, and
warmer (+0.7°C), and pH (- 0.1 pH units) and
people. As the International Year of the Reef 2008 begins, scaled-up management intervention and
carbonate-ion concentrations (~210 mmol kg-1)
decisive action on global emissions are required if the loss of coral-dominated ecosystems is to be avoided.
lower than at any other time during the past
420,000 years (Fig. 1B). These conclusions match
Coralreefsareamongthemostbiologically ingglobalwarmingandoceanacidification,may recentchangesreportedformeasurementsofocean on June 10, 2010
diverse and economically important eco-
be the final insult to these ecosystems. Here, we
temperature, pH, and carbonate concentration (8).
systems on the planet, providing ecosys-
review the current understanding of how anthro-
In addition to the absolute amount of change, the
tem services that are vital to human societies and
pogenic climate change and increasing ocean acid-
rate at which change occurs is critical to whether
industries through fisheries, coastal protection,
ity are affecting coral reefs and offer scenarios for
organisms and ecosystems will be able to adapt or
building materials, new biochemical compounds,
how coral reefs will change over this century. The
accommodate to the new conditions (11). Notably,
and tourism (1). Yet in the decade since the in-
scenarios are intended to provide a framework for
rates of change in global temperature and [CO2]atm
augural International Year of the Reef in 1997 (2),
proactive responses to the changes that have
over the past century are 2 to 3 orders of mag-
which called the world to action, coral reefs have
begun in coral reef ecosystems and to provoke
nitude higher than most of the changes seen in
continued to deteriorate as a result of human in-
thinking about future management and policy
the past 420,000 years (Table 1). Rates of change
www.sciencemag.org
fluences (3, 4). Rapid increases in the atmospheric
challenges for coral reef protection.
under both low (B1) and high (A2) Intergovern-
carbon dioxide concentration ([CO2]atm), by driv-
mental Panel on Climate Change (IPCC) emission
Warming and Acidifying Seas
scenarios are even higher, as are recent measure-
1Centre for Marine Studies, The University of Queensland,
The concentration of carbon dioxide in Earth's
ments of the rate of change of [CO2]atm (9). The
St. Lucia, 4072 Queensland, Australia. 2Marine Spatial
atmosphere now exceeds 380 ppm, which is
only possible exceptions are rare, short-lived
Ecology Laboratory, School of BioSciences, University of
more than 80 ppm above the maximum values
spikes in temperature seen during periods such
Exeter, Prince of Wales Road, Exeter EX4 4PS, UK. 3AJH
Environmental Services, 4900 Auburn Avenue, Suite 201,
of the past 740,000 years (5, 6), if not 20 million
as the Younger Dryas Event (12,900 to 11,500 yr
Bethesda, MD 20814, USA. 4University of Maine, School
years (7). During the 20th century, increasing
B.P.) (12). Given that recent and future rates of
Downloaded from
of Marine Sciences, Darling Marine Center, Walpole, ME
[CO2]atm has driven an increase in the global
change dwarf even those of the ice age transitions,
04573, USA. 5The Chancellery, University of Queens-
oceans
land, St. Lucia, 4072 Queensland, Australia. 6Marine Science
' average temperature by 0.74°C and sea
when biology at specific locations changed dramat-
Institute, University of the Philippines, Diliman, Quezon City,
level by 17 cm, and has depleted seawater car-
ically, it is likely that these changes will exceed the
Philippines. 7Ecology and Evolutionary Biology, E321 Corson
bonate concentrations by ~30 mmol kg-1 seawater
capacity of most organisms to adapt.
Hall, Cornell University, Ithaca, NY 14853, USA. 8International
and acidity by 0.1 pH unit (8). Approximately
Network on Water, Environment and Health, United Nations
25% (2.2 Pg C year-1) of the CO
Ocean Acidification and Reef Accretion
2 emitted from
University, 50 Main Street East, Hamilton, Ontario L8N 1E9,
Canada. 9School of Biology, Ridley Building, University of
all anthropogenic sources (9.1 Pg C year-1) cur-
Many experimental studies have shown that a
Newcastle, Newcastle upon Tyne, NE1 7RU, UK. 10Department of
rently enters the ocean (9), where it reacts with
doubling of pre-industrial [CO2]atm to 560 ppm
Global Ecology, Carnegie Institution of Washington, 260
water to produce carbonic acid. Carbonic acid
decreases coral calcification and growth by up to
Panama Street, Stanford, CA 94305, USA. 11National Museum
dissociates to form bicarbonate ions and protons,
40% through the inhibition of aragonite formation
of Natural History, Smithsonian Institution, Washington, DC
which in turn react with carbonate ions to produce
(the principal crystalline form of calcium carbonate
20013, USA. 12National Oceanic and Atmospheric Administra-
tion, Coral Reef Watch, E/RA31, 1335 East West Highway, Silver
more bicarbonate ions, reducing the availability of
deposited in coral skeletons) as carbonate-ion con-
Spring, MD 20910­3226, USA. 13Unidad Académica Puerto
carbonate to biological systems (Fig. 1A). De-
centrations decrease (13). Field studies confirm that
Morelos, Instituto de Ciencias del Mar y Limnología, Universidad
creasing carbonate-ion concentrations reduce the
carbonate accretion on coral reefs approaches zero
Nacional Autónoma de México, Apdo. Postal 1152, Cancún
rate of calcification of marine organisms such as
or becomes negative at aragonite saturation values
77500 QR, México. 14Wildlife Conservation Society, 2300
Southern Boulevard, Bronx, New York, NY 10460, USA.
reef-building corals, ultimately favoring erosion
of 3.3 in today's oceans (Fig. 4), which occurs
15Resource Management in Asia-Pacific Program, Australian
at ~200 mmol kg-1 seawater (7, 10).
when [CO2]atm approaches 480 ppm and carbonate-
National University, Canberra, 0200 Australia. 16Institute of
We used global [CO2]atm and temperature
ion concentrations drop below 200 mmol kg-1 in
Marine Sciences, University of Dar es Salaam, Tanzania. 17Envi-
data from the Vostok Ice Core study (
ronment Department, MC5-523, The World Bank, 1818 H
5) to ex-
most of the global ocean (10, 13). These find-
Street, NW, Washington, DC 20433, USA.
plore the ocean temperature and carbonate-ion
ings are supported by the observation that reefs
concentration (
*To whom correspondence should be addressed. E-mail:
10) seen today relative to the re-
with net carbonate accretion today (Fig. 4, 380 ppm)
oveh@uq.edu.au
cent past for a typical low-latitude sea maintain-
are restricted to waters where aragonite saturation
www.sciencemag.org SCIENCE VOL 318 14 DECEMBER 2007
1737

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REVIEW
Fig. 1. (A) Linkages between the buildup of atmospheric CO2 and the slowing
(25°C), and total alkalinity (2300 mmol kg-1). Further details of these
of coral calcification due to ocean acidification. Approximately 25% of the
calculations are in the SOM. Acidity of the ocean varies by ± 0.1 pH units
CO2 emitted by humans in the period 2000 to 2006 (9) was taken up by the
over the past 420,000 years (individual values not shown). The thresholds for
ocean where it combined with water to produce carbonic acid, which releases a
major changes to coral communities are indicated for thermal stress (+2°C) and
proton that combines with a carbonate ion. This decreases the concentration of
carbonate-ion concentrations ([carbonate] = 200 mmol kg-1, approximate
carbonate, making it unavailable to marine calcifiers such as corals. (B) Tem-
aragonite saturation ~Waragonite = 3.3; [CO2]atm = 480 ppm). Coral Reef
perature, [CO
on June 10, 2010
2]atm, and carbonate-ion concentrations reconstructed for the past
Scenarios CRS-A, CRS-B, and CRS-C are indicated as A, B, and C, respectively,
420,000 years. Carbonate concentrations were calculated (54) from CO2 atm and
with analogs from extant reefs depicted in Fig. 5. Red arrows pointing
temperature deviations from today's conditions with the Vostok Ice Core data set
progressively toward the right-hand top square indicate the pathway that is
(5), assuming constant salinity (34 parts per trillion), mean sea temperature
being followed toward [CO2]atm of more than 500 ppm.
exceeds 3.3 (10). Geological studies report a no-
have deleterious consequences for reef ecosys-
density. However, erosion could be promoted
table gap in the fossil record of calcified organisms,
tems. First, the most direct response is a decreased
by the activities of grazing animals such as
including reef-building corals (14) and calcare-
linear extension rate and skeletal density of coral
parrotfish, which prefer to remove carbonates
ous algae (15), during the early Triassic when
colonies. The massive coral Porites on the Great
from lower-density substrates. Increasingly
www.sciencemag.org
[CO2]atm increased dramatically and reached levels
Barrier Reef has shown reductions in linear ex-
brittle coral skeletons are also at greater risk
at least five times as high as today's (16). Phylo-
tension rate of 1.02% year-1 and in skeletal den-
of storm damage (21); thus, if rates of erosion
genetic studies suggest that corals as a group
sity of 0.36% year-1 during the past 16 years (20).
outstrip calcification, then the structural com-
survived the Permian-Triassic extinction event (14)
This is equivalent to a reduction of 1.29% year-1
plexity of coral reefs will diminish, reducing
but may have done so through forms lacking cal-
or a 20.6% drop in growth rate (the product of
habitat quality and diversity. A loss of struc-
cified skeletons (17, 18). Although Scleractinian
linear extension rate and skeletal density) over the
tural complexity will also affect the ability of
(modern) corals arose in the mid-Triassic and lived
16-year period. While at present it is not possible
reefs to absorb wave energy and thereby impairs
under much higher [CO2]atm, there is no evidence
to confidently attribute the observed decrease in
coastal protection.
Downloaded from
that they lived in waters with low-carbonate
growth and calcification to ocean acidification, it
Third, corals may maintain both skeletal growth
mineral saturation. Knoll et al. succinctly state that
is consistent with changes reported in oceanic pH
and density under reduced carbonate saturation
"it is the rapid, unbuffered increase in [CO2]atm
and carbonate-ion concentrations.
by investing greater energy in calcification. A
and not its absolute values that causes impor-
Second, corals may maintain their physical
likely side effect of this strategy is the diversion
tant associated changes such as reduced [CO 2-
3
],
extension or growth rate by reducing skeletal
of resources from other essential processes, such
pH, and carbonate
as reproduction, as
Table 1.
saturation of sea wa-
Rates of change in atmospheric CO2 concentration ([CO2 ]atm, ppm/100 years) and global temperature
seen in chronic stress
ter" (19). The rate of
(°C/100 years) calculated for the past 420,000 yr B.P. using the Vostok Ice Core data (5) and compared to changes
(21), which could ul-
over the last century and those projected by IPCC for low-emission (B1) and high-emission (A2) scenarios (8). Rates
[CO2]atm change is
timately reduce the
were calculated for each successive pair of points in the Vostok Ice Core record by dividing the difference between two
critical given that
larval output from
sequential values (ppm or °C) by the time interval between them. Rates were then standardized to the change seen
modern genotypes
reefs and impair the
over 100 years. Ratios of each rate relative to the mean rate seen over the past 420,000 years are also calculated.
and phenotypes of
potential for recolo-
corals do not appear
nization following
[CO2]atm
Ratio (relative to
Temperature
Ratio (relative to
to have the capacity
Period
disturbances.
(ppm century-1) past 420,000 years) (°C century-1) past 420,000 years)
to adapt fast enough
Past 420,000 years (99%
0.07 + 0.223
1
0.01 + 0.017
1
to sudden environ-
Resilience and
confidence interval; n = 282)
mental change.
Tipping Points
Past 136 years (1870­2006)
73.53
1050
0.7
70
Reef-building
Maintaining ecologi-
IPCC B1 scenario: 550 ppm
170
2429
1.8
180
corals may exhibit
cal resilience is the
at 2100
several responses
central plank of any
IPCC A2 scenario: 800 ppm
420
6000
3.4
420
to reduced calcifi-
strategy aiming to
at 2100
cation, all of which
preserve coral reef
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14 DECEMBER 2007 VOL 318 SCIENCE www.sciencemag.org

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REVIEW
ecosystems. Ecological resilience (4)
grazers like the sea urchin, Diade-
90
is a measure of the rate at which an
ma antillarum, which essentially
ecosystem returns to a particular state
disappeared from Caribbean reefs
80
Coral-dominated stable equilibrium
(e.g., coral-dominated communities)
in the early 1980s after a massive
after a perturbation or disturbance
Unstable equilibrium with 20%
disease outbreak, highly produc-
70
(e.g., hurricane impacts). Recent
reduction in coral linear extension rate
tive reefs would likely require the
changes to the frequency and scale
60
Combinations of coral
highest levels of parrotfish grazing
of disturbances such as mass coral
cover and grazing that
(i.e., ~ 40% of the reef being grazed)
bleaching, disease outbreaks, and
50
permit reef recovery
for a reef to be able to recover from
destructive fishing, coupled with a
between disturbance
disturbance. The loss of ecological
events under reduced
decreased ability of corals to grow
40
resilience occurs because coral
coral growth
and compete, are pushing reef ecosys-
cover increases more slowly after
tems from coral- to algal-dominated
30
disturbance and competitive inter-
Unstable equilibrium
states (4, 22). If pushed far enough,
with current coral
actions with macroalgae become
the ecosystem may exceed a "tipping
20
linear extension rate
more frequent and longer in dura-
point" (22) and change rapidly into
tion (Fig. 3) (23) (table S1). Al-
an alternative state with its own in-
10
Equilibrial coral cover after 50 years (%)
Algal-dominated stable equilibrium
though the ecological model only
herent resilience and stability, often
represents a single Caribbean reef
making the possibility of returning
0
habitat in a very productive physical
0.1
0.2
0.3
0.4
0.5
0.6
to a coral-dominated state difficult.
Grazing (proportion of reef grazed in 6 months)
environment and has not incor-
To examine the ecological impli-
porated several other putative con-
cations of the 20.6% reduction in
Fig. 2. Reduction in the resilience of Caribbean forereefs as coral growth
sequences of acidification such as
coral growth rate that Cooper et al.
rate declines by 20%. Reef recovery is only feasible above or to the right of
a loss of rugosity, sensitivity analy-
measured in Great Barrier Reef
the unstable equilibria (open squares). The "zone of reef recovery" (pink) is
ses reveal that changes to coral
Porites (20), we simulated a similar
therefore more restricted under reduced coral growth rate and reefs require
growth rate have a relatively large
reduction in the growth of massive
higher levels of grazing to exhibit recovery trajectories.
impact on model predictions (22),
on June 10, 2010
brooding and spawning corals on exposed Carib-
rium values of coral cover were plotted to illustrate
and therefore the conclusions of a reduction in
bean forereefs specifically to investigate what hap-
potential resilience (Fig. 2). The unstable equilibria
resilience appear to be robust.
pens to the balance between corals and macroalgae
represent thresholds, and for recovery to outweigh
in a system of high primary production (Fig. 2).
mortality reefs must lie either above or to the right
Thermal Stress, Synergies, and
The ecological model (22) simulated a 50-year time
of the threshold. For example, if coral cover is low
Ecological Feedback Loops
series for a wide range of initial coral cover and
(<5%), the intensity of fish grazing on benthic algal
The sensitivity of corals and their endosymbiotic
grazing rates by fish on benthic algae while hold-
competitors needed to shift the reef into a state
dinoflagellates (Symbiodinium spp.) to rising
ing all other factors (e.g., nutrient concentrations)
where recovery is possible (i.e., to the right or
ocean temperatures has been documented ex-
constant. Each time series revealed the underlying
above the unstable equilibrium) moves from 30%
tensively (24). Symbiodinium trap solar energy
www.sciencemag.org
trajectory of coral recovery, stasis, or degradation
to almost a half of the reef having to be grazed.
and nutrients, providing more than 95% of the
between major disturbances, and the final equilib-
This implies that in the absence of invertebrate
metabolic requirements of the coral host, which
Downloaded from
Fig. 3. Ecological feedback processes on a coral reef showing pathways of
first factor has a negative (decreasing) influence on the box indicated. Green
disturbance caused by climate change. Impact points associated with ocean
arrows denote positive (increasing) relationships. Over time, the levels of
acidification (e.g., reduced reef rugosity, coralline algae) are indicated by the
factors in hexagonal boxes will increase, whereas those in rectangular boxes
blue arrows, and impact points from global warming (e.g., bleached and
will decline. Boxes with dashed lines are amenable to local management
dead corals) by the red arrows. Boxes joined by red arrows denote that the
intervention.
www.sciencemag.org SCIENCE VOL 318 14 DECEMBER 2007
1739

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REVIEW
is consequently able to maintain high calcification
how long we stay within each of the three sce-
diversity of corals on reefs are likely to decline,
rates. When temperatures exceed summer maxima
narios will depend on the CO2 emission rate, with
leading to vastly reduced habitat complexity and
by 1° to 2°C for 3 to 4 weeks, this obligatory
each scenario highlighting the context against which
loss of biodiversity (31), including losses of coral-
endosymbiosis disintegrates with ejection of the
management and policy actions must be devised.
associated fish and invertebrates (32).
symbionts and coral bleaching (24). Bleaching and
If conditions were stabilized at the present
Coralline algae are a key settlement substrate
mortality become progressively worse as thermal
[CO2]atm of 380 ppm, that is, Coral Reef Scenario
for corals, but they have metabolically expensive
anomalies intensify and lengthen (24). Indeed,
CRS-A (Figs. 1B and 5A), coral reefs will con-
high-magnesium calcite skeletons that are very
mass coral bleaching has increased in intensity
tinue to change but will remain coral dominated
sensitive to pH (33). Hence, coral recruitment may
and frequency in recent decades (24­27). At the
and carbonate accreting in most areas of their
be compromised if coralline algal abundance de-
end of the International Year of the Reef in 1997,
current distribution. Local factors--i.e., those not
clines. Coral loss may also be compounded by an
mass bleaching spread from the Eastern Pacific to
directly related to global climate change, such as
increase in disease incidence (34). Ultimately, the
most coral reefs worldwide, accompanied by
changes to water quality--affecting levels of sedi-
loss of corals liberates space for the settlement of
increasing coral mortality during the following 12
ment, nutrients, toxins, and pathogens, as well as
macroalgae, which in turn tends to inhibit coral
months (24). Corals may survive and recover their
fishing pressure, will be important determinants of
recruitment, fecundity, and growth because they
dinoflagellate symbionts after mild thermal stress,
reef state and should demand priority attention in
compete for space and light, and also produce anti-
but typically show reduced growth, calcification,
reef-management programs. However, as we move
fouling compounds that deter settlement by
and fecundity (24) and may experience greater
toward higher [CO2]atm, coral-community compo-
potential competitors. Together these factors allow
incidences of coral disease (28, 29).
sitions will change with some areas becoming
macroalgae to form stable communities that are
To illustrate the combined effects of acidifica-
dominated by more thermally tolerant corals like
relatively resistant to a return to coral domination
tion and bleaching on reefs, we simplified the coral
the massive Porites (31) and others potentially dom-
(Figs. 2 and 3) (22, 23, 35). As a result of weak-
ecosystem into the nine features required to model
inated by thermally sensitive but rapidly coloniz-
ening of coral growth and competitive ability, reefs
feedback mechanisms (Fig. 3). Although it is not
ing genera, such as the tabulate Acropora. Under
within the CRS-B scenario will be more sensitive
comprehensive, the model provides a theoretical
the current rate of increase in [CO2]atm (>1 ppm
to the damaging influence of other local factors,
framework indicating that acidification and bleach-
year-1), carbonate-ion concentrations will drop
such as declining water quality and the removal of
ing enhance all deleterious feedbacks, driving the
below 200 mmol kg-1 and reef erosion will exceed
key herbivore fish species.
coral ecosystems toward domination by macro-
calcification at [CO2]atm = 450 to 500 ppm, i.e.,
Increases in [CO2]atm > 500 ppm (11) will
on June 10, 2010
algae and noncoral communities (Fig. 3) (table S1).
Scenario CRS-B (Figs. 1 and 5B). The density and
push carbonate-ion concentrations well below
Trajectories in Response to Climate Change
Global temperatures are projected to increase rap-
idly to 1.8°C above today's average temperature
under the low-emission B1 scenario of the IPCC,
or by 4.0°C (2.4° to 6.4°C) under the higher-
emission A1F1 scenario (Table 1) (8). Increases in
the temperature of tropical and subtropical waters
www.sciencemag.org
over the past 50 years (24) have already pushed
reef-building corals close to their thermal limits.
Projections for ocean acidification include reduc-
tions in oceanic pH by as much as 0.4 pH units by
the end of this century, with ocean carbonate
saturation levels potentially dropping below those
required to sustain coral reef accretion by 2050
(Fig. 4) (7, 10, 13). Changes in ocean acidity will
Downloaded from
vary from region to region, with some regions,
such as the Great Barrier Reef and Coral Sea, and
the Caribbean Sea, attaining risky levels of arag-
onite saturation more rapidly than others (Fig. 4).
Just as carbonate coral reefs do not exist in waters
with carbonate-ion concentrations < 200 mmol kg-1
(10), they are likely to contract rapidly if future
[CO2]atm levels exceed 500 ppm. Similarly, un-
less thermal thresholds change, coral reefs will
experience an increasing frequency and severity
of mass coral bleaching, disease, and mortality
as [CO2]atm and temperatures increase (24­27).
We have projected three scenarios for coral
reefs over the coming decades and century. In
doing so, we recognize that important local threats
to coral reefs, such as deterioration of water quality
Fig. 4. Changes in aragonite saturation {W
2-
aragonite = ([Ca2+].[CO3
])/Ksp aragonite)} predicted to occur as at-
arising from sediment and nutrient inputs associ-
mospheric CO2 concentrations (ppm) increase (number at top left of each panel) plotted over shallow-water coral
ated with coastal development and deforestation,
reef locations shown as pink dots (for details of calculations, see the SOM). Before the Industrial Revolution (280
and the overexploitation of marine fishery stocks,
ppm), nearly all shallow-water coral reefs had Waragonite > 3.25 (blue regions in the figure), which is the
may produce synergies and feedbacks in concert
minimum Waragonite that coral reefs are associated with today; the number of existing coral reefs with this
with climate change (30) (Fig. 3) [supporting on-
minimum aragonite saturation decreases rapidly as [CO2]atm increases. Noticeably, some regions (such as the
line material (SOM)]. How quickly we arrive at or
Great Barrier Reef) attain low and risky levels of Waragonite much more rapidly than others (e.g., Central Pacific).
1740
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REVIEW
Fig. 5. Extant examples of reefs from the Great Barrier Reef that are used
the locations photographed. (A) Reef slope communities at Heron Island.
as analogs for the ecological structures we anticipate for Coral Reef
(B) Mixed algal and coral communities associated with inshore reefs
on June 10, 2010
Scenarios CRS-A, CRS-B, and CRS-C (see text). The [CO2]atm and tem-
around St. Bees Island near Mackay. (C) Inshore reef slope around the
perature increases shown are those for the scenarios and do not refer to
Low Isles near Port Douglas. [Photos by O. Hoegh-Guldberg]
200 mmol kg-1 (aragonite saturation < 3.3) and sea
coral reefs as we know them today would be ex-
through their impact on coastal protection, fish-
temperatures above +2°C relative to today's val-
tremely rare at higher [CO2]atm.
eries, and tourism. These consequences become
ues (Scenario CRS-C, Fig. 1). These changes will
We recognize that physiological acclimation or
successively worse as [CO2]atm increases, and un-
reduce coral reef ecosystems to crumbling frame-
evolutionary mechanisms could delay the arrival of
manageable for [CO2]atm above 500 ppm.
works with few calcareous corals (Fig. 5C). The
some scenarios. However, evidence that corals and
Although reefs with large communities of coral
continuously changing climate, which may not
their symbionts can adapt rapidly to coral bleach-
reef-related organisms persist under CRS-A and
www.sciencemag.org
stabilize for hundreds of years, is also likely to
ing is equivocal or nonexistent. Reef-building
CRS-B, they become nonfunctional under CRS-C,
impede migration and successful proliferation of
corals have relatively long generation times and
as will the reef services that currently underpin
alleles from tolerant populations owing to con-
low genetic diversity, making for slow rates of
human welfare. Climate change is likely to fun-
tinuously shifting adaptive pressure. Under these
adaptation. Changes in species composition are
damentally alter the attractiveness of coral reefs to
conditions, reefs will become rapidly eroding
also possible but will have limited impact, as even
tourists (compare Fig. 5, A and C), which is an
rubble banks such as those seen in some inshore
the most thermally tolerant corals will only sustain
important consideration for the many low-income
regions of the Great Barrier Reef, where dense
temperature increases of 2° to 3°C above their
coastal countries and developing small island states
populations of corals have vanished over the
long-term solar maxima for short periods (24, 31).
lying within coral reef regions. Under-resourced
Downloaded from
past 50 to 100 years. Rapid changes in sea level
However, such changes come at a loss of bio-
and developing countries have the lowest capacity
(+23 to 51 cm by 2100, scenario A2) (8),
diversity and the removal of important redundan-
to respond to climate change, but many have
coupled with slow or nonexistent reef growth,
cies from these complex ecosystems. Some studies
tourism as their sole income earner and thus are at
may also lead to "drowned" reefs (36) in which
have shown that corals may promote one variety
risk economically if their coral reefs deteriorate
corals and the reefs they build fail to keep up
of dinoflagellate symbiont over another in the
(40). For instance, tourism is a major foreign ex-
with rising sea levels.
relatively small number of symbioses that have
change earner in the Caribbean basin and in some
The types of synergistic impacts on coral and
significant proportions of multiple dinoflagellate
countries accounts for up to half of the gross do-
reef-dependent organisms defined for Scenario
types (38). These phenotypic changes extend the
mestic product (40). Coral reefs in the United
CRS-B (Fig. 5B) will be magnified substantially
plasticity of a symbiosis (e.g., by 1° to 2°C) (21)
States and Australia may supply smaller compo-
for CRS-C (Fig. 5C), with probably half, and pos-
but are unlikely to lead to novel, long-lived as-
nents of the total economy, but still generate con-
sibly more, of coral-associated fauna becoming rare
sociations that would result in higher thermal
siderable income (many billions of U.S. $ per year)
or extinct given their dependence on living corals
tolerances (39). The potential for acclimation even
from reef visitors that are increasingly responsive
and reef rugosity (37). Macroalgae may dominate
to current levels of ocean acidification is also low
to the quality of reefs (41).
in some areas and phytoplankton blooms may be-
given that, in the many studies done to date, coral
Reef rugosity is an important element for the
come more frequent in others, as water quality de-
calcification has consistently been shown to de-
productivity of all reef-based fisheries, whether sub-
clines owing to the collateral impact of climate
crease with decreasing pH and does not recover as
sistence, industrial, or to supply the aquarium trade.
change on associated coastal areas, drying catch-
long as conditions of higher acidity persist (13).
The density of reef fish (32) is likely to decrease as
ments and causing episodic heavy rainfall that
a result of increasing postsettlement mortality aris-
transports nutrients and sediments into coastal areas.
Socioeconomic Impacts of Coral Reef Decline
ing from a lack of hiding places and appropriate
Whether or not one defines the transition from
The scenarios presented here are likely to have se-
food for newly settled juveniles (42). Regardless of
CRS-B to CRS-C and [CO2]atm of 450 to 500 ppm
rious consequences for subsistence-dependent so-
future climate-change influences, the total landing
as the tipping point for coral reefs, it is clear that
cieties, as well as on wider regional economies
of coral reef fisheries is already 64% higher than
www.sciencemag.org SCIENCE VOL 318 14 DECEMBER 2007
1741

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REVIEW
can be sustained, with an extra 156,000 km2 of
reef fish, especially grazers such as parrotfish,
State of Queensland Greenhouse Taskforce through the
coral reef estimated as being needed to support
would be expected to result in an improved ability
Department of Natural Resources and Mining, Townsville"
(2003).
anticipated population growth by 2050 (43). For
of coral reefs to bounce back from disturbances (51),
27. S. D. Donner, W. J. Skirving, C. M. Little, M. Oppenheimer,
example, in Asia alone coral reefs provide about
as long as other factors such as water quality are not
O. Hoegh-Guldberg, Glob. Change Biol. 11, 2251 (2005).
one-quarter of the annual total fish catch and food
limiting. Unfortunately, with the exception of marine
28. C. D. Harvell et al., Science 296, 2158 (2002).
to about 1 billion people (43). Climate-change im-
reserves, there is negligible explicit management
29. J. F. Bruno et al., PLoS Biol. 5, e124 (2007).
30. K. Newton, I. M. Cote, G. M. Pilling, S. Jennings, N. K. Dulvy,
pacts on available habitat will only exacerbate al-
of herbivores in most countries, but this could be
Curr. Biol. 17, 655 (2007)
ready overstretched fisheries resources.
improved by setting catch limits (52). Diversifica-
31. Y. K. Loya et al., Ecol. Lett. 4, 122 (2001).
The role of reefs in coastal protection against
tion of the herbivore guild to include modest den-
32. S. K. Wilson et al., Glob. Change Biol. 12, 2220 (2006).
storms (44) has been highlighted in analyses of
sities of invertebrates like sea urchins will also
33. B. Honisch, N. G. Hemming, Earth Planet. Sci. Lett. 236,
exposed and reef-protected coastlines (45, 46). We
enhance the resilience of coral reef ecosystems.
305 (2005)
34. L. Mydlarz, L. Jones, C. D. Harvell, Annu. Rev. Ecol. Evol.
do not yet have estimates for how fast reef barriers
Syst. 37, 251 (2006).
will disappear (47), but we can anticipate that
Conclusion
35. R. S. Steneck, in Proceedings of the Colloquium on Global
decreasing rates of reef accretion, increasing rates of
It is sobering to think that we have used the lower
Aspects of Coral Reefs: Health, Hazards and History,
bioerosion, rising sea levels, and intensifying storms
range of IPCC scenarios in our analysis yet still
R. N. Ginsburg, Ed. (Univ. of Miami Press, FL, 1994).
36. R. W. Grigg et al., Coral Reefs 21, 73 (2002).
may combine to jeopardize a wide range of coastal
envisage serious if not devastating ramifications for
37. N. Knowlton, Am. Zool. 32, 674 (1992).
barriers. People, infrastructure, and lagoon and es-
coral reefs. Emission pathways that include higher
38. R. Rowan, N. Knowlton, A. Baker, J. Jara, Nature 388,
tuarine ecosystems, including mangroves, seagrass
[CO
265 (1997).
2]atm (600 to 1000 ppm) and global temper-
meadows, and salt marshes, will become increas-
atures of 3° to 6°C defy consideration as credible
39. M. Stat, D. Carter, O. Hoegh-Guldberg, Plant Ecol. Evol. Syst.
8, 23 (2006).
ingly vulnerable to growing wave and storm im-
alternatives. Equally important is the fact that IPCC
40. D. L. Bryant, D. L. Burke, J. McManus, M. Spalding, Reefs
pacts. Observations of increasingly intense tropical
scenarios are likely to be cautious given scientific
at Risk: A Map-Based Indicator of Threats to the World's
hurricanes and cyclones in all oceans (48) suggest
reticence and the inherently conservative nature of
Coral Reefs (World Resources Institute, Washington, DC,
that losses of beach sand from coastal zones are
consensus seeking within the IPCC process (53).
1998).
41. H. Hoegh-Guldberg, O. Hoegh-Guldberg, Biological,
likely to increase (49). Further losses may occur
Consequently, contemplating policies that result in
Economic and Social Impacts of Climate Change on the
from reduced sand production, formed in many
[CO2]atm above 500 ppm appears extremely risky
Great Barrier Reef (World Wildlife Fund, Sydney, 2004).
cases by coral reefs, as a consequence of ocean
for coral reefs and the tens of millions of people
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on June 10, 2010
acidification and thermal stress on calcareous algae
who depend on them directly, even under the most
43. UNEP, "Marine and coastal ecosystems and human
and other sand producers. Beaches are also under
optimistic circumstances.
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Environmental Programme, 2006).
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(many thousands of km2). Nevertheless, new tech-
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niques for the mass culture of corals from frag-
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ments and spat may assist local restoration or the
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W. W. Fischer, Earth Planet. Sci. Lett. 256, 295 (2008)
the memory of Kim Mitchell, who saw the value of and
worked hard for the future of the world's natural
At the 100- to 1000-km scale of coral reefs,
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Global Change Biol., in press.
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one of the most practical interventions is to facil-
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This is likely to play an important role in situations
Supporting Online Material
23. P. J. Mumby et al., Proc. Natl. Acad. Sci. U.S.A. 104,
www.sciencemag.org/cgi/content/full/318/5857/1737/DC1
like that of the Caribbean where densities of one
8362 (2007).
SOM Text
24. O. Hoegh-Guldberg, Mar. Freshw. Res. 50, 839 (1999).
important herbivore, the sea urchin Diadema
Table S1
25. O. Hoegh-Guldberg, J. Geophys. Res. 110, C09S06 (2005).
antillarum, were decimated by disease in the early
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10.1126/science.1152509
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