BLEACHING GUIDE 17

CORAL BLEACHING –

A REVIEW OF THE CAUSES

AND CONSEQUENCES

CHAPTER 4

A REEF MANAGER’S GUIDE TO CORAL BLEACHING

4. CORAL BLEACHING – A REVIEW OF THE

CAUSES AND CONSEQUENCES

The mass coral bleaching events that have occurred throughout the tropics over the last

decade have provided unprecedented opportunity, and motivation, to study this

phenomenon.As a result, knowledge about the causes and consequences of coral bleaching

has increased substantially in recent years. This accumulating body of information is

providing critical advances in our understanding and has generated new insights, which can

assist reef managers to respond to the threat of coral bleaching. This section aims to

provide a summary of recent developments in the science of coral bleaching, highlighting

emerging knowledge and recent insights that are most relevant to reef managers.

4.1 What is coral bleaching?

4.1.1 The coral-algal symbiosis

The great majority of corals live in a symbiotic relationship

with zooxanthellae, a type of single-celled dinoflagellate

algae.These microscopic algae live within the coral's tissues.

Zooxanthellae produce energy-rich compounds through

photosynthesis, providing a food source that is absorbed and

used by the coral. In general, corals are highly dependent on

this symbiotic relationship, receiving up to 90 per cent of

their energy requirements in this way

Bleaching is a stress response that results when the coral-

algae relationship breaks down. The term 'bleaching'

describes the loss of colour that results when zooxanthellae

are expelled from the coral hosts or when pigments within

the algae are degraded. Because the photosynthetic pigments found in zooxanthellae give

corals most of their colouration, the loss of zooxanthellae renders the tissue largely

transparent.The white of the calcium carbonate skeleton is then clearly visible through the

un-pigmented tissue, making the coral appear bright white or 'bleached'

. Bleaching also

occurs in other animals that are engaged in symbiotic relationships with zooxanthellae, such

as foraminifera, sponges, anemones and giant clams.

In some instances, coral bleaching will result in corals

taking on a pastel shade of blue, yellow or pink rather

than turning bright white. This is due to proteins

produced by some corals, which tint the coral tissue and

become the dominant pigment during bleaching, when

zooxanthellae are absent

110, 111

Bleaching is a stress response that

results when the coral-algae

relationship breaks down

The zooxanthellae can be clearly

seen as golden-coloured dots in

this close-up image of a coral

polyp.The symbiotic relationship

with these tiny dinoflagellates

enables corals to gain energy

from sunlight

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It isn't only corals that bleach; other organisms that have zooxanthallae, such as this (a) giant clam and (b)

anemone can also bleach in response to thermal stress

a b

4.1.2 The causes of coral bleaching

The primary cause of mass coral bleaching is increased

sea temperatures

9,13, 18, 23, 53

.At a local scale, many stressors

including disease, sedimentation, cyanide fishing,

pollutants and changes in salinity may cause corals to

bleach. Mass bleaching, however, affects reefs at regional

to global scales and cannot be explained solely by localised stressors operating at small

scales. Rather, a continuously expanding body of scientific evidence indicates that such mass

bleaching events are closely associated with large-scale, anomalously high sea surface

temperatures

8, 9, 13

. Temperature increases of only 1-2ºC can trigger mass bleaching events

because corals already live close to their maximum thermal limits

9, 23

The role of temperature and light. Increased temperatures cause bleaching by reducing the

ability of the photosynthetic system in the zooxanthellae to process light. When

temperatures exceed certain thresholds, incoming light overwhelms the photosynthetic

apparatus, resulting in the production of reactive oxygen species that damage cellular

structures

24, 112

. Corals cannot tolerate high levels of these toxic molecules, and they must

expel the zooxanthellae to avoid tissue damage. Because of the low tolerance of the

photosynthetic process to high temperatures, even normal levels of sunlight are enough to

damage the photosynthetic system of the zooxanthellae when temperatures exceed

certain levels

23, 113

. Furthermore, as light levels increase the amount of damage due to

thermal stress increases as well

The relationship between temperature and light in

causing coral bleaching helps explain observations of

reduced bleaching on shaded parts of coral colonies or

in shaded reef areas

9, 114, 115

. It also suggests that the spatial

extent and patterns of bleaching responses may be

influenced by factors that determine the amount of solar radiation to which corals are

exposed. These factors might include cloud cover

, attenuation in the water column

116

stratospheric ozone

and shading by large landforms such as steep-sided shorelines

Mass coral bleaching affects reefs at

regional to global scales – it is

primarily caused by unusually high

sea temperatures

Bleaching is reduced in shaded reef

areas because light levels influence

the amount of damage caused by

temperature stress

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Natural variations in turbidity may also play an important role in determining bleaching risk.

A recent study of the patterns in underwater light levels on a coastal coral reef found that

there were periodic intervals of low light levels due to cloud cover and sediment re-

suspension (high turbidity), which were driven by large-scale pressure systems

117

. Such

natural variability has strong implications for bleaching risk, and knowledge of these factors

can be used to prioritise management effort to other factors that are amenable to

management intervention.

4.2 Factors that confer resilience to coral bleaching

Resilience to bleaching is determined by the outcome of three key aspects of the bleaching

process: resistance to bleaching, ability to survive the bleached state (tolerance) and rate of

reef recovery after coral mortality. Understanding the factors that influence each of these

steps is central to our ability to understand, and potentially manage, the factors that confer

resilience to bleaching on corals.

4.2.1 Factors that influence resistance

The variability that characterises bleaching events points

to an important fact: individual corals vary in their

responses to heat and light stress.Variability in bleaching

response has been observed within individual coral

colonies, among colonies of the same species, and

between colonies of different species

23,118

. These

taxonomic variations are further compounded by

spatial patterns, with corals of the same species often showing different bleaching responses

at different locations

18, 19, 79, 118

. These patterns have been observed at scales ranging from

metres to thousands of kilometres. Knowledge of the factors, both external and intrinsic to

individual corals, that determine whether corals bleach is an important basis for

management actions in response to the threat of bleaching. Better understanding these

factors is the central aim of an integrated research strategy being taken in the US territory

of American Samoa as a management response to climate change (case study 9).

External factors. Externally, there is considerable variation in the environmental conditions

experienced by coral colonies. This variation creates critical differences in exposure to

heat, light or other stressors, leading to many of the patterns seen in bleaching responses.

Some of this patchiness can be attributed to patterns in sea surface temperatures,

especially at larger spatial scales

. Regional and local differences in weather can also cause

differential heating of the water, while proximity to upwelling of cooler waters, mixing by

currents and other large-scale processes can help keep temperatures below local

bleaching thresholds. At smaller scales, the microenvironment of corals can also vary.

Water currents and flow regimes increase water movement around corals, helping them

to get rid of metabolic waste and toxic molecules

, thereby potentially reducing their

susceptibility to thermal stress.

Understanding the factors that

determine variation in bleaching

response of corals exposed to

temperature stress provides an

important basis for management

actions in responding to the threat of

bleaching

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Box 4.1 Coral taxa and resistance to mass bleaching

Bleaching resistance is highly variable among corals, as evidenced by the extremely

variable responses of coral species to thermal stress. While some corals will show visible

signs of bleaching after only one or two weeks at temperatures 1.5ºC above the normal

maximum, others at the same location will not bleach unless these temperatures persist

for more than four to six weeks.

A strong hierarchy of resistance can be detected in diverse coral assemblages, such as

those in the western Pacific and Indian Oceans

(Figure 4.1).Typically, fine-structured and

fast-growing corals with thin tissue and good connections between polyps tend to be the

most susceptible to bleaching. Tissue thickness has been shown to correlate with

susceptibility to bleaching

123, 124

, although the role and relative importance of these various

traits remain to be thoroughly explored.

Common examples of corals with low resistance are the pocilloporids and many

acroporids (especially the branching and tabular growth forms), as well as the hydrocoral

millepora. Species that are more resistant tend to be characterised by solid, massive

skeletons, with thick tissue and slow growth rates, such as porites, faviids, and mussids.

Interestingly, some of the species most often associated with inshore or turbid reef systems

are among the most resistant to bleaching, such as turbinaria

125

RESISTANCE

GROWTH FORM

Fine branching

Branching, tabulate,

encrusting/foliose

Acropora

Montipora

CORAL FAMILY EXAMPLES

HIGH

LOW

MEDIUM

Pocilloporidae

Seriatopora

Stylophora

Pocillopora

Acroporidae

Massive, brain

Favia

Favities

Leptoria

Goniastrea

Platygyra

Faviidae

Massive, boulder

Por i te s

Goniopora

Poritidae

Various

Turbinaria

Cyphastrea

Various

Figure 4.1 A generalised hierarchy of coral susceptibility to bleaching

Corals vary in their susceptibility to bleaching. While many factors influence bleaching resistance, the

growth form or family of a coral provides a rough but reliable indication of its susceptibility to heat stress.

An integrated research strategy to assist

management responses to climate change – American

Samoa

Identifying the need for research

Resource managers increasingly struggle to determine local level responses to climate change.

In the US territory of American Samoa, coral reef managers and scientists have identified climate

change as a key and imminent threat to the health of the islands' fringing reef system. Physical

dangers posed by wave action due to coral loss, increased or decreased rainfall, phase and

community shifts on reefs, and sea level rise are just a few of the things that reef managers and

policy-makers may have to contend with in coming years at this location. Residents of American

Samoa have relied on the reef ecosystem for protection, food, goods and services for millennia.

However, they are likely to face severe disruptions to lifestyle, public health hazards, and a

decreased ability to be self-supportive if projected increases in the frequency and severity of

bleaching eventuate.

In response, local policy-makers are facilitating climate-related research around the islands of

American Samoa. It is hoped that data derived from these projects will give managers options

for site-specific protection measures, such as Marine Protected Areas, targeted reductions in

location-specific land-based sources of pollution, restrictions on use, and even, if appropriate,

artificial propagation of coral.

Ofu Island – a laboratory in the field

The most notable of the recent research

initiatives within American Samoa is being

conducted in the lagoonal system along the

south shore of Ofu Island.This area is the focus

of research aimed at determining whether

some of the coral species residing there have

adapted to bleaching stresses.The hydrography

of the lagoon ensures that there is little, if any,

flushing during low tides. It is during these times

that temperatures and ultraviolet radiation

(UV) around shallow water corals increase

dramatically. The extreme temperature ranges

that corals in Ofu can withstand on a regular basis indicate that this site may be a natural climate

refuge

164.

The warmer water temperatures projected to accompany climate change are likely to

result in calmer, clear water (due to stratification and the loss of UV blocking compounds in the

water column itself). Knowledge about the characteristics that confer stress resistance to corals

of Ofu lagoon can thus be used to understand the features that will help corals survive future

thermal stress events in more open reef habitats.

Research projects

Four research projects have been developed by American Samoa in conjunction with various

partners. In combination, they will provide valuable insights to guide management efforts aimed

at helping American Samoan reefs survive future coral bleaching events.

CASE STUDY 9

Ofu Island in American Samoa

Are some corals better prepared for climate change? MMA concentrations in Ofu lagoon corals

(WWF /Emerald Coast Consulting).

This study examines the microsporine-like amino acid (MAA) concentrations in corals in the

lagoons and near-shore (cooler, deeper) reefs of Ofu. Microsporine-like amino acids act as a kind

of sunscreen, protecting corals from damaging UV light. Coral nubs are being collected from a

combination of species found in all lagoons and paired with samples of the same species from

outside of the lagoons, as well as from species only found in some lagoons. These samples will

be compared to determine whether their history has imparted some selective advantage in

terms of their capacity to deal with the thermal stress associated with future climate scenarios.

Nearshore hydrodynamic modeling for Marine Protected Areas (MPAs) in American Samoa

(Eric Treml and Patrick Halpin, Duke University)

This research uses a spatially explicit, hydrodynamic modelling approach to address high-priority

MPA management issues, such as coral bleaching, land-based sources of pollution, and over-

fishing. The aim is to identify connections among the design of MPAs, long-term monitoring

methods and the local needs of American Samoa. Working closely with the local marine

management community, this research will result in the development of spatial management

strategies and tools for coral reef protection and MPA site development.

Coral disease prevalence on the reefs of American Samoa

(Greta Aeby, Hawaii Department of Land and Natural Resources)

This study addresses issues related to coral disease, coral bleaching and pollution and works to

examine the relationships between water quality, coral bleaching and the susceptibility of

organisms to disease.The goals of the research are to: (a) conduct a baseline assessment of the

abundance and distribution of bleached and diseased corals and of crustose coralline algae at

sites throughout American Samoa; (b) correlate the incidence of bleached and diseased colonies

with environmental data, and (c) systematically describe gross and microscopic morphology of

lesions in corals and crustose coralline algae. This work will help to develop a standardised

nomenclature for identifying and classifying diseases.This is a particularly important task as the

frequency of disease is expected to increase due to climate change and increases in land-based

sources of pollution in reef areas worldwide

Extrinsic and intrinsic factors affecting the resilience of corals to climate change and their use in

designing marine reserve networks (Charles Birkeland, University of Hawaii)

This three-year study aims to determine the intrinsic and extrinsic factors that enhance the

ability of a diverse set of corals (approximately 100 species) to resist environmental stressors,

such as extreme upper temperature limits, temperature fluctuations, and low and high levels of

dissolved oxygen. Intrinsic factors include: zooxanthellae types, microbial community

composition, microsporine-like amino acid levels and genetic traits. Understanding these factors,

and their relevance, will improve knowledge of ecosystem response to environmental factors,

and of how future environmental conditions may affect community structure and functions. Such

information will ultimately inform managers and scientists designing Marine Protected Areas and

similar conservation strategies.

For more information contact:

Chris Hawkins

University of Massachusetts at Amherst

ha[email protected]

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Other stresses in the external environment of corals can also have an affect on their

susceptibility to thermal stress. Preliminary research indicates that synergies between

temperature and other stressors, such as pollution, turbidity and sedimentation, changes in

salinity or exposure to pathogens, may interact to trigger or exacerbate bleaching

.The role

of pathogens in localised bleaching may also warrant further consideration, as recent

studies have demonstrated the induction of bleaching by bacteria in certain corals from the

Mediterranean and Red Seas

119, 120

. Further investigation of these issues, and confirmation of

key mechanisms driving synergistic effects involving coral bleaching, have the potential to

reveal opportunities for management interventions that could reduce bleaching impacts.

Internal factors. Intrinsically, both the genetic identity and the history of coral colonies and

their zooxanthellae can contribute to variation in bleaching susceptibility

23, 121

. This may be

observable in individual colonies, or the effect may be observable in the bleaching

susceptibility of entire reef communities

122

. At the colony level, species characterised by

branching or tabular growth forms and thin or well-connected tissue, tend to bleach more

than species with massive growth forms and thicker or less-integrated tissues (see Box 4.1).

Thicker tissue may shade zooxanthellae and increase resistance to bleaching

9, 123

.The ranking

of common coral groups by bleaching susceptibility is remarkably consistent between sites

on opposite sides of the world, suggesting that the properties of the animal host (above

and beyond differences in zooxanthellae type) play an important role in determining the

response of corals to thermal stress

The intrinsic characteristics of corals that enable them to

adjust to elevated light levels also play a role in

determining their resistance to bleaching. Coral polyps

that have experienced higher light levels have been

shown to be more resistant to bleaching when exposed

to high water temperatures

115

, suggesting that corals

acclimatised to high light will be less likely to bleach in

response to thermal stress. This implies that corals that

have experienced (and survived) extreme environmental

conditions in the recent past may be more resistant to

bleaching stress in the future. However, the effects of

historical exposure to light are subtle, and acclimatisation

is unlikely to allow corals to withstand the large

temperature anomalies that have triggered recent mass

bleaching episodes

Genetic variation in zooxanthellae is another intrinsic

characteristic that could influence the bleaching

resistance of corals (Box 4.2). Differences in thermal

tolerance among varieties, or clades, of zooxanthellae

suggest that coral hosts that have high densities of heat-

tolerant algae may be less susceptible to coral bleaching

126

. Shifts toward more heat-

tolerant populations of corals or zooxanthellae can be expected to arise from selective

mortality of more sensitive genotypes during severe bleaching events. However, corals

Genetic variation among individual

zooxanthallae (shown here)

influences the resistance of corals to

heat stress and bleaching. Although

corals may be able to shift the

relative dominance of different

varieties of zooxanthallae within

their tissues in order to increase

their resistance to bleaching, there

are limits to the extent that corals

can use this strategy to acclimatise

to large temperature anomalies

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may also be capable of forming new symbioses with more tolerant zooxanthellae in

response to changing temperature regimes (the Adaptive Bleaching Hypothesis)

127

; this

possibility remains the focus of ongoing research and discussion (for example, Hoegh-

Guldberg et al (2002)

113

4.2.2 Factors that influence survival

Bleached corals are still living, and if temperature stress subsides soon enough, most are

capable of surviving the bleaching event and repopulating their tissues with zooxanthellae.

The mechanism by which corals regain their symbiotic algae probably varies among species.

It may occur through uptake of new zooxanthellae from

the water column, although the most likely process is

multiplication of surviving zooxanthellae that remain in

the bleached coral's tissues at very low levels. Even a

coral that appears much bleached to the human eye can

still retain as many as 100-1000 cells per cm

(normal

densities are 1-2 x 10

per cm

)

130

Corals that survive bleaching events

are still likely to suffer sub-lethal

impacts, such as reduced rates of

growth and reproduction and

increased susceptibility to diseases

Box 4.2 Zooxanthellae and resistance to mass bleaching

A characteristic that appears to be important in determining resistance of corals to bleaching

is the type of zooxanthellae hosted. Numerous different types, or clades, of zooxanthellae have

been recognised, and there is some evidence that they have different susceptibilities to thermal

stress

128

. Many corals have multiple varieties of zooxanthellae within their tissue, and the

relative proportion of the different varieties is variable. A recent experiment has revealed that

some corals can vary the ratio of zooxanthellae clades, with a resulting improvement of their

thermal tolerance

129

.This feature is akin to acclimatisation as it involves the use of pre-existing

strategies within the coral-zooxanthellae association. If bleaching events increase in both

severity and frequency in the future, this may play a small role in determining bleaching

response patterns on larger spatial scales. As with other examples of acclimatisation, there is

a limit to the extent that corals can use this strategy to shift their thermal tolerance.

Another possible mechanism by which corals could increase their thermal tolerance is to swap

their zooxanthellae for more resistant varieties

127

. While this idea continues to be debated

113

it seems increasingly likely that changes in zooxanthellae populations are most likely to occur

through shifts in the relative dominance of heat-tolerant varieties already within a coral's

tissues, rather than by taking on new varieties.The potential for corals to adopt new varieties

of zooxanthellae remains an area of active research.

The role of coral pigments in sheltering zooxanthellae from light stress is another area of active

research that could help explain some of the differences in bleaching resistance

110, 111

Fluorescent pigment granules (FPGs) are common in many corals, at least in the western

Pacific. They are positioned within the coral's tissue to optimise the light environment for

zooxanthellae, concentrating light in low-light habitats, and shielding zooxanthellae in high light

conditions. In this way, corals with high concentrations of FPGs may be less vulnerable to

bleaching when water temperatures reach stressful levels.

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Corals that survive bleaching events can still suffer significant impacts. Reproduction of

corals that have bleached and recovered, for example, is much lower than that of corals

that have not bleached

26, 114, 131

. Growth of bleached corals is also reduced, probably due to

the combined effects of the stress and the reduced supply of energy following decreased

zooxanthellae densities

. Bleached corals may also have reduced immunity to pathogens,

making them more susceptible to disease

The condition, or health, of individual coral colonies is emerging as a particularly important

factor in determining whether or not a bleached coral survives. Recent and ongoing studies

predict that coral condition (as determined by its energy status or the size of its lipid stores)

will affect mortality risk during and following a bleaching event

. Specifically, large energy

stores are likely to help a coral survive the period of starvation associated with depleted

zooxanthellae populations. With adequate energy stores, a healthy coral will be able to

maintain itself while bleached, until zooxanthellae populations and photosynthesis can be

restored. Similarly, coral species that rely more heavily on heterotrophy (feeding on organic

material from the water column) for their energy supply

132

, such as those on coastal reefs,

are also more likely to be able to tolerate the loss of zooxanthellae.

Box 4.3 How managers can help corals survive bleaching

While extreme temperature stress is almost certain to result in widespread coral mortality,

the effects of more moderate temperature anomalies are highly variable. When

temperatures do not greatly exceed bleaching thresholds, the coral loses its zooxanthellae,

but its tissue may not be directly damaged. Whether mortality follows bleaching in these

circumstances is thought to be largely dependent on the coral's ability to endure

starvation, or to supplement its energy requirements from food particles captured from the

water column (heterotrophy).

Without their energy-providing zooxanthallae, bleached corals essentially enter a period of starvation.

The condition of a coral as it enters this state is an important factor determining whether the coral can

survive a bleaching-induced 'famine'. Another factor influencing coral survival during bleaching is the

coral's ability to feed on plankton and other organic matter in the water column by using its feeding

tentacles, as shown here

107

Some corals, especially species adapted to turbid environments, have been shown to rely

heavily on heterotrophy. These corals may be less dependent on the energy provided by

their zooxanthellae and thus less prone to starvation during a bleaching event. While the

importance of heterotrophy to turbid-water corals has been demonstrated

132

, its role in

helping corals to survive bleaching requires further study. A better understanding of this

issue may help managers identify coral communities that are at reduced risk of mortality

from coral bleaching.

Coral health prior to exposure to heat stress may be the most important factor influencing

colony survivorship during bleaching events. Most corals rely very heavily on the energy

provided by their zooxanthellae, and bleaching effectively robs them of their main energy

source. As a result, corals in the bleached state are beginning to starve, and their ability to

endure this hardship is likely to be important in determining whether they survive. Like

many animals, corals store surplus energy as lipids (fats). Corals in good condition will have

relatively high lipid levels, endowing them with a buffer against periods of low energy

supply. For this reason, it is thought that the condition of a coral at the time it bleaches

may play a key role in determining whether it will be able to survive the period of

starvation that follows. This implies that chronic stresses, such as water pollution or

increased turbidity, which can negatively affect a coral's condition, could increase the risk

of corals dying from the acute stress caused by bleaching. While these ideas have only

recently begun to be examined for corals

, they suggest that coral health should be

considered as a priority focus for reef managers wanting to increase coral survival during

moderate coral bleaching events.

4.2.3 Factors that influence recovery

Significant recovery can occur in only two to three years if mortality is minor (when there

is an abundance of colonies that completely or partially survive the bleaching event).

However, recovery of coral communities following severe mortality is likely to take much

longer

5, 133, 134

. This is because reef recovery is a complex process influenced by multiple,

interacting factors. On severely damaged reefs, recovery is dependent on the arrival of

suitable coral larvae that have survived the bleaching event elsewhere, and their successful

settlement, survival and growth

134

. Even assuming conditions favour recruitment, the

recovery process is subject to the vagaries of larval supply and the many risks that confront

the young coral, such as predation, smothering by sediments or algae, overgrowth by other

corals, etc. In combination, these uncertainties mean that recovery of a site to an

abundance, density and diversity of corals comparable to pre-bleaching conditions is a long-

term prospect measured in terms of decades

133, 134

A particularly sensitive step in the recovery process is larval recruitment.The production,

settlement and survival of coral larvae is dependent on the availability of 'source' reefs to

provide new larvae, good water quality to promote spawning, fertilisation and larval

development, and suitable substrate for settlement and survival of coral larvae

45, 134

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Degraded water quality can affect the fertilisation success of corals

72, 135, 136

, potentially placing

severe limitations on the ability of coral communities to recover after bleaching-induced

mortality. Water quality can also have a negative impact on recovery by encouraging algal

growth, which in turn can reduce larval recruitment

44, 45

. Coral mortality allows an opening

for frondose (leaf-like) and filamentous macroalgae ('seaweeds') to take on a more

dominant role in reef ecosystems, often at the expense of coral recruitment

42, 45, 137

. This

window of opportunity for algae following mortality events such as those associated with

severe coral bleaching events means that the influence of nutrients in accelerating growth

is more pronounced.

The abundance of herbivorous fish populations is another

critical factor influencing the success of recovery processes.

In situations where herbivores have been heavily depleted

through a combination of overfishing and disease, recovery

of coral communities following disturbance has been greatly

lengthened, or even stalled, resulting in a persistent shift

from coral-dominated to algal-dominated reef for over a

decade

82, 138

Recovery can be even further compromised on reefs that

are threatened by both degraded water quality and

depleted herbivore populations. Increased nutrient levels

greatly increase the potential for the excessive growth of

algae that can occur when herbivory is reduced. Water

quality and herbivore populations are each important, but

in combination they become critical in determining the

coral-algae balance after a disturbance

42, 45

a b

Recovery of severely damaged

reefs is dependent on 'source'

reefs to provide new larvae, good

water quality, and suitable

substrate. Where these

conditions exist, new corals can

settle and become established

relatively quickly

Reef recovery after severe coral mortality is a complex process influenced by multiple, interacting factors.These

reefs in Palau demonstrate significant differences in their ability to recover. Both were severely affected by mass

bleaching in 1998. Seven years after the event, only (a) minimal recovery is evident in one reef, while the (b)

other has shown dramatic recovery of coral cover

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The importance of local processes highlights the pivotal role that effective management of

local stressors can have in supporting the ability of reefs to recover from mortality

associated with severe coral bleaching. In keeping with the example above, algal growth and

herbivory could be optimised by limiting water pollution and fishing pressure. Furthermore,

recent studies suggest that the 'source' of coral recruits is often from within the same or

nearby reefs.Together, these insights emphasise the importance of managing local stressors

when aiming to support the natural ability of reefs to recover from global stressors like

bleaching events

4.3 Can corals adapt to climate change?

The impact of mass coral bleaching on coral reef ecosystems over the long term will

depend on the environmental changes that occur in tropical seas, the extent to which

corals can acclimatise or adapt to changing conditions, and the ways in which repeat

disturbances compound one another to shape coral reef ecosystems.

4.3.1 Future climates

Coral reefs are currently experiencing temperature regimes that exceed any they have

experienced over at least the last 400 000 years

. Projections of temperature increases

suggest that conditions will develop that are vastly different to those in which the majority

of coral reefs have developed over the same time frame

Global ocean temperature has increased by an estimated 0.6ºC between the mid-1950s

and mid-1990s. Some studies predict future increases in global sea temperatures of 1.4-

5.8ºC by 2100

, suggesting that mass bleaching events, which may be induced at only 1-2ºC

above normal summer temperatures, are likely to be a much more frequent phenomenon

in the future

9, 13, 28

Herbivores, such as grazing fishes, play a key role in

maintaining the conditions that are required for the

recovery of reefs damaged by coral bleaching

Algae can overgrow established corals, or inhibit

recruitment of new corals, when there are excess

nutrients in the system or inadequate levels of herbivory

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110

Oceanic currents and atmospheric conditions may also

be affected by rising sea temperatures. Changes in the

strength and direction of currents are likely to have a

strong influence on local temperatures, while changes in

atmospheric circulation may influence upwelling,

precipitation patterns and the frequency and intensity of

regional weather extremes

.All of these factors have the

potential to increase the extent and severity of mass coral bleaching events. Importantly

though, while the potential for these very significant changes is recognised, there remains

substantial uncertainty about the direction, magnitude and location of changes in oceanic

circulation due to climate change

Potential effects of climate change on coral reefs. Climate change may influence coral reef

ecosystems through processes such as mass coral bleaching, changes in the frequency or

severity of storms

, greater virulence of diseases

, sea level rise

139

, and reduced calcification

rates in reef-building

(see Box 4.4). Of these, mass bleaching events are likely to be the

most influential in determining future coral reef condition

13, 28

. By itself, mass bleaching has

resulted in significant ecological impacts to coral reef areas unaffected by local stressors. For

many other reefs, mass coral bleaching is an additional stress that exacerbates the impacts

of local stressors

.The influence of mass bleaching events on coral reefs and, in particular,

how it interacts with local stressors, will be one of the most important determinants of the

future of coral reef ecosystems over the next 50 years

Projections of future sea temperature

increase suggest that conditions will

develop that are vastly different to

those in which the majority of coral

reefs have developed over the last

400 000 years

Box 4.4 Coral reefs and climate change: implications beyond mass bleaching

Climate change threatens coral reef ecosystems in other ways aside from increasing the

frequency and severity of bleaching impacts. Climate model projections indicate that we

can also expect increases in sea level, greater incidence of coral disease and changes in

ocean chemistry

. While the rates of coral reef growth are likely to keep pace with

projections of sea level rise, shoreline inundation with rising water levels pose other risks.

Among these are an increase in the export of sediments, nutrients and pollutants from

flooded coastal areas. Animals that rely on the low-lying habitat provided by coral reef

islands and cays, such as sea turtles and seabirds, are likely to be significantly affected,

although these potential impacts are just beginning to be explored.

Many coral diseases increase in virulence at higher temperatures, suggesting greater

prevalence of disease outbreaks as average sea temperatures increase. Diseases have

already caused chronic coral mortality in many reef areas, such as the Florida Keys and

the Caribbean, and reports of coral disease are increasing in other regions including the

Great Barrier Reef and other Indo-Pacific locations.

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At a regional or global level, changes in ocean

chemistry will result from changes in the

earth's climate. In particular, dramatic

increases in the levels of carbon dioxide (CO

)

in the earth's atmosphere are leading to a

reduction in the pH of seawater, which in turn

is decreasing the availability of carbonate

ions. Reduced calcium carbonate saturation

states of seawater are expected to

significantly reduce the rates of calcification in

key reef-building organisms such as corals

and coralline algae

20, 140

. The implications of

this for the ability of coral reefs to withstand

storms and to maintain their role in shoreline

protection are still being examined, but early

indications are that these changes will be

important, even if they manifest themselves

only slowly or subtly. This has particular

significance for the ability of coral reefs to

maintain their roles in protecting shorelines

from oceanic swells and supporting

fisheries–both critical ecosystem functions in

many tropical regions.

The impacts of mass coral bleaching will be

compounded by other climate-related

stressors. In particular, reduced calcification

rates and increases in coral disease (shown

here) are significant concerns.The incidence of

coral disease can be expected to increase

because disease virulence increases at higher

temperatures and because the incidence of

disease has been observed to increase

following mass bleaching events, when corals

are in a weakened condition

4.3.2 Can corals keep up?

Comparing projected sea temperature increases with existing coral reef temperature

thresholds indicates that the frequency and severity of mass bleaching events can be

expected to increase significantly. Studies on this issue have concluded that bleaching could

become an annual event in coming decades as conditions that are known to have caused

major mortality events in the past become more frequent

9, 28, 29

. However, these predictions

assume that bleaching thresholds will not change over time, and do not allow for the effect

of adaptation. The actual impacts on coral reefs will depend strongly on the capacity of

corals to adapt and the rate at which they do so.

Adaptation. There is clear evidence of substantial variation in the resistance and survival of

corals to bleaching, raising the possibility that these variations might be attributable to past

adaptation. For example, corals of the same species may have a bleaching threshold of 28ºC

in the Galapagos but be able to tolerate temperatures

over 34ºC in the Persian Gulf.While these observations

suggest that corals have historically had sufficient time

and genetic variability to adapt, it is unknown whether

they have the capacity to adapt fast enough to keep

pace with current rates of change.

Studies that have compared future

climate scenarios with current coral

bleaching thresholds predict that the

frequency and severity of mass

bleaching events can be expected to

increase significantly

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Adaptation involves genetic shifts in populations through selection of more resistant

genotypes. This evolutionary process begins as soon as less resistant genotypes are killed.

At that point, genotypes that are more resistant begin to make a greater contribution to

the next generations of corals. However, the rate of adaptation depends on numerous

factors, including the heritability of thermal tolerance, intensity of coral bleaching as a

selective process, and the genetic structure of coral populations

11, 23, 28

. While there are

differing degrees of optimism among recent studies, there is widespread agreement that

the abundance and composition of reef communities will change substantially over coming

decades, with large-scale degradation and losses of biodiversity possible in the longer term.

Acclimatisation. Acclimatisation refers to the ability of corals to make biochemical or

physiological adjustments that increase their ability to withstand higher sea temperatures

This mechanism occurs at the biochemical or cellular level, usually over time frames of

hours or days. Physiological adjustments that give rise to acclimatisation may be highly

ephemeral, lasting only as long as the stress, or they may be persistent, endowing a coral

with the ability to withstand future stress (such as high temperatures during the following

summer). Such adjustments, even short-term ones, usually come with costs, including the

diversion of energy away from other processes (such as reproduction). Additionally, for

acclimatisation to be effective it must outpace the rate of increases in temperature, which

becomes decreasingly likely at the upper level of projected temperature rise.

Incorporation of more heat resistant zooxanthellae within coral tissues is one of the major

mechanisms proposed for acclimatisation; however, the extent to which coral species can

swap algal symbionts remains unclear. This mechanism, called the Adaptive Bleaching

Hypothesis (after Buddemeier and Fautin

127

), proposes that corals may swap their

zooxanthellae for a more tolerant type following exposure to sub-lethal thermal stress.This

idea is a subject of continuing debate

113, 141

Corals may also acclimatise to warmer conditions by altering the density or positioning of

pigments within their tissue. These pigments, such as fluorescent pigment granules, can

shade the zooxanthellae during thermal stress, reducing damage to the photosynthetic

system and the risk of bleaching

43, 111

. Enhanced fluorescence seen in some corals that

appear to be more resistant to bleaching may be evidence of the role of pigmentation in

helping corals acclimatise to thermal stress.

Range-shifts in response to increasing sea temperatures. Coral populations may be able to

adjust to increasing temperature regimes through migration of heat-tolerant genotypes.The

large differences in the severity of bleaching suffered by corals exposed to otherwise similar

conditions strongly suggest that corals differ in their inherent ability to resist bleaching. At

least some of the properties that confer thermal tolerance to corals are likely to be

heritable (genetically coded).This leads to the potential for larvae from heat-resistant corals

to travel to reefs formerly dominated by less hardy genotypes, where they may settle and

re-populate areas affected by bleaching-induced mortality. Over time, this could lead to

heat-tolerant species or genotypes shifting their range into habitats previously dominated

by other species.

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The success of this process will depend on the

existence and survival of heat-tolerant genotypes, and

on connectivity among reefs. In addition, the location

and extent of particular thermal realms is not likely to

be static as the climate continues to change.This means

that range-shifts would need to occur at rates that equal

or exceed the rate of movement of thermal realms in

order for this process to compensate for the loss of

corals due to increasing temperatures.

There have also been suggestions that coral reefs may expand into the subtropics as the

temperature warms (see review by Coles and Brown

). However, there is a decrease in

shallow-water areas and an increase in siliceous sediments further from the equator,

creating conditions that are less suitable for reef development.Therefore, although changes

in climate may result in more suitable temperatures for coral growth away from the tropics,

higher latitude marine environments tend to have substrata that are much less suited to

development of carbonate reef structures, resulting in limited potential for reef

communities to move towards the poles.

4.4 Reefs and people in the future

There is now abundant evidence that corals are highly sensitive to increases in sea

temperature

5, 9, 11, 13, 80

. Their ability to adjust, either through acclimatisation or adaptation, is

limited or widely thought to be too slow to keep pace with even conservative climate

projections

23, 28

. The implication of these conclusions is that coral reef ecosystems are

destined for further change as sea temperatures continue to warm

9, 11, 23

. While there

remains great uncertainty about the rate, extent and precise impacts of this deterioration,

the future will almost certainly see degradation of reef systems and consequent losses in

ecosystem services

9, 13, 23, 31, 37

4.4.1 Ecological implications

Effects of mass bleaching on coral cover and biodiversity. The temperature sensitivity of corals,

and the likely limitation in their rate of acclimatisation and adaptation, suggests that coral

reefs are likely to have less live coral cover and lower biodiversity as a result of increases

in the frequency and severity of mass bleaching events

11, 23, 28

. Among the coral species most

likely to show declines in abundance immediately after a severe bleaching event are those

that tend to be relatively fast growing and visually dominant, such as staghorn and tabular

Acropora

19, 80, 115, 118

. The loss of these species is likely to have a noticeable impact on the

aesthetics of many reefs, as well as altering the amount of habitat for many reef-dependent

species

. While these species may also be among the quickest to recover by way of larval

recruitment and rapid growth, it remains highly likely that differences in bleaching

susceptibility among corals will result in significant shifts in the community structure of coral

reefs.This change is likely to result in flow-on affects to other organisms, as many species,

including a variety of fish and invertebrates, are dependent on the habitat provided by

branching corals (Box 4.5).

The temperature sensitivity of

corals, and the likely limitation in

their rate of acclimatisation and

adaptation, suggests that coral

reefs are likely to have less live coral

cover and lower biodiversity as a

result of a warming climate

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114

Reefs dominated by corals most sensitive to thermal stress, such as plate and staghorn Acropora, are more likely

to suffer severe impacts from coral bleaching. Loss of these species is likely to have a noticeable impact on the

aesthetics values of reefs as well as the amount of habitat available for many reef-dependent species

Differences in the ability of species to

migrate and to adapt will further

exacerbate changes in community

structure due to differential mortality

from severe bleaching. If bleaching

events become increasingly frequent,

the more susceptible species may have

trouble re-establishing between

bleaching events, leaving abundant

space available for algal growth.

Decreasing time intervals between

bleaching events would also limit

opportunities for resistant species to

establish sustainable populations before

temperatures increase again. While the

exact change to reefs based on

projected increases in the frequency

and severity of mass bleaching are

highly uncertain, recent modelling

studies

9, 31, 47

report the possibility of

extensive degradation.

The differential susceptibility of coral species to thermal

stress can result in severe shifts in community composition.

At this site in the Lakshadweep Islands, India, massive corals

such as Porites are now the dominant members of the coral

community. Prior to the 1998 bleaching event, these sites

were dominated by staghorn Acropora

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Box 4.5 Implications of coral bleaching

for reef biodiversity

Our understanding of the impacts of climate

change on biodiversity is in its infancy. While the

pathway and time course of this change is

undefined, most experts agree that biodiversity

will be affected to some extent by a rapid loss of

reef-building corals resulting from major

disturbances such as coral bleaching events.

Given the strong relationships that characterise

reef ecosystems, many other species are also

vulnerable to the impacts of coral bleaching.

Organisms that depend on corals for food or

shelter and which reproduce via external

fertilisation may be most threatened by

bleaching, with extinction becoming a real risk as

the primary habitat provided by corals becomes

rarer.The kinds of organisms most at risk include

the obligate corallivores: those species that eat only corals. These species are directly

dependent on the presence of coral for their existence and disappear quickly if coral is

removed. The orange-spotted filefish (Oxymonacanthus longirostris) is an example; it

rapidly disappeared from reefs around Okinawa after the 1998 bleaching event

142

The response of the broader coral reef fish community to bleaching-induced losses of corals

has proven more complex. Declines in some species (especially damselfishes that are

strongly associated with branching corals) have been recorded following bleaching

63, 64, 143

.In

one recent study

143

, over 75 per cent of reef fish species declined in abundance, and 50

per cent declined to less than half their original numbers, following a devastating decline

in coral cover caused in part by coral bleaching. However, the overall structure of fish

communities in the Seychelles changed very little despite massive (threefold-twentyfold)

decreases in live coral cover after the 1997-98 bleaching event

.Abundances of some fish

have even appeared to increase following the loss of reef-building corals, with an overall

increase in fish abundance observed after the 1998 mass bleaching event on Tanzanian

reef systems

. These increases in fish populations appear to be caused by increases in

herbivorous fishes, which may be responding to the greater availability of algae following

reductions in coral cover.

Other organisms are also likely to respond to changes in coral cover. For example, over 55

species of decapod crustaceans are associated with living colonies of a single coral species,

Pocillopora damicornis

144, 145

. Nine of these are known to be completely dependant on

living pocilloporid coral colonies. Similarly, branching corals of the genus Acropora have 20

species that depend solely on the habitat they provide.

Coral bleaching also has implications for

biodiversity. For example, the orange-

spotted filefish rapidly disappeared from

reefs around Okinawa after the 1998

coral bleaching event

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Prospects for future coral reef condition. Even under

relatively conservative projections, many reefs

previously dominated by a diverse assemblage of hard

corals may give way to low-diversity, low-cover reef

communities. In the extreme, this may lead to algal-

dominated reefs with low habitat complexity and

limited scope for recovery by hard corals, all within 50

years. Although these projections may sound severe,

they do not rely on catastrophic change. Rather, they

assume, very conservatively, that reefs can recover

between bleaching events as long as there are fewer than three massive mortality events

per decade

28, 29

. Additionally, these projections do not consider the cumulative or synergistic

effects of other stresses, such as water pollution or destructive fishing practices.

Reef recovery between mass bleaching events may be impeded by several factors (see

Section 4.2.3 for information about factors that support reef recovery). Recovery

processes can be substantially hindered by erosion of reef structures following coral

mortality. The grazing of sea urchins in very high densities has led to erosion of reef

structures in eastern Pacific reefs, such that the degraded state of reefs has persisted for

two decades after the mass bleaching event of 1983

146, 147

. Projected reductions in the pH

of upper ocean waters are likely to further encourage both biological and chemical erosion

of reefs. Severe erosion can also lead to a shift toward an unstable substrate of coral rubble,

making recovery from bleaching-induced coral mortality difficult

106

.The evidence from past

mass bleaching events is that, while there are reports of active recovery from some sites,

in general damaged reefs remain degraded compared to their pre-bleaching condition. It

seems likely that the impacts of bleaching-induced mortality are likely to be evident for at

least a decade at many locations.

While coral reefs are unlikely to be eliminated globally because of mass bleaching events,

predicted declines in reef condition have serious implications. Reduced coral cover and

degraded community structures are expected to reduce the suitability of coral reefs as

habitat for many species, impacting the biodiversity and ecosystem services upon which

humans depend. Although knowledge of the inter-dependencies is only beginning to

accumulate, managers are becoming increasingly concerned about the effects of

deterioration in reef condition on the human communities and industries that have come

to rely on healthy ecosystems for their livelihood and lifestyle.

4.4.2 Social and economic implications

Impacts on fisheries. Changes in coral reef ecosystems resulting from bleaching are expected

to translate into shifts in fish species composition and, possibly, reduced fishery catches

59, 148-151

Coral reef ecosystems support fisheries by providing food and habitat for a diversity of

species. Coral mortality from mass bleaching events leads to loss of reef structure and

habitat, as dead coral skeletons erode and break down. This deterioration of the reef

structure is probably not much different in nature from that caused by other disturbances,

such as coral disease or outbreaks of the coral-feeding sea star Acanthaster plancii.

However, the effects of coral bleaching events can extend over hundreds or thousands of

Even under relatively conservative

projections of sea temperature

warming, many reefs previously

dominated by a diverse assemblage

of hard corals may give way to low-

diversity, low-cover reef communities,

reducing the ecosystem services

upon which humans depend

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kilometres

152

, causing stress or damage

on scales not normally experienced by

coral reef ecosystems. Where

significant coral mortality occurs, coral

bleaching can result in dramatic

decreases in the amount of habitat

available for fish and other mobile reef

species that depend on the structure

provided by healthy coral reefs

64, 143

Strongly coral-dependent fish species

are expected to be the most affected

by bleaching-induced coral mortality.

Several species of fish are reliant on

coral as a primary food source, and

many other species use coral for shelter from predators. Post-bleaching declines in

populations were recorded following the 1997-98 mass bleaching episode for several fish

species that feed exclusively on corals

64, 142, 153

, as well as for those that rely on coral for habitat,

such as species of damselfishes that are strongly associated with branching corals

63, 64

Coral-dependent fishes are important

prey for larger species, many of which

are targeted in coral reef fisheries.

Bleaching events that result in

widespread loss of physical habitat

would be expected to have 'flow-on'

effects for the higher trophic level

predator fishes often targeted. Yet,

while impacts on fish populations of the

1997-98 mass bleaching event have

been clearly documented in several

locations, evidence of impacts on

fishery yields and income has been