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Cutting-Edge Research on Environmental Processes & Impacts

Volume 10 | Number 1 | January 2008 | Pages 1–148

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10th Anniversary Review Janice LoughA changing climate for coral reefs

EditorialRichard PikeThe way forward

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Cutting-Edge Research on Environmental Processes & Impacts

Volume 9 | Number 8 | August 2007 | Pages 773–896

Journal of Environmental Monitoring

Volume 9 | N

umber 8 | 2007

Journal of Environmental M

onitoringPages 773–896

Critical ReviewEnvironmental applications of single collector HR-ICP-MS

Critical ReviewDesalination of seawater using reverse osmosis

Reid et al.Impact of rainbow trout on phosphorus concentrations

Covaci et al.Penguin colonies as secondary sources of POP contamination 1464-0325(2007)9:8;1-4

10th Anniversary Review: a changing climate for coral reefs

Janice M. Lough

Received 21st September 2007, Accepted 29th October 2007

First published as an Advance Article on the web 7th December 2007

DOI: 10.1039/b714627m

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.

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 tempera-

ture 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, Aus-

tralia’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 biolo-gical 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

Janice Lough was born inNewcastle, UK in 1955. Shehas a BSc in EnvironmentalSciences (1976) and a PhD intropical climate variations,undertaken at the ClimaticResearch Unit (1982), bothfrom the University of EastAnglia, UK. She was a Re-search Associate at the Tree-Ring Laboratory, Universityof Arizona, USA from 1982to 1986 applying dendrocli-matic reconstructions to un-

derstanding climate variation and change over North Americaand the North Pacific. She joined the Australian Institute ofMarine Science in 1986 where she is now a Principal ResearchScientist leading the Responding to Climate Change ResearchTeam and affiliated with the ARC Centre of Excellence forCoral Reef Studies at James Cook University. Her currentresearch activities include obtaining high-resolution proxy cli-mate and environmental information from annually bandedmassive corals over the past several centuries and assessing thenature of regional climate changes due to the enhanced Green-house effect and their impacts and consequences for tropicalcoral reefs.

Australian Institute of Marine Science, PMB 3, Townsville MC,Queensland, 4810, Australia. E-mail: j.lough@aims.gov.au;www.aims.gov.au

This journal is �c The Royal Society of Chemistry 2008 J. Environ. Monit., 2008, 10, 21–29 | 21

CRITICAL REVIEW www.rsc.org/jem | Journal of Environmental Monitoring

formed only within the past 8–10 000 years, since sea level rose

from B125 m below present at the height of the last glacial

maximum (B19 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). Photosyn-

thetic 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 calcifi-

cation 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 extra-

ordinary 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 B2000 km along the northeast coast of Aus-

tralia and covers B35 million hectares (an area larger than

Italy), contains nearly 3000 coral reefs built from over 360

species of hard coral. These reefs harbour B1500 species of

fish, B4000 species of molluscs (shells), B400 species of

sponges, B800 species of echinoderms (starfish, urchins

etc.), B500 species of macroalgae (seaweeds), 23 species of

marine mammals, extensive sea grass beds (home to interna-

tionally 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 re-

flected in its inscription on the World Heritage List in

1981 (http://www.environment.gov.au/heritage/worldheritage/

sites/gbr/values.html). 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 B10% 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, includ-

ing their geological history, growth and structure, biological

adaptation, evolution and biogeography, community struc-

ture, organisms and ecosystem metabolism and physical re-

gimes. Globally, coral reefs provide ecosystem goods and

services valued at 4US$375 billion per year.14 Despite their

relatively small area, coral reefs contain B30% of the world’s

marine fish and reef fish account for B10% 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 eco-

systems.15 For humans, these goods and services include:

fisheries, natural breakwaters, protection of coastal settle-

ments, building materials, novel pharmaceuticals and bur-

geoning 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 B300 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 accu-

mulate 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 con-

sidered 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 geo-

graphic locations of coral reefs (ReefBase http://www.reefba-

se.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 1C and ranges from a seasonal mini-

mum of 16.0 1C to a seasonal maximum of 34.4 1C (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 ofB18.0 1C

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 dis-

tribution 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).

22 | J. Environ. Monit., 2008, 10, 21–29 This journal is �c The Royal Society of Chemistry 2008

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 interna-

tional 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 with-

out 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 pollu-

tion 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 coast-

al 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, poten-

tially, manageable and possibly reversible. This requires both

active conservation measures, such as integrated catchment

management reducing land-based pollution of reefs, elimina-

tion 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 major-

ity 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 green-

house gas, carbon dioxide, is now B40% higher than in the

late 18th century. Based on instrumental records, global

average temperatures are now B0.7 1C warmer and sea level

B20 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 accus-

tomed to since current sea level was reached B8–10 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 reefstructures

More intense tropicalcyclones

�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 furtherout on reefs

Changes to ocean currents �Affect connectivity (e.g. larval supply)amongst reefs�Affect nutrient supply from upwelling

El Nino–SouthernOscillation events

�Extreme weather events that enhanceprobability of bleaching

Wind fields andatmospheric circulationpatterns

�Changed prevailing weatherconditions

This journal is �c The Royal Society of Chemistry 2008 J. Environ. Monit., 2008, 10, 21–29 | 23

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 cal-

cium carbonate skeleton becomes visible through the translu-

cent 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 ob-

served 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 1C) 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 1C and range between 28.2–34.4 1C.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 Nino 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 im-

proved, 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 ex-

tensive coral bleaching event on record occurred during the

major El Nino–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 experi-

enced unusually warm SSTs during its annual seasonal max-

imum, catalysed efforts to monitor the occurrence of

conditions conducive to coral bleaching. The advent of satel-

lite-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 hot-

spots’’,46 are now routinely produced by the US National

Oceanographic and Atmospheric Administration (NOAA;47

http://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 ob-

servations 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, impor-

tantly, 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 compro-

mised 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 condi-

tions 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 be-

tween 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 in-

creased 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 1C

since the 19th century and those of the tropical oceans by

about half the global average.1 Average water temperatures

24 | J. Environ. Monit., 2008, 10, 21–29 This journal is �c The Royal Society of Chemistry 2008

for the most recent 30 years on the GBR, for example, are only

0.4 1C warmer than at the end of the 19th century but could be

1–3 1C 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 1C warming

of the GBR would result in B80–100% bleaching compared

toB50% 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 1C 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 sym-

bionts and may be able to change the relative abundances of

these clades—‘‘symbiont shuffling’’.66 This strategy may, how-

ever, 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 1C, 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 dis-

tribution 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 acidifi-

cation. 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

B100 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, echino-

derms, 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. In-

creased 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 calcify-

ing 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 51 latitude, are common and natural disturbances to many

coral reefs regions.83 Tropical cyclones are ‘‘agents of mortal-

ity’’ on coral reefs and, primarily through the large waves they

generate, can directly influence the structure and local

This journal is �c The Royal Society of Chemistry 2008 J. Environ. Monit., 2008, 10, 21–29 | 25

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 destruc-

tive 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 destruc-

tive 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 fre-

quency 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 contami-

nants 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 exam-

ple, 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 B20 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 accel-

erated 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 magni-

tude 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 Nino–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 Nino

and La Nina, are typically associated with distinct and differ-

ent anomalies of the tropical atmosphere and ocean climate.98

The major 1982–83 El Nino event first triggered warnings of a

link between ENSO and mass coral bleaching events.99,100 The

1997–98 El Nino event (coinciding with what was then the

warmest year on record) was also one of the most extreme

El Nino events on record43 and coincided with the greatest

recorded thermal stress at many coral reef sites.101 El Nino

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, signifi-

cantly 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 circula-

tion 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.

26 | J. Environ. Monit., 2008, 10, 21–29 This journal is �c The Royal Society of Chemistry 2008

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 undoubt-

edly 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 esti-

mate isB10% of the world’s population live within 100 km of

coral reefs and B90% of these people live in developing

nations—B63% of people (415 million) living within 100 km

of coral reefs live in countries where per capita GDP is

oUS$5000.109 This compares with a per capita GDP for

Australia, which contains B22% of the world’s coral reef

area, ofB$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, im-

pacts and potential consequences of ongoing rapid climate

change for coral reefs, as well as local direct human im-

pacts.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 distur-

bances, such as coral bleaching (resistance), and some coral

reefs have shown the ability to recover from such distur-

bances (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 inter-

national actions and a greatly expanded network of marine

protected areas.24

Even with rapid global implementation of stringent mitiga-

tion strategies to stabilize and reduce greenhouse gas emis-

sions, 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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