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Volume 10 | Number 1 | 2008
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Cutting-Edge Research on Environmental Processes & Impacts
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Volume 10 | Number 1 | January 2008 | Pages 1–148
Journal of Environmental Monitoring
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Journal of Environmental Monitoring
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Editorial
Richard Pike
The way forward
10th Anniversary Review
Janice Lough
A changing climate for coral reefs
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CRITICAL REVIEW
www.rsc.org/jem | Journal of Environmental Monitoring
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 overexploitation 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 temperature changes greatest at high latitudes.1 Yet ecosystems in
the naturally warm tropical ocean waters—coral reefs—are
already showing evidence of global warming impacts. It is
now 200 years since Matthew Flinders provided the above
evocative description (that resonates with modern coral reef
experiences) of the world’s largest coral reef ecosystem, Australia’s Great Barrier Reef. Why are these ecosystems now
considered as one of the ‘‘most vulnerable’’ to climate change?2
In this article I consider the mounting body of scientific evidence
(though in the space available it is not possible to do full justice
to the burgeoning literature) that a rapidly changing climate due
to human activities is a major threat to the maintenance of
present-day coral reefs as we know and rely on them.
Coral reefs—what are they?
Janice Lough was born in
Newcastle, UK in 1955. She
has a BSc in Environmental
Sciences (1976) and a PhD in
tropical climate variations,
undertaken at the Climatic
Research Unit (1982), both
from the University of East
Anglia, UK. She was a Research Associate at the TreeRing Laboratory, University
of Arizona, USA from 1982
to 1986 applying dendroclimatic reconstructions to understanding climate variation and change over North America
and the North Pacific. She joined the Australian Institute of
Marine Science in 1986 where she is now a Principal Research
Scientist leading the Responding to Climate Change Research
Team and affiliated with the ARC Centre of Excellence for
Coral Reef Studies at James Cook University. Her current
research activities include obtaining high-resolution proxy climate and environmental information from annually banded
massive corals over the past several centuries and assessing the
nature of regional climate changes due to the enhanced Greenhouse effect and their impacts and consequences for tropical
coral reefs.
Coral reefs are complex ecosystems that are uniquely defined
amongst the world’s ecosystems in terms of both their bioloAustralian Institute of Marine Science, PMB 3, Townsville MC,
Queensland, 4810, Australia. E-mail: [email protected];
www.aims.gov.au
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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
J. Environ. Monit., 2008, 10, 21–29 | 21
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). Photosynthetic products of the algae provide the coral host with cheap
energy.5–9 The zooxanthellae also play a role in light-enhanced
calcification of scleractinian corals, allowing the rapid calcification necessary to form reef structures.10 In return, the algae
obtain protection and essential nutrients from their coral
host. The photosynthetic pigments within the algae give corals
their colours. Together these organisms produce the extraordinary variety of coral skeletal forms and structures that
form massive carbonate structures that can withstand the
natural forces of erosion and provide the basis of coral reef
ecosystems.11
Coral reefs are not just corals. They provide complex
habitats that support a great diversity of reef-associated fauna
and flora. Australia’s Great Barrier Reef (GBR), for example,
which extends B2000 km along the northeast coast of Australia 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 internationally endangered dugongs), 6 of the world’s 7 species of
marine turtle species, and 30% of the world’s soft coral
species, several hundred species of seabirds, breeding grounds
for humpback whales from Antarctica. . .. . .. . .. . ...and the list
continues (http://www.gbrmpa.gov.au/). No ecosystem is an
island and coral reefs, such as the GBR, are intimately linked
with coastal ecosystems, such as mangroves, wetlands and
estuaries. The international significance of the GBR is reflected in its inscription on the World Heritage List in
1981 (http://www.environment.gov.au/heritage/worldheritage/
sites/gbr/values.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 interreefal 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, including their geological history, growth and structure, biological
adaptation, evolution and biogeography, community structure, organisms and ecosystem metabolism and physical regimes. Globally, coral reefs provide ecosystem goods and
services valued at 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
22 | J. Environ. Monit., 2008, 10, 21–29
with coral reefs along their coastline depend on the economic
and social goods and services provided by these rich ecosystems.15 For humans, these goods and services include:
fisheries, natural breakwaters, protection of coastal settlements, building materials, novel pharmaceuticals and burgeoning tourism industries. Coral reef ecosystems also
provide habitat, food and shelter for many other organisms,
and therefore, harbour a significant proportion of the world’s
marine biodiversity.
Where are coral reefs?
Globally, coral reefs are estimated to cover an area 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 accumulate sufficient calcium carbonate to form a coral reef
structure.17 The latter are often more isolated and close or
beyond the limits of coral reef distribution.
The global distribution of coral reefs has long been considered to be constrained to shallow, warm, well-lit, clear, low
nutrient and low sediment waters, as well as by their geological
and climate history and local bathymetry.18,19 A more recent
comprehensive analysis has clarified the environmental limits
to coral reef development using up-to-date data on the geographic locations of coral reefs (ReefBase http://www.reefbase.org/main.aspx) and improved instrumental environmental
data sets.20 Temperature, salinity, nutrients, light availability
and the aragonite saturation state of seawater were considered
as the ‘‘first-order determinants of reef distribution’’ with
regional-scale reef distribution being affected by factors, such
as waves, ocean currents, larval sources etc. The aragonite
saturation state of seawater is a measure of how easily
aragonite, the main form of CaCO3 created by reef-building
corals, can form and depends on the concentration of calcium
and carbonate ions in seawater, i.e. the carbonate chemistry of
seawater.21 This analysis found water temperature at reef
locations averages 27.6 1C and ranges from a seasonal minimum 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 of B18.0 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 distribution are important in assessing the potential responses of
coral reefs to changes in their physical environment due to the
enhanced greenhouse effect. Although an important factor,
light is unlikely to change on large spatial scales but significant
changes in water temperature and aragonite saturation state
are highly likely (discussed below).
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Before climate change: coral reefs already under
threat
Our major finding is that human pressures pose a far greater
immediate threat to coral reefs than climate change, which may
only threaten reefs in the distant future.23
The conclusion, that climate change was not a near-term
threat to coral reefs, was drawn only 14 years by an international team of coral reef experts. What has been termed the
‘‘coral reef crisis’’ was already well underway before we realised
the potential fragility of these highly diverse marine ecosystems
to global climate change. The significant ecosystem goods and
services and direct economic benefits that coral reefs provide to
the large and expanding populations of tropical coastal regions
have been progressively over-exploited. As a result, even without the climate change impacts discussed below, coral reefs have
been declining at an alarming rate, due to direct local and
regional human pressures, such as over-fishing, destructive
fishing (e.g. dynamite), decline in water quality due to increased
sediment from land-use changes, nutrient and chemical pollution and development on coasts (dredging, land clearing for
ports, harbours etc., mining of coral reefs etc.).23–27
Only 30% of the world’s coral reefs are considered at low risk
from these increasing human stresses and 20% of reefs have,
effectively, been destroyed.28 The highly biodiverse reefs of
Southeast Asia and the Indian Ocean (where human pressures
continue to increase) are most badly affected. Indeed, an
historical study of 14 coral reef regions suggests that human
exploitation of coral reefs is not a recent phenomenon but has
been occurring over thousands of years.29 This exploitation,
primarily through over fishing, which has impacted other coastal ecosystems,30 has resulted in a trajectory of decline in coral
reefs worldwide, even before concerns of global climate change
impacts. Even what are regarded as pristine, well-protected
reefs, such as the outer GBR, are already on this declining
trajectory due to the loss of large herbivores and carnivores.
These primary and ongoing causes of coral reef decline all
occur at the local- and regional-scale. They are a direct result
of human-induced pressures and, therefore, are also, potentially, manageable and possibly reversible. This requires both
active conservation measures, such as integrated catchment
management reducing land-based pollution of reefs, elimination of destructive fishing practices, sustainable management
of reef fisheries, and implementing and managing expanded
Marine Protected Areas.31 Reversal of the trend also requires
national and international initiatives to provide the many
countries with degraded and degrading coral reefs, the majority of which are developing countries, with the capacity and
necessary assistance to effectively manage their coral reef
ecosystems.24,26,28 Human interference with the global climate
system has now added an additional set of threats to the
survival of coral reef ecosystems—threats that are occurring at
the global level and cannot be effectively managed locally.
Climate change—observed impacts and additional
threats
Warming of the climate system is unequivocal, as is now evident
from observations of increases in global average air and ocean
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temperatures, widespread melting of snow and ice, and rising
global average sea level.1
Observational evidence from all continents and most oceans
shows that many natural systems are being affected by regional
climate changes, particularly temperature increases.2
Global climate has varied and changed in the past on a
range of timescales, and organisms and ecosystems have
survived, changed their distribution and adapted to such
changes. It is now, however, clear that human activities since
the Industrial Revolution began in the late 18th century,
primarily through burning of fossil fuels, land-use changes
and agriculture, have altered and are significantly altering
the composition of the earth’s atmosphere. These changes
are resulting in more heat being trapped in the global climate
system (the enhanced greenhouse effect) and are causing
rapid and significant global warming and a changing global
climate.1 The atmospheric concentration of the main greenhouse gas, carbon dioxide, is now 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 accustomed 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
Weaker coral skeletons and reef
structures
Physical destruction of reef
Ocean acidification
More intense tropical
cyclones
Rising sea level
More extreme rainfall &
flood events
Changes to ocean currents
El Niño–Southern
Oscillation events
Wind fields and
atmospheric circulation
patterns
Coastal erosion
Higher storm surges
‘Drowning’ of some reefs
Increased area for some reefs
Low salinity waters extend further
out on reefs
Affect connectivity (e.g. larval supply)
amongst reefs
Affect nutrient supply from upwelling
Extreme weather events that enhance
probability of bleaching
Changed prevailing weather
conditions
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 calcium carbonate skeleton becomes visible through the translucent tissue layer. Coral bleaching is not a new phenomenon
due to global warming. Corals are known to bleach in
response to a range of environmental stresses (e.g. low salinity,
pollution, unusually high or low water temperatures). In the
past, however, such occurrences of bleaching were only observed on small spatial scales in response to localized stresses.
What is new, and now clearly related to global warming, is an
increase in frequency of large-scale, mass coral bleaching
events, where entire reefs are affected.
Pioneering studies in the 1970s demonstrated just how close
(within 1–2 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 Niño events.35,36 This
was largely due to the lack of reliable long-term records of
SSTs and other environmental variables on coral reefs. As
more mass bleaching events occurred and observations improved, the link was made with unusually warm waters.37–40
The suggestion that these unusual occurrences on coral reefs
might be linked to global climate change due to the enhanced
greenhouse effect,41,42 is now no longer considered ‘‘dubious’’
but ‘‘incontrovertible.24
Large-scale SST anomalies in the tropical oceans create
conditions that can result in coral bleaching. The most extensive coral bleaching event on record occurred during the
major El Niño–Southern Oscillation event of 1997–1998,43
with 1998 being the then warmest year on record globally.44
Mass bleaching was reported from nearly every coral reef
region of the world.45 Sixteen percent of the world’s coral reefs
were estimated to be damaged by this unprecedented event
and, of these, only 40% appear to have recovered and 60%
have not.28 The scale and magnitude of this event, that could
essentially be tracked around the world as each region experienced unusually warm SSTs during its annual seasonal maximum, catalysed efforts to monitor the occurrence of
conditions conducive to coral bleaching. The advent of satellite-based observations of the oceans since the early 1980s has
dramatically increased our capabilities to observe global-scale
patterns and anomalies in ocean surface climate. A range of
products, derived from the original concept of ‘‘oceanic hotspots’’,46 are now routinely produced by the US National
Oceanographic and Atmospheric Administration (NOAA;47
http://coralreefwatch.noaa.gov) and provide the basis for
24 | J. Environ. Monit., 2008, 10, 21–29
identifying potential bleaching conditions in near-real time.
These bleaching alerts need to be confirmed with field observations and there is some evidence emerging that for
particular reefs, the thresholds for the occurrence and intensity
of bleaching may be modified by the history of past bleaching
events.48 Although such monitoring cannot prevent coral
bleaching or mortality, timely information about bleaching
potential enables scientists and reef managers to document the
intensity, impact and subsequent effects more comprehensively
than possible only 10–20 years ago. Improved knowledge of
the links between the physical environment and biological
processes of coral bleaching helps managers develop and test
strategies to protect corals from bleaching and also, importantly, identify bleaching-resistant reefs. The latter are clear
targets for enhanced protection efforts, as they may provide
important refugia for coral reef organisms and sources for
recruitment for bleaching-affected reefs as climate continues to
change and increasingly stresses the world’s already compromised coral reef ecosystems.
At the local scale, the occurrence and intensity of bleaching
can be highly variable, both within a coral colony, between
coral colonies, within a reef and between reefs in a region.49
Such variations are in addition to the different susceptibility of
different coral species to thermal stress.50 Other local physical
factors can enhance or suppress the impacts of warmer than
normal regional SSTs and thus the intensity of bleaching.
Observations that corals often bleach more on their upper
surface than at the sides of colonies clearly implicates light as
an additional factor and frequently the local weather conditions that cause intense warming of the water column (calm
conditions, low cloud amount, little water motion) allow
increased light penetration at the coral surface.51 Increased
cloudiness can also mitigate bleaching, even when SSTs are
high.52 Lowered salinity due to a major flood event increased
the intensity of coral bleaching on inshore reefs of the central
Great Barrier Reef in 1998.53 There can also be considerable
local-scale variations in water temperatures within and between reefs that can also affect the occurrence and intensity
of bleaching.34,54,55 Such local-scale variations that reduce
thermal stress can be linked to water movements, such as
upwelling, mixing, tidal range and wave energy.51,56,57 The
continued existence of such bleaching-resistant sites may
be critical for recovery of nearby bleaching impacted coral
populations.58
As a result of bleaching, corals may die, partially die or
recover. Recovery depends on the coral rapidly regaining its
zooxanthellae population soon after the bleaching stress.59
Even for corals that appear to recover fully, there is mounting
evidence of long-term consequences as a result of the thermal
stress associated with the bleaching event. These consequences
include reduced reproduction, reduced growth rates and increased susceptibility to other disturbances, such as coral
diseases.60 In addition, due to the different susceptibility of
different species,50 the overall effect of a bleaching event can be
to reduce species richness and diversity and change the
community structure of the coral reef.61
Global average temperatures have warmed less than 1 1C
since the 19th century and those of the tropical oceans by
about half the global average.1 Average water temperatures
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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
to B50% 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 symbionts and may be able to change the relative abundances of
these clades—‘‘symbiont shuffling’’.66 This strategy may, however, be at the expense of growth rates, competition and
reproduction,67 may only occur in a few species68 and may
not occur sufficiently rapidly to keep up with warming ocean
temperatures.69 Changing from type C to the more thermallytolerant 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 distribution as the world continues to warm. This is due to lack of
suitable substrate combined with greater changes in ocean
chemistry that are detrimental for reef development at these
higher latitudes.3,26,71
Increasing frequency of mass coral bleaching events is not
the only impact of warming oceans on coral reef ecosystems.
There is also an increasing frequency of reports of disease
outbreaks affecting corals and other marine organisms72 and
evidence is mounting that these occurrences are related to
warmer ocean temperatures.73 Warmer waters appear to be
increasing the severity of diseases in the ocean, which will
reduce the vitality of marine ecosystems, such as coral
reefs.74,75
Ocean acidification—weaker reef structures
There is growing concern about a more insidious effect of
enhanced greenhouse gas concentrations on coral reefs and
other marine calcifying organisms—progressive ocean acidification. About 30% of the excess carbon dioxide (the principal
greenhouse gas) released into the atmosphere by human
activities since the Industrial Revolution has been absorbed
by the oceans.76,77 This is changing the chemistry of the
oceans, which become more acidic, though still alkaline. The
pH of the oceans has already decreased by 0.1 and is projected
to be 0.4–0.5 lower by the end of this century. The rate of
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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, echinoderms, foraminifera, coccolithophores, shelled pteropods) use
calcium and carbonate ions from seawater to secrete calcium
carbonate. Changing the ocean chemistry essentially shifts the
geochemical equations by which these organisms ‘‘calcify’’ and
reduces their ability to form their skeletons and shells. Increased ocean acidification has been demonstrated by various
modelling and experimental studies to reduce the ability of
corals to form their skeletal structures—the very heart of
tropical coral reef ecosystems.21,79,80 The general scientific
consensus is that changes in ocean chemistry due to increasing
CO2 has serious implications for coral reefs and other calcifying organisms of the open ocean and could alter the makeup
of marine ecosystems, disrupt food webs and weaken coral
reef structures. For coral reefs, weaker reef structures would
reduce their resilience to the natural forces of erosion, and
slower growth will set back recovery after bleaching and
other disturbances. An additional threat to the ability of coral
reefs to maintain their structure in an increasingly acidic
ocean environment, is the particular sensitivity of coralline
algae (crustose calcareous algae, CCA). These contribute
significantly to coral reefs by secreting skeleton that forms
part of the reef structure itself and by cementing loose
material together.81 CCA calcify high-magnesium calcite at
a greater metabolic cost than aragonite calcification by
corals. This mineralogy makes them particularly sensitive
to changes in ocean chemistry, which may not only reduce
their ability to calcify but may even result in dissolution of
their calcified structures, thus further destabilizing the reefbuilding 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 mortality’’ on coral reefs and, primarily through the large waves they
generate, can directly influence the structure and local
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 destructive storm surges. Such natural events can cause significant
local disturbance but, given time and the absence of other
stressors, coral reefs can recover.86,87 Recent studies in the
Caribbean suggest, however, that these already seriously
degraded reefs are not recovering as well as they used to from
tropical cyclone impacts.88 Ironically, the passage of a tropical
cyclone, by rapidly cooling surface ocean temperatures, can
reduce the impact of elevated water temperatures and thus the
intensity of bleaching, at least on small space scales.89
There is already some evidence to suggest that the destructive potential of tropical cyclones around the world has
increased in recent decades.90,91 Although warming ocean
waters might be expected to increase the intensity and frequency of occurrence of tropical cyclones, their formation
depends upon a number of other factors.83 Current projections
give no clear indication as to whether the number and
preferred locations of tropical cyclones will change in a
warming world. The intensity of tropical cyclones is, however,
expected to increase,1 which will result in increased localised
physical destruction on coral reefs—another disturbance from
which reefs need time to recover.
More intense rainfall and river flow events—low salinity and
terrestrial inputs
Coral reefs exist in a range of environments, with some
regularly influenced by low salinity and naturally turbid
waters from the adjacent land masses. This can introduce
large cross-shelf gradients in coral reef communities between
turbid inshore and clear oceanic offshore waters as happens,
for example, on the GBR.92 In some locations, changes in land
use on the mainland has been a significant source of contaminants and sediments to nearshore reefs that can be detrimental
to their well being and part of the ongoing catalogue of local
human impacts on the health of the world’s coral reefs.26,28
Any change in regional rainfall and river flow regimes, as a
consequence of global warming, can potentially impact coral
reefs. Such projections need to be regionally specific and,
unfortunately, unlike water temperature changes, are less
well understood. There is, however, a general consensus that
the intensity of extreme flood and drought events are likely to
increase,1 which would affect coral reefs. There is, for example, evidence from paleo-records of river runoff contained
in massive coral cores, of a recent increase in such extreme
events on Australia’s GBR, with the wet years being wetter
and dry years drier than in previous centuries. Enhanced
river flood events are also likely to take freshwater further
out to midshelf reefs that are not used to such low salinity
waters.93
Rising sea level—winners and losers
Global sea level has already increased 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 accelerated in recent decades.94 This rise will continue with sea level
26 | J. Environ. Monit., 2008, 10, 21–29
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 lowlying coastal communities,97 a steady rise in sea level is not
considered to be a major source of stress to coral reefs. Global
sea level has been fairly stable for the last several thousand
years and some reefs have grown vertically to the level where
they are limited by present day sea level. So, some sea-level rise
would be beneficial to such reefs, although some reefs in
deeper water could eventually drown due to reduced light
availability with increased water depth. The rate and magnitude of projected sea level rise are considered ‘‘well within the
ability of most reefs to keep up’’.41
Changing atmospheric weather patterns (ENSO) and ocean
circulation
El Niño–Southern Oscillation (ENSO) events involve largescale anomalies of the ocean–atmosphere system and are the
major source of short-term climate variability within the
tropics which, through teleconnections, also impact climate
in extra-tropical latitudes. The two phases of ENSO, El Niño
and La Niña, are typically associated with distinct and different anomalies of the tropical atmosphere and ocean climate.98
The major 1982–83 El Niño event first triggered warnings of a
link between ENSO and mass coral bleaching events.99,100 The
1997–98 El Niño event (coinciding with what was then the
warmest year on record) was also one of the most extreme
El Niño events on record43 and coincided with the greatest
recorded thermal stress at many coral reef sites.101 El Niño
events do not cause mass coral bleaching, but they do increase
the likelihood of anomalous ocean warming that results in
bleaching,102 and mass coral bleaching can occur in the
absence of ENSO extremes when other climate anomalies
cause regional warming; e.g., Great Barrier Reef in early
1982,103 Moorea in 1994;104 Hawaii in 1996,105 and the
Caribbean in 2005.106 The risk of anomalous SST conditions
that might trigger coral bleaching has been, however, significantly modulated by ENSO events. It is, therefore, important
to understand how the frequency and intensity of ENSO
events might change as the world continues to warm. There
is, however, no consistent picture of whether there will be
changes in ENSO intensity or frequency of occurrence
associated with continued global warming.1
The present-day distribution of ocean currents and circulation in the vicinity of coral reefs are important controls on the
ecosystem dynamics as amongst other factors, these can have
significant effects on the connectivity between reef systems that
can control larval dispersal etc. Little is known as yet as to
how ocean currents will change as the world continues to
warm, although there is evidence in some areas of significant
changes already occurring. The East Australian Current, for
example, flows southwards from its origin in the Coral Sea.
There is already some evidence that its southern extension is
strengthening and carrying sub-tropical marine species further
south.107 Changes in ocean current strength and location will
also impact other coral reef ecosystems.
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Summary—is there a future for coral reefs?
Vague hopes that the biology of coral reefs will keep up with the
pace of change are not matched by current observations or our
understanding of past changes.108
The world’s coral reef ecosystems were in serious trouble
before the advent of rapid climate change due to the enhanced
greenhouse effect. The prognosis for their future is undoubtedly dire and their loss, severe degradation and change
in community structure that will result from ongoing climate
changes, would be catastrophic at many levels. These threats
are in addition to ongoing localized degradation and
deterioration of coral reef ecosystems due, primarily, to over
exploitation.27 Although many value coral reefs for their
aesthetics, the majority of people who depend on coral reefs
for their livelihoods (fisheries, tourism, shoreline protection)
live in poor, developing countries who contribute only a tiny
part of the world’s greenhouse gas emissions. A recent estimate is B10% 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$5000.109 This compares with a per capita GDP for
Australia, which contains B22% of the world’s coral reef
area, of B$US33 000. As with many aspects of climate change,
the people who are likely to suffer the greatest impacts are
those from developing countries who have contributed the
least to global warming.110
A plethora of scientific papers, national and international
reports and scholarly books now document the nature, impacts and potential consequences of ongoing rapid climate
change for coral reefs, as well as local direct human impacts.58,111–113 There is a clear consensus that the world’s
coral reefs are in trouble and that the alarm bells have been
ringing for decades. The future of coral reefs as climate
continues to change is inextricably linked to coral reef health.
Some coral reefs have shown the ability to withstand disturbances, such as coral bleaching (resistance), and some coral
reefs have shown the ability to recover from such disturbances (resilience).114,115 These attributes can be the result
of such coral reefs being dominated by resistant species or
to their physical environment reducing the probability of
stress. Reducing and reversing local, direct insults to coral
reefs clearly increases their resilience to global-scale climate
change—‘‘healthy’’ coral reefs, for example, recovered better
after the major 1997–98 world-wide coral bleaching event
than those already compromised by local anthropogenic
stresses or diseases.28 Increasing the resilience of the world’s
coral reef ecosystems requires integrated national and international actions and a greatly expanded network of marine
protected areas.24
Even with rapid global implementation of stringent mitigation strategies to stabilize and reduce greenhouse gas emissions, the world and coral reefs are committed to significant
rapid climate change, increased acidification of the oceans and
accelerated sea-level rise. The issue is not just a ‘‘change’’ from
one climate regime to a new one, to which organisms have to
adapt BUT that for the foreseeable future, climate will be
changing and it could be a long time before a new, relatively
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The Royal Society of Chemistry 2008
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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