10th Anniversary Review: a changing climate for coral reefs

Abstract

Tropical coral reefs are charismatic ecosystems that house a significant proportion of the world’s marine biodiversity. Their valuable goods and services are fundamental to the livelihood of large coastal populations in the tropics. The health of many of the world’s coral reefs, and the goods and services they provide, have already been severely compromised, largely due to over-exploitation by a range of human activities. These local-scale impacts, with the appropriate government instruments, support and management actions, can potentially be controlled and even ameliorated. Unfortunately, other human actions (largely in countries outside of the tropics), by changing global climate, have added additional global-scale threats to the continued survival of present-day coral reefs. Moderate warming of the tropical oceans has already resulted in an increase in mass coral bleaching events, affecting nearly all of the world’s coral reef regions. The frequency of these events will only increase as global temperatures continue to rise. Weakening of coral reef structures will be a more insidious effect of changing ocean chemistry, as the oceans absorb part of the excess atmospheric carbon dioxide. More intense tropical cyclones, changed atmospheric and ocean circulation patterns will all affect coral reef ecosystems and the many associated plants and animals. Coral reefs will not disappear but their appearance, structure and community make-up will radically change. Drastic greenhouse gas mitigation strategies are necessary to prevent the full consequences of human activities causing such alterations to coral reef ecosystems.

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Janice M. Lough

Janice Lough was born in Newcastle, UK in 1955. She has a BSc in Environmental Sciences (1976) and a PhD in tropical climate variations, undertaken at the Climatic Research Unit (1982), both from the University of East Anglia, UK. She was a Research Associate at the Tree-Ring Laboratory, University of Arizona, USA from 1982 to 1986 applying dendroclimatic reconstructions to understanding climate variation and change over North America and the North Pacific. She joined the Australian Institute of Marine Science in 1986 where she is now a Principal Research Scientist leading the Responding to Climate Change Research Team and affiliated with the ARC Centre of Excellence for Coral Reef Studies at James Cook University. Her current research activities include obtaining high-resolution proxy climate and environmental information from annually banded massive corals over the past several centuries and assessing the nature of regional climate changes due to the enhanced Greenhouse effect and their impacts and consequences for tropical coral reefs.

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Introduction

We had wheat sheaves, mushrooms, stags horns, cabbage leaves, and a variety of other forms, glowing under water with vivid tints of every shade betwixt green, purple, brown and white; equalling in beauty and excelling in grandeur the most favourite parterre of the curious florist. – (Matthew Flinders, October 1802)

Global warming due to the enhanced greenhouse effect is already occurring, with observed and projected temperature changes greatest at high latitudes.¹ Yet ecosystems in the naturally warm tropical ocean waters—coral reefs—are already showing evidence of global warming impacts. It is now 200 years since Matthew Flinders provided the above evocative description (that resonates with modern coral reef experiences) of the world’s largest coral reef ecosystem, Australia’s Great Barrier Reef. Why are these ecosystems now considered as one of the “most vulnerable” to climate change?² In this article I consider the mounting body of scientific evidence (though in the space available it is not possible to do full justice to the burgeoning literature) that a rapidly changing climate due to human activities is a major threat to the maintenance of present-day coral reefs as we know and rely on them.

Coral reefs—what are they?

Coral reefs are complex ecosystems that are uniquely defined amongst the world’s ecosystems in terms of both their biological components and the geological structures they create by the build up of calcium carbonate.³ Although the organisms that make up present-day coral reefs have evolved over the past 40–55 million years, contemporary coral reefs have formed only within the past 8–10 000 years, since sea level rose from ∼125 m below present at the height of the last glacial maximum (∼19 000 years ago).⁴

Tropical coral reefs are the result of a mutually beneficial relationship (symbiosis) between the coral animal (Phylum Cnidaria, Class Scleractinia) and single-celled photosynthetic plants called zooxanthellae (genus Symbiodinium). Photosynthetic products of the algae provide the coral host with cheap energy.^5–9 The zooxanthellae also play a role in light-enhanced calcification of scleractinian corals, allowing the rapid calcification necessary to form reef structures.¹⁰ In return, the algae obtain protection and essential nutrients from their coral host. The photosynthetic pigments within the algae give corals their colours. Together these organisms produce the extraordinary variety of coral skeletal forms and structures that form massive carbonate structures that can withstand the natural forces of erosion and provide the basis of coral reef ecosystems.¹¹

Coral reefs are not just corals. They provide complex habitats that support a great diversity of reef-associated fauna and flora. Australia’s Great Barrier Reef (GBR), for example, which extends ∼2000 km along the northeast coast of Australia and covers ∼35 million hectares (an area larger than Italy), contains nearly 3000 coral reefs built from over 360 species of hard coral. These reefs harbour ∼1500 species of fish, ∼4000 species of molluscs (shells), ∼400 species of sponges, ∼800 species of echinoderms (starfish, urchins etc.), ∼500 species of macroalgae (seaweeds), 23 species of marine mammals, extensive sea grass beds (home to internationally endangered dugongs), 6 of the world’s 7 species of marine turtle species, and 30% of the world’s soft coral species, several hundred species of seabirds, breeding grounds for humpback whales from Antarctica…………..and the list continues (http://www.gbrmpa.gov.au/). No ecosystem is an island and coral reefs, such as the GBR, are intimately linked with coastal ecosystems, such as mangroves, wetlands and estuaries. The international significance of the GBR is reflected in its inscription on the World Heritage List in 1981 (http://www.environment.gov.au/heritage/worldheritage/sites/gbr/values.htm). In addition, coral reefs only occupy about 10% of the GBR shelf and we are only beginning to understand the rich biodiversity of the 90% of inter-reefal areas.¹² Internationally, it has been estimated that we only know of ∼10% of the total number of species living on coral reefs.¹³

Why are coral reefs important?

Tropical coral reefs are the most biologically diverse of marine ecosystems. They are complex ecosystems at all levels, including their geological history, growth and structure, biological adaptation, evolution and biogeography, community structure, organisms and ecosystem metabolism and physical regimes. Globally, coral reefs provide ecosystem goods and services valued at >US$375 billion per year.¹⁴ Despite their relatively small area, coral reefs contain ∼30% of the world’s marine fish and reef fish account for ∼10% of fish consumed by humans. Tens of millions of people in over 100 countries with coral reefs along their coastline depend on the economic and social goods and services provided by these rich ecosystems.¹⁵ For humans, these goods and services include: fisheries, natural breakwaters, protection of coastal settlements, building materials, novel pharmaceuticals and burgeoning tourism industries. Coral reef ecosystems also provide habitat, food and shelter for many other organisms, and therefore, harbour a significant proportion of the world’s marine biodiversity.

Where are coral reefs?

Globally, coral reefs are estimated to cover an area ∼300 000 km², representing only 0.1–0.5% of the ocean floor.¹⁶ The distinction should also be recognized between reef-building coral communities which form coral reef structures and coral communities (such as those at Easter Island and the Solitary Islands south of Australia’s GBR) which are unable to accumulate sufficient calcium carbonate to form a coral reef structure.¹⁷ The latter are often more isolated and close or beyond the limits of coral reef distribution.

The global distribution of coral reefs has long been considered to be constrained to shallow, warm, well-lit, clear, low nutrient and low sediment waters, as well as by their geological and climate history and local bathymetry.^18,19 A more recent comprehensive analysis has clarified the environmental limits to coral reef development using up-to-date data on the geographic locations of coral reefs (ReefBase http://www.reefbase.org/main.aspx) and improved instrumental environmental data sets.²⁰ Temperature, salinity, nutrients, light availability and the aragonite saturation state of seawater were considered as the “first-order determinants of reef distribution” with regional-scale reef distribution being affected by factors, such as waves, ocean currents, larval sources etc. The aragonite saturation state of seawater is a measure of how easily aragonite, the main form of CaCO₃ created by reef-building corals, can form and depends on the concentration of calcium and carbonate ions in seawater, i.e. the carbonate chemistry of seawater.²¹ This analysis found water temperature at reef locations averages 27.6 °C and ranges from a seasonal minimum of 16.0 °C to a seasonal maximum of 34.4 °C (both in the northern Arabian Gulf) and salinity averages 34.8 PSU and ranges from 23.3 to 41.8 PSU. As noted in many earlier studies, these two variables are important controls on coral reef formation, and minimum water temperatures of ∼18.0 °C have long been considered the lower limit for coral reef formation.²² In contrast to earlier studies, low concentrations of nutrients were found to be of lesser importance as a limiting factor to coral reef development. The aragonite saturation state and light penetration, which both covary with water temperature, were likely limiting at higher latitudes. These perspectives on the environmental controls of coral reef distribution are important in assessing the potential responses of coral reefs to changes in their physical environment due to the enhanced greenhouse effect. Although an important factor, light is unlikely to change on large spatial scales but significant changes in water temperature and aragonite saturation state are highly likely (discussed below).

Before climate change: coral reefs already under threat

Our major finding is that human pressures pose a far greater immediate threat to coral reefs than climate change, which may only threaten reefs in the distant future.²³

The conclusion, that climate change was not a near-term threat to coral reefs, was drawn only 14 years by an international team of coral reef experts. What has been termed the “coral reef crisis” was already well underway before we realised the potential fragility of these highly diverse marine ecosystems to global climate change. The significant ecosystem goods and services and direct economic benefits that coral reefs provide to the large and expanding populations of tropical coastal regions have been progressively over-exploited. As a result, even without the climate change impacts discussed below, coral reefs have been declining at an alarming rate, due to direct local and regional human pressures, such as over-fishing, destructive fishing (e.g. dynamite), decline in water quality due to increased sediment from land-use changes, nutrient and chemical pollution and development on coasts (dredging, land clearing for ports, harbours etc., mining of coral reefs etc.).^23–27

Only 30% of the world’s coral reefs are considered at low risk from these increasing human stresses and 20% of reefs have, effectively, been destroyed.²⁸ The highly biodiverse reefs of Southeast Asia and the Indian Ocean (where human pressures continue to increase) are most badly affected. Indeed, an historical study of 14 coral reef regions suggests that human exploitation of coral reefs is not a recent phenomenon but has been occurring over thousands of years.²⁹ This exploitation, primarily through over fishing, which has impacted other coastal ecosystems,³⁰ has resulted in a trajectory of decline in coral reefs worldwide, even before concerns of global climate change impacts. Even what are regarded as pristine, well-protected reefs, such as the outer GBR, are already on this declining trajectory due to the loss of large herbivores and carnivores.

These primary and ongoing causes of coral reef decline all occur at the local- and regional-scale. They are a direct result of human-induced pressures and, therefore, are also, potentially, manageable and possibly reversible. This requires both active conservation measures, such as integrated catchment management reducing land-based pollution of reefs, elimination of destructive fishing practices, sustainable management of reef fisheries, and implementing and managing expanded Marine Protected Areas.³¹ Reversal of the trend also requires national and international initiatives to provide the many countries with degraded and degrading coral reefs, the majority of which are developing countries, with the capacity and necessary assistance to effectively manage their coral reef ecosystems.^24,26,28 Human interference with the global climate system has now added an additional set of threats to the survival of coral reef ecosystems—threats that are occurring at the global level and cannot be effectively managed locally.

Climate change—observed impacts and additional threats

Warming of the climate system is unequivocal, as is now evident from observations of increases in global average air and ocean temperatures, widespread melting of snow and ice, and rising global average sea level.¹

Observational evidence from all continents and most oceans shows that many natural systems are being affected by regional climate changes, particularly temperature increases.²

Global climate has varied and changed in the past on a range of timescales, and organisms and ecosystems have survived, changed their distribution and adapted to such changes. It is now, however, clear that human activities since the Industrial Revolution began in the late 18th century, primarily through burning of fossil fuels, land-use changes and agriculture, have altered and are significantly altering the composition of the earth’s atmosphere. These changes are resulting in more heat being trapped in the global climate system (the enhanced greenhouse effect) and are causing rapid and significant global warming and a changing global climate.¹ The atmospheric concentration of the main greenhouse gas, carbon dioxide, is now ∼40% higher than in the late 18th century. Based on instrumental records, global average temperatures are now ∼0.7 °C warmer and sea level ∼20 cm higher than in the late 19th century¹ and there are already discernible changes in many natural biological and physical systems, which are consistent with a warming climate, even with the relatively modest global warming observed to date.²

There are several aspects of anthropogenic climate change that have affected and will affect the environmental envelope of coral reef ecosystems—one to which they have been accustomed to since current sea level was reached ∼8–10 thousand years ago (Table 1). The most significant of these appear, at present, to be warming ocean temperatures increasing the frequency of mass coral bleaching events and absorption by the oceans of a significant proportion of the excess carbon dioxide, altering ocean chemistry and potentially reducing the ability of corals to form their skeletons and thus the very basis of coral reef ecosystems.

Table 1 Climate changes that affect coral reef ecosystems

Climate variable	Consequences
Warmer waters	•Coral bleaching
	•Coral diseases
	•Affect other reef organisms
Ocean acidification	•Weaker coral skeletons and reef structures
More intense tropical cyclones	•Physical destruction of reef
Rising sea level	•Coastal erosion
	•Higher storm surges
	•‘Drowning’ of some reefs
	•Increased area for some reefs
More extreme rainfall & flood events	•Low salinity waters extend further out on reefs
Changes to ocean currents	•Affect connectivity (e.g. larval supply) amongst reefs
	•Affect nutrient supply from upwelling
El Niño–Southern Oscillation events	•Extreme weather events that enhance probability of bleaching
Wind fields and atmospheric circulation patterns	•Changed prevailing weather conditions

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Warming oceans—coral bleaching and diseases

Coral bleaching is the term used to describe the loss by the coral animal of all or some of their symbiotic algae and photosynthetic pigments—with the result that the white calcium carbonate skeleton becomes visible through the translucent tissue layer. Coral bleaching is not a new phenomenon due to global warming. Corals are known to bleach in response to a range of environmental stresses (e.g. low salinity, pollution, unusually high or low water temperatures). In the past, however, such occurrences of bleaching were only observed on small spatial scales in response to localized stresses. What is new, and now clearly related to global warming, is an increase in frequency of large-scale, mass coral bleaching events, where entire reefs are affected.

Pioneering studies in the 1970s demonstrated just how close (within 1–2 °C) reef-building corals are living to their upper thermal tolerance limit before bleaching occurs.^32,33 The threshold for bleaching becomes critical during the seasonal maximum of sea surface temperatures (SSTs) at a given locality. Maximum SSTs at 1000 reef locations averages 29.5 °C and range between 28.2–34.4 °C.²⁰ Various studies have identified that there is not an absolute temperature at which corals will bleach but rather that the temperature threshold varies with ambient water temperatures on each reef.³⁴ This demonstrates that over long time scales, corals have adapted to their local environmental conditions.

The first “most alarming” reports of mass coral bleaching events were not initially linked with unusually warm SSTs, although a connection was made with El Niño events.^35,36 This was largely due to the lack of reliable long-term records of SSTs and other environmental variables on coral reefs. As more mass bleaching events occurred and observations improved, the link was made with unusually warm waters.^37–40 The suggestion that these unusual occurrences on coral reefs might be linked to global climate change due to the enhanced greenhouse effect,^41,42 is now no longer considered “dubious” but “incontrovertible.²⁴

Large-scale SST anomalies in the tropical oceans create conditions that can result in coral bleaching. The most extensive coral bleaching event on record occurred during the major El Niño–Southern Oscillation event of 1997–1998,⁴³ with 1998 being the then warmest year on record globally.⁴⁴ Mass bleaching was reported from nearly every coral reef region of the world.⁴⁵ Sixteen percent of the world’s coral reefs were estimated to be damaged by this unprecedented event and, of these, only 40% appear to have recovered and 60% have not.²⁸ The scale and magnitude of this event, that could essentially be tracked around the world as each region experienced unusually warm SSTs during its annual seasonal maximum, catalysed efforts to monitor the occurrence of conditions conducive to coral bleaching. The advent of satellite-based observations of the oceans since the early 1980s has dramatically increased our capabilities to observe global-scale patterns and anomalies in ocean surface climate. A range of products, derived from the original concept of “oceanic hotspots”,⁴⁶ are now routinely produced by the US National Oceanographic and Atmospheric Administration (NOAA;⁴⁷http://coralreefwatch.noaa.gov) and provide the basis for identifying potential bleaching conditions in near-real time. These bleaching alerts need to be confirmed with field observations and there is some evidence emerging that for particular reefs, the thresholds for the occurrence and intensity of bleaching may be modified by the history of past bleaching events.⁴⁸ Although such monitoring cannot prevent coral bleaching or mortality, timely information about bleaching potential enables scientists and reef managers to document the intensity, impact and subsequent effects more comprehensively than possible only 10–20 years ago. Improved knowledge of the links between the physical environment and biological processes of coral bleaching helps managers develop and test strategies to protect corals from bleaching and also, importantly, identify bleaching-resistant reefs. The latter are clear targets for enhanced protection efforts, as they may provide important refugia for coral reef organisms and sources for recruitment for bleaching-affected reefs as climate continues to change and increasingly stresses the world’s already compromised coral reef ecosystems.

At the local scale, the occurrence and intensity of bleaching can be highly variable, both within a coral colony, between coral colonies, within a reef and between reefs in a region.⁴⁹ Such variations are in addition to the different susceptibility of different coral species to thermal stress.⁵⁰ Other local physical factors can enhance or suppress the impacts of warmer than normal regional SSTs and thus the intensity of bleaching. Observations that corals often bleach more on their upper surface than at the sides of colonies clearly implicates light as an additional factor and frequently the local weather conditions that cause intense warming of the water column (calm conditions, low cloud amount, little water motion) allow increased light penetration at the coral surface.⁵¹ Increased cloudiness can also mitigate bleaching, even when SSTs are high.⁵² Lowered salinity due to a major flood event increased the intensity of coral bleaching on inshore reefs of the central Great Barrier Reef in 1998.⁵³ There can also be considerable local-scale variations in water temperatures within and between reefs that can also affect the occurrence and intensity of bleaching.^34,54,55 Such local-scale variations that reduce thermal stress can be linked to water movements, such as upwelling, mixing, tidal range and wave energy.^51,56,57 The continued existence of such bleaching-resistant sites may be critical for recovery of nearby bleaching impacted coral populations.⁵⁸

As a result of bleaching, corals may die, partially die or recover. Recovery depends on the coral rapidly regaining its zooxanthellae population soon after the bleaching stress.⁵⁹ Even for corals that appear to recover fully, there is mounting evidence of long-term consequences as a result of the thermal stress associated with the bleaching event. These consequences include reduced reproduction, reduced growth rates and increased susceptibility to other disturbances, such as coral diseases.⁶⁰ In addition, due to the different susceptibility of different species,⁵⁰ the overall effect of a bleaching event can be to reduce species richness and diversity and change the community structure of the coral reef.⁶¹

Global average temperatures have warmed less than 1 °C since the 19th century and those of the tropical oceans by about half the global average.¹ Average water temperatures for the most recent 30 years on the GBR, for example, are only 0.4 °C warmer than at the end of the 19th century but could be 1–3 °C warmer by the end of this century.⁶² The weather conditions (1–2 weeks of calm, cloudless conditions) that allow rapid warming of the water column in the summer season do not appear to have changed but this seemingly modest increase in baseline temperatures has been sufficient to take corals over the bleaching threshold in 1998, 2002 and again in 2006. Modelling of future impacts suggest that a 1–3 °C warming of the GBR would result in ∼80–100% bleaching compared to ∼50% in 1998 and 2002.^49,55 Maintenance of the hard coral at the heart of coral reefs cover requires corals to increase their upper thermal tolerance limits by 0.1–1.0 °C per decade.^63–65

Is it possible that corals and coral reefs can adapt or acclimate to these changing conditions? Some evidence is emerging that corals can respond to bleaching by changing the dominant type of symbiotic algae to more thermally tolerant partners. Corals can contain different types of symbionts and may be able to change the relative abundances of these clades—“symbiont shuffling”.⁶⁶ This strategy may, however, be at the expense of growth rates, competition and reproduction,⁶⁷ may only occur in a few species⁶⁸ and may not occur sufficiently rapidly to keep up with warming ocean temperatures.⁶⁹ Changing from type C to the more thermally-tolerant D, for example, would raise the thermal tolerance by 1–1.5 °C, which only matches the most optimistic projected warming for the end of this century.⁷⁰

Given that minimum water temperatures are a limitation on tropical coral reef development and the oceans are warming, why will coral reefs not simply expand into higher latitudes? Unfortunately, water temperatures are not the only limitation to coral reef development and there appears to be little opportunity for significant poleward expansion of their distribution as the world continues to warm. This is due to lack of suitable substrate combined with greater changes in ocean chemistry that are detrimental for reef development at these higher latitudes.^3,26,71

Increasing frequency of mass coral bleaching events is not the only impact of warming oceans on coral reef ecosystems. There is also an increasing frequency of reports of disease outbreaks affecting corals and other marine organisms⁷² and evidence is mounting that these occurrences are related to warmer ocean temperatures.⁷³ Warmer waters appear to be increasing the severity of diseases in the ocean, which will reduce the vitality of marine ecosystems, such as coral reefs.^74,75

Ocean acidification—weaker reef structures

There is growing concern about a more insidious effect of enhanced greenhouse gas concentrations on coral reefs and other marine calcifying organisms—progressive ocean acidification. About 30% of the excess carbon dioxide (the principal greenhouse gas) released into the atmosphere by human activities since the Industrial Revolution has been absorbed by the oceans.^76,77 This is changing the chemistry of the oceans, which become more acidic, though still alkaline. The pH of the oceans has already decreased by 0.1 and is projected to be 0.4–0.5 lower by the end of this century. The rate of current and future carbon dioxide increase is estimated to be ∼100 times faster than at anytime over the past 650 000 years.⁷⁸ Increasing the amount of carbon dioxide dissolved by the oceans lowers the pH and decreases the availability of carbonate ions in the water and thus lowers the saturation state of the major shell-forming carbonate minerals.²¹ Many marine organisms (corals, coralline algae, molluscs, echinoderms, foraminifera, coccolithophores, shelled pteropods) use calcium and carbonate ions from seawater to secrete calcium carbonate. Changing the ocean chemistry essentially shifts the geochemical equations by which these organisms “calcify” and reduces their ability to form their skeletons and shells. Increased ocean acidification has been demonstrated by various modelling and experimental studies to reduce the ability of corals to form their skeletal structures—the very heart of tropical coral reef ecosystems.^21,79,80 The general scientific consensus is that changes in ocean chemistry due to increasing CO₂ has serious implications for coral reefs and other calcifying organisms of the open ocean and could alter the makeup of marine ecosystems, disrupt food webs and weaken coral reef structures. For coral reefs, weaker reef structures would reduce their resilience to the natural forces of erosion, and slower growth will set back recovery after bleaching and other disturbances. An additional threat to the ability of coral reefs to maintain their structure in an increasingly acidic ocean environment, is the particular sensitivity of coralline algae (crustose calcareous algae, CCA). These contribute significantly to coral reefs by secreting skeleton that forms part of the reef structure itself and by cementing loose material together.⁸¹ CCA calcify high-magnesium calcite at a greater metabolic cost than aragonite calcification by corals. This mineralogy makes them particularly sensitive to changes in ocean chemistry, which may not only reduce their ability to calcify but may even result in dissolution of their calcified structures, thus further destabilizing the reef-building process.^21,78,82 Our understanding of the full range of consequences of changing ocean chemistry is, however, extremely limited at present and, as with many aspects of climate change, the experiment is occurring in real time in the real world. This is now a major focus of international research efforts.^21,78

Other climatic stresses to coral reefs

More intense tropical cyclones—localised destruction

The natural environment of corals reefs (at the interface of land, sea and the atmosphere) can be highly dynamic and potentially stressful. Reef organisms have, however, evolved strategies to cope with occasional environmental disturbances, such as tropical cyclones, and given sufficient time between disturbances, damage and destruction would normally be followed by recovery and regrowth.

Tropical cyclones are amongst the most destructive weather systems on earth, and although rarely observed equatorward of 5° latitude, are common and natural disturbances to many coral reefs regions.⁸³ Tropical cyclones are “agents of mortality” on coral reefs and, primarily through the large waves they generate, can directly influence the structure and local distribution of coral reef assemblages.^84,85 Tropical cyclones can also result in reduced salinity due to heavy rainfall and enhanced river flows onto nearshore reefs, as well as coastal destruction due to elevated sea levels associated with destructive storm surges. Such natural events can cause significant local disturbance but, given time and the absence of other stressors, coral reefs can recover.^86,87 Recent studies in the Caribbean suggest, however, that these already seriously degraded reefs are not recovering as well as they used to from tropical cyclone impacts.⁸⁸ Ironically, the passage of a tropical cyclone, by rapidly cooling surface ocean temperatures, can reduce the impact of elevated water temperatures and thus the intensity of bleaching, at least on small space scales.⁸⁹

There is already some evidence to suggest that the destructive potential of tropical cyclones around the world has increased in recent decades.^90,91 Although warming ocean waters might be expected to increase the intensity and frequency of occurrence of tropical cyclones, their formation depends upon a number of other factors.⁸³ Current projections give no clear indication as to whether the number and preferred locations of tropical cyclones will change in a warming world. The intensity of tropical cyclones is, however, expected to increase,¹ which will result in increased localised physical destruction on coral reefs—another disturbance from which reefs need time to recover.

More intense rainfall and river flow events—low salinity and terrestrial inputs

Coral reefs exist in a range of environments, with some regularly influenced by low salinity and naturally turbid waters from the adjacent land masses. This can introduce large cross-shelf gradients in coral reef communities between turbid inshore and clear oceanic offshore waters as happens, for example, on the GBR.⁹² In some locations, changes in land use on the mainland has been a significant source of contaminants and sediments to nearshore reefs that can be detrimental to their well being and part of the ongoing catalogue of local human impacts on the health of the world’s coral reefs.^26,28 Any change in regional rainfall and river flow regimes, as a consequence of global warming, can potentially impact coral reefs. Such projections need to be regionally specific and, unfortunately, unlike water temperature changes, are less well understood. There is, however, a general consensus that the intensity of extreme flood and drought events are likely to increase,¹ which would affect coral reefs. There is, for example, evidence from paleo-records of river runoff contained in massive coral cores, of a recent increase in such extreme events on Australia’s GBR, with the wet years being wetter and dry years drier than in previous centuries. Enhanced river flood events are also likely to take freshwater further out to midshelf reefs that are not used to such low salinity waters.⁹³

Rising sea level—winners and losers

Global sea level has already increased ∼20 cm over the past century as a consequence of thermal expansion and melting of land-based ice¹ and the rate of increase seems to have accelerated in recent decades.⁹⁴ This rise will continue with sea level projected to be up to 60 cm higher by the end of this century,¹ although this may well be a conservative projection, as it does not allow for changes in the rate of loss of the vast Greenland and Antarctic ice sheets.^95,96 Although rising sea levels will have significant impacts on the many densely populated low-lying coastal communities,⁹⁷ a steady rise in sea level is not considered to be a major source of stress to coral reefs. Global sea level has been fairly stable for the last several thousand years and some reefs have grown vertically to the level where they are limited by present day sea level. So, some sea-level rise would be beneficial to such reefs, although some reefs in deeper water could eventually drown due to reduced light availability with increased water depth. The rate and magnitude of projected sea level rise are considered “well within the ability of most reefs to keep up”.⁴¹

Changing atmospheric weather patterns (ENSO) and ocean circulation

El Niño–Southern Oscillation (ENSO) events involve large-scale anomalies of the ocean–atmosphere system and are the major source of short-term climate variability within the tropics which, through teleconnections, also impact climate in extra-tropical latitudes. The two phases of ENSO, El Niño and La Niña, are typically associated with distinct and different anomalies of the tropical atmosphere and ocean climate.⁹⁸ The major 1982–83 El Niño event first triggered warnings of a link between ENSO and mass coral bleaching events.^99,100 The 1997–98 El Niño event (coinciding with what was then the warmest year on record) was also one of the most extreme El Niño events on record⁴³ and coincided with the greatest recorded thermal stress at many coral reef sites.¹⁰¹El Niño events do not cause mass coral bleaching, but they do increase the likelihood of anomalous ocean warming that results in bleaching,¹⁰² and mass coral bleaching can occur in the absence of ENSO extremes when other climate anomalies cause regional warming; e.g., Great Barrier Reef in early 1982,¹⁰³ Moorea in 1994;¹⁰⁴ Hawaii in 1996,¹⁰⁵ and the Caribbean in 2005.¹⁰⁶ The risk of anomalous SST conditions that might trigger coral bleaching has been, however, significantly modulated by ENSO events. It is, therefore, important to understand how the frequency and intensity of ENSO events might change as the world continues to warm. There is, however, no consistent picture of whether there will be changes in ENSO intensity or frequency of occurrence associated with continued global warming.¹

The present-day distribution of ocean currents and circulation in the vicinity of coral reefs are important controls on the ecosystem dynamics as amongst other factors, these can have significant effects on the connectivity between reef systems that can control larval dispersal etc. Little is known as yet as to how ocean currents will change as the world continues to warm, although there is evidence in some areas of significant changes already occurring. The East Australian Current, for example, flows southwards from its origin in the Coral Sea. There is already some evidence that its southern extension is strengthening and carrying sub-tropical marine species further south.¹⁰⁷ Changes in ocean current strength and location will also impact other coral reef ecosystems.

Summary—is there a future for coral reefs?

Vague hopes that the biology of coral reefs will keep up with the pace of change are not matched by current observations or our understanding of past changes.¹⁰⁸

The world’s coral reef ecosystems were in serious trouble before the advent of rapid climate change due to the enhanced greenhouse effect. The prognosis for their future is undoubtedly dire and their loss, severe degradation and change in community structure that will result from ongoing climate changes, would be catastrophic at many levels. These threats are in addition to ongoing localized degradation and deterioration of coral reef ecosystems due, primarily, to over exploitation.²⁷ Although many value coral reefs for their aesthetics, the majority of people who depend on coral reefs for their livelihoods (fisheries, tourism, shoreline protection) live in poor, developing countries who contribute only a tiny part of the world’s greenhouse gas emissions. A recent estimate is ∼10% of the world’s population live within 100 km of coral reefs and ∼90% of these people live in developing nations—∼63% of people (415 million) living within 100 km of coral reefs live in countries where per capita GDP is <US$5000.¹⁰⁹ This compares with a per capita GDP for Australia, which contains ∼22% of the world’s coral reef area, of ∼$US33 000. As with many aspects of climate change, the people who are likely to suffer the greatest impacts are those from developing countries who have contributed the least to global warming.¹¹⁰

A plethora of scientific papers, national and international reports and scholarly books now document the nature, impacts and potential consequences of ongoing rapid climate change for coral reefs, as well as local direct human impacts.^58,111–113 There is a clear consensus that the world’s coral reefs are in trouble and that the alarm bells have been ringing for decades. The future of coral reefs as climate continues to change is inextricably linked to coral reef health. Some coral reefs have shown the ability to withstand disturbances, such as coral bleaching (resistance), and some coral reefs have shown the ability to recover from such disturbances (resilience).^114,115 These attributes can be the result of such coral reefs being dominated by resistant species or to their physical environment reducing the probability of stress. Reducing and reversing local, direct insults to coral reefs clearly increases their resilience to global-scale climate change—“healthy” coral reefs, for example, recovered better after the major 1997–98 world-wide coral bleaching event than those already compromised by local anthropogenic stresses or diseases.²⁸ Increasing the resilience of the world’s coral reef ecosystems requires integrated national and international actions and a greatly expanded network of marine protected areas.²⁴

Even with rapid global implementation of stringent mitigation strategies to stabilize and reduce greenhouse gas emissions, the world and coral reefs are committed to significant rapid climate change, increased acidification of the oceans and accelerated sea-level rise. The issue is not just a “change” from one climate regime to a new one, to which organisms have to adapt BUT that for the foreseeable future, climate will be changing and it could be a long time before a new, relatively stable climate regime is reached (i.e. one not influenced by human activities). Indeed, even if it were possible to stabilize greenhouse gas concentrations at their present levels, we are still committed to “future climate changes that will be greater than those we have already observed”.^116,117 Although coral reefs have a long geological history, there is now a severe mismatch in timescales for successful organism adaptation (thousands to millions of years vs. tens to hundreds of years).

Various aspects of our current experiment with the global climate system pose significant challenges for even the most well-managed and highly protected of the world’s coral reefs, such as the GBR—a vast ecosystem that we do not even fully understand in its present form. Coral reefs are unlikely to disappear everywhere, although some are clearly already beyond recovery. We may well witness within our lifetimes a shift from coral reefs dominated by corals to reef communities dominated by algae and filter feeders. Coral reefs are also not just corals, these rich, biodiverse marine ecosystems provide habitat and food to a wealth of other animals and plants which, in turn, provided millions of people with economic and social benefits. To enter a world of “low coral cover” could be one of the earliest and most profound consequences of global climate change due to human activities.

Acknowledgements

The author thanks two anonymous reviewers for their very helpful comments.

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