C S I R O
P U B L I S H I N G
Marine
Freshwater
Research
&
Volume 50, 1999
© CSIRO Australia 1999
A journal for the publication of original contributions
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Mar. Freshwater Res., 1999, 50, 839–66
Climate change, coral bleaching and the future of the world’s coral reefs
Ove Hoegh-Guldberg
School of Biological Sciences, A08, University of Sydney, NSW 2006, Australia.
email: oveh@bio.usyd.edu.au
Abstract. Sea temperatures in many tropical regions have increased by almost 1°C over the past 100
years, and are currently increasing at ~1–2°C per century. Coral bleaching occurs when the thermal tolerance of corals and their photosynthetic symbionts (zooxanthellae) is exceeded. Mass coral bleaching
has occurred in association with episodes of elevated sea temperatures over the past 20 years and involves
the loss of the zooxanthellae following chronic photoinhibition. Mass bleaching has resulted in significant losses of live coral in many parts of the world. This paper considers the biochemical, physiological
and ecological perspectives of coral bleaching. It also uses the outputs of four runs from three models of
global climate change which simulate changes in sea temperature and hence how the frequency and intensity of bleaching events will change over the next 100 years. The results suggest that the thermal tolerances of reef-building corals are likely to be exceeded every year within the next few decades. Events as
severe as the 1998 event, the worst on record, are likely to become commonplace within 20 years. Most
information suggests that the capacity for acclimation by corals has already been exceeded, and that adaptation will be too slow to avert a decline in the quality of the world’s reefs. The rapidity of the changes
that are predicted indicates a major problem for tropical marine ecosystems and suggests that unrestrained
warming cannot occur without the loss and degradation of coral reefs on a global scale.
Extra keywords: global climate change, zooxanthellae, temperature, photoinhibition
Environmental and economic importance of the world’s
coral reefs
Coral reefs are the most spectacular and diverse marine
ecosystems on the planet. Complex and productive, coral
reefs boast hundreds of thousands of species, many of which
are undescribed by science. They are renowned for their
beauty, biological diversity and high productivity.
Coral reefs have had a crucial role in shaping the ecosystems that have dominated tropical oceans over the past 200
million years. Early scientists such as Charles Darwin
puzzled over the unusual positioning of these highly productive ecosystems in waters that are very low in the nutrients
necessary for primary production (Darwin 1842; Odum and
Odum 1955). Consequently, coral reefs are often likened to
‘oases’ within marine nutrient deserts. In the open sea surrounding coral reefs, productivity may fall as low as 0.01 gC
m–2 day–1 Hatcher (1988) and yet may be many thousands of
times higher within associated coral reef systems (e.g. algal
turfs: 280 gC m–2 day–1; corals: 40 gC m–2 day–1; benthic
microalgae: 363 gC m–2 day–1; reviewed by Hatcher 1988).
Their high productivity within these otherwise unproductive
waters makes coral reefs critical to the survival of tropical
marine ecosystems and hence of local people.
The elimination of coral reefs would have dire consequences. Coral reefs represent crucial sources of income and
resources through their role in tourism, fishing, building
materials, coastal protection and the discovery of new drugs
and biochemicals (Carte 1996). Globally, many people
depend in part or wholly on coral reefs for their livelihood,
and ~15% (0.5 billion people) of the world’s population live
within 100 km of coral reef ecosystems (Pomerance 1999).
Tourism alone generates billions of dollars for countries associated with coral reefs; $US1 billion is generated annually by
the Great Barrier Reef (Australia: Done et al. 1996), $US1.6
billion by Floridean reefs (USA: Birkeland 1997) and
~$US90 billion by reefs throughout the Caribbean (Jameson
et al. 1995).
Tourism is the fastest growing economic sector associated
with coral reefs and is set to double in the very near future.
One hundred million tourists visit the Caribbean each year
and SCUBA diving in the Caribbean alone is projected to
generate almost $US1 billion by the year 2005 (US
Department of State 1998). The fisheries associated with
coral reefs also generate significant wealth for countries with
coral reef coastlines. Annually, fisheries in coral reef ecosystems yield at least 6 million metric tonnes of fish catches
world-wide (Munro 1996) and provide employment for millions of fishers (Roberts et al. 1998). Fisheries in coral reef
areas also have importance beyond the mere generation of
monetary wealth and are an essential source of protein for
many millions of the world’s poorer societies. For example,
25% of the fish catch in developing countries is provided
from fisheries associated with coral reefs (Bryant et al. 1998).
Coral reefs also protect coastlines from storm damage,
erosion and flooding by reducing wave action across tropical
coastlines. The protection offered by coral reefs also enables
10.1071/MF99078
1323-1650/99/080839
840
the formation of associated ecosystems (e.g. seagrass beds
and mangroves) which allow the formation of essential habitats, fisheries and livelihoods. The cost of totally losing coral
reefs would run into hundreds of billions of dollars each year.
For example, the cost of losing 58% of the world’s coral reefs
has been estimated as $US90 billion in lost tourism alone
(Bryant et al.1998). If these direct costs are added to the indirect losses generated by losing the protection of tropical
coastlines, the economic effect of losing coral reefs becomes
truly staggering.
Despite their importance and persistence over geological
time, coral reefs appear to be one of the most vulnerable
marine ecosystems. Dramatic reversals in their health have
been reported from every part of the world. Between 50% and
70% of all coral reefs are under direct threat from human activities (Goreau 1992; Sebens 1994; Wilkinson and Buddemeier
1994; Bryant et al. 1998; Wilkinson 1999 this volume). Like
their terrestrial counterparts—rainforests—coral reefs are
being endangered by a diverse range of human-related threats.
Eutrophication and increased sedimentation flowing from disturbed terrestrial environments, over-exploitation of marine
species, mining and physical destruction by reef users are the
main causes of reef destruction (Sebens 1994). Mass coral
‘bleaching’ is yet another major contributing factor to decline
of coral reefs (Glynn 1993; Brown 1997a; Hoegh-Guldberg et
al.1997). Six major episodes of coral bleaching have occurred
since 1979, with the associated coral mortality affecting reefs
in every part of the world. Entire reef systems have lost almost
all their living reef-building corals following bleaching events
(e.g. Brown and Suharsono 1990).
The decline in reef systems world-wide has begun to
receive attention at the top levels of world governments.
Actions such as the recent formation of the US and
International Coral Reef Initiatives and US President William
J. Clinton’s Executive Order 13089 on 11 June 1998 emphasize this point. The latter states at one point that ‘All Federal
agencies whose actions may affect U.S. coral reef ecosystems
… should seek or secure implementation of measures necessary to reduce and mitigate coral reef ecosystem degradation
and to restore damaged coral reefs’.
The size and scale of coral bleaching, the most recent
addition to the barrage of human-related assaults on coral
reefs, has attracted considerable social, political and scientific comment. Despite this, there are many questions that
remain unanswered. For example, is coral bleaching a
natural signal that has been misinterpreted as a sign of
climate change? Has the incidence of coral bleaching
increased since 1979 or has it simply been overlooked before
1979? Are bleaching events likely to increase or decrease in
intensity in the next 100 years? These questions lie at the
heart of debate associated with human-induced climate
change and the cost that may be borne by both developed and
developing countries world-wide.
Ove Hoegh-Guldberg
This article reviews what we know about coral bleaching
and its effect on coral reef ecosystems. It reviews the scientific evidence that coral bleaching is a sign of climate change
and builds a case for the prediction that thermally triggered
coral bleaching events will increase in frequency and severity in the next few decades. In particular, this article rationalizes known thermal thresholds of coral reefs with the output
of the main global circulation models used internationally,
which all predict rapid rises in tropical sea temperature over
the next 100 years if greenhouse gas concentrations continue
to increase. The present understanding of coral bleaching
suggests that corals are not keeping up with the rate of
warming and that they may be the single largest casualty of
‘business-as-usual’ greenhouse policies. Although reefbuilding corals are not likely to not become extinct in the
long term, their health and distribution will be severely compromised for many hundreds of years unless warming is mitigated. The implications of this ‘future’ are enormous and
should be avoided with all the resources at our disposal.
Central role of symbioses in coral reefs
The central feature of shallow-water coastal ecosystems is
the predominance of symbioses between invertebrates and
dinoflagellate microalgae (zooxanthellae; Odum and Odum
1955). Coral reefs depend on an array of symbioses that
serve to restrict the outward flow of life-supporting nutrients
to the water column; corals and their zooxanthellae live by
limiting the flow of nitrogen and other essential nutrients to
the nutrient “desert” represented by tropical seas.
Muscatine and Porter (1977) emphasize this point with
respect to the endosymbiosis (one organism living inside the
cells of the other) between dinoflagellates and invertebrates.
Reef-building corals, the heart of coral reefs, are all symbiotic with a diverse range of dinoflagellates. Close association
of primary producer and consumer makes possible the tight
nutrient recycling that is thought to explain the high productivity of coral reefs.
Corals are central to coral reef ecosystems. The vigorous
growth of reef-building corals in tropical seas is responsible
for the framework of coral reef systems. While other organisms serve to weld the structure together (e.g. calcareous red
algae) and populate it (e.g. fish, algae, invertebrates and bacteria), corals have been the underlying reason for the structure of coral reef ecosystems for at least 200 million years;
they have built the primary structure of entire reefs, islands
and such massive oceanic barriers as the Great Barrier Reef.
The symbiosis between corals and zooxanthellae (Fig. 1)
has been the subject of considerable interest since the odd
brown cells of corals and other symbiotic invertebrates were
classified as separate organisms by Brandt (1881). The symbiotic dinoflagellates of corals and invertebrates from at least
five other phyla live symbiotically within the cells of their
hosts. Representatives are found in the Mollusca (snails and
Climate change, coral bleaching and the future
841
clams), Platyhelminthes (flatworms), Cnidaria (corals and
anemones), Porifera (sponges) and Protista (e.g. singlecelled ciliates).
Histology and physiology
Except in giant clams (Norton and Jones 1992; Norton et
al. 1992), zooxanthellae are intracellular (Trench 1979) and
are found within membrane-bound vacuoles in the cells of
the host. Until recently, most zooxanthellae were considered
to be members of a single pandemic species, Symbiodinium
microadriaticum. Pioneering studies by Trench (Trench
1979; Schoenberg and Trench 1980a, 1980b) and Rowan
(Rowan and Powers 1991, 1992) have revealed that zooxanthellae are a highly diverse group of organisms which may
include hundreds of taxa with perhaps as many as two or
three species per host in some invertebrate species (Rowan et
al. 1997; Loh et al. 1997).
Zooxanthellae photosynthesize while residing inside their
hosts, and provide energy and nutrients for the invertebrate
host by translocating up to 95% of their photosynthetic production to it (Muscatine 1990). Zooxanthellae selectively
leak amino acids, sugars, complex carbohydrates and small
peptides across the host–symbiont barrier. These compounds
provide the host with a supply of energy and essential compounds (Muscatine 1973; Trench 1979; Swanson and HoeghGuldberg 1998). Corals and their zooxanthellae form a
mutualistic symbiosis, as both partners appear to derive
benefit from the association. Corals receive photosynthetic
products (sugars and amino acids) in return for supplying
zooxanthellae with crucial plant nutrients (ammonia and
phosphate) from their waste metabolism (Trench 1979). The
latter appear to be crucial for the survival of these primary
producers in a water column that is normally devoid of these
essential inorganic nutrients.
Corals and the associated organisms that make up coral
reefs contribute heavily to the primary production of coral
reefs. The benefits of this production flow down a complex
food chain (Odum and Odum 1955) and provide the basis of
the most diverse marine ecosystem on the planet. Fish, bird,
marine reptile and mammal communities within coral reefs
are substantial and contrast the usually clear and unpopulated
waters that surround most coral reef ecosystems.
Mass coral bleaching and the role of temperature
Environmental factors affecting reef-building corals and
their zooxanthellae
Coral reefs dominate coastal tropical environments between
the latitudes 25°S and 25°N and roughly coincide with water
temperatures between 18°C and 30°C (Veron 1986). Below
18°C (generally at latitudes greater than 30°), the number of
reef-building coral species declines rapidly and reefs do not
form. Reefs at these temperatures are dominated by forests of
kelp and other macroalgae. While low water temperature is
Fig. 1. Symbiotic alga or zooxanthella from a reef-building coral. P, pyrenoid;
N, nucleus; Cl, chloroplast; S, starch. (Photographer: Misaki Takabayashi.)
correlated with the decline of coral reefs in a poleward direction, other variables such as light and the carbonate alkalinity of seawater (Gattuso et al 1999; Kleypas et al. 1999a)
may also play significant roles in determining the distribution of reefs. The combined influence of these factors determines how well corals compete with macroalgae and other
organisms that flourish at higher latitudes.
Reef-building corals are greatly influenced by the biological and physical factors of their environment. Predators such
as the crown-of-thorns starfish Acanthaster planci (Moran
1986) and disease greatly affect the survivorship of reefbuilding corals and a range of other coral-associated invertebrates. Temperature, salinity and light have major effects on
where reef-building corals grow. Environments in which coral
reefs prosper are also typified by a high degree of stability. Not
only are seasonal and diurnal fluctuations in tropical sea temperature generally small, but evidence suggests that mean sea
temperatures in tropical oceans may have varied by less than
2°C over the past 18 000 years (Thunnell et al. 1994). Corals
exist naturally at salinities that range from 32 to 40 (Veron
1986). Rapid decreases in salinity cause corals to die (HoeghGuldberg and Smith 1989a), an effect that probably underlies the mass mortalities of corals after severe rain storms or
flood events (Goreau 1964; Egana and DiSalvo 1982).
Fluctuations in salinity are thought to play an important role
in limiting the distribution of reef-building corals in coastal
regions. The proximity of rivers to coral reefs is a very
important determinant of reef distribution; not only are rivers
842
the principal source of sediments, nutrients and salinity stress
along tropical coastlines, but they now carry a range of other
substances that may affect corals and coral reef organisms
(e.g. pesticides, herbicides: Goreau 1992; Wilkinson and
Buddemeier 1994).
Light plays a major role in providing the energy that drives
the photosynthetic activity of the zooxanthellae (Chalker et al.
1988). Consequently, light has a profound effect on determining where corals may grow, and in influencing other aspects
such as colony morphology (Muscatine 1990). Reef-building
corals are found within the top 100 m of tropical oceans,
except in the case of some deeper-water corals in which
pigment adaptations increase the ability of the zooxanthellae
to collect light for photosynthesis (Schlichter et al. 1985).
Limits to coral growth are much shallower in areas where sedimentation reduces the transmission of light through the water
column or smothers corals. Corals may be eliminated altogether in areas where large amounts of sediment enter the sea,
such as those close to river mouths (Veron 1986). In the latter
case, sediment may have additional effects such as causing the
smothering of corals.
Corals and their zooxanthellae have some versatility with
respect to their ability to acclimatize to low or high light
intensity. Concentrations of chlorophyll and other photosynthetic pigments within zooxanthellae increase under low
light intensity (Falkowski and Dubinsky 1981; Porter et al.
1984) and decrease under high light intensity. Under
extremely high light intensity the photoinhibition of zooxanthellae can be a significant problem, and reef-building corals
and their zooxanthellae appear to have a series of ‘quenching’
mechanisms to reduce the impact of excess light (HoeghGuldberg and Jones 1999; Ralph et al. 1999). These protective
measures against high light intensity have even been reported
for corals growing on reefs at high latitudes in winter (HoeghGuldberg and Jones 1999), suggesting that light intensity over
the geographic range of corals is usually higher than these
organisms require for growth. The mechanisms by which
quenching is achieved appear to involve changes in xanthophyll pigments (Brown et al. 1999), as has been described for
sometime in higher plants (Bilger et al. 1987; DemmigAdams 1990) and marine algae (Franklin et al. 1996).
In addition to visible light (photosynthetically active radiation, PAR), short-wavelength radiation (290–400 nm) such as
ultra-violet radiation (UVR) strongly influences both the distribution and physiology of marine plants and animals (Jokiel
1980). It also has destructive effects on marine organisms
(Jokiel 1980) including corals and their symbiotic dinoflagellates (Lesser 1996; Shick et al. 1996). Effects of UVR on cultured symbiotic dinoflagellates include decreased growth rates,
cellular chlorophyll a concentrations, carbon : nitrogen ratios,
photosynthetic oxygen evolution and ribulose bisphosphate
carboxylase/oxygenase (Rubisco) activities (Banaszak and
Trench 1995; Lesser 1996). Similar effects have been reported
for symbiotic dinoflagellates living within cnidarian tissues
Ove Hoegh-Guldberg
(Jokiel and York 1982; Lesser and Shick 1989; Shick et al.
1991, 1995; Gleason 1993; Gleason and Wellington 1993;
Kinzie 1993; Banaszak and Trench 1995). Both host and symbiont have been reported to have a range of protective mechanisms to counteract the direct and indirect influences of UVR.
These include the production of mycosporine-like amino acids,
which are natural sunscreen (UVR blocking) compounds, and
a range of active oxygen scavenging systems (for review, Shick
et al. 1996).
Mass coral bleaching and its causes
Population densities of zooxanthellae in reef-building
corals range between 0.5 × 106 and 5 × 106 cells cm–2 (Drew
1972; Porter et al. 1984; Hoegh-Guldberg and Smith 1989a,
1989b). Zooxanthellae inhabiting the tissues of corals normally show low rates of migration or expulsion to the water
column (Hoegh-Guldberg et al. 1987). Despite these low rates,
population densities have been reported to undergo seasonal
changes (Jones 1995; Fagoonee et al. 1999; W. K. Fitt personal
communication). These seasonal changes are far from uniform
and probably depend on changes in the physical variables of
the immediate environment. Changes are gradual and probably represent slow adjustments of symbioses that optimize the
physiological performance of the two-genome syncytium as
the environment changes. Under a range of physical and
chemical conditions, however, sudden reductions in the
density of zooxanthellae may lead to greater rates of loss from
symbiotic corals and other invertebrate hosts (Brown and
Howard 1985; Hoegh-Guldberg and Smith 1989a).
Reduced salinity (Goreau 1964; Egana and DiSalvo
1982), increased or decreased light (Vaughan 1914; Yonge
and Nichols 1931; Hoegh-Guldberg and Smith 1989a;
Gleason and Wellington 1993; Lesser et al. 1990) or temperature (Jokiel and Coles 1977, 1990; Coles and Jokiel 1978;
Hoegh-Guldberg and Smith 1989a; Glynn and D’Croz 1990)
can cause corals and other symbiotic invertebrates to rapidly
pale. Chemical factors such as copper ions (Jones 1997a),
cyanide (Jones and Steven 1997; Jones and Hoegh-Guldberg
1999), herbicides, pesticides and biological factors (e.g. bacteria, Kushmaro et al. 1996) can also cause the loss of algal
pigments from symbiotic invertebrates. Because corals
rapidly lose colour and turn a brilliant white, this phenomenon has been referred to as ‘bleaching’. In most cases
the rapid bleaching of corals, especially during mass bleaching events, is found to be due to the loss of zooxanthellae
and/or the loss of the pigments of the zooxathellae (HoeghGuldberg and Smith 1989a).
Bleaching may occur at local scales (e.g. parts of reefs:
Goreau 1964; Egana and DiSalvo 1982) or at geographic
scales that may involve entire reef systems and geographic
realms (‘mass bleaching’: Glynn 1984; Goreau 1990; Williams
and Williams 1990; Hoegh-Guldberg and Salvat 1995; Brown
1997a). Because of the intensity and geographic scale of
recent bleaching events and associated coral mortalities, mass
843
Climate change, coral bleaching and the future
bleaching is considered by most reef scientists to be a serious
and relatively new challenge to the health of the world’s coral
reef (e.g. Glyn 1993, Goreau and Hayes 1994, HoeghGuldberg and Salvat 1995, Brown 1997a).
Increased water temperature and mass bleaching events
Most evidence indicates that elevated temperature is the
cause of mass bleaching events. Increasing water temperature
rapidly causes zooxanthellae to leave the tissues of reef-building corals and other invertebrates resulting in a reduced
number of zooxanthellae in the tissues of the host (Coles and
Jokiel 1977, 1978; Hoegh-Guldberg and Smith 1989a; Glynn
and D’Croz 1990; Lesser et al. 1990). Changes to PAR or
UVR aggravate the effect of temperature (Hoegh-Guldberg
and Smith 1989a; Gleason and Wellington 1993; Lesser
1996). But as pointed out by Hoegh-Guldberg and Smith
(1989), the effect of changes in PAR or UVR alone does not
closely match the characteristics in corals collected during
mass bleaching events. During recent global bleaching corals
were characterized by reduced population densities of zooxanthellae (with or without a decrease in zooxanthellae-specific pigments). The changes associated with mass coral
bleaching have never been reported as solely due to the loss
of photosynthetic pigments, as sometimes occurs under
extremely high PAR and UVR (e.g. Hoegh-Guldberg and
Smith 1989a; Lesser 1996).
Other factors such as reduced salinity may cause colour
loss but do not resemble corals after mass bleaching events
(Hoegh-Guldberg and Smith 1989a). For example, in some
cases of ‘bleaching’ caused by reduced salinity, loss of coral
tissue may be confused with the loss of zooxanthellae that is
characteristic of mass bleaching. Corals survive salinities
down to 23 (two-thirds the strength of seawater) but then die,
with tissue sloughing off to reveal the white skeleton below
(Hoegh-Guldberg and Smith 1989a). Although superficially
the same (i.e. whitened corals), the physiological mechanism
and the lack of tissue do not generally resemble those of
corals collected during mass bleaching events. A key characteristic of mass bleaching events (Fig. 2A) is that the host
tissue remains on the skeleton but is relatively free of zooxanthellae (Fig. 2B).
Correlative field studies have pointed to warmer-thannormal conditions as being responsible for triggering mass
bleaching events (reviews: Glynn 1993; Brown 1997a;
Hoegh-Guldberg et al. 1997; Winter et al. 1998). Glynn (1984,
1988) was the first to provide substantial evidence of the
association of mass coral bleaching and mortality with
higher-than-normal sea temperature. Glynn (1993) indicated
that 70% of the many reports of coral bleaching were associated with reports of warmer-than-normal conditions. Goreau
(1990), Glynn (1991) and Hayes and Goreau (1991) were
among the first to suggest that the projected increases in sea
temperature associated with global climate change were
likely to push corals beyond their thermal limits. The associ-
A.
B.
Fig. 2. (A) Bleached corals on northern reef slope of Moorea, French
Polynesia, 1994. (Photographer: R. Grace/Greenpeace International.)
(B) Close-up of bleached corals from Lizard Island, central Great Barrier
Reef; note fully extended polyps despite the conspicuous lack of zooxanthellae. (Photographer: O. Hoegh-Guldberg.)
ation of bleaching and higher-than-normal sea temperatures
has become even stronger with a proliferation of correlative
studies for different parts of the world (e.g. Goreau et al.
1993; Goreau and Hayes 1994; Hoegh-Guldberg and Salvat
1995; Brown 1997a; Hoegh-Guldberg et al. 1997; Jones
1997b; Jones et al. 1997; Winter et al. 1998). These studies
show a tight association between warmer-than-normal conditions (at least 1°C higher than the summer maximum) and
the incidence of coral bleaching.
The severe bleaching event in 1998 have added further
weight to the argument that elevated temperature is the
primary variable triggering coral bleaching. Not only were
most incidents of bleaching in 1998 associated with reports
of warmer-than-normal conditions, but the ‘Hotspot’
program (Goreau and Hayes 1994) run by the US National
Oceanic and Atmospheric Administration (NOAA) predicted
(days or weeks in advance) bleaching for most geographic
regions where bleaching occurred during 1998. NOAA/
NESDIS (NOAA/National Environmental Satellite Data and
844
Ove Hoegh-Guldberg
Information Service) established in January 1997 an interactive Web site based on the use of ‘hotspots’ (when sea surface
temperatures(SSTs) exceed the monthly maximum climatological value by 1°C) to predict bleaching. One of the most
graphic examples of the success of this program was the prediction of the record bleaching event on the Great Barrier
Reef sent by email to the CHAMP (Coral Health and
Monitoring Program: coral-list@coral.aoml.noaa.gov) network email list (Hendee 1998) by A. E. Strong on 10 February
1998: ‘SSTs have warmed considerably off the eastern coast
of Australia during the past few weeks. Our “HotSpot” chart
indicates bleaching may have begun in the southernmost
region of the Great Barrier Reef. To my knowledge, our SSTs
from 1984 have not seen anything quite this warm’.
What happened next was truly remarkable. The CHAMP
Network (Hendee 1998) received the first reports of bleaching on the Great Barrier Reef four days later (M. Huber,
Townsville, 14 February 1998). By 27 February, reports
(B. Willis, Bundaberg, Qld; D. Bucher, Lismore, NSW; R.
Berkelmans, Townsville, Qld) had been returned from both
the southern and northern regions of the Great Barrier Reef
that heavy bleaching was occurring on a number of inshore
reefs. By mid March, extensive surveys run by the Great
Barrier Reef Marine Park Authority (GBRMPA) (Berkelmans
and Oliver 1999) and the Australian Institute of Marine
Sciences (AIMS) revealed that the inner reefs along the entire
length of the Great Barrier Reef had experiencing a major
bleaching event. More than 100 observational reports from
other areas across the globe during 1998 that documented the
tight correlation between positive thermal anomalies and
bleaching can be obtained from the NOAA web site
(http://coral.aoml.noaa.gov, April 1999). Similar conclusions
can be drawn from events occurring during 1995–97 (Goreau
et al. 1997).
world recorded severe bleaching events (Fig. 3). In some
places (e.g. Singapore, ISRS 1998a), bleaching was recorded
for the first time. Many massive corals (which may live for
well over 1000 years) have died as a result of the 1998 event,
including some with an age of up to 700 years (ISRS 1998a);
this, although in need of study, suggests that for these corals
at least, conditions in 1998 were extreme relative to the previous 700 years.
Bleaching began in 1997–98 in the Southern Hemisphere
during summer. Incidents of bleaching in the 1997–98
episode were first reported on the CHAMP Network (Hendee
1998) in the eastern Pacific (Galapagos) and parts of the
Caribbean (Grand Cayman) in late 1997, and spread across
the Pacific to French Polynesia, Samoa and Australia by
early February 1998. Soon afterwards (March and April
1998), bleaching was being reported at sites across the Indian
Ocean, with reports being received from South-east Asia in
May 1998. As summer began in the Northern Hemisphere,
north-east Asian and Caribbean coral reefs began to bleach in
June, with bleaching continuing until early September 1998
(Fig. 4). Reports supplied to CHAMP Network on the
1997–98 bleaching episode have been archived by NOAA
(http://coral.aoml.noaa.gov, April 1999; Hendee 1998) and
have been collated by Wilkinson (1999).
The pattern associated with the 1997–98 bleaching
episode strongly resembles patterns seen during the strong
1982–83, 1987–88 and 1994–95 bleaching episodes. Southern
Hemisphere reefs (both Pacific and Indian Oceans) tend to
experience the major episodes of bleaching during
February–April, South-east Asian reefs in May, and Caribbean
reefs during July–August (CHAMP Network 1997–99,
Hendee 1998). Bleaching in the Northern Hemisphere tends to
occur after the appearance of bleaching in the Southern
Hemisphere, although this is not always the case.
Global patterns of coral bleaching
The mass coral bleaching event of 1998 is considered to
be the most severe on record (NOAA 1998; ISRS 1998a),
with bleaching affecting every geographic coral-reef realm
in the world (Fig. 3). This was the sixth major episode of
coral bleaching since 1979 to affect coral reefs across a significant portion of the world’s oceans.
Strong bleaching episodes coincide with periods of high
SST and are associated with disturbances to the El
Niño–Southern Oscillation (ENSO; Fig. 3). Most occur
during strong El Niño periods, when the Southern Oscillation
Index (SOI) is negative (< –5). However, some regions such
as the southern parts of the Cook Islands experience bleaching in strong La Niña periods due to southward shifts in the
position of the south Pacific Convergence zone and associated water masses. In 1997–98 the most extensive and
intense bleaching event on record coincided with (by some
indices) the strongest ENSO disturbance on record (Kerr
1999). For the first time, coral reefs in every region of the
Importance of light: the photoinhibition model of coral
bleaching
Elevated sea temperatures explain most incidents of mass
bleaching. It is pertinent to point out, however, that there is
still variability associated with mass bleaching events that is
not completely explained by sea temperature anomalies. At a
local scale, there is often a gradation of bleaching intensity
within colonies (Fig. 5), with the upper sides of colonies
tending to bleach first and with the greatest intensity
(Goenaga et al. 1988). Given that temperature is unlikely to
differ between the top and sides of a coral colony (mostly
because of the high thermal capacity of water), other explanations are needed.
The extent of bleaching can also differ between colonies
that are located side by side. At a geographic scale, the intensity of bleaching does not always correlate perfectly with
anomalies in SST. Aside from arguments based on instrument precision and accuracy (e.g. Atwood et al. 1992),
several other factors have been evoked to clarify patterns not
845
Climate change, coral bleaching and the future
Number of reef provinces with
moderate to severe bleaching
12
10
8
6
4
2
1978
1979
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
0
Year
Fig. 3. Number of reef provinces bleaching since 1979. (Graph modified from Goreau and Hayes
(1994) with data added for 1992 onwards.) Arrows indicate strong El Niño years.
Fig. 4. Dates and locations of when severe bleaching began in 1998. Data obtained from Coral Health and Monitoring Network
e-mail list (http://coral.aoml.noaa.gov).
completely explained by increased water temperature. These
are principally the proximal factors light intensity and the
genotype of the coral and zooxanthellae. Consideration of
these factors provides important insight into the physiological basis of mass bleaching.
The intensity of various forms of solar radiation has long
been suspected to play a role in bleaching events. Several
investigators have also proposed that elevated levels of UVR
have been instrumental in causing bleaching in corals (Jokiel
1980; Fisk and Done 1985; Harriott 1985; Oliver 1985;
Goenaga et al. 1988; Lesser et al. 1990; Gleason and Wellington
1993). Evidence, however, for a primary role of UVR has
been circumstantial and has been restricted to the observations that (1) doldrum periods (when waters are clear and
846
Ove Hoegh-Guldberg
Fig. 5. (Left) Coral showing normally pigmented regions and bleached regions to the upper (more sunlit) side of colony. (Right) Coral in shallows showing
similar pattern. (Photographer: O. Hoegh-Guldberg.)
calm and the penetration of UVR is high) have preceded some
bleaching events (e.g. Great Barrier Reef 1982–83, Harriott
1985; French Polynesia 1994, Drollet et al. 1994), (2) corals
tend to bleach on their upper, most-sunlit surfaces first, and
(3) experimental manipulation of the UVR and PAR above
reef-building corals and symbiotic anemones can also cause a
bleaching response (Gleason and Wellington 1993).
The complete absence, however, of mass bleaching events
occurring in the presence of high UVR intensity and normal
temperatures argues against high UVR intensity being a
primary factor in causing mass bleaching. The statement that
bleaching events are solely caused by UVR has not been the
claim of recent authors (e.g. Lesser 1996), who now consider
that a combination of high temperature and UVR may be
involved. Certainly, the observation that corals bleach on the
upper surfaces first during exposure to elevated temperature
argues that the quality and quantity at solar radiation are
important secondary factors (Hoegh-Guldberg 1989). Work by
Fitt (Fitt and Warner 1995) has reinforced the importance of
light quality, finding that blue light enhances temperaturerelated bleaching.
Recent evidence suggests that the fact that the upper surfaces of corals bleach before their shaded bases is more
related to presence of PAR as opposed to UVR (Jones et al.
1998; Hoegh-Guldberg and Jones 1999). The explanation for
the role that PAR plays came from a series of studies aiming
to decipher the specific site of action of heat stress on the
metabolism of the symbiotic algae. Hoegh-Guldberg and
Smith (1989) confirmed that the photosynthetic activity of
heat-stressed corals is drastically reduced, an observation
first made by Coles and Jokiel (1977) for corals affected by
the heat effluent flowing from a power plant in Hawaii. Some
of the reduced photosynthetic output seen by Coles and
Jokiel (1977) was due to the reduced population density of
zooxanthellae in the heat-stressed corals, but subsequent
studies have found that heat stress also acts to reduce the
photosynthetic rate of the zooxanthellae (Hoegh-Guldberg
and Smith 1989a; Iglesias-Prieto et al. 1992; Fitt and Warner
1995; Iglesias-Prieto 1995; Warner et al. 1996).
The application of pulse amplitude modulated (PAM) fluorometry (Schreiber and Bilger 1987) to heat-stressed corals
has initiated the identification of the component of the photosynthetic metabolism that fails when zooxanthellae are
exposed to heat stress. Variable fluorescence (measured by the
PAM fluorometer) is a relative measure of the rate at which
one of two photosystems (PS II) can use light to process electrons flowing from the water-splitting reactions of photosynthesis. This affords a measure of the efficiency (activity) of the
847
Climate change, coral bleaching and the future
H2O + O2+ MDA
APO
A.
Lumen
Stroma
H2O2
O2 -
NADP
NADPH
e-
+ ATP
Rubisco
O2
PSI
(Stromal SOD and
APO not shown)
SOD
O2 -
H+
POOL
PSII
O2
LHC
H2 O
CO2
Organic C
(Dark Reactions)
H+
NPQ
Diatoxanthin
Ascorbate
POOL
DVE
Diadinoxanthin
H2O + O2+ MDA
APO
Lumen
H+
POOL
O2
-
Stroma
H2O2
O2
O2 -
O2 PSI
eO2
H2 O
PSII
LHC
-
(Stromal SOD and
APO not shown)
O2 O2 -
O2
O2 O2 - O2 - O2 O
2
O2
O2 -
NPQ
Diatoxanthin
DVE
Diadinoxanthin
Rubisco
B.
SOD
light reactions of photosynthesis. Complete inhibition of photosynthetic oxygen evolution and a loss of variable fluorescence has been reported in cultured zooxanthellae exposed to
temperatures of 34–36°C (Iglesias-Prieto et al. 1992), and in
zooxanthellae within Caribbean corals exposed to 32° and
34°C (Fitt and Warner 1995; Warner et al. 1996). These studies
demonstrated a decrease in the efficiency of PS II when corals
and their zooxanthellae were exposed to heat and led to the
suggestion that the primary effect of temperature was to cause
a malfunction of the light reactions of photosynthesis.
However, when a PAM fluorometer was used to trace the
effects of experimental manipulations of corals from One
Tree Island on the southern Great Barrier Reef, Jones et al.
(1998) showed that first site of damage due to thermal stress
in zooxanthellae was the dark reactions of photosynthesis
and not the light reactions as previously thought (Fig. 6). A
second important observation by Jones et al (1998) was that
light amplified the extent of damage caused by thermal
stress, almost perfectly replicating the many field reports of
corals bleaching on their upper, most-sunlit surfaces
(Goenaga et al. 1988).
The key observation of this work is that coral bleaching is
related to the general phenomenon of photoinhibition (Walker
1992) and to the general response shown by terrestrial plants
and other photosynthetic organisms to heat stress (Schreiber
and Bilger 1987). Normally, increasing light intensity will
lead to an increased photosynthetic rate up to a point at which
the relationship between photosynthesis and light saturates.
At relatively high light intensities, increasing light levels
lead to the over-reduction of the light reactions and the production of potentially harmful products such as oxygen free
radicals. Oxygen free radicals, if not detoxified by several
enzyme systems found in higher plants (and zooxanthellae,
Lesser 1996) will rapidly lead to cellular damage. In the case
of higher plants, failure of the ability of the dark reactions to
process photosynthetic energy results in an increased sensitivity of these organisms to photoinhibition. The overriding
conclusion of the work of Jones et al. (1998) and HoeghGuldberg and Jones (1999) is that bleaching is due to a lowering of the sensitivity of zooxanthellae to photoinhibition.
Basically, light, which is essential for the high productivity of
coral reefs under normal conditions, becomes a liability under
conditions of higher than normal temperatures.
The model presented in Fig. 6 has a number of properties
that lead to predictions and explanations outlined in Table 1.
Firstly, PAR assumes an important secondary role to that of
UVR. Although temperature has to be higher than normal for
a mass bleaching event to occur, light will cause damage to the
photosystems even at normal intensities when water temperature is elevated above a critical maximum (Property 1, Table
1). This explains the frequent observation that the extent of
damage is light dependent (Goenaga et al. 1988, Salih et al.
1997a) and that most coral bleaching starts on the upper, moresunlit surfaces of corals. It also links thermal-stress-related
CO2
Organic C
(Dark Reactions)
H+
Ascorbate
POOL
Fig. 6. Photoinhibition model of coral bleaching (Jones et al. 1998).
Detail of events occurring on the thylakoid membrane of the chloroplast of
zooxanthellae. (A) Under normal circumstances, the two photosystems (PSI
and PSII) pass light energy to the dark reactions where CO2 is fixed by the
enzyme Rubisco. The amount of light energy flowing to the dark reactions
is regulated by the interconversion of the two pigments diatoaxanthin and
diadinoxanthin. Any active oxygen (O 2– ) is soaked up by the SOD and APO
enzyme systems. (B) Heat stress interrupts the flow of energy to the dark
reactions. The light reactions are then destroyed by the buildup of light
energy which is passed to oxygen rather than the dark reactions, creating
active oxygen that then begins to denature the proteins that make up the photosynthetic components of the zooxanthellae. Not shown are the singlet
oxygen species that are generated in PSII, by triplet chlorophyll in the reaction centre, and which are more abundant when PSII is over-reduced in high
light under heat stress. SOD, superoxide dismutase; APO, ascorbate peroxidase; VDE, violaxanthin de-epoxidase.
bleaching directly to the solar bleaching studied by Brown and
co-workers (Brown et al. 1994a; Brown 1997a).
Brown (1997a) has already made the important link
between photo-protective measures adopted by zooxanthellae and coral bleaching, and suggests that photo-protective
measures are likely to play an important part in the way that
corals and their zooxanthellae may be able to limit the effect
of bleaching stresses arising from a combination of increased
temperature and irradiance in the field. This linkage also
848
Ove Hoegh-Guldberg
explains several unusual bleaching patterns, such as when the
bases but not the tips bleached in relatively shallow populations
of Montastrea spp. in Panama in 1995. In this case, more lighttolerant zooxanthellae (found in the tips) were actually more
resistant to thermal stress than shade-adapted genotypes living
in other places within the same colonies (Rowan et al. 1997).
Property 2 (Table 1) emphasizes the fact that zooxanthellae that
are able to evoke protective measures by acclimation (phenotype) or through adaptation (genotype) should be more tolerant
of anomalous high sea temperature. Property 3 predicts that any
stress (chemical or physical) that blocks the energy flow to the
dark reactions will lead to photoinhibitory stresses at lower
light intensities. Symptoms similar to bleaching will follow. So
far, the response of corals and their zooxanthellae to cyanide
appears to conform to the same model, as discussed by Jones
and Hoegh-Guldberg (1999). One might expect other factors
that block the dark reactions or lead to the over-energization of
the light reactions of photosynthesis to exhibit similar symptoms (e.g. herbicides, UVR, high PAR stress).
Climate change and coral bleaching
Why is the incidence of bleaching increasing?
One of the most important questions facing scientists,
policy makers and the general public is the question of why
there has been an apparent increase in the incidence of coral
Table 1.
bleaching and mortality since 1979. Since 1979, scores of
reports of mass bleaching events have been made in the
primary literature. Prior to 1979, reports of bleaching events
in the primary literature are virtually non-existent and are
restricted to largely unpublished observations or recollections (e.g. Puerto Rican bleaching in 1969, Winter et al.
1998). Some commentators have suggested that the answer
lies in the increase in the number of reef observers and the
ease with which these reports can be brought to the attention
of the scientific community (e.g. Internet). Although this
argument is probably true to some extent, it does not explain
the absence of scientific reports of mass coral bleaching
around intensively studied sites such as those around
research stations (e.g. Heron Island, Australia; Florida Keys,
USA) and tourist resorts prior to 1979. Underwater film
makers who filmed extensively on the Great of Barrier Reef
during the 1960s and 1970s never saw coral bleaching on the
scale seen since 1979 (e.g. Valerie Taylor, personal communication). It seems certain that brilliant white coral as far as
the eye could see, plus the associated mortality and stench
from bleached reefs that had died would have been noticed.
Similarly, indigenous fishers, who have an extensive knowledge of coral reefs, seem to have been unaware of coral
bleaching in the past and do not appear to have a traditional
terminology to describe it (e.g. French Polynesia, HoeghGuldberg unpublished; Okinawa, Y. Laya, pers. comm.).
Predictions or explanations stemming from the Photoinhibition model of coral bleaching proposed by Jones et al. (1998)
Prediction or Explanation
Support or Further prediction
(1) Light (PAR) is required for elevated temperature to trigger
bleaching. The extent of damage during bleaching will be directly
correlated with the intensity of light. Elevated temperature will
have a reduced effect if corals are shielded from normal sunlight.
May indicate possible ways to effect small-scale amelioration
during bleaching conditions (e.g small-scale shading of sections
of reef with high tourist or other value).
(a) Upper surfaces of corals bleach preferentially in most cases (Goenaga et al. 1988;
Jones et al. 1998). But see complication outlined in Prediction 2.
(b) Species with deeper tissues (hence more shade) are more resistant to bleaching.
Hence, the deeper tissues of Porites spp. are less susceptible to bleaching than the veneer
tissue configuration of Acropora spp. or Pocillopora spp. (Salvat 1991; Gleason 1993;
Glynn 1993; Hoegh-Guldberg and Salvat 1995). This explains some of the variability
among sites and depths in coral communities (e.g. Hoegh-Guldberg and Salvat 1995)
(c) Tissue retraction may be an important mechanism that some species use to reduce
damage during thermal bleaching stress as suggested for solar bleaching by Brown et al.
(1994b).
(d) Coral species have mechanisms (pigmentation) by which they shade their zooxanthellae during bleaching stress (Salih et al. 1997a; Hoegh-Guldberg and Jones 1999).
Enhanced fluorescence of stressed corals may represent attempts to bolster this strategy.
(2) Coral and zooxanthella species that are better able to photoacclimatize may be better able to resist bleaching stress.
Differences in the ability to resist bleaching stress will be related
to the ability to produce and regulate accessory pigments such as
the xanthophylls (Brown 1997a; Hoegh-Guldberg and Jones
1999; Brown et al. 1999).
(a) Light-adapted zooxanthellae (putatively Clade A) are better able to resist thermal
stress in Montastrea spp. than shade-adapted genotypes (Clade C, Rowan et al. 1997).
(b) Patterns associated with bleaching will be complicated by genotype, acclimatory state
and environment interactions. This may explain some depth gradients that show greater frequencies of bleaching in deeper water but communities with similar species compositions.
(3) Any stress that blocks the dark reactions before the light reactions of photosynthesis will result in similar bleaching phenomena.
(a) Cyanide stress results in a series of responses that are identical to those seen during
temperature-related bleaching (Jones and Hoegh-Guldberg 1999).
(b) UVR enhances bleaching. Lesser et al. (1990) speculated that a similar blocking of
the principal carboxylation enzyme in zooxanthellae could lead to a buildup of redox
energy within the light reactions of zooxanthellae. This is essentially consistent with
Jones et al. (1998).
849
Climate change, coral bleaching and the future
Although rigorous analysis is needed, it appears that the case
for regular yet unnoticed massive bleaching events prior to
1979 is extremely scant at best.
So why have bleaching events increased in frequency
since 1979? Given the strong correlation between bleaching
events and high sea surface temperatures (Goreau and Hayes
1994), recent and historic SSTs should provide insight into
the triggers of the recent series of strong mass bleaching
episodes. The following analysis reveals the answers to both
these questions.
Tropical seas have undergone warming in the past 100 years
(Bottomley et al. 1990; Brown 1997a; Cane et al. 1997; Winter
et al. 1998; see also historic temperature data for seven tropical
sites, Table 2). Coral cores from the central Pacific confirm this
warming trend (Wellington, Linsley and Hoegh-Guldberg,
unpublished). Increases of 1–2°C in sea temperature are
expected by 2100 in response to enhanced concentrations of
atmospheric greenhouse gases (Bijlsma et al. 1995). Goreau
(1990), Glynn (1991) and many others (e.g. Hoegh-Guldberg
and Salvat 1995; Brown 1997a) have pointed to the significance of this trend for reef-building corals and have stated
variously that global climate change is likely to increase the
frequency and intensity of bleaching.
Trends in SST can also be used to shed light on the
apparent advent of mass coral bleaching since 1979 and on
how the frequency of mass coral bleaching will change in
the next few decades. Sea temperatures over the past 20
years, extensively measured and cross-compared by instruments on satellites, ships and buoys, have shown upward
trends in all regions, and blended data from the three sources
have shown that rates of change are now greater than 2°C
per century in many tropical seas (Table 3; IGOSS-nmc
blended data, Integrated Global Ocean Services System,
http://ioc.unesco.org/igossweb/igoshome.htm). Simple correlations (P ≤ 0.05 in all cases, most with P < 0.001) through
IGOSS-nmc blended data reveal rates of change in SST that
range from 0.46°C per century (northern Great Barrier Reef)
to 2.59°C per century (central Great Barrier Reef, waters off
Townsville, Qld).
These trends may reflect longer-term cycles of change.
However, they have been confirmed by a growing number
studies of SST trends that go back at least 40–150 years using
Table 2. Rates of warming detected by regression analysis within Trimmed Monthly Summaries from the
Comprehensive Ocean-Atmosphere Data Set (COADS, up to Dec 1992) and IGOSS-nmc blended data (January
1993–April 1999)
Data obtained from the Lamont Doherty Earth Observatory server (http://rainbow.ldgo.columbia.edu/). Data were included
only if all months were recorded (hence shorter periods for some parts of the world). All trends were highly significant with
the possible exception of Rarotonga. GBR, Great Barrier Reef
Locality
Position
Jamaica
Phuket
Tahiti
Rarotonga
Southern GBR
Central GBR
Northern GBR
17.5°N,76.5°W
7.5°N,98.5°E
17.5°S,149.5°W
21.5°S,159.5°W
23.5°S,149.5°E
18°S,147.5°E
11°S,143°E
Period of data examined
Rate
(°C per 100 years)
1903–99
1904–99
1926–99
1926–99
1902–99
1902–99
1903–99
1.25
1.54
0.69
0.84
1.68
1.55
1.25
Significance of trend
< 0.001
< 0.001
0.003
0.05
< 0.001
< 0.001
< 0.001
Table 3. Rates of warming in tropical oceans for period 1981–99
Rates determined from regressions done on Integrated Global Ocean Services System (IGOSS) nmc blended weekly sea surface temperature data obtained from data sets available at the Lamont Doherty Earth Observatory server (http://rainbow.ldgo.columbia.edu/).
Seasonal variability within the data was removed by applying a 12-month moving-point average before the regression analysis.
GBR, Great Barrier Reef
Locality
Position
Jamaica
Phuket
Tahiti
Rarotonga
Southern GBR
Central GBR
Northern GBR
17.5°N,76.5°W
7.5°N,98.5°E
17.5°S,149.5°W
21.5°S,159.5°W
23.5°S,149.5°E
18°S,147.5°E
11°S,143°E
Rate
(°C per 100 years)
Significant of trend
2.29
2.30
1.44
2.27
2.54
2.59
0.47
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
Other data
2.53, Winter et al. (1998)
1.26, Brown (1997a)
850
other data sets and such sources as coral cores (e.g. Brown
1997a; Winter et al. 1998). For example, measurements
made by researchers at the research station at La Parguera in
Puerto Rico registered a rate of change of 2.53°C per century
(Winter et al. 1998) while the IGOSS-nmc data for the same
area records a rate of increase of SST of 2.29°C per century
(Table 3). Similar comparisons can be made between rates of
change reported by Brown (1997a) using different data
(MOHSST 6) going back to 1946 (Brown 1997a: 1.26°C per
century v. 2.30°C per century reported here). There is no evidence of a slowing or reversing of this rate of change.
Whereas small errors have been noted for pure satellite
SST data (Hurrell and Trenberth 1997), blended data have the
advantage that bias is reduced or eliminated as data are generally confirmed (usually) by several sources. Correlations
between in situ instrument readings at study sites on coral
reefs and blended SST data are high, as shown by numerous
authors including Wellington and Dunbar (1995) and Lough
(1999). For example, Lough has shown that regressions
between IGOSS-nmc blended data and in situ data have
regression coefficients that range between 0.93 and 0.98 for
five sites on the Great Barrier Reef.
Will the frequency and intensity of coral bleaching continue
to increase?
An important question follows from the fact that sea
surface temperatures in the tropics are increasing: How will
increases in SST affect the frequency and severity of bleaching events in the future? We can deduce the thermal thresholds of corals and their zooxanthellae from the past
behaviour of corals during bleaching events over the past 20
years. This is the basis for the highly successful predictions
of the ‘Hotspot’ program (Strong et al. 1998). If this is combined with projections of future SSTs then the number of
times that thermal thresholds are exceeded can be predicted.
If corals are not adapting or acclimating fast enough, then
each of these points will translate as a bleaching event. The
issue of adaptation or acclimation is discussed below. Corals
have acclimatory abilities in many circumstances (Gates and
Edmunds 1999), but evidence from the past 20 years suggests that corals and their zooxanthellae are not able to acclimatize or adapt fast enough to the short, sporadic thermal
events typical of recent ‘bleaching’ episodes.
Projecting future changes to sea temperatures can not be
based solely on what has happened in the past. Seasonality and
differences between years due to variation in the strength of
the El Niño–Southern Oscillation complicates attempts to
predict future tropical sea temperatures. Additionally, use of
data from the past 20 years to predict the future has the
problem that stochastic and improbable events (e.g. the
cooling effects of two major volcanic eruptions over the past
20 years) would be extrapolated at a high frequency to future
temperature trends. Global Circulation Models (GCMs), that
show an increasing level of accuracy and coherence, however,
Ove Hoegh-Guldberg
provide an opportunity to examine how sea temperatures are
likely to change in the future.
SST data for this study were simulated using the following Global Circulation Models (GCM):
(A) ECHAM4/OPYC3 IS92a. The global coupled atmosphere–ocean–ice model (Roeckner et al. 1996) was developed by the Max-Planck-Institut für Meteorologie and is used
by the United Nations for climatology simulations. Data from
this model run and those described below in B and C were
kindly provided by Dr Axel Timmermann of KNMI,
Netherlands. Horizontal resolution is roughly equivalent to 2.8°
× 2.8° latitude–longitude. This model has been used in studies
of climate variability (Roeckner et al. 1996; Bacher
et al 1997; Christoph et al. 1999), climate prediction (Oberhuber
et al. 1998) and climate change with a high degree of accuracy
(Timmermann et al. 1999; Roeckner et al. in press). In order to
reduce the drift of the unforced-coupled model, a yearly flux
correction for heat and freshwater flux was employed. Simulation of the El Niño–Southern Oscillation is essential for
approximating tropical climate variability and is handled well
by the ECHAM4/OPYC3 model (Roeckner et al. 1996;
Oberhuber et al. 1998; Timmermann 1999). Changes in greenhouse gases that were used in the model were derived as
follows: Observed concentrations of greenhouse gases were
used up to 1990, and changes outlined in the IPCC scenario
IS92a (IPCC 1992) were implemented thereafter. The midrange emission scenario (IS92a) is one of six specified by the
Intergovernmental Panel on Climate Change (IPCC) in 1992.
It is the central estimate of climate forcing by greenhouse
gases and assumes a doubling of 1975 CO2 levels by the year
2100, with sulfate aerosol emissions, which have a cooling
effect, remaining at 1990 levels. Greenhouse gases are prescribed as a function of time: CO2, CH4, N2O and also a series
of industrial gases including CFCs and HCFCs.
(B) ECHAM4/OPYC3 IS92a (with aerosol integration),
the global coupled atmosphere–ocean–ice model (Roeckner
et al. 1996) but with the influence of aerosols added. Horizontal resolution is also roughly equivalent to 2.8° × 2.8° latitude–longitude. Changes in greenhouse gases and aerosols
were prescribed as follows. Observed concentrations of
greenhouse gases and sulfate aerosols were used up to 1990,
and changes outlined in the IPCC scenario IS92a (IPCC
1992) were implemented thereafter. Greenhouse gases are
prescribed as a function of time: CO2, CH4, N2O and also a
series of industrial gases including CFCs and HCFCs. The
tropospheric sulfur cycle was also incorporated but with only
the influence of anthropogenic sources considered. Natural
biogenic and volcanic sulfur emissions are neglected, and the
aerosol radiative forcing is generated through the anthropogenic part of the sulfur cycle only.
(C) ECHAM3/LSG IS92a. This earlier model differs substantially from its descendant ECHAM4/OPYC3. The LSG
ocean model and the ECHAM3 atmosphere model are
coupled via the heat, freshwater and momentum fluxes.
851
Climate change, coral bleaching and the future
Ocean SSTs plus a few correction terms are taken as boundary conditions for the atmosphere. In order to avoid climate
drift in the coupled mode, the flux-correction technique
(Sausen et al. 1988) is applied, which is equivalent to coupling
both subsystems by their individual flux-anomalies relative to
their equilibrium states. Horizontal resolution is approximately
equivalent to 5.6° × 5.6° latitude–longitude. ECHAM3/LSG is
built on a different ocean model to ECHAM4, and only crudely
captures thermocline processes. El Niño-related variability is
underestimated by a factor of three. Further details of the model
and the coupling strategy can be found in Voss et al. (1998) and
Maier-Reimer et al. (1993). Changes in greenhouse gases were
derived as in A (above).
(D) CSIRO DAR Model. This coupled model with dynamic
sea ice is run by the Division of Atmospheric Research at
Australia’s Commonwealth Scientific and Industrial Research
Organisation (CSIRO). It is a comprehensive coupled model
that contains atmospheric, oceanic, sea-ice and biospheric
submodels. The resolution is to 5.6° longitude by 3.2° latitude. The model is described in full by Gordon and O’Farrell
(1997). Greenhouse gas concentrations were derived for use
as follows. Historic concentrations (CO2 equivalents) from
the IPCC combined historic data were used up to 1990. After
that, emissions specified by the IS92a scenario were used
(IPCC 1992).
Temperatures were generated for each month from 1860
to 2100 (2060 in the case of model B). Data generated by all
four models for past sea temperatures show a close correspondence to actual sea temperature records. The later-generation model runs (ECHAM4, A and B) performed the best
with respect to this criterion. Model C simulates El Niño with
a high degree of realism (Timmermann et al. 1999) and shows
similar mean and maximal values as well as range of sea temperatures (Table 4). Mean sea temperatures predicted for the
period November 1981 to December 1994 were approximately 0.05° and 1.22°C greater than the temperatures in the
IGOSS-nmc data set. As outlined above, summer maximum
temperatures are the key factors that predict when corals will
bleach. Maximum temperatures predicted by model A were
only –0.15° to 0.46°C different from the summer maxima
reported in the IGOSS-nmc data set (Table 4). A similar situation held for SST data in the other three models (Table 5A,
5B). In this case, the predicted mean summer temperatures
(calculated from the average of the sea temperatures over
three months) were generally within 0.5°C of the observed
mean summer temperatures for data from 1903 to 1999. Only
model D delivered a few of the larger differences on a consistent basis.
The thermal thresholds of corals were derived by using the
IGOSS-nmc data set and both literature and Internet reports of
bleaching events (Glynn 1993; Goreau and Hayes 1994;
Hoegh-Guldberg and Salvat 1995; Brown 1997a; HoeghGuldberg et al. 1997; Hendee 1998; Jones et al. 1998; CHAMP
Network 1999). For example (Fig. 7), bleaching events were
reported in French Polynesia (17.5°S,149.5°W,) in 1983,
1986, 1991, 1994, 1996 and 1998 and correspond to periods
when SSTs rose above 29.2°C. This temperature was consequently selected as the presumed thermal trigger for corals at
this locality (Hoegh-Guldberg and Salvat 1995, see also
Brown 1997a, Hoegh-Guldberg et al. 1997). This was
repeated for the south coast of Jamaica (17.5°N,76.5°W),
Phuket (7.5°N,98.5°E), Rarotonga (21.5°S,159.5°W), and
three sites on the Great Barrier Reef—in the southern (23.5°S,
149.5°E), central (18°S,147.5°E) and northern (11°S,143°E)
sections. Thermal thresholds (Figs 8 and 10; Rarotonga not
shown) ranged from 28.3°C at Rarotonga to 30.2°C at
Phuket (previously reported by Brown 1997a). Table 6 lists
the thermal thresholds derived and used in this study.
The sea temperature data generated by the GCM model
runs were used with the threshold values to predict the frequency and intensity of coral bleaching. Differences between
predicted and observed sea temperature data (although
minor) were subtracted from model data prior to analysis
(using data from 1903–94, Table 5b). An example of the
Table 4.
Comparison between Integrated Global Ocean Services System (IGOSS) nmc blended monthly sea surface
temperature data and output from the global coupled atmosphere–ocean–ice model (ECHAM4/OPYC3, Roeckner et al. 1996)
IGOSS-nmc data available from Lamont Doherty Earth Observatory (http://rainbow.ldgo.columbia.edu/) and model data kindly provided
by Dr Axel Timmermann of KNMI, Netherlands. All data are in °C. GBR, Great Barrier Reef
Locality
Jamaica (S coast)
Phuket
Tahiti
Rarotonga
GBR (S)
GBR (C)
GBR (N)
Mean
(IGOSSnmc)
Mean
ECHAM4/O
PYC3a
27.95
29.08
27.51
25.43
25.04
26.21
27.39
28.36
29.13
27.85
26.35
26.25
27.43
28.38
Difference
0.41
0.05
0.34
0.92
1.21
1.22
0.99
Max
(IGOSSnmc)
Max
ECHAM4/
OPYC3a
Difference
29.40
30.48
29.57
28.49
28.51
29.61
29.89
29.25
30.87
29.96
28.88
28.87
30.07
30.38
–0.15
0.39
0.39
0.39
0.36
0.46
0.48
Range
(IGOSSnmc)
3.24
2.70
3.92
5.59
8.27
7.28
5.45
Range
ECHAM4/
OPYC3a
1.95
3.00
3.46
4.42
5.08
4.76
3.62
852
Ove Hoegh-Guldberg
Table 5. Differences between summer sea surface temperatures (Integrated Global Ocean Services
System (IGOSS) nmc blended monthly sea surface temperature data) and summer sea surface temperatures calculated from the global coupled atmosphere–ocean–ice model (ECHAM4/OPYC3,
Roeckner et al. 1996) with and without the influence of aerosols
IGOSS-nmc data obtained from Lamont Doherty Earth Observatory (http://rainbow.ldgo.columbia.edu/) and
model data kindly provided by Dr Axel Timmermann of KNMI, Netherlands and the Commonwealth Scientific
and Industry Research Organisation (CSIRO Australia). Summer temperatures were calculated using the mean
SST for the three-month period (January–March, Southern Hemisphere; June–August, Northern Hemisphere)
for the periods from (a) 1981–99 and (b) 1903–94. All data are in °C. GBR, Great Barrier Reef
Locality
ECHAM4/OPYC3a
ECHAM4/OPYC3a
(with aerosol effect)
ECHAM3/LCG
CSIRO-DAR
(a) 1981–99
Jamaica (S coast)
Phuket
Tahiti
Rarotonga
GBR (S)
GBR (C)
GBR (N)
0.44
0.44
0.39
–0.05
–0.05
–0.36
–0.15
0.73
0.32
–0.10
0.16
0.01
–0.34
0.37
–0.59
–0.28
–1.16
–1.25
–0.98
–1.06
–0.99
0.60
–0.23
0.76
0.50
2.14
1.13
0.47
(b) 1903–94
Jamaica (S coast)
Phuket
Tahiti
Rarotonga
GBR (S)
GBR (C)
GBR (N)
–0.03
–0.04
0.03
–0.58
0.10
0.15
–0.15
–0.32
0.23
0.31
–0.69
0.26
0.28
–0.62
0.26
–0.13
1.30
0.30
0.72
0.66
0.42
–0.54
0.08
–0.10
–0.98
–1.20
–1.19
–0.82
Sea Surface Temperature (oC)
Table 6.
Estimated temperatures at which corals bleach (thermal
thresholds) for seven sites)
GBR, Great Barrier Reef. Thermal thresholds were derived by comparing
reports of when bleaching events have occurred since 1979 with weekly sea
temperature records obtained from IGOSS-nmc blended data from the
Lamont-Doherty Climate Center at Columbia University
30
29
28
Locality
27
Jamaica
Phuket
Tahiti
Rarotonga
Southern GBR
Central GBR
Northern GBR
26
1999
1998
1997
1996
1995
1994
1993
1992
1991
1990
1989
1987
1986
1985
1984
1983
1982
1981
25
Fig. 7. Weekly sea surface temperature data for Tahiti (17.5°S,149.5°W).
Arrows indicate bleaching events reported in the literature. Horizontal line
indicates the minimum temperature above which bleaching events occur
(threshold temperature). IGOSS-nmc blended data courtesy of the LamontDoherty Climate Center at Columbia University.
analysis comparing predicted sea temperature data from
model A and the known thermal thresholds of corals for
seven sites in tropical oceans is shown in Figs 8, 9, 10 and 11.
Model A, like the other three, shows the universal trend
within tropical seas of increasing sea temperature under the
Position
(°C)
Thermal threshold
17.5°N,76.5°W
7.5°N,98.5°E
17.5°S,149.5°W
21.5°S,159.5°W
23.5°S,149.5°E
18°S,147.5°E
11°S,143°E
29.2
30.2
29.2
28.3
28.3
29.2
30.0
moderate global climate change scenario, IS92a. Model A
also includes the most accurate simulation of El Niño activity
(Timmermann et al. 1999; Roeckner et al. in press) and confirms that future ENSO events are likely to reach higher and
higher sea temperature thresholds. By comparing simulated
sea temperatures to the thermal thresholds listed in Table 6,
we can estimate the frequency with which sea temperatures
will exceed the thermal threshold of corals and their zooxanthellae. If corals are incapable of changing their physiology
to cope with this stress, bleaching will occur. As men-
853
Climate change, coral bleaching and the future
tioned previously, the key assumption here is that reef-building corals and their zooxanthellae are unable to adapt (genetically) fast enough or acclimate (phenotypically) to sporadic
thermal stress.
The change in the frequency of bleaching events per
decade predicted by the four models is shown in Figs 9 and
11. The trends in these graphs reveal four important points
that are confirmed by all four model runs. Firstly, the frequency of bleaching is set to rise rapidly, with the rate being
highest in the Caribbean and slowest in the Central Pacific.
Secondly, the intensity of bleaching will increase at a rate
proportional to the probability that the thermal maxima of the
corals will be exceeded by future SSTs. Thirdly, most regions
will be experiencing bleaching conditions every year within
30–50 years. Lastly, the reason for the relatively low frequency of bleaching events before 1979 becomes clear; tropical sea temperatures have been rising over the past 100 years
(Bijlsma et al. 1995) and have brought corals ever closer to
their upper thermal limit. The ability for an El Niño event to
trigger bleaching was only reached in most oceans in the
period from 1970 to 1980 (the abscissa intercept values of the
rapid rise in the frequency of bleaching events in Figs 9 and
11 occurs around 1970–1980). This explains why mass bleaching events are not seen to any great extent before 1979 (Table 7).
This conclusion is also supported by the actual sea temperatures records from the Comprehensive Ocean-Atmosphere
Data set (COADS, up to December 1992) and IGOSS-nmc
blended data set (January 1993–April 1999).
The use of a number of powerful climate models has
important ramifications for the conclusion of this report.
Firstly, the conclusions are not dependent on which climate
model is used. A second important point can be made. The
Table 7.
Fig. 8. Sea surface temperature data generated by the global coupled
atmosphere–ocean–ice model (ECHAM4/OPYC3, Roeckner et al. 1996)
and provided by Dr Axel Timmermann of KNMI, Netherlands. Temperatures were generated for each month from 1860 to 2100, and were forced
by greenhouse gas concentrations that conform to the IPCC scenario IS92a
(IPCC 1992). Effects of El Niño–Southern Oscillation (ENSO) events are
included. Horizontal lines indicate the thermal thresholds of corals at each
site. Date were generated for four regions: Tahiti (17.5°S,149.5°W), Phuket
(7.5°N,98.5°E), Jamaica (17.5°N,76.5°W), and Rarotonga (data not shown).
fact that all seven sites within the three models (4 runs) all
show the same increasing trends, suggest that the trends
illustrated by this analysis are a consistent feature of projected climate change over the next century. Thirdly, factors
such as cooling by anthropogenic aerosols produce only
Major issues resolved by the examination of the patterns of increasing sea temperature
(1) Why are corals growing so close to their thermal limit?
Before recent increases in sea temperature, corals and their zooxanthellae lived in water that
typically never rose above their maximum thermal limits. Because of the increases in SST
over the past hundred years (~1°C), corals are now just below their upper thermal limits.
Before this warming, corals would always have been a degree or two below these critical
level in summer. The fact that corals are so close to their thermal limits is also evidence that
they have not been able to acclimatize or adapt to these increase to any real extent.
(2) Why are there few reports of coral bleaching
before 1979?
Increases in sea temperatures have only become critical since the late 1970s, when El
Niño events disturbances began to exceed the thermal tolerances of corals and their zooxanthellae. Before this, El Niño disturbances did not exceed the thermal limits of corals and
zooxanthellae on a regular basis.
(3) Will coral bleaching increase in the future?
Bleaching events are likely to increase in frequency until they become annual by 2050 in
most oceans. In some areas (e.g. south-east Asia, Caribbean, GBR) this will occur more
rapidly (by 2020). In 30–50 years from now, bleaching will be triggered by seasonal
changes in water temperature and will no longer depend on El Niño events to push corals
over the limit. This will become critical as bleaching events exceed the frequency at which
corals can recover from bleaching-related mortality. Most evidence suggests that coral
reefs will not be able to sustain this stress and a phase shift to algae-dominated communities is a likely outcome.
854
Ove Hoegh-Guldberg
Fig. 9. Number of times per decade that predicted temperatures (see Fig. 8) exceed coral threshold levels
(bleaching events) for (A) Jamaica (17.5°N,76.5°W), (B) Phuket (7.5°N,98.5°E), (C) Tahiti (17.5°S,149.5°W)
and (D) Rarotonga (21.5°S,159.5°W). Key to models: j ECHAM4/OPYC3; h ECHAM4/OPYC3 with
aerosol effect added; mECHAM3/LSG; and r CSIRO DAR GCM.
minor delays (mostly ~20–40 years) in the rate of warming
of tropical seas. If the critical point for coral reefs occurs
when bleaching occurs every two years with the intensity of
the 1998 event, then these delays will be less (10–20 years;
compare with and without aerosols in Figs 9 and 11).
The conclusions of this analysis are a matter of great
concern. If sea temperatures continue to increase with time
and corals continue to show an inability to acclimatize or
adapt fast enough to these changes, coral bleaching events
will increase in frequency and intensity (proportional to the
size of the thermal anomaly) with serious consequences. It is
hard to believe that coral reefs will be able to survive yearly
bleaching events (let alone events every two years) of the
same scale and intensity of the bleaching episode in 1998. By
approximately 2050, however, sea temperatures in tropical
oceans will experience anomalies every year that will be
several times those seen in 1998.
Biotic responses to changes in sea temperature: acclimation v. adaptation
A crucial part of what will happen to reef-building corals
depends on how they and their zooxanthellae will respond to
the increases in sea temperature outlined here and by leading
climate physicists (e.g. 1–2°C by 2100, IPCC 1992, Bijlsma
et al. 1995). There are two broad ways that marine biota can
respond to temperature change (Clarke 1983). Firstly, marine
organisms can ‘acclimatize’ by modifying the various component processes that make up their cellular metabolism to
perform better at the new temperatures; for example, corals
might be able to change their physiology such that they are
more tolerant of higher temperatures. Secondly, marine biota
may ‘adapt’ via the selection of individuals within populations that are better able to cope with the new temperatures;
these individuals survive while others that are less temperature tolerant either do not survive or do not breed. In the case
of corals and zooxanthellae, populations would evolve new
‘adaptations’ to cope with the higher temperature regimes
over time.
The question of whether corals and their zooxanthellae
will acclimatize and/or adapt to temperature change is
dependent on the time-scale of the predicted changes. The
time required for plants and animals to acclimatize to temperature change is likely to be on the order of hours or days,
irrespective of such aspects as their generation times. In contrast, the adaptation of plants and animals to temperature
change may require hundreds or even thousands of years,
and depends on the generation time of the organism.
Organisms that reproduce relatively early in their lives (e.g.
855
Climate change, coral bleaching and the future
whereas organisms with longer generation times such as fish
and reef-building corals were severely affected by global
crises (Plaziat and Perrin 1992; Copper 1994).
Fig. 10. Sea surface temperature data generated by the global coupled
atmosphere–ocean–ice model (ECHAM4/OPYC3, Roeckner et al. 1996)
and kindly provided by Dr Axel Timmermann of KNMI, Netherlands:
(A) southern, 23.5°S,149.5°E, (B) central (18°S,147.5°E) and (C) northern
(11°S,143°E) Great Barrier Reef. Temperatures were generated for each
month from 1860 to 2100, and were forced by greenhouse warming which
conformed to the IPCC scenario IS92a (IPCC 1992). Effect of El
Niño–Southern Oscillation (ENSO) events included. Horizontal lines:
thermal thresholds of corals at each site.
bacteria, phytoplankton, ephemeral algae) can adapt or
evolve in a matter of days to years. Organisms with longer
generation times (e.g. fish, corals) are only likely to respond
evolutionarily over decades to centuries. This observation is
supported by the fossil record of past major extinction events
(e.g. at the end of Cretaceous); organisms that appear to have
resisted extinction include those with short generation times
(e.g. cyanobacteria, calcareous algae, foraminiferans),
Adaptation
The fact that corals and their zooxanthellae have different
thermal optima and maxima suggests that corals have adapted
genetically to different thermal regimes (e.g. Table 6). Coles
et al. (1976) formally presented evidence for the existence of
geographical variation in the temperature tolerance of corals
and zooxanthellae; corals from Enewetak (average water
temperature 28.5°C) could survive a 10 h exposure to 35.6°C
whereas most corals from Hawaii (average water temperature 24.5°C) died when water temperatures were raised to
32.4°C. Corals from Malaysia and from Orpheus Island and
One Tree Island in Australia show significant shifts in the
temperature at which they bleach; corals from cooler regions
bleach at lower temperatures (Yang Amri and HoeghGuldberg, unpublished).
The observation that corals have adapted to local temperature regimes is not surprising and is a universal feature of all
organisms, especially those such as corals that are ectothermic (with no internal temperature control). The observation of
heat-sensitive clones (Edmunds 1994; Brown 1997b) among
populations of corals suggests that differences in the genetic
tolerance of host and zooxanthellae will provide the ground
substance of change as habitats move to higher and higher
thermal regimes. Recent work by Salih et al. (1997b) suggests that intertidal corals with fluorescent pigmentation
may be more tolerant to heat stress than those without.
These studies suggest that there are genotypes with current
populations of corals that may be selected under regimes of
increasing temperature. What is clear, however, is that
change towards a population dominated by these genotypes
may still be a slow process and may depend on the stabilization of sea temperatures.
Fig. 11. Number of times per decade that predicted temperatures (see Fig. 10) exceed coral threshold levels (bleaching events)
for (A) southern, 23.5°S,149.5°E, (B) central (18°S,147.5°E) and (C) northern (11°S,143°E) localities on the Great Barrier Reef.
Models: j ECHAM4/OPYC3; h ECHAM4/OPYC3 with aerosol effect added; mECHAM3/LSG; and r CSIRO DAR GCM.
856
In the case of reef-building corals, genes flowing from
reefs at warmer latitudes will also influence the rate of
change. Currents flowing from latitudes that are warmer may
be crucial in the rate of change within a community of corals.
These observations do not, however, give us reason to believe
that populations of corals and their zooxanthellae will be able
to shift rapidly to contain individuals that are better able to
stand the increase in temperatures across tropical oceans.
Such changes to population structure are likely to take several
hundred years. If the close proximity of corals to their thermal
maxima is due their inability to respond to the 1°C increase in
SST over the past 100 years, then we must conclude that there
has been little response from reef-building corals to the
changes over those 100 years. The multiple recurrence at the
same sites of bleaching events over the past 20 years (some
coral reefs have bleached during every major bleaching
episode) strongly suggests that populations are not rapidly
changing their genetic structure to one dominated by more
heat-tolerant individuals.
A second way that corals might increase their survival is
to change their zooxanthellae for more heat-tolerant varieties
(‘Adaptive bleaching hypothesis’, Buddemeier and Fautin
1993). Recent evidence suggests that zooxanthellae represent a highly diverse group of organisms (Rowan and Powers
1991; Loh et al 1997). Although this idea has attracted much
discussion, it is currently not well supported by critical evidence. The key observation—that corals when heat stressed
expel one variety of zooxanthellae and take on another more
heat-tolerant variety while the heat stress is still present—has
never been made. The observation that corals may have a
variety of different types of zooxanthellae in the one colony
and experience the selective loss of one type during temperature stress (Rowan et al. 1997) does not necessarily demonstrate that bleaching is adaptive. Again, if the tips were
re-populated by a heat-tolerant form of zooxanthellae during
the period in which the stress was present, then the adaptive
bleaching hypothesis might have some basis.
Several other features of bleaching that argue against its
being adaptive. One of the premises of the Adaptive
Bleaching hypothesis is that zooxanthellae of one type are
expelled from the host in preparation for being replaced by
another variety. Most studies that have measured the concentration of zooxanthellae remaining in bleached corals have
found that bleached corals (even the whitest) still have substantial concentrations of the original population of zooxanthellae (103 cells cm–2, Hoegh-Guldberg and Smith 1989a;
Hoegh-Guldberg and Salvat 1995). This suggests that
bleaching has more to do with expulsion of damaged zooxanthellae and their host cell (Gates et al. 1992, but see discussion in Brown 1997a) than with the complete removal of
one genotype. This does not preclude the possibility that the
diversity of different types of zooxanthellae might have a
very important role in influencing the rate at which populations of reef-building corals evolve towards greater heat tol-
Ove Hoegh-Guldberg
erance. However, there is no evidence that corals bleach
specifically to exchange one genotype of zooxanthellae in
their tissues for another.
Acclimation
Corals and their zooxanthellae are able to acclimatize to a
wide range of changes in the environment that may vary on
a diurnal, weekly or even yearly basis (Gates and Edmunds
1999). Responses to changes in the light environment is a
good example. Zooxanthellae acclimatize to higher light
intensities during the day by modifying the concentration
ratios of quenching xanthophylls (Brown et al. 1999), which
in turn modify the efficiency of the light reactions (HoeghGuldberg and Jones 1999); these changes take a few hours to
occur. Over longer periods, zooxanthellae can acclimatize
their photosystems to changes in the light environment by
regulating the amount of chlorophyll per cell and, hence, the
harvesting of light being carried out in a zooxanthella
(Falkowski and Dubinsky 1981). Similar modifications are
likely to occur with the change in light intensity from
summer to winter. As with all physiological systems, there
are limits to the extent to which organisms can acclimatize.
For example, beyond a certain depth, light intensities are so
low that no amount of physiological acclimation by reefbuilding corals and their zooxanthellae will allow them to
live there.
Acclimation to temperature is no different from acclimation to other variables. Reef-building corals live within a
thermal range in which they can optimize their physiological
performance at set temperatures. If water temperatures are
slowly increased, the temperature at which corals bleach can
be increased (R. Berkelmans, Great Barier Reef Park
Authority, personal communication; Yang Amri and HoeghGuldberg, unpublished). If temperatures are decreased,
however, physiological performance will slowly shift back to
the original state. These changes include adjustments to the
expression of proteins such as heat shock proteins (hsp 70,
Sharp et al. 1997) and other physiological systems as discussed by Brown 1976b, Gates and Edmunds (1999).
Despite their ability to acclimatize to changing environmental conditions, reef-building corals do not appear to have
acclimatized to the rapid increases in sea temperature over
the past 20 years. There is no broad pattern suggesting that
corals are better at coping when their maximal temperatures
are exceeded. During the six major episodes of bleaching,
some regions experienced bleaching events every time
(Brown 1997a; Berkelmans and Oliver 1999). Corals seem
to be just as close to their thermal limits as they were at the
beginning of the 1980s, suggesting that acclimation (as well
as adaptation) does not seem to have occurred to any great
extent. If corals were acclimating (or adapting), then we
should see a reduction in the gross extent of bleaching across
reefs. The fact that this has not occurred suggests three possibilities: (a) the sporadic and seasonal nature of thermal
Climate change, coral bleaching and the future
stress is such that acclimatory changes do not occur to any
extent as thermal stress sets in, (b) the extent to which corals
and their zooxanthellae can acclimatize has been exceeded,
and/or (c) the rates of change in sea temperature are too fast
for adaptation to occur in time.
It can be argued that the complex and sporadic nature of
the rise in sea temperature coupled with the variation due to
season and El Niño–Southern Oscillation disturbances make
acclimation by corals extremely unlikely. Physiological
changes during acclimation may also take days and will only
remain in place as long as conditions stay the same (Withers
1992). Acclimatory states will change if the environment
changes. At present, temperatures exceed the thermal thresholds of corals for part of the year only and are followed by a
seasonal decline in temperature; cooler years also usually
follow. These two features mean that any thermal acclimation that has occurred during a bleaching year will be lost by
the time thermal maxima are exceeded next time. This leads
to the second point: although corals and their zooxanthellae
may have substantial abilities to acclimatize to changing
conditions (Brown 1997b; Gates and Edmunds 1999), there
are genetic limits to acclimatization. This may be the reason
behind the increase from 1979 onwards in the tendency of
reefs to bleach. Increasing sea temperatures have brought
corals closer to the limit of their ability to acclimatize over
the past 100 years. Any increase above this limit leads to the
degeneration of the zooxanthellae and to bleaching.
The rapidity of the changes in the thermal environment may
also be a serious challenge to reef-building corals and their
zooxanthellae. Much slower temperature changes (e.g. 5–7°C
over 5000–7000 years) occurred during the last transition from
glacial to post-glacial climates (Schneider 1989; Folland et al.
1990) yet were accompanied by dramatic changes in local
fauna and flora due to either extinction or migration. Similar
changes have been noted for some coral assemblages: Pandolfi
(1999) reports the rapid extinction of two species of widespread
Caribbean corals (Pocillopora cf. palmata and Montastraea
‘annularis’ species complex), which appears to coincide with
the reduction in sea level at the last glacial maximum (18 000
years BP). Pandolfi (1999) proposes that the rapid reduction in
habitat at this time for both species may have fallen below a
critical threshold size such that coral metapopulation structure
may have become critically disrupted.
Broad geological overviews (e.g. Brown 1997b) do not
negate the possibility that reefs may decline as environmental conditions change. Coral species have survived greater
changes over geological time and are unlikely to be forced
into extinction by the projected changes to sea temperatures
(Brown 1997b). Hence, the issue is not that corals will
become extinct as a result of the projected increases in sea
temperature. The projected increases in sea temperature will
cause the condition of coral reefs to be severely compromised over the next several hundred years at least. Although
short in geological time, this time scale is significant to the
857
present human use of coral reefs. This is perhaps the key
issue associated with the present rates of change in the environment surrounding coral communities.
Consequences of an increased frequency of bleaching
How coral reef ecosystems will change in response to the
reduced viability of reef-building corals is a complex question.
In theoretical terms, a huge number of endpoints are possible,
given the number of interactions that make up an ecosystem as
complex and diverse as a coral reef (Hughes and Jackson
1985; Hughes 1989; Tanner et al. 1994). Lessons from the past
20 years of mass bleaching, however, have allowed some
important insights into the effects to be expected under future
changes to tropical sea temperature (Glynn 1993).
Increased coral mortality
One of the most direct effects that coral bleaching has on
corals and coral reefs is that affected organisms tend to die at
greater rates. Estimates of mortality following mass bleaching
range from close to zero in cases of mild bleaching (Harriott
1985) to close to 100% as seen in some shallow-water reefs in
Indonesia (Brown and Suharsono 1990) and eastern Pacific
reefs following the 1982–83 event (Glynn 1990). Mortalities
following mass bleaching in the Central and Western Pacific
in 1991 and 1994 have been as high as 30–50% of living
corals (Salvat 1991; Gleason 1993). Mortality appears to
increase with the intensity of the bleaching event, which is
determined by how much and how long temperatures remain
above the maximum mean summer temperatures.
Although scientific reports are still in the process of being
published, the 1998 bleaching event has been followed by
high and perhaps unprecedented mortality. Mortalities on the
Great Barrier Reef have been recorded at 80–90% in some
sites such as reef crest sites at One Tree Island at the southern end of the reef (Yang Amri, unpublished). Corals of some
genera (e.g. Pocillopora) have become hard to find (S. Ward,
R. Jones and G. Beretta, personal communication). There
have been substantial mortalities among corals in the central
Great Barrier Reef (Baird and Marshall 1998; Marshall and
Baird 1999). Mortality was family specific (similar to that
noted by Glynn 1993 and Hoegh-Guldberg and Salvat 1995)
with staghorn corals (Acroporidae) being the worst affected.
Bleaching affected all colonies of Acropora hyacinthus and
A. gemmifera and 70–80% were dead 5 weeks after the onset
of bleaching. An indication of the severity of the 1998
bleaching event on the Great Barrier Reef is the fact that
corals as old as 700 years died. Given that these corals can
grow to >1000 years old, it has been suggested that 1998 was
one of the most severe events in the past several hundred
years (ISRS 1998b).
Data from other localities (mainly personal communications) suggest similar patterns of mortality: French Polynesia
(J. Jaubert), Maldives (W. Allison), Indian Ocean (D. Obura,
858
pers. comm.,Wilkinson et al. 1999), Indonesia (M. Erdmann),
north-western Australia (L. Smith and A. Heyward). Bleaching has been followed by mortalities of 20–100% of corals.
Acroporids are consistently the worst affected, with the longlived Porites being the least affected (CHAMP Network
1999; Hendee 1998).
The mortality of corals following a bleaching event is proportional to the length and extent to which temperatures rise
above summer maxima for any locality. There is little doubt
that present rates of warming in tropical seas will lead to
longer and more intense bleaching events. Given the
behaviour of reefs over the past 20 years, most indicators
point to the fact that mortality rates are likely to rise within the
next few decades to levels that may approach almost complete mortalities. In 1998, the greatest mortalities coincided
with the warmest sea temperatures. The increasing frequency
of bleaching events also has implications. The abundance of
corals will be severely affected if bleaching events kill the
adults before they are able to mature and reproduce (HoeghGuldberg and Salvat 1995). For example, acroporid corals
take ~4–5 years to mature (Harrison and Wallace 1990).
Bleaching events at present occur on average every 4 years. If
the frequency continues to increase, the logical prediction is
that most acroporids will fail to reach maturity and hence
reproduce. The problem is exacerbated for corals that take
longer to mature, and this may eventually select for those
corals that are able to reproduce earlier in their life histories
(r-strategists) as opposed to those that need to survive longer
before they reproduce (k-strategists). This type of selection is
balanced against the relative toughness of some long-lived
species (e.g. Porites spp.), and makes the shift in community
structure of corals relatively unpredictable.
Decreased coral reproduction
In addition to killing corals, increased temperature affects
coral populations by reducing reproductive capacity (Szmant
and Gassman 1990). In a comparison of the fecundity of 200
bleached and unbleached colonies of reef-flat corals at Heron
Island after the 1998 bleaching event, bleaching reduced reproductive activity in most reef-flat corals examined; bleached
colonies of many important reef-flat species (Symphyllia sp.,
Montipora sp., Acropora humilis, Favia sp., Goniastrea sp. and
Platygyra daedalea) contained no eggs at all (Ward et al.
1998). These bleached corals, even though having recovered
their zooxanthellae, did not spawn during the normal spawning
period in November. In other prolific reef-flat species
(A. aspera, A. palifera, A. pulchra and M. digitata) there were
significantly fewer eggs in bleached than in unbleached
corals (Ward et al. 1998). These results are particularly
important because they point to a number of insidious effects
of bleaching events on corals that may not be immediately
evident yet may play a very important role in how coral
ecosystems recover. Lower numbers of reproductive propagules after bleaching events may lead to even lower rates at
Ove Hoegh-Guldberg
which coral populations will re-establish themselves.
Persistent bleaching events such as those predicted for 20–40
years’ time may mean that corals that are not killed will fail
to reproduce—with obvious consequences.
Hoegh-Guldberg, Harrison and co-workers have shown
experimentally that the temperatures at which corals bleach
also slow the development of gonads within corals and interrupt a number of other key processes (e.g. fertilization,
Harrison and Ward, unpublished). The significance of these
results is considerable. Although established corals may
recover from some bleaching events, the number of recruits
may be affected. Already, there is field evidence that recruitment may completely fail after severe bleaching events such as
that experienced in the Indian Ocean. A. Heyward, L. Smith
(personal communication) and co-workers at the Australian
Institute of Marine Science noted very low recruitment during
the exceptionally warm periods off the west coast of Australia
at Karatha in 1998.
Changes in reproductive condition are likely to affect the
distribution and abundance of reef-building corals, which is
important for determining how reefs might recover following
disturbances. Differences in the connectivity of reef systems
and the life histories of corals are crucial for determining patterns of recovery or decline in Caribbean reef systems (Hughes
and Tanner 2000). Recent evidence that coral populations may
be largely self-seeding despite relatively high levels of genetic
connectivity (Ayre and Hughes 2000) also challenges the idea
that reef systems may rapidly be repopulated after the removal
of adult corals; for a wide range of reefs across the Great
Barrier Reef, larval dispersal is surprisingly limited (Ayre and
Hughes 2000). This is especially exacerbated for corals that
brood or have short-lived larval stages. Other insights are
changing the view that the supply of new recruits to a reef may
be independent of the health or abundance of the parent generation on a particular reef. A large-scale study (Hughes et al.
1999) has shown a close correlation between the fecundity of
adult corals and the establishment of larval recruits to a particular site: e.g. variation in space and time of the fecundity of
three common Acropora species explained most of the variation (72%) in acroporid recruitment. The dependence of
recruitment on the size and health of the adult population suggests that the direct effects of temperature (or any anthropogenic factor) on the fecundity of corals will have direct
effects on the abundance of new recruits and hence of adult
reef-building corals. These influences of thermal stress on the
reproductive and population biology of corals are likely to be
important in understanding the abilities of reefs to recover
from thermal events like those seen in 1998. However, despite
their importance, these effects are only partly understood and
should be a priority of future studies.
Reduced reef productivity and growth
Although mortality might not always eventuate, reef-building corals that undergo bleaching have reduced growth, calcifi-
Climate change, coral bleaching and the future
cation and repair capabilities following bleaching (Goreau and
Macfarlane 1990; Glynn 1993; Meesters and Bak 1993; Yang
Amri and Hoegh-Guldberg, unpublished). The primary effect
of increased temperature is the loss of zooxanthellae from reefbuilding corals and other symbiotic invertebrates. As zooxanthellae are the principal engine of primary production in these
organisms, the rate of photosynthetic productivity of bleached
reef-building corals and other symbiotic organisms decreases
dramatically (Coles and Jokiel 1977). This has a quite substantial influence on overall reef productivity because reef-building
corals contribute a substantial proportion of the total productivity of coral reef ecosystems (Muscatine 1980, 1990).
The photosynthetic activity of zooxanthellae is also the
chief source of energy for the energetically expensive process
of calcification (Muscatine 1980, 1990). The reduced ability
to grow and calcify may also translate into a reduced ability
to compete for space with other organisms such as macroalgae, which may eventually eliminate reef-building corals from
particular reefs. Changes in community structure have
occurred in coral reefs in the Caribbean and eastern Pacific
(Glynn 1993; Hughes 1994; Shulman and Robertson 1996).
In each case, community structure has moved away from
communities dominated by reef-building corals to communities dominated by macroalgae.
Additional complications: changes in the aragonite
saturation state of sea water
Pittock (1999) points to a range of factors associated with
climate change that are likely to influence the development of
coral reefs. Principally, two other factors are identified as
important in addition to increased sea temperature: decreased
alkalinity and increased sea level rise. The addition of CO2
above a solution will lead to changes in the concentration of
chemical species such as protons (increasing acidity) and carbonate ions. It has been predicted that increases in the CO2
concentration in the atmosphere will decrease the aragonite
saturation state of sea water in the tropics by 30% (Gattuso
et al. 1998; Kleypas et al. 1999b). This would be expected to
decrease the calcification rate of corals and other organisms
by 14–30% by 2050. The ability of organisms to acclimate to
these changes, however, is unknown. Coral reefs represent a
balance between calcification and erosion. Normal rates of
deposition are high (up to 20 cm year–1) compared with rates
of reef growth (1 cm year–1, Done 1999). This suggests that
the rate of physical and biological erosion is huge and that a
decrease in the rate of calcification of as little as 5% will lead
to a net loss of calcium carbonate.
The implications of a net loss of deposited calcium carbonate from the reef systems that protect coastlines are enormous. A reduction in coastal protection due to weakened or
rapidly eroding coral reefs could adversely affect millions of
human dwellings and substantial proportions of coastal habitats such as mangroves and seagrass beds that support fisheries and provide crucial nursery areas for up to 90% of all
859
commercial species.
Coral growth and productivity also interact with changes
in sea level, another consequence of global climate change.
Best estimates suggest that sea level has risen by as much as
25 cm over the past century, with estimates of sea level rise
in the next 100 years approaching 95 cm (Pittock 1999). The
requirements of reef-building corals and their zooxanthellae
for light confine corals to the upper layers of tropical oceans.
Changes in sea level will cause reef ecosystems at the depth
limit of coral growth to experience light conditions that will
no longer sustain coral growth. Consequently, coral communities at these depths would be expected to disappear. As sea
levels rise, however, new spaces for coral growth will
become available at the upper regions of coral growth.
Predictions that coral reefs will drown as a result of sea
level change are not without debate. Fast growing coral
species such as members of the genus Acropora add up to 20
cm per year (Done 1999) to their branch tips and hence will
have no trouble keeping pace with sea level change. The
problem becomes considerable for slower growing species;
rates of the rise in sea level (0.95 cm per year) begin to match
upward growth rates in Porites (~1 cm per year, Barnes 1973;
Barnes and Lough 1989). If growth rates are reduced by
thermal and other stresses, then the sea level change expected
under even moderate global climate change will present additional challenges for coral reefs in the future. However, coral
calcification rates do not translate directly as reef accretion,
which is about 100 times slower; rising sea level may lead to
faster and hence less-consolidated reef accretion. This in turn
may reduce structural strength of coral reefs and hence make
them more vulnerable to storms and other erosional forces.
Interaction between sea temperature rise and other
anthropogenic effects
The loss of vitality of reef-building corals is also likely to
influence how coral reef ecosystems respond in the face of
other anthropogenic influences. Factors such as eutrophication, increased sedimentation, tourism and destructive fishing
practices may interact with global climate change to produce
new and potent synergistic effects (Wilkinson and Buddemeier
1994; Wilkinson 1999, this volume). Changes in sea temperature can combine with other factors to completely destroy
reefs (e.g. Goreau 1992) including those in the Caribbean (e.g.
Hughes 1994). Increased rates of coral disease such as Black
Band disease (Edmunds 1991), the mass mortality of diademid
sea urchins (Hughes et al. 1987) and outbreaks of predators
such as crown-of-thorns starfish (Acanthaster planci; Moran
1986) may also be linked to reef disturbances related to
increased sea temperatures. Influences of increased temperature may be subtle and involve such things as the temperaturerelated death of coral ‘crustacean guards’ (normally protecting
corals from predation by starfish, Glynn 1983) or more rapid
development of larval crown-of-thorns starfish which is temperature-dependent (Hoegh-Guldberg and Pearse 1995).
860
Although hard to prove, these possible connections suggest
that there are a myriad ways that reefs may or may not change
in the face of warmer conditions in tropical seas in the future.
Changing community structure
Reef-building corals are not all equally susceptible to the
influence of increased temperature. For example, some species
such as the massive corals Porites spp. are relatively resistant
to temperature stress, and if they do bleach they tend to recover
with little or no increase in overall mortality (Salvat 1991;
Gleason 1993). In contrast, the staghorn corals (Acropora
spp.) show a greater sensitivity to slight increases in water
temperature (but see Glynn 1993), and up to 95% of colonies
may bleach (Salvat 1991; Gleason 1993; Hoegh-Guldberg and
Salvat 1995) and die in the 3–6 months following the period of
temperature stress (Salvat 1991; Gleason 1993).
Interspecific differences in resistance of corals may relate
to type of zooxanthellae and the light environment within the
tissues of the coral (see Table 1, point 1b). Mass bleaching
episodes have the potential to dramatically alter the species
richness of coral reef communities (Gleason 1993; Glynn
1993). Local extinction of coral species (e.g. Glynn 1988,
1990) and one near-global extinction of a hydrocoral species
(Glynn and de Weerdt 1991, de Weerdt and Glynn 1991)
have been reported. How changes in species composition of
reefs will affect long-term stability of coral reefs is unclear
but has been reviewed by Done (1999).
Done (1999) outlines four possible scenarios for coral reef
systems under the growing stresses of the addition of CO2
and other greenhouse gases to the earth’s atmosphere. These
scenarios are:
(a) Tolerance: it is assumed that corals and other symbiotic
organisms can acclimatize to the changes in aragonite saturation state and in SST, and hence that nothing changes
within reef communities. While probably involved in the
early stages of environmental change, two aspects need to be
added to the discussion of this point. Firstly, current projections suggest that tropical sea-temperatures will keep rising
over the next century at least. Secondly, there are genetic
limits to acclimation and hence tolerance.
(b) Faster turn-over: it is assumed that coral reefs experience
increases in mortality that reduce life expectancy; the same
species are there but communities shift to a younger age
structure.
(c) Strategy Shift: it is assumed that hardier species (e.g. Porites
spp.) replace less hardy species (e.g. Acropora spp.). This is
probably already starting to operate, with differential mortality in many reefs over the past 20 years (e.g. Hoegh-Guldberg
and Salvat 1995) and increasing rarity of some species (e.g.
Glynn and de Weerdt 1991; de Weerdt and Glynn 1991).
(d) Phase shift: it is assumed that corals are replaced altogether by another group of organisms (e.g. macroalgae). This
has been reported for some areas of the Caribbean by Hughes
(1994), Shulman and Robertson (1996), Aronson et al.
Ove Hoegh-Guldberg
(1999) and Precht and Aronson (1999). Ultimately, if sea
temperatures are not constrained, and corals are unable to
acclimatize or adapt, coral communities in all parts of the
tropics will almost certainly undergo phase shifts in the short
term (i.e. next few decades or centuries). Once these communities have shifted, they would be expected to require a
long time to return to their original states.
Consequences for organisms other than reef-building corals
Reef-building corals provide much of the primary productivity of coral reef ecosystems. Solar energy captured by the
zooxanthellae of corals is released directly to the water
column as mucus or is consumed directly by invertebrate and
fish corallivores. In addition to providing much of the primary
energy, the activities of reef-building corals also provide the
primary shelter for the majority of organisms associated with
coral reefs (Muscatine 1980; Crossland et al. 1991). Consequently, reductions in the abundance and diversity of reefbuilding corals are likely to influence the majority of other
coral reef organisms. Fishing yields will be vastly reduced as
reef viability decreases (Carte 1996; Munro 1996), leading to
much-reduced yields of protein for dependent human populations. Tropical fishery yields are already on the decline worldwide in response to many other anthropogenic factors, and
present problems may be exacerbated by the projected
increase in tropical sea temperature.
The effects of reducing the productivity of reef systems on
birds and marine mammals are expected to be substantial.
There are, however, few if any studies that have measured the
impact although there are accounts of sea bird mortalities and
reduced sea turtle conditions associated with severe El Niño
events. On Heron and One Tree islands at the southern end of
the Great Barrier Reef, for example, nesting by the black
noddy tern (Anous minutus) failed in 1998 and this was
coupled with high adult mortality. The reduced productivity of
coral reefs during the earlier part of the year may have been
responsible for reduced populations of fish prey and hence
increased starvation of these island dwelling birds (HoeghGuldberg, personal observation). Although unsupported by
rigorous study at this point, these observations suggest that
considerable ‘downstream’ effects may be felt by organisms
high in the food chain as reef productivity is reduced.
The fate of the Great Barrier Reef over the next 50 years
The Great Barrier Reef, the world’s largest continuous coral
reef, consists of 2100 km of interconnected coral reef and was
proclaimed as a World Heritage Area in 1975. The Great
Barrier Reef Marine Park Authority (GBRMPA) was established to manage the largest marine park system in the world.
As elsewhere in the tropics, land and sea temperatures
have been increasing within the Great Barrier Reef Marine
Park. Jones et al. (1997) noted a significant increase in annual
summer and winter air temperatures around Magnetic Island
861
Climate change, coral bleaching and the future
(an inshore reef of the central section of the Great Barrier
Reef) since 1950 and postulated that unusually high air temperatures drove temperatures upward in shallow waters of the
reef. Aerial surveys across the reef during March and April
1998 revealed that inshore reefs were the worst affected by
bleaching (Berkelmans and Oliver 1999), reflecting the differences in physical factors between inshore and offshore
reefs. Using in situ measurements supplied by GBRMPA, and
data from the Global Ocean Surface Temperature Atlas
(IGOSTA; ‘ships of opportunity’) plus other data sets from
1903–94, Lough (1999) showed that SSTs within the reef
park have steadily increased over the past 100 years and that
SSTs in early 1998 were the warmest in 95 years of instrumental data. The extent of warming over the past century is
~1°C and hence is similar to that being reported for other
tropical localities worldwide (Table 2). The greatest rate of
warming on the Great Barrier Reef has occurred at the southernmost localities; it has increased over the past 30 years and
is now well over 1°C per century (Table 3, Lough 1999).
SSTs are predicted to exceed the thermal threshold for
corals in IPCC scenario A (IS92a) and bleaching to surpass
the 1998 event within the next 20 years (Fig. 10); from 2020
onwards, the average bleaching event is likely to be similar
or greater than the 1998 event.
The early events during the development of the Great
Barrier Reef are described above. As a result of the occurrence
of the highest thermal anomalies ever seen (A. E. Strong, 10
February 1998), 67% of inshore reefs on the Great Barrier
Reef had high levels of coral bleaching (>10%), 25% of
inshore reefs had extreme levels of bleaching (>60%). A large
proportion (>14%) of offshore reefs also showed high levels of
bleaching (Berkelmans and Oliver 1999). Australian coral reefs
other than the Great Barrier Reef were similarly affected; on
Scott Reef off the north-west coast of Australia, hard and soft
corals decreased in abundance from 30–60% cover to <10% at
most sites (Smith and Heyward, personal communication ).
Work is in progress to ascertain how these sites will
recover from impaired reproduction and mortalities of up to
90–100% of all affected corals in some places. Estimates of
the length of time needed for recovery range from 10 to 30
years (Hughes 1994; Connell et al. 1997; Done 1999) and
depend heavily on the frequency and intensity of bleaching
events. There is probably also a strong latitudinal effect; reefs
at higher latitudes and hence lower sea temperatures are likely
to take longer to recover. The frequency of bleaching events
in the Great Barrier Reef region is predicted to increase by as
much as 1.6–1.7 more events per decade (slope of events per
decade v. time in Fig. 11) until it reaches 10 per decade by the
year 2030. On this basis, the reefs are likely to be maintained
in an early successional state or to experience the more
serious Phase Shift outlined by Done (1999), with a shift to
communities dominated by organisms other than reef-building corals (e.g. macroalgae). Given the patterns reported by
Berkelmans and Oliver (1999) for the susceptibility of reefs
on the Great Barrier Reef to local warming effects, the inshore
reef systems would be expected to show the first signs of a
move away from being dominated by reef-building corals.
Conclusions
Even under moderate greenhouse scenarios (IS92a–a doubling of current greenhouse gas concentrations by 2100),
present and future increases in sea temperature are likely to
have severe effects on the world’s coral reefs within 20–30
years. Most coral reef systems are predicted to experiencing
near-annual bleaching events that will exceed the extent of the
1998 bleaching event by the year 2040. Some coral reefs (e.g.
Caribbean, South-east Asian) will reach this point by 2020.
Cooling by anthropogenic aerosols will have little effect on
the time that the endpoint is likely to be reached. On the Great
Barrier Reef, expected changes lie between the rapid rates
expected in the Caribbean and South-East Asian reefs and the
somewhat slower changes of the Central Pacific. A better
understanding of the capacity for corals and zooxanthellae to
adapt to these rapid and on-going changes is required. Present
evidence, however, suggests that corals and their zooxanthellae are unable to acclimate or adapt fast enough to keep pace
with the present rapid rate of warming of tropical oceans. If
the mortality of reef-building corals continues to increase,
changes in the distribution of corals will almost certainly
occur. Given the central role of corals and zooxanthellae in
the structure and function of coral reefs, these changes are
likely to have severe and negative effects on the health of
coral reefs world-wide by the middle to end of next century.
The ecological and economic effects of these changes have
not been properly assessed and should be a priority of future
research. If, however, the scenario presented in this paper
continues to be supported, then a rapid reduction of greenhouse gas emissions (60–80%, Pittock 1999) over the next
decade must be put into effect immediately.
Acknowledgments
The author thanks Erwin Jackson, Dr Axel Timmermann,
Bill Hare, Gareth Walton, Dr Sophie Dove, Dr Geoffrey
Dove, Hans Hoegh-Guldberg, Dr Ross Jones, Professor
A. W. D. Larkum, Ms Antonella Gambotto, Isobel HoeghGuldberg, To Ha Loi, Dr Peter Pockley, Mr Luke Smith and
Dr Bill Allison for discussion and input at various points in
the manuscript. The author also acknowledges the support of
Greenpeace International and the School of Biological
Science during the preparation of this review.
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