Climate Change, Coral Bleaching and the Future of the World’s Coral Reefs Assignment

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CLIMATE CHANGE CORAL BLEACHING and the FUTURE of the WORLDOS CORAL REEFS by O V E H O E G H ? G U L D B E R G ASSOCIATE PROFESSOR, SCHOOL OF BIOLOGICAL SCIENCES, UNIVERSITY OF SYDNEY DIRECTOR, THE CORAL REEF RESEARCH INSTITUTE, UNIVERSITY OF SYDNEY ISBN 90-73361-52-4 Sea temperatures in the tropics have increased by almost 1oC over the past 100 years and are currently increasing at the rate of approximately 1-2oC per century. Reefbuilding corals, which are central to healthy coral reefs, are currently living close to their upper thermal limit. They become stressed if exposed to small slight increases 1-2oC) in water temperature and experience coral bleaching. Coral bleaching occurs when the photosynthetic symbionts of corals (zooxanthellae) become increasing vulnerable to damage by light at higher than normal temperatures. The resulting damage leads to the expulsion of these important organisms from the coral host. Corals tend to die in great numbers immediately following coral bleaching events, which may stretch across thousands of square kilometers of ocean. Bleaching events in 1998, the worst on record, saw the complete loss of live coral from reefs in some parts of the world. This paper reviews our understanding of coral bleaching nd demonstrates that the current increase in the intensity and extent of coral bleaching is due to increasing sea temperature. Importantly, this paper uses the output from four different runs from two major global climate models to project how the frequency and intensity of bleaching events are likely to change over the next hundred years if greenhouse gas emissions are not reduced. The results of this analysis are startling and a matter of great concern. Sea temperatures calculated by all model projections show that the thermal tolerances of reef-building corals are likely to be exceeded within the next few decades.

As a result of these increases, bleaching events are set to increase in frequency and intensity. Events as severe as the 1998 event could be become commonplace within twenty years. Bleaching events are very likely to occur annually in most tropical oceans by the end of the next 30-50 years. There is little doubt among coral reef biologists that an increase in the frequency of bleaching events of this magnitude could have drastic consequences for coral reefs everywhere. Arguments that corals will acclimate to predicted patterns of temperature change are unsubstantiated and evidence suggests that the genetic bility of corals to acclimate is already being exceeded. Corals may adapt in evolutionary time, but such changes are expected to take hundreds of years, suggesting that the quality of the worldOs reefs will decline at rates that are faster than expected. Every coral reef examined in Southeast Asia, the Pacific and Caribbean showed the same trend. The worldOs largest continuous coral reef system (AustraliaOs Great Barrier Reef) was no exception and could face severe bleaching events every year by the year 2030. Southern and central sites of the Great Barrier Reef are likely to be severely ffected by sea temperature rise within the next 20-40 years. Northern sites are warming more slowly and are expected to lag behind changes in the southern end of the Great Barrier Reef by 20 years. In summary, the rapidity and extent of these projected changes, if realized, spells catastrophe for tropical marine ecosystems everywhere and suggests that unrestrained warming cannot occur without the complete loss of coral reefs on a global scale. C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 1 Executive summary Introduction

The environmental and economic importance of the worldOs coral reefs Coral reefs are the most spectacular and diverse marine ecosystems on the planet today. Complex and productive, coral reefs boast hundreds of thousands of species, many of which are currently undescribed by science. They are renown for their extraordinary natural beauty, biological diversity and high productivity. Apart from their beauty, coral reefs have a crucial role in shaping the ecosystems that have inhabited our tropical oceans for the last 250 million years. Early scientists such as Charles Darwin puzzled over the unusual positioning of hese 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 gCm-2d-1 (Hatcher 1988) and yet may be many thousands of times higher within associated coral reef systems (e. g. algal turfs: 280 gCm-2d-1; corals: 40 gCm2d-1; benthic microalgae: 363 gCm-2d-1; reviewed by Hatcher 1988). The high productivity of coral reefs within hese otherwise unproductive waters make coral reefs critical to the survival of the ecosystems and hence 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 providing new drugs and biochemicals (Carte 1996). Globally, many people depend in part or wholly on coral reefs for their livelihood and around 8% (0. 5 billion people) of the worldOs population live within 100 kilometres of coral reef ecosystems (Pomerance 1999).

Tourism alone generates billions of dollars for countries associated with coral reefs: $1. 5 billion is generated annually by the Great Barrier Reef (Australia, Done et al. , 1996), $2. 5 billion by Floridean reefs (USA, Birkeland, 1997) and approximately $140 billion by Caribbean reefs (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 $1. 2 billion by the year 2005 (U. S. 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 tons of fish catch worldwide (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 worldOs poorer societies. For example, 25% of the fish catch in developing countries is provided by coral reef associated fisheries (Bryant et al. 1998).

Coral reefs protect coastlines from storm damage, erosion and flooding by reducing wave action approaching a coastline. The protection offered by coral reefs also enables the formation of associated ecosystems (e. g. sea grass beds and mangroves) which allow the formation of essential habitats, fisheries and livelihoods. The cost of losing coral reefs would run into the 100s of billions of dollars each year. For example, the cost of losing fifty-eight percent of the world’s coral reefs has been estimated as 140 billion dollars in lost tourism alone (Bryant et. al. 1998). If these direct costs are added to the indirect losses generated by osing the protection of tropical coastlines, the economic impact of loosing 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 the health of coral reefs have been reported from every part of the world. Between 50% and 70% of all corals reefs are under direct threat from human activities (Goreau 1992, Sebens 1994, Wilkinson and Buddemeier 1995, Bryant et al. , 1998). Like their terrestrial counterparts, rainforests, coral reefs are being endangered by a diverse range of human-related hreats. 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, Hoegh- Guldberg et al 1997). Six major episodes of coral bleaching have occurred since 1979, with massive mortalities of coral affecting reefs in every part of the world. Entire reef systems have died following bleaching events (e. g. Smith and Heywood 1999, Brown and Suharsono 1995).

The decline in reef systems worldwide has begun to receive attention at the top levels of world governments. Actions such as the recent forming of the US and International Coral Reef Initiatives and the issuing of US President William J ClintonOs Executive Order 13089 on June 11, 1998 emphasize this point. Put simply, the latter states at one point that “All Federal agencies whose actions may affect U. S. coral reef ecosystems E 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 ddition to the barrage of assaults affecting coral reefs, has attracted enormous 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? Are coral bleaching events novel or have they simply been overlooked prior to 1980? Are bleaching events set to increase or decrease in intensity? These are but a few of the questions that are outstanding at this point in time. This article reviews what we currently know about coral bleaching and its impact on coral reef ecosystems.

It C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 2 reviews the scientific evidence for coral bleaching being a sign of climate change and builds a case for the prediction that thermally triggered coral bleaching events will become of increasing seriousness in the next few decades. The current understanding of coral bleaching suggests that corals are not keeping up with the rate of warming that has occurred and that they may be the single largest casualty of “business-as-usual” greenhouse gas emissions. While coral eefs will not become extinct in the long-term, their health and distribution will be severely compromised for at least 500 years unless warming is mitigated. The implications of this are enormous and should be avoided with all the resources at our disposal. The central role of symbioses in coral reefs The central feature of shallow water coastal ecosystems is the predominance of symbioses between invertebrates and dinoflagellates microalgae (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. In many ways, coral reefs are analogous to the actus gardens within deserts. In the same way that cacti live by restricting the flow of water to the desert environment, corals and their zooxanthellae live by limiting the flow of nitrogen and other essential nutrients to the Onutrient desertO 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 for example, the heart of coral reefs, are all symbiotic with a diverse range of dinoflagellates. Close association between primary roducer and consumer makes possible the tight nutrient recycling that is thought to explain the high productivity of coral reefs. Corals are, quite obviously, central to coral reef ecosystems. The vigorous growth of corals in tropical seas is responsible for the structure of coral reefs and hence reef-building corals are often referred to as the “frame-builders” 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 and invertebrates), corals have been the primary reason for the structure of coral reef ecosystems for 200 million years.

Corals have built the primary structure of entire reefs, islands and such massive oceanic barriers as the Great Barrier Reef. The symbiosis between corals and dinoflagellates (zooxanthellae, Figure 1) has been the subject of considerable interest since the brown bodies of corals and other symbiotic invertebrates were classified as separate organisms by Brandt (1881). The symbiotic dinoflagellates of corals and invertebrates from at least 5 other phyla live symbiotically within the cells of their hosts. Representatives are also found in the Mollusca (snails and clams), Platyhelminthes (flatworms), Cnidaria (corals, and anemones),

Porifera (sponges) and Protista (e. g. single-celled ciliates). Histology and physiology With the exception of giant clams (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 (Schoenberg and Trench 1980a,b,c; Trench 1979) and Rowan (Rowan and Powers 1991, 1992) have revealed that zooxanthellae are a highly diverse group of organisms which may include hundreds of taxa (species) with perhaps s many as two or three species per host invertebrate species (Rowan et al. 1997; Loh et al. 1998). Zooxanthellae photosynthesize while residing inside their hosts and provide food for their invertebrate hosts by passing up to 95% of their photosynthetic production to them (Muscatine, 1990). Zooxanthellae have been shown to leak amino acids, sugars, 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 Hoegh- Guldberg 1998). Corals and their zooxanthellae form a utualistic symbiosis, as both partners appear to derive benefit from the association. Corals receive photosynthetic products (sugars and amino acids) in return for supplying zooxanthellae 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 productivity of reefs. The benefits of this production flow down a complex ood chain (Odum and Odum 1955) and provide the basis Figure 1. Zooxanthellae from a reef-building coral. P = pyrenoid, N= nucleus, Cl = Chloroplast, S= starch. Misaki Takabayashi (M. Sc. , 1996, University of Sydney). C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 3 of the most diverse marine ecosystem on the planet. Fish, bird, marine reptile and mammal communities within coral reefs are substantial and stand in stark contrast to the clear and unpopulated waters that surround coral reef ecosystems. Mass Coral Bleaching and the Role of Temperature

Environmental factors affecting reef-building corals and their zooxanthellae Coral reefs are a major feature coastal tropical environments between the latitudes 25oS and 25oN and roughly coincide with water temperatures between 18oC and 30oC (Veron 1986). Below 18oC (generally at latitudes greater than 30o), the number of reef-building coral species declines rapidly and reefs do not form. Reefs at these temperatures are dominated by seaweeds and kelp forests. While low water temperature is correlated with the decline of coral reefs as one moves toward the poles, other variables such as light and the carbonate alkalinity of eawater may play significant roles in determining how well corals do in competition with macroalgae and other organisms that flourish at higher latitudes. Like all organisms, reef-building corals are greatly influenced by the biological and physical factors of their environment. Predators (e. g. Crown-of-Thorns starfish, Moran 1988) and disease (Hoegh-Guldberg 1999) greatly affect the survivability of reef-building corals and a range of other coral associated invertebrates. Temperature, salinity and light have major impacts on where live reefbuilding corals are found. Environments in which coral eefs prosper are also typified by a high degree of stability. Not only are seasonal and diurnal fluctuations in tropical sea temperature small, but recent evidence suggests that tropical oceans have varied by less than 2oC over the past 18,000 years (Thunell et al. 1994). Corals exist naturally at salinities that range from 32%o to 40%o (Veron 1986). Rapid decreases in salinity cause corals to die (Hoegh- Guldberg and Smith 1989), and are the likely cause of the mass mortality of corals after severe rain storms or flood events (Egana and DiSalvo 1982, Goreau 1964). Fluctuations in salinity are thought to play an important ole in limiting the distribution of reef building corals in coastal regions. The proximity of rivers to coral reefs is a very important determinant. Not only are rivers the principal source of sediments, nutrients and salinity stress along tropical coastlines, but they now carry a range of other substances that may impact on 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. Consequently, light has a profound effect on determining here corals may grow and in influencing other aspects like 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 serve to increase the ability of the zooxanthellae to collect light for photosynthesis (Schlichter et al. 1985). Limits to coral growth occur at much shallower depths in areas where sedimentation reduces the transmission of light through the water column. Corals may be eliminated altogether in areas like those in the vicinity of river mouths where large amounts f sediment enter the sea and have a range of effects such as smoothing or burying corals (Veron 1986). Corals and their zooxanthellae have some versatility with respect to their ability to photoacclimate to low or high light settings. Under low light settings, concentrations of chlorophyll and other photosynthetic pigments within zooxanthellae increase in concentration (Falkowski and Dubinsky 1981, Porter et al 1984) and decrease under high light. Under extremely high light conditions the photoinhibition of zooxanthellae can be a significant problem and reef-building corals and their zooxanthellae ppear to have a series of “quenching” mechanisms to reduce the impact of excess light (Hoegh-Guldberg and Jones 1999, Ralph et al. 1999). In addition to visible light (often referred to as Photosynthetically Active Radiation or PAR), short wavelength radiation like Ultra-Violet Radiation (UVR) strongly influences both the distribution and physiology of reef plants and animals (Jokiel 1980). Short wavelength radiation (290 – 400 nm) has a variety of destructive effects on marine organisms (Jokiel 1980), with corals and their symbiotic dinoflagellates being no exception (Shick et al. 1996, Lesser 1996).

Effects of UVR on cultured symbiotic dinoflagellates include decreased growth rates, cellular chlorophyll a, carbon: nitrogen ratios, photosynthetic oxygen evolution and ribulose bisphosphate carboxylase/oxygenase (Rubisco) activities (Banazak and Trench 1995, Lesser 1996). Similar effects have been reported for symbiotic dinoflagellates living within cnidarian tissues (Jokiel and York 1982, Lesser and Shick 1989, Shick et al. 1991, Gleason 1993, Gleason and Wellington 1993, Kinzie 1993, Banazak and Trench 1995, Shick et al. 1991, 1995). Both host and symbiont have been reported to have a range of protective mechanisms to ounteract the direct and indirect influences of UV radiation. These include the production of mycosporinelike 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 and 5 x 106 cell. cm-2 (Drew 1972; Porter et al. 1984, Hoegh-Guldberg and Smith 1989) and 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 ates, population densities have been reported in a number of studies as undergoing seasonal changes (Jones 1995, Fagoonee et al 1999, W. K. Fitt pers com. ). These seasonal C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 4 changes are far from uniform and probably depend on a variety of physical variables in the immediate environment. Changes are gradual and probably represent slow adjustments of symbioses to optimise physiological performance in the face of environment change. Under a range of physical and chemical conditions, however, udden 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 1989). Reduced salinity (Egana and DiSalvo 1982, Goreau 1964), increased or decreased light (Vaughan 1914, Yonge and Nicholls 1931, Hoegh-Guldberg and Smith 1989b, Gleason and Wellington 1993, Lesser et al. 1992) or temperature (Jokiel and Coles 1977, Coles and Jokiel, 1978, Hoegh-Guldberg and Smith 1989, Glynn and DOCroz 1990) can cause corals and other symbiotic invertebrates to rapidly pale. Chemical factors such as opper ions (Jones 1997a), cyanide (Jones and Stevens 1997, Jones and Hoegh-Guldberg 1999), herbicides, pesticides and biological factors (e. g. bacteria, Kushmaro et al. 1996) can also evoke 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 due to the loss of zooxanthellae (Hoegh- Guldberg and Smith 1989). Bleaching may occur at local scales (e. g. parts of reefs, Egana and DiSalvo 1982; Goreau 1964) or at geographic cales that may involve entire reef systems and geographic realms (“mass bleaching”, Glynn 1993, Hoegh-Guldberg and Salvat 1995, Brown 1997a). Because of the increasing intensity and geographic scale of recent bleaching events, mass bleaching is considered by most reef scientists to be a serious challenge to the health of the worldOs coral reefs. Increased water temperature and mass bleaching events Most evidence currently indicates that elevated temperature is the cause of mass bleaching events. Increasing water temperature will rapidly cause zooxanthellae to leave the tissues of reef-building corals and other invertebrates Hoegh-Guldberg and Smith 1989) resulting in a reduced number of zooxanthellae in the tissues of the host (Coles and Jokiel 1977, 1978, Hoegh-Guldberg and Smith, 1989, Glynn and D’Croz 1990, Lesser et al. 1990). Changes to PAR (photosynthetically active radiation) or UVR (ultraviolet light) aggravate the effect of temperature (Hoegh- Guldberg and Smith 1989, Gleason and Wellington 1993, Lesser 1996). However, as pointed out by Hoegh-Guldberg and Smith (1989), the effect of these two variables alone does not closely match the characteristics in corals collected during mass bleaching events. Corals collected during mass leaching events are characterised by reduced population densities of zooxanthellae (with or without a decrease in zooxanthellae-specific pigments). They 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 1989, Lesser 1996). Other factors such as reduced salinity may cause colour loss but do not cause corals to lose zooxanthellae as in mass bleaching events (Hoegh-Guldberg and Smith 1989). For example, in some cases of “bleaching” caused by reduced salinity, loss of coral tissue may be confused with he loss of zooxanthellae that is characteristic of mass bleaching. Corals survive salinities down to 23%o (2/3rd strength of seawater) but then die, with tissue sloughing off to reveal the white skeleton below (Hoegh-Guldberg and Smith 1989). While superficially the same (i. e. whitened corals), the physiological mechanism and general tissue characteristics do not generally resemble those of corals collected during mass bleaching events. A key characteristic of mass bleaching events (Figure 2a) is that the host tissue remains on the skeleton but is relatively free of zooxanthellae (Figure 2b).

Figure 2 A. Bleached corals on northern reef slope of Moorea, French Polynesia in 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 Correlative field studies have pointed to warmer than normal 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 a substantial vidence of the association of mass coral bleaching, mortality and higher than normal sea temperature. Glynn (1993) indicated that 70% of the many reports at that stage were associated with reports of warmer than normal conditions. Glynn (1993) was also the first to indicate that the projected increases in sea temperature associated with global climate change were likely to push corals beyond C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 5 their thermal limits. The association of bleaching and higher than normal sea temperatures has become even tronger with a proliferation of correlative studies for different parts of the world (e. g. Goreau and Hayes 1994, Brown 1997a, Hoegh-Guldberg and Salvat 1995, Hoegh- Guldberg et al. 1997, Jones 1997, Jones et al. 1997, Winter et al. 1998). These studies show a tight association between warmer than normal conditions (at least 1oC higher than the summer maximum) and the incidence of bleaching. The severe bleaching events 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 associated with reports f warmer than normal conditions, but the “Hotspot” program (Goreau and Hayes 1994) run by the U. S. National Oceanic and Atmospheric Administration (NOAA) predicted bleaching for most geographic regions where bleaching occurred during 1998, days and weeks in advance. An interactive web site based on using “hotspots” to predict bleaching (a “hotspot” defined as where sea surface temperatures equal or exceed the annual monthly maximum climatological value by 1oC) was established in January 1997 by NOAA/NESDIS (National Ocean and Atmospheric Administration/National Environmental Satellite Data and Information Service).

One of the most graphic examples of the success of this program was the prediction of the record bleaching event on Great Barrier Reef sent by A. E. Strong on February 10 in 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 Coral Health and Monitoring (CHAM Network) Network (corallist@ coral. aoml. noaa. gov) received the first reports of leaching on the Great Barrier Reef four days later (M. Huber, Townsville, February 14th 1998). By February 27th, 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. By mid March, extensive surveys run by 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 experienced a major bleaching event. More than 100 bservational reports from 1998 that documented the tight correlation between positive thermal anomalies can be obtained from the NOAA web site (http://coral. aoml. noaa. gov, April 1999). Similar conclusions can be made for events occurring from 1995- 97 (Goreau et al. 1997). Global patterns The mass coral bleaching events of 1998 are considered the most severe on record (NOAA 1998, ICRS 1998) bleaching having affected every geographic coral reef realm in the world (Figure 3). This is the sixth major episode of coral bleaching to affect coral reefs worldwide since 1979. Strong bleaching episodes coincide with periods of high sea urface temperature and are associated with disturbances to the El Nino Southern Oscillation (ENSO; Figure 3). Most occur during strong El Nino periods, when the Southern Oscillation Index (SOI) is negative (SOI ; -5). However, some regions such as the southern parts of the Cook Islands experience bleaching in strong La Nina periods due to downward shifts in the position of the South Pacific Convergence zone and associated water masses. 1997-1998 saw the most extensive and intense bleaching event on record, coinciding with (by some indices) the strongest ENSO disturbance on record (Kerr 1999). For the first time, oral reefs in every region of the world recorded severe bleaching events (Figure 3). In some places (e. g. Singapore, ICRS 1998) bleaching was recorded for the first time. Many massive corals have died as a result of the 1998 event ? some as old as 700 years of age (ICRS 1998). The latter strengthens the suggestion that the 1997-98 bleaching event was the most severe bleaching event to hit regions like the Great Barrier Reef in the last 700 years. Incidents of bleaching in the 1997-98 episode were first reported (CHAM Network, Coral Health and Monitoring Network, NOAA) in the eastern Pacific (Galapagos) and arts of the Caribbean (Grand Cayman) in late 1997, and spread across the Pacific to French Polynesia, Samoa and Australia by early February 1998. Soon after (March and April 1998), bleaching was being reported at sites across the Indian Ocean, with reports being received from Southeast Asia in May 1998. Bleaching began in 1997-98 in the Souhtern Hemisphere during summer. As summer began in the Northern Hemisphere (June), northeast Asian and Caribbean coral reefs began to bleach, with bleaching continuing until early September 1998 (Figure 4). Reports supplied to CHAM Network on the 1997-98 bleaching pisode have been archived by NOAA (http://coral. aoml. noaa. gov, April 1999) and have been collated by Wilkinson (1999). The pattern associated with the 1997-98 bleaching episode strongly resembles patterns seen during the 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 between February-April, Southeast Asian reefs in May, and Caribbean reefs between July-August (CHAM Network 1997-1999, Hoegh- Guldberg 1995). Bleaching in the Northern Hemisphere tends to occur after the appearance of bleaching in the

Southern Hemisphere, although this is not always the case. For example mass bleaching on Great Barrier Reef in 1982 preceded Caribbean wide bleaching in 1983. C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 6 The importance of light: the photoinhibition model of coral bleaching Elevated temperature explains most incidents of mass bleaching. It is salient to point out, however, that there is still variability associated with mass bleaching events that is not completely explained by sea temperature anomalies. At local scale, colonies often exhibit a gradation of bleaching intensity within colonies (Figure 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 (due to the high thermal capacity of water and the well mixed nature of the water column), other explanations are needed. The tendency to bleach 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 some sea surface temperature (SST) anomaly data.

Aside from arguments based on instrument precision and accuracy (e. g. Atwood et al 1988), several other factors have been evoked to clarify patterns not completely explained by increased water temperature. These are principally the proximal factors light intensity and the genotype of the coral and zooxanthellae. A consideration of these factors provides C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 7 Figure 4. Dates and locations of when severe bleaching began in 1998. Data obtained from Coral Health and Monitoring Network e-mail list (http://coral. oml. noaa. gov). Figure 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 Nino years. While some of the trend can be explained by some observer bias, this factor does not completely explain the increasing trend with time (see text for discussion). important insight and understanding of the physiological basis of mass bleaching. There are a number of reasons to suspect that the intensity of various forms of solar radiation hasa role to play in bleaching events. Several investigators have also proposed hat elevated levels of ultra-violet radiation (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). Field evidencefor a primary role of UVR, however, has been circumstantial and restricted to the observations that: 1. Doldrum periods (when waters are clear and calm and the penetration of UVR is high) have preceded some bleaching events (e. g. Great Barrier Reef sites, 1982-83 bleaching event, Harriott 1985; French Polynesia, 1994 bleaching event, Drollet et al. 1995). 2.

Corals tend to bleach on their upper, most sunlit surfaces first. 3. Experimental manipulation of the UVR levels 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 levels and normal temperatures argues against high UVR levels being a primary factor in causing mass bleaching events. The latter 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 orals bleach on the upper surfaces first during exposure to elevated temperature argues that light quality and quantity 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 temperature related bleaching. Recent evidence suggests that the fact that the upper surface of corals bleach before their shaded bases is related more to the presence of full spectrum PAR than that of UVR (Jones et al. 1998, Hoegh-Guldberg and Jones 1999). The explanation for the role played by light came from a series f studies aiming to decipher the specific site of heat stress action on the metabolism of the symbiotic algae. Hoegh- Guldberg and Smith (1989) established the fact 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. While some of the reduced photosynthetic output was due to the reduced population density of zooxanthellae in the heat stressed corals, subsequent studies has found that heat stress acts to reduce the photosynthetic rate per zooxanthella (Hoegh-Guldberg nd Smith 1989, Iglesias-Prieto et al. 1992, Fitt and Warner 1995, Iglesias-Prieto 1995, Warner et al. 1996). The application of Pulse Amplitude Modulated Fluorometry (PAM Fluorometry, Schreiber and Bilger 1987) to heat stressed corals enabled scientists to begin to identify the component of the photosynthetic metabolism that fails when zooxanthellae are exposed to heat stress. Iglesias- Prieto et al. (1992) reported a complete inhibition of photosynthetic oxygen evolution and a loss of variable fluorescence in cultured zooxanthellae exposed to temperatures of 34-36oC. Fitt and Warner (1995) and

Warner et al. (1996) measured a range of similar effects in zooxanthellae within Caribbean corals exposed to 32oC and 34oC. Variable fluorescence (measured by the PAM fluorometer) is a relative measure of the rate at which one of two photosystems (PS II) can process electrons flowing from the water splitting reactions of photosynthesis. This affords a C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 8 Figure 5. A. Coral showing normally pigmented regions and bleached regions to the upper side more sunlit side of colony. B.

Coral in shallows showing similar pattern. Photographer: O. Hoegh-Guldberg. measure of the efficiency (activity) of the light reactions of photosynthesis. Fitt and Warner (1995) and Warner et al. (1996) saw a decrease in the efficiency of PS II when corals and their zooxanthellae were exposed to heat. These insightful researchers,along with Iglesias-Prieto and his coworkers, proposed that the primary effect of temperature was to cause a malfunction of the light reactions of photosynthesis. Jones et al (1998) used the PAM fluorometer with different sets of experimental manipulations, and were able to shed ew light on the primary steps leading to the development of thermal stress in zooxanthellae. Working with corals from One Tree Island on the southern Great Barrier Reef, Jones et al (1998) were able to show that the first site of damage was the dark reactions of photosynthesis and not the light reactions as previously thought (Figure 6). A second important observation was that light amplified the extent of damage caused by thermal stress, almost perfectly replicating 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 elated to the general phenomenon of photoinhibition C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 9 LHC Stroma H2O2 (Stromal SOD and APO not shown) H2O + O2+ MDA H+ O2 H2O O2 Rubisco CO2 Organic C (Dark Reactions) NADP NADPH + ATP SOD APO O2 – O2 – e- PSI PSII H+ POOL Ascorbate POOL VDE Diatoxanthin Diadinoxanthin NPQ A. Lumen LHC Stroma H2O2 (Stromal SOD and APO not shown) H2O + O2+ MDA H+ O2 H2O O2 Rubisco CO2 Organic C (Dark Reactions) SOD APO O2 – O2 – e- PSI PSII H+ POOL Ascorbate VDE POOL Diatoxanthin Diadinoxanthin NPQ B.

Lumen O2 – O2 – O2 – O2 – O2 – O2 – O2 – O2 – O2 – O2 – O2 – Figure 6 Figure 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 carbon dioxide 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 (O2 -) 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. Walker 1992) and to the general response seen by terrestrial plants and other photosynthetic organisms to heat stress (Schreiber and Bilger 1987). Normally, increasing light levels will lead to an increased photosynthetic rate up until a point at which the relationship between photosynthesis and light saturates. At relatively high light levels, increasing light leads to an over-reduction of the light reactions and 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, Hoegh-Guldberg and

Jones 1999) 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 to photoinhibition. The over-riding conclusion of the work of Jones et al. (1998) and Hoegh-Guldberg 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. This model has a number of properties that lead to redictions and explanations outlined in Table 1. Firstly, photosynthetically active radiation (PAR) as well as ultraviolet radiation (UVR) assumes an important secondary role. While temperature has to be higher than normal for a mass bleaching event to ensue, light levels will cause damage to the photosystems at any light level above darkness (Property 1, Table 1). This explains the frequent observation that the extent of damage is light dependent and that most coral bleaching starts on the upper, more sunlit surfaces of corals. It also links thermal stress-related bleaching directly to the solar bleaching studied by Brown nd co-workers (Brown et al. 1994a). Brown (1997) has already made the important link between photo-protective measures adopted by zooxanthellae and coral bleaching. Brown (1997) points out that photoprotective 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 stress arising from increased temperature and irradiance in the field. This link also explains several unusual bleaching patterns such as when the tips but not the bases bleached in relatively shallow populations of Montastrea spp. in Panama in 1995.

In this case, more light-tolerant zooxanthellae (found in the tips) were actually more resistant to thermal stress than shadeadapted 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 levels.

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). C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 10 Table 1. Predictions (a priori) or explanations (post hoc) stemming from a model based on Jones et al. (1998). 1. Light (PAR) is required for elevated temperature to cause bleaching. The extent of damage during bleaching will be directly correlated with the amount 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. 2. Coral and zooxanthella species that are better able to photo-acclimate are 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). 3. Any stress that blocks the dark reactions before the ight reactions of photosynthesis will result in similar bleaching phenomena. a) Upper surfaces of corals bleach preferentially in most cases (Goenaga et al. 1988, Jones et al. 1998). But see complication outlined in prediction 3. 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 between 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). Reports of the enhanced fluorescence of stressed corals may represent attempts to bolster this strategy. 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. 997). a) 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. 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). One might expect similar signs from other factors that block the dark reactions or lead to the over-energization of the light reactions of photosynthesis (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 bleaching since 1979. Some commentators have suggested that the nswer to this question 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. via the internet). While this is undoubtedly true to some extent, this argument does not explain the relative absence of reports of mass coral bleaching around intensively studied sites such as research stations (e. g. Heron Island, Australia; Florida Keys, USA) and tourist resorts. Underwater film makers like Valerie Taylor (personal communication) who filmed xtensively on the Great of Barrier Reef during the 1960s and 1970s never saw coral bleaching on the scale seen since 1979. It seems certain that an abundance of brilliant white coral, plus the associated mortality and stench from dead bleached reefs could not have gone unnoticed. It also seems highly unlikely that large-scale mass coral bleaching events could have occurred without even a few reports or photographs entering public and scientific media prior to 1979. It is also not feasible that indigenous fishers, who have an extensive and in depth knowledge of coral reefs and their inhabitants could have been unaware of coral leaching. Despite their comprehensive knowledge of reef biology, it seems extraordinary that they have not developed a terminology to describe the appearance of mass bleaching events (Hoegh-Guldberg 1994b). Although greater analysis is needed, it would appear that the case for massive bleaching events passing unnoticed prior to 1979 is extremely weak. So, why are bleaching events occurring more and more frequently and why did they first appear in the 1980s? Given the strong correlation between bleaching events and high sea surface temperatures (Goreau and Hayes 1994), recent and historic sea surface temperatures should provide nsight 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, Cane et al 1997, Brown 1997a, Winter et al. 1999; see also historic temperature data for seven tropical sites, Table 2). Coral cores from the central Pacific confirm this warming trend (e. g. Wellington, Linsley and Hoegh-Guldberg, in preparation). Increases in sea temperature of 1-2oC are expected by 2100 in response to enhanced atmospheric greenhouse gas concentrations Bijlsma et al. 1995). Glynn (1993), Hoegh-Guldberg and Salvat (1995) and Brown (1997) have pointed to the significance of this trend for reef-building corals and have stated variously that global climate change will increase the frequency of bleaching. Trends in sea surface temperature can also be used to shed light on the advent of mass coral bleaching in the 1980s and on how the frequency of mass coral bleaching will change in the next few decades. Sea temperatures over the past 20 years have been extensively measured by a combination of satellite, ship and buoy instrument readings and reveal pward trends in all regions. Blended data from all three sources (satellite, ship and buoy, IGOSS-NME blended data, Integrated Global Ocean Services System, http://ioc. unesco. org/igossweb/igoshome. htm) from the past 20 years reveal that rates of change in sea surface temperature are now much greater than 2oC per century in many tropical seas (Table 3). Simple correlations through IGOSS-NMC blended data reveal rates of change in SST that range between 0. 46oC per century (Northern GBR) to 2. 59oC per century (central GBR, waters off Townsville, Qld). While these trends may reflect longer-term cycles of hange, they have been confirmed by a growing number studies of sea surface temperature trends going back 40-150 years, using other data sets and such sources as coral cores (e. g. Brown 1997a, Winter et al. 1999, Wellington, Linsley and Hoegh-Guldberg, in preparation). For example, C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 11 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 (Jan 1993-Apr 1999).

Data available obtained from the Lamont Doherty Earth Observatory server (http://rainbow. ldgo. columbia. edu/). Data were only included if all months were present (hence shorter periods for some parts of the world. All trends were highly significant with the possible exception of Rarotonga. GBR = Great Barrier Reef. Location Position Period of data examined Rate oC per 100 years Significance of trend Jamaica 76. 5oW, 17. 5oN 1903-1999 1. 25 ; 0. 001 Phuket 98. 5oE, 7. 5oN 1904-1999 1. 54 ; 0. 001 Tahiti 149. 5oW, 17. 5oS 1926-1999 0. 69 0. 003 Rarotonga 159. 5oW, 21. 5oS 1926-1999 0. 84 0. 05 Southern GBR 149. oE, 23. 5oS 1902-1999 1. 68 ; 0. 001 Central GBR 147. 5oE, 18oS 1902-1999 1. 55 ; 0. 001 Northern GBR 143oE, 11oS 1903-1999 1. 25 ; 0. 001 measurements made by researchers at the research station at La Parguera in Puerto Rico registered a rate of change of 2. 53oC per century (Winter et al. 1999), while the IGOSSNMC data for the same area records a rate of increase of SST of 2. 29oC per century (Table 3). Similar comparisons can be made between rates of change reported by Brown (1997) using different data (MOHSST 6) going back to 1946 (Brown 1997a: 1. 26oC per century versus 2. 30 of oC per century reported here).

There is no evidence of a slowing or reversing of this rate of change. While small errors have been noted for pure satellite sea surface temperature data (Hurrell and Trenberth 1997), blended data have the advantage that bias is reduced or eliminated as data are confirmed and crossed checked against several sources. Correlations between in situ instrument readings and 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 had regression coefficients that ranged between 0. 93 and 0. 8 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: Iif corals are sensitive to small changes in temperature, how will projected future increases in sea temperature affect the frequency and severity of bleaching events in the future? We can obtain the thermal thresholds of corals and their zooxanthellae from the past behaviour of corals during bleaching events. This is the basis for the highly successful predictions of the “Hotspot” program run by NOAA (Strong t al. 1997). If this information is combined with projected sea surface temperatures then the number of times that the thermal threshold is exceeded can be estimated. If corals are not adapting or acclimating in time, then each of these points will translate as a bleaching event. The issue of adaptation or acclimation is discussed below. All evidence suggests that corals and their zooxanthellae are not showing signs of being able to acclimate or adapt to short, sporadic thermal events typical of the past 20 years. Predicting future sea surface temperatures cannot be based solely on what has happened in the past. Seasonality and ifferences between years due to variation in the strength of the El Nino Southern Oscillation complicate attempts to predict future tropical sea temperatures. In addition, the use of data from the past 20 years to predict the future presents a problem in that stochastic and improbable events (e. g. the two major volcanic eruptions over the last 20 years) would be extrapolated at a high frequency incorrectly to future temperature trends. Sophisticated Global Climate Models (GCMs), combined with scenarios of future greenhouse gas and sulfur dioxide emissions, however, provide an opportunity to simulate future sea temperatures.

Sea surface temperature data for this study were generated using three variants of the Max Planck Institute ECHAM and the CSIRO Global Climate Models (GCM): A. ECHAM4/OPYC3 IS92a. The global coupled atmosphere-ocean-ice model (Roeckner et al. 1996). Data from this model and those described in B and C were kindly provided by Dr Axel Timmermann of KNMI, Netherlands. This model has been used in climate variability (Roeckner et al. 1996, Bacher et al 1997, Christoph et al. 1998), climate prediction (Oberhuber et al. 1998) and climate change studies 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 Nino-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). B. ECHAM4/OPYC3 IS92a (aerosol integration). The global coupled atmosphere-ocean-ice model (Roeckner et al. 1996) but with the influence of sulphur dioxide emissions (aerosols) added. Observed concentrations of greenhouse gases and sulfate aerosols were used up to 1990 and thereafter change according to the IPCC cenario IS92a. 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 C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 12 Table 3. Rates of warming in tropical oceans for the period 1981-1999. Rates are 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. dgo. 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. Location Position Rate oC per 100 years Significance of trend Other data Jamaica 76. 5oW, 17. 5oN 2. 29 ; 0. 001 2. 53, Winter et al. (1998) Phuket 98. 5oE, 7. 5oN 2. 30 ; 0. 001 1. 26, Brown (1997a Tahiti 149. 5oW, 17. 5oS 1. 44 ; 0. 001 Rarotonga 159. 5oW, 21. 5oS 2. 27 ; 0. 001 Southern GBR 149. 5oE, 23. 5oS 2. 54 ; 0. 001 Central GBR 147. 5oE, 18oS 2. 59 ; 0. 001 Northern GBR 143oE, 11oS 0. 47 ; 0. 001 nly the influence of anthropogenic sources considered. Natural biogenic and volcanic sulfur emissions are neglected, and the aerosol radiative forcing generated through the anthropogenic part of the sulfur cycle only. The space/time evolution in the sulfur emissions has been derived from ? rn et al. (1996) and from Spiro et al. (1992). C. ECHAM3/LSG IS92a. This model differs strongly from the ECHAM4/OPYC3. ECHAM3/LSG uses a resolution of roughly 5 degrees and is built upon a completely different ocean model, which only crudely captures thermocline processes. El Nino-related variability is underestimated by a factor of three.

D. CSIRO DAR Coupled Model (Gordon and OOFarrell 1997). This model is run by the Department of Atmospheric Research at AustraliaOs Commonwealth Scientific and Industrial Research Organisation. This model involves atmospheric, oceanic, comprehensive sea-ice and biospheric subcomponent models that allow the temperature across in small latitudinal-longitudinal cells to be projected. This model forms the basis for CSIRO climate projections given various climate scenarios and is renown for its accurate predictions of surface temperature and such elements as sea-ice distributions at both poles. The current set of projections as been based on a carbon dioxide equivalent scenario (as in B. ) Temperatures were generated for each month from 1860, ending in 2100, and were forced by Greenhouse gas emissions that conformed to the IPCC scenario IS92a (IPCC, 1992). The mid-range emission scenario (IS92a) is one of six specified by the Intergovernmental Panel on Climate Change (IPCC) in 1992. Data generated by all four models for past sea temperatures show a close correspondence to actual sea temperature records. For example, the ECHAM4/OPYC3 IS92a model simulates El Nino with a high degree of realism (Timmermann et al. 1999) and shows a similar mean and aximal 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. 22oC greater than those were in the IGOSS-NMC data set. As outlined above summer maximum temperatures are the key factor that predict when corals will bleach. Maximum temperatures predicted by the ECHAM4/OPYC3 IS92a model were only -0. 15 to 0. 46oC different from the summer maxima reported in the IGOSSNMC data set (Table 4). A similar situation held for sea surface temperature data in the other three model runs (Table 5). In this case, the predicted mean summer emperatures (calculated from the average of the sea temperatures over three months) were generally within 0. 5oC of the observed mean summer temperatures. Only one model (CSIRO DAR model) delivered a few of the larger differences. The thermal thresholds of corals were derived by using the IGOSS-NMC data set and both literature (Glynn 1993, Goreau and Hayes 1994, Hoegh-Guldberg and Salvat 1995, Brown 1997a, Hoegh-Guldberg et al. 1997, Jones et al. 1998) and internet (CHAM Network 1999) reports of bleaching events . An example is shown in Figure 7. Bleaching events were reported in French Polynesia (149. 5oW, 17. oS) in 1983, 1986, 1991, 1994, 1996 and 1998 and correspond to when the sea surface temperatures rose above 29. 2oC. This temperature was selected as the thermal trigger for corals at this location (Hoegh-Guldberg and Salvat 1995). This was repeated for the south coast of Jamaica (76. 5oW, 17. 5oN), Phuket (98. 5oE, 7. 5oN), Rarotonga (159. 5oW, 21. 5oS) and three sites on the Great Barrier Reef. The latter were in the southern (149. 5oE, 23. 5oS), central (147. 5oE, 18oS) and northern (143oE, 11oS) sections of the Great Barrier Reef. Thermal thresholds are shown in Figures 8 and 10 (horizontal lines; Rarotonga not hown) and ranged from 28. 3oC at Rarotonga and 30. 2oC at Phuket (previously reported by Brown 1997a). Table 6 lists the thermal set points derived and used in this study. The predicted sea temperature data were used in concert with the threshold values to project the frequency and intensity of coral bleaching. Differences between projected and observed sea temperature data (although minor) were subtracted from model data prior to analysis (Table 5). Differences were calculated using summer temperatures C L I M A T E C H A N G E , C O R A L B L E A C H I N G A N D T H E F U T U R E O F T H E W O R L D O S C O R A L R E E F S 13

Table 4. Comparison between on 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) for the period November 1981 to December 1994. 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 oC. GBR = Great Barrier Reef. Location Mean (IGOSSNMC) Mean ECHAM4/ OPYC3a Difference Max (IGOSSNMC) MAX ECHAM4/ OPYC3a Difference RANGE (IGOSS-NMC)

Range ECHAM4/OPY C3a South coast of Jamaica 27. 95 28. 36 0. 41 29. 40 29. 25 -0. 15 3. 24 1. 95 S-GBR 25. 04 26. 25 1. 21 28. 51 28. 87 0. 36 8. 27 5. 08 C-GBR 26. 21 27. 43 1. 22 29. 61 30. 07 0. 46 7. 28 4. 76 N-GBR 27. 39 28. 38 0. 99 29. 89 30. 38 0. 48 5. 45 3. 62 Rarotonga 25. 43 26. 35 0. 92 28. 49 28. 88 0. 39 5. 59 4. 42 Tahiti 27. 51 27. 85 0. 34 29. 57 29. 96 0. 39 3. 92 3. 46 Phuket 29. 08 29. 13 0. 05 30. 48 30. 87 0. 39 2. 70 3. 00 were calculated using the mean SST for the three month period (Jan-Mar, southern hemisphere; Jun-Aug, northern hemisphere) for the period from 1903 to 1994. The ationale for using summer temperatures was that the upper temperature reached by a model is the critical feature associated with the onset of coral bleaching. An example of the analysis comparing projected sea temperature data from the ECHAM4/OPYC3 IS92a model and the known thermal thresholds of corals for 7 sites in the worldOs tropical oceans is shown in Figure 8 and 10. This model run, like the other three, shows the universal trend within tropical seas of increasing sea temperature under a moderate global climate change scenario. This particular model also includes the most accurate representation of El Nino activity (Timmermann et al. 999, Roeckner et al. , in press) and projects that future ENSO events will generate higher and higher sea temperature maxima. By comparing projected sea temperat