Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook

Abstract

Since the early 1980s, episodes of coral reef bleaching and mortality, due primarily to climate-induced ocean warming, have occurred almost annually in one or more of the world's tropical or subtropical seas. Bleaching is episodic, with the most severe events typically accompanying coupled ocean–atmosphere phenomena, such as the El Niño-Southern Oscillation (ENSO), which result in sustained regional elevations of ocean temperature. Using this extended dataset (25+ years), we review the short- and long-term ecological impacts of coral bleaching on reef ecosystems, and quantitatively synthesize recovery data worldwide. Bleaching episodes have resulted in catastrophic loss of coral cover in some locations, and have changed coral community structure in many others, with a potentially critical influence on the maintenance of biodiversity in the marine tropics. Bleaching has also set the stage for other declines in reef health, such as increases in coral diseases, the breakdown of reef framework by bioeroders, and the loss of critical habitat for associated reef fishes and other biota. Secondary ecological effects, such as the concentration of predators on remnant surviving coral populations, have also accelerated the pace of decline in some areas. Although bleaching severity and recovery have been variable across all spatial scales, some reefs have experienced relatively rapid recovery from severe bleaching impacts. There has been a significant overall recovery of coral cover in the Indian Ocean, where many reefs were devastated by a single large bleaching event in 1998. In contrast, coral cover on western Atlantic reefs has generally continued to decline in response to multiple smaller bleaching events and a diverse set of chronic secondary stressors. No clear trends are apparent in the eastern Pacific, the central-southern-western Pacific or the Arabian Gulf, where some reefs are recovering and others are not. The majority of survivors and new recruits on regenerating and recovering coral reefs have originated from broadcast spawning taxa with a potential for asexual growth, relatively long distance dispersal, successful settlement, rapid growth and a capacity for framework construction. Whether or not affected reefs can continue to function as before will depend on: (1) how much coral cover is lost, and which species are locally extirpated; (2) the ability of remnant and recovering coral communities to adapt or acclimatize to higher temperatures and other climatic factors such as reductions in aragonite saturation state; (3) the changing balance between reef accumulation and bioerosion; and (4) our ability to maintain ecosystem resilience by restoring healthy levels of herbivory, macroalgal cover, and coral recruitment. Bleaching disturbances are likely to become a chronic stress in many reef areas in the coming decades, and coral communities, if they cannot recover quickly enough, are likely to be reduced to their most hardy or adaptable constituents. Some degraded reefs may already be approaching this ecological asymptote, although to date there have not been any global extinctions of individual coral species as a result of bleaching events. Since human populations inhabiting tropical coastal areas derive great value from coral reefs, the degradation of these ecosystems as a result of coral bleaching and its associated impacts is of considerable societal, as well as biological concern. Coral reef conservation strategies now recognize climate change as a principal threat, and are engaged in efforts to allocate conservation activity according to geographic-, taxonomic-, and habitat-specific priorities to maximize coral reef survival. Efforts to forecast and monitor bleaching, involving both remote sensed observations and coupled ocean–atmosphere climate models, are also underway. In addition to these efforts, attempts to minimize and mitigate bleaching impacts on reefs are immediately required. If significant reductions in greenhouse gas emissions can be achieved within the next two to three decades, maximizing coral survivorship during this time may be critical to ensuring healthy reefs can recover in the long term.

Full text

Climate change and coral reef bleaching: An ecological assessment
of long-term impacts, recovery trends and future outlook
Andrew C. Baker
a
,
b
,
1
, Peter W. Glynn
a
,
*
,
1
, Bernhard Riegl
c
,
1
a
Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA
b
Wildlife Conservation Society, Marine Program, 2300 Southern Boulevard, Bronx, NY 10460, USA
c
National Coral Reef Institute, Oceanographic Center, Nova Southeastern University, 8000 North Ocean Drive, Dania, FL 33004, USA
article info
Article history:
Received 18 July 2008
Accepted 4 September 2008
Available online xxx
Keywords:
coral bleaching
reefs
zooxanthellae
Symbiodinium
stress
global warming
conservation
prediction
forecast
ecosystem
recovery
community
abstract
Since the early 1980s, episodes of coral reef bleaching and mortality, due primarily to climate-induced
ocean warming, have occurred almost annually in one or more of the world’s tropical or subtropical seas.
Bleaching is episodic, with the most severe events typically accompanying coupled ocean–atmosphere
phenomena, such as the El Nin
˜o-Southern Oscillation (ENSO), which result in sustained regional
elevations of ocean temperature. Using this extended dataset (25þyears), we review the short- and long-
term ecological impacts of coral bleaching on reef ecosystems, and quantitatively synthesize recovery
data worldwide. Bleaching episodes have resulted in catastrophic loss of coral cover in some locations,
and have changed coral community structure in many others, with a potentially critical influence on the
maintenance of biodiversity in the marine tropics. Bleaching has also set the stage for other declines in
reef health, such as increases in coral diseases, the breakdown of reef framework by bioeroders, and the
loss of critical habitat for associated reef fishes and other biota. Secondary ecological effects, such as the
concentration of predators on remnant surviving coral populations, have also accelerated the pace of
decline in some areas. Although bleaching severity and recovery have been variable across all spatial
scales, some reefs have experienced relatively rapid recovery from severe bleaching impacts. There has
been a significant overall recovery of coral cover in the Indian Ocean, where many reefs were devastated
by a single large bleaching event in 1998. In contrast, coral cover on western Atlantic reefs has generally
continued to decline in response to multiple smaller bleaching events and a diverse set of chronic
secondary stressors. No clear trends are apparent in the eastern Pacific, the central-southern-western
Pacific or the Arabian Gulf, where some reefs are recovering and others are not. The majority of survivors
and new recruits on regenerating and recovering coral reefs have originated from broadcast spawning
taxa with a potential for asexual growth, relatively long distance dispersal, successful settlement, rapid
growth and a capacity for framework construction. Whether or not affected reefs can continue to
function as before will depend on: (1) how much coral cover is lost, and which species are locally
extirpated; (2) the ability of remnant and recovering coral communities to adapt or acclimatize to higher
temperatures and other climatic factors such as reductions in aragonite saturation state; (3) the changing
balance between reef accumulation and bioerosion; and (4) our ability to maintain ecosystem resilience
by restoring healthy levels of herbivory, macroalgal cover, and coral recruitment. Bleaching disturbances
are likely to become a chronic stress in many reef areas in the coming decades, and coral communities, if
they cannot recover quickly enough, are likely to be reduced to their most hardy or adaptable constit-
uents. Some degraded reefs may already be approaching this ecological asymptote, although to date
there have not been any global extinctions of individual coral species as a result of bleaching events.
Since human populations inhabiting tropical coastal areas derive great value from coral reefs, the
degradation of these ecosystems as a result of coral bleaching and its associated impacts is of consid-
erable societal, as well as biological concern. Coral reef conservation strategies now recognize climate
*Corresponding author.
E-mail address: pglynn@rsmas.miami.edu (P.W. Glynn).
1
All authors have contributed equally to this review.
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science
journal homepage: www.elsevier.com/locate/ecss
ARTICLE IN PRESS
0272-7714/$ – see front matter Ó2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2008.09.003
Estuarine, Coastal and Shelf Science xxx (2008) 1–37
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

change as a principal threat, and are engaged in efforts to allocate conservation activity according to
geographic-, taxonomic-, and habitat-specific priorities to maximize coral reef survival. Efforts to forecast
and monitor bleaching, involving both remote sensed observations and coupled ocean–atmosphere
climate models, are also underway. In addition to these efforts, attempts to minimize and mitigate
bleaching impacts on reefs are immediately required. If significant reductions in greenhouse gas emis-
sions can be achieved within the next two to three decades, maximizing coral survivorship during this
time may be critical to ensuring healthy reefs can recover in the long term.
Ó2008 Elsevier Ltd. All rights reserved.
1. Introduction
Climate change is now firmly established as a scientific reality,
with a variety of emergent challenges for societies in the coming
decades. Global warming and associated increases in sea surface
temperatures (SSTs) are now projected to be very likely in the
coming decades (IPCC, 2001, 2007; Phinney et al., 2006), and the
human ‘‘fingerprint’’ of increased atmospheric CO
2
on the climate
signal is also clear (Santer et al., 2007). Combined with the acidi-
fying effect of increasing dissolved carbon dioxide in the ocean
(Caldeira and Wickett, 2003; Feely et al., 2004; Kleypas and Lang-
don, 2006), there is a clear research need to understand the likely
impacts of climate change on marine ecosystems, and identify
strategies to mitigate harmful effects, where possible. These
assessments are already underway (Sarmiento et al., 2004; Greb-
meier et al., 2006), but as changes in the climate system begin to
mature over the coming years, it will be increasingly important to
refine these forecasts by ground-truthing them against observa-
tions. This research strategy offers the greatest likelihood of iden-
tifying trends in ecosystem response, and maximizes the accuracy
of updated forecasts.
Coral reef ecosystems are particularly sensitive to climate-
induced changes in the physical environment. Since the 1980s,
coral reef ‘‘bleaching’’, caused by unusually high sea temperatures,
has had devastating and widespread effects worldwide. As a result,
a significant body of research has accumulated on the causes and
consequences of bleaching. Research spans the fields of cellular
physiology, organismal biology, ecology and ecosystem biology, and
includes timescales ranging from milliseconds to decades. This
justifies a critical re-assessment of the accumulated knowledge
base, focusing on the long-term ecological impacts of warming, and
recovery trajectories following disturbance. Moreover, the more
recent discovery that coral reefs are not only threatened by
increasing temperatures, but also by ocean acidification (Gattuso
et al., 1998; Kleypas et al., 1999), galvanizes the need for
a comprehensive update on bleaching that highlights uncertainties
in how climate change effects might interact. The objective of this
review is therefore to synthesize knowledge on the long-term
ecological effects of coral bleaching, including a quantitative
synthesis of biogeographic differences in recovery response, collate
information on timescales and trends in recovery processes, refine
our forecasts where necessary, and identify potential strategies that
might maximize coral reef survival in the coming years.
1.1. Coral reef bleaching: Definition
Reef-building corals, as well as numerous species of reef-
dwelling cnidarians, mollusks, polychaetes, protists and other taxa,
are hosts to dinoflagellate symbionts in the genus Symbiodinium.
These symbionts, commonly referred to as ‘‘zooxanthellae’’, are
generally obligate for their hosts, contributing to their host’s
energetic budgets through the provision of photosynthates, as well
as accelerating calcification in many skeleton-forming taxa (Mus-
catine and Porter, 1977). This dependence on photosynthetic,
oxygen-producing autotrophs, while having clear benefits, also
imparts distinct costs. Environmental extremes, such as high
temperature or irradiance, damage the symbionts’ photosynthetic
machinery, resulting in the overproduction of oxygen radicals. This
leads to eventual cellular damage in the symbionts and/or their
hosts, and can lead to the expulsion of symbionts and the eventual
breakdown of the symbiosis (Lesser, 2006). The loss of zooxan-
thellae (and/or a reduction in their pigment concentrations) as
a result of this process is referred to as ‘‘bleaching’’. In extreme
cases, bleaching leads to the visible paling of the host organism, as
the yellow-brown pigmentation of the symbionts is lost (Fig. 1). In
scleractinian (stony) corals some 50% or more of the total symbiont
community must be lost before paling is typically visible to the
naked eye (Fitt et al., 2000), and in many taxa, including corals,
bleaching turns the host organism white, as the calcareous skeleton
becomes visible through the coral’s transparent tissues.
Many coral species contain a variety of non-photosynthetic
pigments of host origin that are not diminished in concentration or
lost during bleaching events. These pigments can result in bleached
corals that appear pink, chartreuse, purple, yellow or other colors,
rather than the more typical white. Bleaching events, when they
occur, are usually not confined to the principal reef-builders
themselves, the scleractinian corals, but also involve numerous
other metazoan and protist hosts on reefs. Consequently, the term
‘‘coral reef bleaching’’ is a better descriptor of these reef-wide
events (rather than the more restrictive term ‘‘coral bleaching’’).
1.2. Coral reef bleaching events
The number of coral reef bleaching reports, driven principally by
episodic increases in sea temperature, has increased dramatically
since the early 1980s (Glynn,1993; Hoegh-Guldberg, 1999; Hughes
et al., 2003; Hoegh-Guldberg et al., 2007). Many of these events,
and recovery from them, have now been studied over decadal
scales. The frequency and scale of coral bleaching events during the
past few decades have been unprecedented, with hundreds of reef
areas exhibiting bleaching at some point, and, on occasion, whole
ocean basins affected. Consequently, much has been written about
coral reef bleaching during the past three decades, and several
compilations are available in the published literature (Williams and
Bunkley-Williams, 1990; Glynn, 1996; Brown, 1997a; Wilkinson,
2000, 2004; Coles and Brown, 2003; Wilkinson and Souter, 2008),
as well as online in various databases maintained by agencies such
as the WorldFish Center, NOAA, and GBRMPA.
The occurrence of mass bleaching events correlates well with
observed increases in global sea temperatures, and particularly
thermal anomalies. This relationship was clearly observed in the
Caribbean basin during the 1980s and 1990s, when annual coral
bleaching increased logarithmically with SST anomalies (McWil-
liams et al., 2005). A 0.1

C rise in regional SST resulted in a 35%
increase in the number of areas that reported bleaching, and mass
bleaching events occurred at regional SST anomalies of 0.2

C and
above (Fig. 2). Bleaching within affected regions is not uniform,
exhibiting patchy affects over micro (mm to cm) to meso (km)
scales. Such variability results from fluctuations in environmental
conditions, spatial heterogeneity of reef surfaces, genetic
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–372
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

differences in hosts or symbionts, and differences in environmental
history, all of which will be reviewed here. What has become
evident is that, over the last three decades, bleaching has been
reported from virtually every region that supports coral reefs, and
no region of the world’s tropical and subtropical seas appears safe
from bleaching (Fig. 3). Only West Africa has yet to report a coral
reef bleaching event, an outlier which is more likely due to an
absence of observers, rather than an absence of bleaching. Even
some non reef-building (but nevertheless zooxanthellate) Medi-
terranean corals and gorgonians have been severely affected by
temperature-related bleaching and mortality (Cerrano et al., 2000;
Rodolfo-Metalpa et al., 2005, 2006).
Meta-analysis has recently become a method of choice for
describing large-scale and long-term trends in coral reefs and other
ecosystems (Parmesan and Yohe, 2002; Co
ˆte
´et al., 2005, 2006).
Gardner et al. (2003) and Bruno and Selig (2007) used this
approach to document regional declines in coral cover in the
Caribbean and Pacific, respectively, and Gardner et al. (2005) also
used the approach to study hurricane effects on Caribbean reefs, as
did McWilliams et al. (2005) for bleaching in the region. In addition,
Jackson et al. (2001) and Pandolfi et al. (2003, 2005) used a mixture
of meta-analysis and their own data to describe trends in reefs
worldwide. Although meta-analysis is recognized as a subject with
its own statistical methods, advantages and pitfalls (Co
ˆte
´et al.,
2005), some of these papers nevertheless drew criticism for the
way their findings were interpreted (Aronson et al., 2003; Aronson
and Precht, 2006). Other reviews of coral reef decline have avoided
meta-analysis in favor of expert consensus; such consensus views
Fig. 1. Bleached corals. (a) Porites lobata and Pocillopora spp. totally bleached. Corals in the background partially bleached. Hanga Roa, Easter Island, March 2000, about 12 m depth.
(b) Differential bleaching in the free-living Diaseris distorta. Gala
´pagos, Corona del Diablo, March 1998. (c) Completely bleached Acropora formosa at Halfway Island, Great Barrier
Reef, February 2002 (photo by R. Berkelmans). (d) Completely bleached Acropora cervicornis at Andros Island, Bahamas, August 1998, 1 m depth. (e) Pavona clavus partially bleached
at Silva de Afuera Island, Panama
´, March 1998, 10 m depth.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 3
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

have been useful in standardizing viewpoints on the subject of coral
reefs and climate change (Hughes et al., 2003; Hoegh-Guldberg
et al., 2007), and on the whole have been less contentious, perhaps
because their conclusions tend to be less quantitative. Regardless,
both approaches have generally supported one another in their
overall conclusions regarding the causes and rate of coral reef
decline. These reviews have tended to focus on declines and
impacts, rather than on recovery and regeneration (but see Shep-
pard, 2006). Here we aim to focus on the longer-term ecological
impacts of bleaching and the potential for recovery, rather than
providing a review of bleaching mechanisms and immediate
effects, which have already been covered by a number of recent
reviews (Fitt et al., 2001;Hughes et al., 2003; Lesser, 2006; Hoegh-
Guldberg et al., 2007).
2. Causes of coral reef bleaching
2.1. The cellular and physiological basis of bleaching
Injury to corals as a result of naturally-occurring high temper-
atures appears to have been first observed by L.R. Cary in 1911,
following several days of hot, calm weather in the Dry Tortugas,
Florida (reported in Mayer, 1914). During the Great Barrier Reef
Expedition of 1928–29, coral ‘‘bleaching’’ was a central focus of
several experiments, including the effects of high temperatures
(Yonge and Nicholls, 1931). Few studies followed until the 1970s,
when seminal experiments by Jokiel and Coles (1974, 1977) and
Coles and Jokiel (1977, 1978) attempted to quantify the bleaching
phenomenon. Following episodes of mass coral reef bleaching
occurring in response to high temperatures in 1982–83 and 1987–
88 in the eastern Pacific and Caribbean, respectively (Glynn, 1991),
the 1990s experienced rapid progress in understanding the
molecular underpinnings of bleaching, in particular how interac-
tions between temperature and light result in damage to Photo-
system II (Iglesias-Prieto et al., 1992; Fitt and Warner, 1995; Lesser,
1996; Warner et al., 1996, 1999; Jones et al., 1998; Brown et al.,
2000;Fitt et al., 2001); how enzymatic antioxidants degrade
Reactive Oxygen Species (ROS) (Lesser et al., 1990), and how the
xanthophyll cycle dissipates excess absorbed energy (Brown et al.,
1999).
More recently, it has been shown that the lipid composition of
symbiont thylakoid membranes affects their structural integrity at
high temperatures, resulting in damage to Photosystem II when
this integrity is compromised (Tchernov et al., 2004), and that
increased nitric acid synthase also accompanies bleaching (Tra-
pido-Rosenthal et al., 2005). In general, bleaching results from
accumulated oxidative stress on the thylakoid membranes of
symbiont chloroplasts (Lesser, 1996, 1997; Downs et al., 2002)as
a result of damage to Photosystem II (see Lesser, 2006 for review).
This damage results in the degradation and eventual expulsion of
symbionts from host tissue, although the exact cellular processes
involved in symbiont release are still unclear (but see Gates et al.,
1992; Dunn et al., 2002; Franklin et al., 2004).
2.2. The environmental basis of coral reef bleaching
Reef corals and other zooxanthellate organisms live close to
their upper thermal tolerance limits and are confined to the
shallow waters of the photic zone. Because of the interacting
negative effects of high temperature and light, bleaching has most
commonly been associated with high irradiance environments
experiencing unusually warm conditions (typically 1.0– 1.5

C
above seasonal maximum mean temperatures). A variety of other
stressors have also been documented to result in bleaching (Glynn,
1993; Brown,1997a; Coles and Brown, 2003; Lesser, 2004), but the
physiological and cellular mechanisms by which these stressors
cause bleaching are not as well understood (Douglas, 2003).
Bleaching and mortality due to low temperatures has long been
known (Coles and Jokiel, 1977; Glynn and D’Croz, 1990; Coles and
Fadlallah, 1991), but it has only recently been shown that cold
stress, like heat stress, leads to bleaching by impairing the function
of Photosystem II (Saxby et al., 2003; LaJeunesse et al., 2007).
Hoegh-Guldberg et al. (2005) also reported bleaching in intertidal
corals exposed to cold winds, although the role of desiccation in
contributing to this phenomenon is not clear. Bleaching induced by
cyanide exposure also impairs photosynthesis, resulting in
symbiont expulsion (Jones et al., 1999).
Increased solar radiation, both in the visible (400–700 nm) and
the ultraviolet (290–400 nm) regions of the spectrum, have also
been variably implicated in mass coral bleaching (Hoegh-Guldberg
and Smith, 1989; Brown et al., 1994; Fitt and Warner, 1995; Shick
et al., 1996; Brown, 1997a,b; Lesser, 1997; Brown et al., 1999; Dunne
and Brown, 2001; Coles and Brown, 2003; Lesser, 2004; Smith et al.,
2005). These findings have also been confirmed in other zoox-
anthellate organisms such as symbiont-bearing foraminifera (Wil-
liams and Hallock, 2004; Hallock et al., 2006). Because of the
relatively high doses of UV radiation found in shallow tropical
marine environments, corals typically contain a variety of protec-
tive screening pigments, such as mycosporine-like amino acids
(MAAs), which absorb these wavelengths and prevent cellular
damage. Higher rates of UV radiation as a result of atmospheric
ozone depletion are potentially an important element of global
change, with harmful future effects on coral reef ecosystems. With
the dramatic reductions in CFCs and other ozone-depleting
compounds, however, this stressor is now less of a threat than was
previously considered. While it can exacerbate bleaching under
0
Re
g
ional summer SST anomal
y
(
°C
)
Log(percentage of coral reef
cells reporting bleaching)
0 0.2 0.4 0.6 0.8 1.0
1999
2.0
1.5
1.0
0.5
-0.2-0.4-0.6
Fig. 2. The relationship between regional SST anomalies and the percentage of 1latitude/longitude cells from which at least one coral bleaching occurrence was recorded during
August-October in the Caribbean between 1983 and 2000. Each data point represents one year. Solid circles represent years described in the literature as mass bleaching events,
open circles represent other years. The solid line represents the regression line: log (cells) ¼1.34 (SST) þ0.71; r
2
¼0.86, n¼18, p<0.001. The dashed line shows the SST at which
maximum bleaching extent should occur based on extrapolation of the regression line. Adapted from McWilliams et al., 2005.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–374
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

certain conditions (cloudless days accompanied by calm, doldrum-
like conditions), its role in explaining the worldwide increase in
coral bleaching events over the last 25 years is probably not a major
one. The single most important factor driving these outbreaks of
coral bleaching is the increasing frequency of high temperature
anomalies: all regional episodes of coral reef bleaching docu-
mented to date have implicated high temperatures as the under-
lying stressor. These anomalies typically push shallow corals in
high-light environments beyond their current photoinhibitory
thresholds, resulting in bleaching.
When was climate change first suspected as driving the
increase in bleaching events? From the very beginning it was
surmised that higher than normal temperatures were a principal
driver of mass coral reef bleaching events (Glynn, 1983; Glynn
and D’Croz, 1990; Williams and Bunkley-Williams, 1990; but see
also Goreau, 1964). Increases in temperature and/or irradiance
pointed early on to climatic or oceanographic causes, and large-
scale ocean–atmosphere phenomena, in particular the El Nin
˜o-
Southern Oscillation (ENSO), were quickly identified as likely
causal agents (Von Prahl, 1983, 1985; Glynn, 1984, 1990a,b, 1993;
Wilkinson, 1999). ENSO has since been implicated as the trigger
for bleaching in the eastern Pacific (Podesta
´and Glynn, 1997;
Glynn and Colley, 2001) and Palau (Bruno et al., 2001), while the
Pacific Decadal Oscillation (PDO) and the Indian Ocean Dipole
(IOD) appear to be drivers of bleaching events in Hawaii and the
western Indian Ocean, respectively (Jokiel and Brown, 2004;
McClanahan et al., 2007a).
But how much heat is needed, and over how long (anomaly
excursion, length, timing) to cause bleaching? The heat-threshold
idea was pioneered by Glynn (1993, 1996), Goreau and Hayes
(1994), Goreau et al. (1993, 1997) and Hoegh-Guldberg (1999), and
was furthered by Berkelmans (2002a,b), Dunne (2002) and many
others, but also contested by Fitt et al. (2001). The original idea was
that upper and lower temperature thresholds exist which, when
exceeded, result in physiological stress resulting in the breakdown
of symbiosis. Exactly how these thresholds are defined, whether
they need to be exceeded only once, or repeatedly, and for how
long, and how much, as well as the role of past temperature vari-
ability, is still debated today (Manzello et al., 2007a; McClanahan
et al., 2007a). The question of whether damaging heat stress is an
acute event, or a chronic, cumulative phenomenon, was also
debated early on.
Fig. 3. Incidence of coral reef bleaching on a worldwide scale. (a) Selected bleaching years and locations (from various sources; Brown, 1987; Glynn, 1993,1996; Coles and Brown,
2003; Wilkinson and Souter, 2008; Savimi, pers. commun.). (b) Locations of bleaching reports (map from ReefBase, www.reefbase.org): 1, Arabian Gulf (United Arab Emirates, Qatar,
Iran); 2, Red Sea; 3, east Africa; 4, southern Africa (Mozambique, South Africa); 5, Madagascar; 6, Mauritius, Reunion; 7, Seychelles; 8, Chagos; 9, Maldives; 10, Sri Lanka/southern
India; 11, Andaman Sea (Andamans, Thailand, Malaysia); 12, South China Sea (Vietnam, Paracel Islands); 13, Philippines; 14, Indonesia; 15, western Australia; 16, Great Barrier Reef;
17, Ryukyu Islands; 18, Mariana Islands; 19, Palau; 20, Papua New Guinea, Vanuatu; 21, Fiji; 22, Samoa; 23, French Polynesia (including Moorea); 24, Hawaiian Islands; 25, Easter
Island; 26, Gala
´pagos Islands; 27, equatorial eastern Pacific (Costa Rica, Cocos Island, Panama
´, Colombia, Ecuador); 28, subtropical eastern Pacific (Me
´xico); 29, Mesoamerican reef
system (Me
´xico, Belize, Honduras, Nicaragua); 30, Greater Antilles (Cuba, Haiti, Dominican Republic, Puerto Rico, Virgin Islands); 31, Bahamas, Florida; 32, Bermuda; 33, Lesser
Antilles; 34, Curaçao, Aruba, Bonaire, Los Roques; 35, Brazil.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 5
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Indicators used to hindcast and forecast bleaching episodes have
included monthly mean sea temperatures above a local threshold
(Goreau et al., 1993; Brown et al., 1996) as well as cumulative heat-
stress (Gleeson and Strong,1995; Podesta
´and Glynn, 1997). Goreau
and Hayes (1994) developed a Degree Heating Month (DHM) index,
defined as the cumulative sum of anomalies more than 1

C above
long-term monthly averages, and used this index to identify ocean
‘‘hotspots’’ (now a somewhat confusing term due to its use in
marine biodiversity conservation (Roberts et al., 2002). A modified
version of this index is now used by NOAA as part of its Coral Reef
Watch program. Podesta
´and Glynn (1997) developed a ‘‘degree
days’’ (DD) index, which is a summation of differences between
daily SST values and mean SSTs over the warm phase of the year.
This index is a good hindcaster of bleaching events (Fig. 4). Time-
integrated bleaching thresholds were proposed by Berkelmans
(Fig. 5), who refined this using a 3-day maximum temperature to
best explain bleaching intensity on the Great Barrier Reef (Berkel-
mans, 2002a; Berkelmans et al., 2004). In Puerto Rico, Winter et al.
(1998) observed a log-log relationship between temperature and
number of days above that temperature for bleaching, which was
later re-evaluated by Sammarco et al. (2006), who surmised that it
was the size of biweekly temperature variance that differentiated
bleaching years from non-bleaching years. Recently, Manzello et al.
(2007a) evaluated bleaching in the Florida Keys and the U.S. Virgin
Islands to determine whether it was short-term temperature stress,
cumulative temperature stress, or temperature variability that best
predicted the onset of bleaching. They found that maximum
monthly SST, and the number of days spent above a threshold of
30.5

C, were the most significant conditions.
As a measure of cumulative heat stress, Liu et al. (2003) devel-
oped the Degree Heating Week (DHW) index, which measures
accumulated thermal stress over a 12-week period by calculating
the number of degree-weeks by which temperatures exceed the
mean annual maximum temperature: two DHWs are equivalent to
two weeks at one degree above the mean summertime maximum
or one week of two degrees above the mean summertime
maximum. Although sensitive to the baseline period used to define
mean summertime maxima, DHWs have been fairly successful in
predicting coral bleaching events, and have been incorporated into
NOAA’s Coral Reef Watch program. McClanahan et al. (2007b),
however, found that DHWs, combined with information on past
temperature anomalies and coral community sensitivity, only
predicted about one-half of Indian Ocean bleaching in 2005, sug-
gesting that these metrics might not be good predictors of milder
bleaching events. Barton and Casey (2005) extended the DHW
index to a degree heating month (DHM) index, which allowed them
to use longer-term SST reconstructions (such as HadISST, ERSST and
GISST) for hindcasting past bleaching events. It appears that acute
(maximum short-term heat stress, Podesta
´and Glynn, 1997;
Manzello et al., 2007a), as well as cumulative temperature stress
(Liu et al., 2003) together best predict bleaching, with prior
temperature variability also increasing accuracy (McClanahan et al.,
2007a,b).
Besides mean sea surface temperature, it also appears that
regional weather conditions are of great importance. Short- and
long-term effects of large-scale weather patterns (such as the
ENSO) are intertwined, and local conditions are important in
modulating the bleaching response (Skirving et al., 2006). Since
heat-flux into the ocean is controlled by vapor content in the
atmosphere (cloudiness), strongest heat absorption will be
observed on clear, calm days. Mumby et al. (2001a) attributed
absence of excessive bleaching in the Tuamotu Islands in 1998 to
high cloud cover. In addition to clouds, any type of aerosol will have
the effect of scattering radiation and thus decreasing heat-flux to
the ocean. Gill et al. (2006) showed that high levels of aerosols (dust
and sulfides, largely created by volcanic activity) effectively miti-
gated bleaching conditions, even during ENSO years that would
Fig. 4. The proposed degree days (DD) index of Podesta
´and Glynn (1997, 2001) captures bleaching events reasonably well in the eastern Pacific. The dashed boxes enclose years in
which bleaching was detected.
Fig. 5. The ‘‘time-integrated bleaching threshold’’ of Berkelmans (2002a) and
Manzello et al. (2007a) for reef sites on the Great Barrier Reef, Australia and the
Caribbean respectively. Note that thresholds are not uniform, but rather site-specific
and can vary even within a region by several degrees.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–376
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

normally have created bleaching-favorable conditions. Particulate
matter in the ocean can also scatter and attenuate radiation that
can be harmful to corals in shallow water, performing a similar
function to atmospheric aerosols. Otis et al. (2004) demonstrated
the potential importance of this process in a study of remotely-
sensed colored dissolved organic matter (CDOM) concentrations
over the Bahama banks.
In addition to clouds, storm conditions can also be beneficial in
times of bleaching. Storms and even hurricanes can mitigate
bleaching, since wave action can lead to strong vertical mixing,
removing excess heat from shallow water (Heron et al., 2004;
Skirving et al., 2006; Strong et al., 2006; Manzello et al., 2007b). If
the incidence and severity of storms increase as a result of climate
change, it appears that, besides the undeniable physical impacts of
extreme storm events, thermally stressed coral reefs probably
benefit more from storms than they do from calm seas (Riegl,
2007).
Waves not only dissipate heat by mixing but they can also
generate water motion. The latter has been shown to be helpful in
mitigating coral bleaching by thinning boundary layers and accel-
erating mass transfer, especially the removal of toxic oxygen radi-
cals (Nakamura and van Woesik, 2001; Nakamura et al., 2003,
2005; van Woesik and Koksal, 2006), and the dissipation of heat
(Fabricius, 2006). Craig et al. (2001) and Birkeland et al. (2008)
believe that the resilience of corals in lagoons in American Samoa,
which persist in one of the warmest known environments, may be
largely due to high water flow, with healthier corals found near
tidal passes. In the Arabian Gulf, where corals persist at even
warmer temperatures, it has been suggested that preferential
survival on offshore islands during the 2002 bleaching event might
have been due to higher water motion than further inshore (Riegl,
2003). McClanahan et al. (2005a,b), however, were not able to
confirm in field investigations that flow necessarily mitigated
bleaching damage, and argued that high-flow environments reduce
environmental variability and canrender corals more susceptible to
disturbances (but see van Woesik et al., 2005).
Brown et al. (1994) and Fabricius (2006) also observed that coral
color had an important influence on temperature at the tissue–
water interface, and Fabricius (2006) demonstrated that dark
(highly pigmented) corals (measured with the color chart of Sie-
beck et al., 2006) could be up to 1.5

C warmer than the
surrounding seawater. Thus, darkly pigmented corals, characteristic
of turbid or high nutrient environments, might be at a greater risk
of thermal damage than their paler counterparts, although this
effect might be mitigated by lower light levels and/or strong flow.
2.2.1. Environmental factors that mitigate bleaching
Numerous environmental and physical factors reduce the inci-
dence or severity of bleaching (Craig et al., 2001; Salm et al., 2001).
These factors include low light (due to depth, shading, turbidity or
cloud cover (Mumby et al., 2001a), high flow (Nakamura and van
Woesik, 2001; Nakamura et al., 2003), lower temperatures (Riegl,
2003; McClanahan, 2008) and higher nutrients (Grottoli et al.,
2006). These factors are observed to correlate with particular
habitats, such as deeper reefs near the thermocline, reefs in
upwelling areas, coastal areas with high levels of suspended
terrigenous sediment, areas subject to strong currents, and shore-
line and lagunal reefs that are shaded by high islands, for example
in the south Pacific (Glynn, 1996; Riegl and Piller, 2001; Salm et al.,
2001; West and Salm, 2003). Corals in these ‘‘refuge’’ habitats are
expected to be less likely to bleach than at other reef sites subject to
the same degree of heat stress.
In contrast, shallow areas subject to both high temperature and
high light are likely to be the most subject to continued bleaching
threats. Weak water currents further increase the likelihood of
bleaching by reducing the ability of corals to remove cellular toxins
that accumulate as a result of photoinhibition. Consequently, areas
which experience the highest bleaching risk are likely to be warm,
shallow waters with low flow, such as those found in lagoons and
restricted embayments. All other things being equal, these sites are
assumed to have lower conservation priority than sites that might
be protected from bleaching (Salm et al., 2001).
Nonetheless, McClanahan et al. (2005a,b) have argued that corals
in low flow areas can sometimes be more resistant to bleaching
because these sites are often characterized by dramatic temperature
fluctuations as a result of restricted circulation (but see van Woesik
et al., 2005). In these cases, the role of the environment in helping
corals acclimatize to temperature stress may be more important
than its role in alleviating the metabolic effects of the stress itself.
This complicates attempts to identify bleaching refugia using phys-
ical habitat characteristics because previous ‘‘experience’’ (not
necessarily predictable from simple habitat characteristics) is likely
to play a critical role in determining whether or not corals actually
bleach in response to putative stressors (Brown et al., 2000, 2002).
Even experience can be a double-edged sword, however. A past
history of environmental stress can either harden coral communi-
ties to further change (through acclimatization mechanisms and
adaptive processes) or degrade them (through the chronic deple-
tion of energy reserves). Understanding how these factors interact
remains one of the greatest challenges to forecasting bleaching
response. Without reliable information on whether or not corals in
a particular area have survived high bleaching stress in the past, it is
very difficult to forecast site- and habitat-specific variability in
bleaching severity. Moreover, because limits to short-term accli-
matization or adaptation are likely, even hardened corals from high
temperature environments might still be considered vulnerable to
bleaching threats because they have exhausted their short-term
response potential. For example, corals on a shallow reef in an
enclosed bay in a relatively warm region of the world might be
considered likely to survive bleaching because theyare already pre-
adapted to high levels of environmental stress (McClanahan et al.,
2007c). Conversely, the combination of high temperature, irradi-
ance stress and low flow might suggest these corals are already
dangerously close to a critical stress threshold and therefore highly
vulnerable to potential bleaching.
Coral communities found in extreme environments that are
close to the limits of their thermal distribution (e.g., the Arabian
Gulf, or the lagoon at Ofu in American Samoa) provide unique
opportunities to study how genes, environment and time interact
to determine organismal response (Riegl, 2003; Baker et al., 2005;
Smith et al., 2008). These interactions will be complex (Edmunds
and Gates, 2008), and are likely only resolvable by the application
of genomics tools, an area that is poised to become a principal
research focus of the next decade.
3. Detecting bleaching
3.1. Detecting ongoing bleaching events
Detecting bleaching, when it occurs, is not always as easy as it may
appear, and is complicated by numerous physiological and physical
factors that confound simple observations. Problems arise at both the
individual colony scale (assessing whether a coral is bleached or not)
and at the reef and regional scales (how large an area is bleached). The
first problem can be solved using a diver-based approach, the second
encounters logistic limitations if divers are involved, and requires
mapping procedures and various remote-sensing approaches.
Bleaching can be described by matching affected colonies to
a color scale to differentiate various degrees of paling. Ranked scales
of paling have been proposed (Gleason, 1993; Hoegh-Guldberg and
Salvat, 1995; Edmunds et al., 2003; McClanahan et al., 2004) that
have eventually developed into more refined scales using a color
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 7
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

reference card (Fabricius, 2006; Siebeck et al., 2006). Some caveats
apply to visual identification, especially by non-experts, since
extreme polyp retraction (Brown et al., 1994), as well as some kinds
of disease, can be misinterpreted as bleaching. In addition, loss of
algal symbionts begins long before bleaching becomes visually
apparent (Fitt et al., 2000). In some cases, chlorophyll alevels can
remain unchanged despite significant changes in other pigments,
such as peridinin, which respond to light and nutrients (Iglesias-
Fig. 6. Provided one can be certain that the bright areas are not sand, then coral bleaching provides a very clear spectral signature that can be mapped on images with adequate
resolution. (a, b) Great Keppel Island, Great Barrier Reef, bleached in 2002. (c) Individual bleached corals stand out as white patches on this aerial image of Nelly Reef, Great Barrier
Reef, which bleached in 1998. (d) Quickbird satellite image on which bleached Acropora cervicornis were identified spectrally (a, b communicated by R. Berkelmans, c by
S. Andre
´foue
¨t, d from Rowlands et al., 2008).
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–378
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Prieto and Trench, 1997). Nevertheless, semi-quantitative data
provided by color scales are generally considered useful for
a synoptic description of bleaching status, and have proved useful in
rapid field surveys using towed observers, or downward-facing
video cameras (English et al., 1997; Berkelmans and Oliver, 1999;
Jordan and Samways, 2001; Riegl et al., 2001; Kenyon et al., 2006).
More quantitative methods of evaluating coral bleaching have
recently become available with satellite- and aircraft-based imaging
sensors of sufficiently high resolution (Fig. 6). Although the term
‘‘bleaching’’ implies that an optical signature should be present that is
sufficiently unequivocal to allow remote detection by imagery, much
research has gone into testing this assumption. Holden and LeDrew
(1998) used clustering and ordination coupled with derivative spec-
troscopy (which refers to the sharpening of spectral features by using
higher derivatives of the original spectral values: Tsai and Philpot,
1998) to demonstrate that spectral differences do exist between
healthy and bleached corals.Libraries of the spectralqualities of corals
(Holden and LeDrew, 2001a,b; Hedley and Mumby, 2002; Hochberg
et al., 2004) should be helpful in obtaining comparative spectra or
calibration values for future bleaching studies.
In addition to spectral resolution, spatial resolution is equally
important. Larger pixel sizes lead to more mixed spectral signatures,
since many different substrate signals besides the coral signal willbe
included. Andre
´foue
¨t et al. (2002) specifically investigated this
aspect by using digitized aerial (3-band)imagery, and suggested that
a range of 40–80 cm provides suitable accuracy. This is still beyond
the capability of most readily available satellite sensors (Ikonos 4 m,
Quickbird 2.4 m), spurring investigation into other approaches.
Hedley et al. (in press) recently discussed, from both theoretical and
experimental considerations, whether spectrally unequivocal
signatures that detect bleaching can actually be developed. They
concluded that obtaining a clear bleaching signature remains diffi-
cult due to its similarity to that of sand. Nonetheless, several studies
have shown thatbleaching is indeed detectable at some level, at least
in situations wherebleached corals make up the majority of the pixel
(Andre
´foue
¨t et al., 2002; Yamano et al., 2003; Elvidge et al., 2004;
Yamano and Tamura, 2004; Rowlands et al., 2008), so the discussion
on what can and cannot be achieved, and the search for the adequate
remote-sensing tool, is likely to continue for a while.
Remote assessments of the extent of coral mortality after
a bleaching event, or the longer-term trajectory of a coral assem-
blage in response to bleaching, are burdened with many problems.
The spectral signatures of formerly bleached (and now dead or
regenerated) corals can change dramatically. Regenerated corals
regain their ‘‘healthy’’ signature (essentially, two spectral end-
members exist in corals: those of brown-mode corals are domi-
nated by the zooxanthellae, those of blue-mode corals by non-
fluorescent pigments: Hochberg et al., 2004), and dead corals are
often overgrown by algae. Clark et al. (20 00) showed that derivative
analysis of coral spectral properties was indeed able to discriminate
between different health states of corals after the 1998 bleaching
event. Hochberg and Atkinson (2003) used a variety of sensors
(AAHIS, AVIRIS, Ikonos, Landsat ETMþ, SPOT-HRV), and Andre
´foue
¨t
et al. (2004) used CASI data, to demonstrate spectral differences
between algae and corals. This distinction is key to differentiating
between live and dead corals, because dead corals have no unique
spectral signature (other than immediately post-mortem, while the
skeleton is still white (Clark et al., 2000). Mumby et al. (2004) used
CASI in two configurations (6-band, 10-band) and derivative spec-
troscopy to show that hyperspectral imagery was indeed capable of
detecting dead versus live corals, and favored larger pixels with
more spectral information. Building on these findings, Purkis
(2005) used Ikonos imagery to detect corals that had died 5 years
previously using a signal of macroalgal overgrowth. This informa-
tion was used by Purkis and Riegl (2005) and Purkis et al. (2005) to
measure the spatial footprint of coral mass mortality due to
bleaching, and to study the resultant coral community, sedimen-
tary and landscape dynamics.
The availability of imagery time-series greatly aids in the
detection of bleaching or related changes in reefs. Andre
´foue
¨t et al.
(2001) showed that spectral discrimination of change was possible
between the very broad classes of ‘‘sand’’, ‘‘background’’ (rubble,
pavement, heavily grazed dead coral) and ‘‘foreground’’ (living
corals and macroalgae). Dustan et al. (2001) and Palandro et al.
(2003a,b) used spectral characteristics of Landsat-5 and -7, as well
as Ikonos, to identify a continuous decline in coral cover in response
to repeated bleaching and diseases. A bleaching-specific study on
a timeseries of Ikonos imagery by Elvidge et al. (2004) showed that,
under good conditions (70–90% coral cover), image differencing
was indeed successful. Yamano and Tamura (2002, 2004) explored
the limits of bleaching detectability of Landsat TM after atmo-
spheric correction and found that if 25–55% of coral cover was
bleached detection was possible in band 1. Holden et al. (2001) and
LeDrew et al. (2004) pioneered the use of textural characteristics
based on spatial autocorrelation, rather than relying solely on
spectral signatures, arguing that healthy reefs would be more
heterogeneous than dead reefs covered by algae. These analyses are
especially powerful with the use of time-sequential imagery, in
which changes in spatial texture can be measured as a proxy of reef
stress (LeDrew et al., 2004).
Acoustic methods have only been successful in detecting
bleaching after the fact, when coral structures have already begun
to break down. In comparison to the optical method, Riegl and
Purkis (2005) were unable to find acoustic differences between
live and dead corals in single-beam acoustic ground discrimina-
tion surveys at 50 and 200 kHz frequency. This analysis was based
on the classification of acoustic diversity of echo-shapes, and
found that, while rough seafloor (corals and/or macroalgae) could
be discriminated against bare seafloor, standing dead or live corals
could not be credibly discriminated, particularly if dead corals had
not yet disintegrated into rubble. Collier and Humber (2007)
showed, using a textural approach applied to 675 kHz sidescan
sonar (SSS) imagery, that a difference between standing corals
(dead or alive) and corals broken down to rubble could be
detected by evaluating distinct acoustic shadows formed by
upright structures. LIDAR (light detection and ranging) methods
presently do not have the ability to detect bleaching. Since they
are tuned for bathymetry they operate under the same restrictions
as the acoustic methods described above (Brock et al., 2004).
While the reflectance properties of the bottom return could
conceivably be harnessed for bleaching detection, this has not yet
been attempted.
3.2. Detecting past episodes of bleaching
If structural or geochemical clues can be found in corals or reefs,
for example on the surfaces of dead corals or in their skeletons, it
may be possible to hind-cast past bleaching events and determine
how unusual the current period of frequent and intense bleaching
events really is. Geochemical signatures pointing to bleaching in
the fossil record have so far only been established, by Wade et al.
(2008), for the tests of the Eocene planktonic foraminifer Morozo-
vella crassatus, not the skeletons of reef corals. Leder et al. (1991)
found that prolonged bleaching of Montastraea faveolata caused
a suppression of the coral’s low-density annual bands. Using the
isotopic composition of the skeleton, they were able to identify the
gap in coral growth. Halley and Hudson (2007) used hiatuses in
fluorescent and density banding of 38 cores from the northern
Florida Keys reef tract to suggest that bleaching events were rare
prior to 1980.
To go further into the geologic past and reconstruct bleaching
events remains problematic. Greenstein (2007) reviews the
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 9
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

taphonomic signatures that exist in (sub-)fossil coral assemblages.
At present, no signals have been identified that would allow
unequivocal identification of bleaching in these records. Clear
signatures of mass mortality and associated shifts in coral commu-
nity structure, have been detected (Bahamas: Curran et al., 1994;
Belize: Aronson et al., 2002, 2004; Jamaica: Wapnick et al., 2004).
While the taphonomic signature clearly points to rapid death
(Aronson et al., 2002) what exactly killed these corals remains
problematic, with some researchers pointing to diseases, while
others suggest episodes of bleaching that facilitate epizootics (Lesser
et al., 2007). Pandolfi (1999) documented the apparent persistence
of coral communitystructure throughout thePleistocene, and, given
the dramatic changes of recent years caused in part by bleaching
events, Pandolfi and Jackson (2006) concluded that anthropogenic
effects were responsible for these changes.
4. Ecological effects of coral reef bleaching
Here we examine the immediate (hours to days) ecological
responses of reef corals and other biota to bleaching, as well as the
more prolonged (months to years) changes affecting reef commu-
nity structure and function. Relatively few observations have been
made on the immediate ecological effects of coral reef bleaching,
compared with longer-term responses of these communities.
4.1. Immediate effects
4.1.1. Coral associates
Bleaching and mortality of reef corals can have severe
effects on numerous species that live in close association with
these hosts. Obligate crustacean symbionts of corals were
observed to die several days following the onset of bleaching
when food supplies, mainly mucus and entrapped detritus and
microorganisms, were declining or no longer available (Glynn
et al., 1985). Coral host colonies assessed during the 1982–83
bleaching event in Panama
´showed significant declines in
mucus production and the disappearance of crustacean
symbionts as their condition deteriorated (Fig. 7). The feeding
behavior of Trapezia crabs also changed from gathering mucus
from healthy colonies to suspension feeding on bleached
colonies (S. Gilchrist in Glynn, 1990a). As corals continue to live
in a weakened state, or die, numerous metazoan associates also
die on their host colonies, or emigrate from them. Crustaceans
leaving colonies experience an increased risk of predation
(Castro, 1978). In assessing the effects of mass coral bleaching
on the obligate symbionts of pocilloporid and acroporid corals,
Tsuchiya et al. (1992), Tsuchiya (1999),andIglesias-Prieto et al.
(2003) found that the following taxa were significantly reduced
in abundance (or disappeared entirely) from bleached and dead
corals: brachyuran crustaceans (Trapezia:6species;Tetralia:4
species; Cymo: 2 species); gobiid fishes (Paragobiodon:likely
two species).
Large numbers of other obligate symbionts and parasites asso-
ciated with pocilloporid, acroporid and other coral genera, such as
ciliate protozoans, flatworms, copepods, cirripeds, decapod crus-
taceans (crabs, shrimps), and fishes (Bruce, 1976; Patton, 1976;
Castro, 1988) likelyalso experience high mortality during bleaching
events. Recent studies offer evidence that some species of
eukaryotic and prokaryotic (Eubacteria and Archaea) microorgan-
isms associate specifically with certain coral hosts (Rohwer et al.,
2002; Knowlton and Rohwer, 2003). If some of these protists and
microbes are restricted to particular coral species, they are also
likely to disappear with the demise of their hosts.
The shedding of zooxanthellae, during the initial phases of
bleaching, is evident as mucus strings or organic aggregates that
separate from the colony’s soft tissues. This expulsion activity,
which can be accompanied by the sloughing of coral tissues, can be
substantial, and contributes large amounts of particulate organic
matter to reef waters. This potential food source, plus associated
moribund and dead metazoans (see above), attracts large numbers
of opportunistic omnivorous fishes such as wrasses, pomacentrids
and haemulids (Eakin et al., 1989).
4.1.2. Tissue and skeletal growth
As a result of less autotrophic inputs due to reduced of photo-
synthesis, tissue growth, regeneration and calcification are
compromised during bleaching events. Bleached corals often
recover and survive following periods of warm water stress, but
tissue and skeletal growth typically decline, or cease altogether,
during these events. Compared to normally-pigmented tissues,
bleached tissues demonstrate reduced biomass and thickness
(Porter et al., 1989; Fitt et al., 1993; Mendes and Woodley, 2002),
and also have lower concentrations of lipid, protein and carbohy-
drate (Glynn et al., 1985; Szmant and Gassman, 1990). While highly
variable among species, field experiments in the Caribbean have
shown that bleached corals regenerate tissue lesions more slowly
than unbleached corals (Meesters and Bak, 1993; Mascarelli and
Bunkley-Williams, 1999). Skeletal growth was greatly reduced in
bleached massive corals in Florida (Leder et al., 1991), Jamaica
(Goreau and Macfarlane, 1990;Mendes and Woodley, 2002),
Thailand (Tudhope et al., 1992) and the Ryukyu Islands (Suzuki
et al., 2000). When bleaching was severe and prolonged, colonies
experienced partial to complete loss of the annual skeletal banding
over the period of stress. The interruption of skeletogenesis during
strong ENSO warming events prevents isotopic analyses; stress
bands instead characterize these periods (Wellington and Dunbar,
(8)
(8) (8)
(8)
0.02>P>0.01 p<0.01
0
DFBPBN DFBPBN
0.3
0.2
0.1
(10)
(10)
(19)
(10)
10
20
Mucus released
(ml.100cm
-3
.10min
-1
)
Crustacean density
(no.col
-1
)
ab
Fig. 7. Decline in mucus release (a) and abundances of obligate crustacean crab (Trapezia spp.) and shrimp (Alpheus lottini) symbionts (b) as a function of coral host condition during
the 1983 El Nin
˜o bleaching event in Panama
´(after Glynn, 1985b). Median values, 0.95 confidence limits of medians, and number of colonies sampled (in parentheses) shown for
each condition. Kruskal–Wallis significance levels are indicated on each plot; horizontal lines along abscissas join statistically equal median values (multiple comparisons procedure,
a
¼0.15). Coral condition: N, normal with full pigmentation; PB, partially bleached; FB, fully bleached; D, dead.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3710
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

1995). In bleached colonies exhibiting some skeletal growth,
carbon and oxygen isotopic signatures suggested that elevated
water temperatures were accompanied by reduced energy inputs
from zooxanthellae during the bleaching period.
4.1.3. Coral disease
Bleaching weakens corals and, in combination with other
secondary stressors, may lead to a series of problems that result in
an overall decline in coral health, including increased incidence of
disease (Lesser et al., 2007). Coral diseases have been observed to
correlate with bleaching and/or heat stress, and as corals undergo
thermal stress (Lesser, 2004), bacteria can increase in virulence and
antibiotic resistance (Martinez and Baquero, 2002; Rosenberg and
Ben-Haim, 2002; Ben-Haim et al., 2003). On the Great Barrier Reef,
Selig et al. (2006) and Bruno et al. (2007) found that disease
outbreaks were facilitated by positive temperature anomalies and
previous bleaching. They also observed that the densest coral cover
correlated with the highest frequency of disease. Coles and Seapy
(1998) observed a high frequency of tumors on corals exposed to
high temperatures at Fahl Island in Oman, and Riegl (2002)
observed a decline in the frequency of coral diseases, after high
initial infection levels, following a major bleaching event in the
Arabian Gulf. He attributed this to the most frequently diseased
corals (six species in the genus Acropora) having all but disappeared
from the affected coral communities. He also found that diseases in
the region that were previously specific to Acropora, such as Black
Band Disease, had completely disappeared from the area, while
non-specific diseases remained at lower densities. Such decreases
in disease frequency have also been observed by Richardson (1998).
Reshef et al. (2006) have suggested that the failure of the bleaching
pathogen Vibrio shiloi to infect previously susceptible corals is
a sign of newly-developed resistance.
4.1.4. Coral mortality
Coral mortality varies greatly among bleaching events, across
large and small spatial scales, and according to the affected taxa.
Additionally, coral colonies may suffer from partial or absolute
mortality. In the former instance, parts of colonies die, and in the
latter entire colonies succumb. Large colonies often experience
partial mortality whereas entire small colonies may suffer absolute
mortality. In general, coral mortality is low (Harriott, 1985) and
nearly all corals recover (Gates, 1990) from bleaching following
mild events when temperature anomalies are minor and short-
lived. Severe bleaching events may result in near 100% mortality
with local extirpations of some taxa. For example, on oceanic
islands in the eastern Pacific, overall coral mortality due to the
1982–83 El Nin
˜o bleaching event amounted to 90% at Cocos Island
(Guzma
´n and Corte
´s, 1992) and 97% inthe Gala
´pagos Islands (Glynn
et al., 1988). Notably high coral mortality was also reported by Riegl
(1999) with near-total extirpation of six species of Acropora from
the southeastern Arabian Gulf (United Arab Emirates and Qatar) in
1996 (mortality >90%), which after nearly a decade had only
recovered in a small area (Burt et al., 2008).
4.2. Longer term effects
4.2.1. Coral reproduction and recruitment
Corals that recover from bleaching with no mortality can
nevertheless experience significant long-term sublethal effects.
Following the 1987–88 bleaching event in the Caribbean, the
predominant frame-building coral Montastraea annularis failed to
complete gametogenesis during the reproductive period (Szmant
and Gassman, 1990). Most reef flat corals that bleached during the
1998 bleaching event at Heron Island (Great Barrier Reef) demon-
strated a reduction in percent fertile polyps and number of eggs per
polyp (Ward et al., 2000). Fertilization success declined in
acroporid corals in Okinawa, also following the 1998 bleaching
event. Omori et al. (2001) hypothesized that the significant decline
in fertilization in 1999 was due to decreased sperm motility,
probably a result of energy depletion caused by the loss of
zooxanthellae during bleaching in 1998. Unexpectedly, a Hawaiian
coral (Montipora capitata) that bleached in 2004 completed
gametogenesis and spawned normally in 2005 (Cox, 2007). Since
this species is capable of significant heterotrophic suspension
feeding on allochthonous energy sources (Grotolli et al., 2004,
2006), it is likely that its reproductive activities were not
compromised.
Surveys conducted after severe bleaching events in Belize
(Mumby, 1999) and southern Japan (Loya et al., 2001; van Woesik
et al., 2004) showed juvenile and small colonies of some species
surviving better than large colonies. In the Arabian Gulf, Riegl
(2002) encountered Acropora recruitment from 1998 onwards.
Since the majority of Acropora had died in 1996 and 1998, colonies
must have spawned prior to death and larvae/recruits survived
serious temperature stress. Fadlallah et al. (1992) and Fadlallah
(1996) observed Saudi Arabian Acropora spawning despite a major
cold event, which caused Acropora mortality, so potentially the
same could happen during heat stress. Some young colonies
survived the 1998 bleaching, which killed adults, to reach the
documented sizes in 1999 (Riegl, 2002). If bleaching disturbances
indeed increase in frequency (Hoegh-Guldberg,1999; Hughes et al.,
2003; Sheppard, 2003; Done and Jones, 2006; Hoegh-Guldberg
et al., 2007; Kleypas, 2007; Riegl, 2007), stable age distribution
could shift toward juvenile and small colonies that would be pre-
reproductive or display lower fecundities (Done, 1999). This may
not be true of all species or locations: based on coral population
responses to non-climate stressors, such as sedimentation,
turbidity and nutrient loading in Curaçao and Florida, Bak and
Meesters (1999) hypothesized that deteriorating global change
conditions would favor the survival of large colonies and thus
gamete output and reproductive success.
In addition to interrupted or compromised reproduction, Bassim
et al. (2002) showed developmental aberrations during embryo-
genesis in a coral in the Gulf of Mexico. Additional reproductive
implications also arise from shrinking populations following large
scale mortality, and Knowlton (2001) has drawn attention to the
Allee effect, whereby reduced abundance of reproducing species
results in fewer gametes being released and failed fertilization due
to the low concentration of spawn. In conclusion, these findings
indicate that coral reproduction can be compromised at several
levels during and following a bleaching episode. Any one of these
setbacks can lead to reduced recruitment, but the levels remain
elusive.
The effects of mildly increased temperatures on corals (insuffi-
cient to cause visible bleaching) are less clear-cut. In at least two
regions moderate temperature increases have been associated with
neutral to positive effects on gonad development, spawning, and
recruitment success. In the eastern Pacific, gonad development has
proceeded normally in some coral species during mild El Nin
˜o
conditions (Colley et al., 2004). In Panama
´, annual coral recruitment
was highest in an agariciid coral (Pavona varians) during the 1990s,
when monthly maximum temperature anomalies (MMTAs) were
elevated, ranging between 0.5 and 1.5

C(Glynn et al., 2000).
Recruitment failed in 1983, following the very strong 1982–83 El
Nin
˜o event when MMTAs reached 1.9

C. A high recruitment event
on a Maldivian reef 21 months after the severe bleaching event of
1998 was hypothesized to be the result of a non-stressful increase
in temperature that caused mass spawning (Loch et al., 2002;
Schuhmacher et al., 2005). As in Panama
´, post-bleaching recruit-
ment was especially high among agariciid species with Pavona
varians ranking highest. A similar shift in recruitment from previ-
ously dominant acroporid and pocilloporid species to agariciids
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 11
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

was reported by McClanahan (2000a) and Zahir et al. (2002) for
other areas in the Maldives.
4.2.2. Differences in coral bleaching response related to coral
taxonomy, morphology and size
Changes in coral community structure following bleaching can
take two forms, namely: (1) changes in the relative abundances of
surviving zooxanthellate corals, and (2) changes in the dominance
of non-coral taxa associated with reef assemblages. When
pronounced and long-lasting, the latter changes are termed phase
shifts and can lead to fundamental differences in the structure of
reef communities. Phase shifts can result from a variety of distur-
bances, such as overfishing, epizootics, predatory sea star outbreaks
and eutrophication, as well as coral reef bleaching.
Surveys conducted over a broad range of habitats, biogeographic
regions and different sea warming events have demonstrated that
scleractinian corals with branching colony morphologies generally
suffer higher rates of mortality than species with massive and
encrusting morphologies (Glynn, 1983, 1990a; Corte
´s et al., 1984;
Brown and Suharsono, 1990; Jokiel and Coles, 1990; Hoegh-Guld-
berg and Salvat, 1995; Fujioka, 1999; Marshall and Baird, 2000;
McClanahan, 2000a; Wilkinson, 2000; Loya et al., 2001; Loch et al.,
2002; McClanahan and Maina, 2003). Coral species with massive
and encrusting morphologies frequently bleach during periods of
elevated temperature, but they also often demonstrate a high rate
of survival, and it has been hypothesized that these species provide
greater mass-transfer efficiency, facilitating the removal of poten-
tially damaging cellular toxins (Loya et al., 2001; Nakamura and van
Woesik, 2001). Massive corals with thick tissue that penetrates
deeply into the coral skeleton, such as Porites, may also afford
zooxanthellae with a greater degree of photoprotection (Salvat,
1992; Gleason, 1993; Glynn, 1993; Hoegh-Guldberg and Salvat,
1995).
Field observations supporting differential mortality of branch-
ing and massive species have been supported experimentally for
five species in the eastern Pacific (Hueerkamp et al., 2001). Massive
species of Porites and Diploastrea are frequently among the survi-
vors (McClanahan and Maina, 2003; Schuhmacher et al., 2005).
Favia spp. often survive, as do non-branching species in the family
Agariciidae (McClanahan, 2000a; Loya et al., 2001; Loch et al.,
2002). Large massive colonies often experience partial mortality,
with patches of dead skeletal areas interspersed among live
patches. As the live patches continue to grow vertically and spread
laterally, the dead surfaces eventually disappear. It should be noted
that no species are immune from bleaching-induced mortality and
virtually all genera have suffered high mortality during severe
bleaching events in one location or another. For example, in French
Polynesia whole colony mortality of massive Porites spp. in 1998
amounted to 25% at one sampling site, and 40–80% loss of live cover
at two other sites (Mumby et al., 2001b). Some of the larger colonies
were up to 8 m in diameter and were estimated to be hundreds of
years old. Numerous large massive colonies (Porites lobata and
Pavona clavus) died in the Gala
´pagos Islands during the 1982–83 El
Nin
˜o warming event. Many of these colonies were between 200
and 400 years of age (Glynn, 1990a). In the Java Sea, Brown (1997a)
observed that community composition changed from sensitive
Acropora to resistant Porites.
McClanahan et al. (2007b) studied sites across the Indian Ocean
and used coral community structure as a proxy for past distur-
bance, largely based on observed patterns of taxon-specific
susceptibility to bleaching (Loya et al., 2001; McClanahan, 2004).
Sites with high cover of Acropora and Montipora were considered to
have experienced low frequency of bleaching. Porites and Pavona
were identified as relatively bleaching resistant, and Pavona and
Pocillopora as resilient, with high post-bleaching recruitment.
Monospecific genera of small colony size (Gyrosmilia,Oxypora,
Plesiastrea,Plerogyra,Physogyra) were identified as in relatively
high danger of extinction due to susceptibility to bleaching and
relative rareness. Other more bleaching-susceptible genera (such as
Stylophora,Acropora,Pocillopora) were not considered as much at
risk of extinction due to their overall abundance over wide regions.
However, with increased bleaching frequency their abundances
might decline. While Acropora may be less threatened in the Indo-
Pacific, Caribbean populations have suffered dramatic reductions in
population size (w97% range wide), to the extent that they have
now been listed as ‘‘threatened’’ under the U.S. Endangered Species
Act (see Bruckner, 2003). Whether caused primarily by bleaching
(Lesser et al., 2007) or diseases (Aronson et al., 1998), these changes
have led to phase-shifts away from coral dominance in many
regions (Hughes, 1994), and are leading to persistent changes in
coral community structure in others (Aronson et al., 2002, 2004).
Hydrocorals (Millepora spp.), especially those species with
branching or upright platy colony morphologies, also experience
high mortality rates and can even disappear locally in some areas
(McClanahan, 2000a; Loya et al., 2001; Mate
´, 2003; McClanahan
and Maina, 2003; Schuhmacher et al., 2005). Millepora boschmai,
initially considered to be an eastern Pacific endemic species, could
not be found several years after its disappearance following the
1982–83 El Nin
˜o bleaching event. This led Glynn and de Weerdt
(1991) to conclude incorrectly that the species was extinct, which
would have represented the first documented zooxanthellate coral
extinction. A few years later a small population (five colonies) was
discovered in the Gulf of Chiriquı
´(Glynn and Feingold, 1992).
Continuing monitoring revealed that all colonies in this remnant
population died during the 1997–98 El Nin
˜o bleaching event. Also,
formerly known colonies elsewhere in the Gulf of Chiriquı
´could
not be found after 1998 (Mate
´,2003). With the discovery of a few
living colonies of M. boschmai in Indonesia (Razak and Hoeksema,
2003), this species is now possibly only regionally extirpated.
Another widespread Indo-Pacific hydrocoral that disappeared from
the Gulf of Chiriquı
´after 1982–83 was Millepora platyphylla. This
species was known only from a single reef and may now be absent
from the eastern Pacific.
Scleractinian corals can also temporarily disappear from local
faunas. Riegl (1999, 2002) demonstrated the loss of six species of
Acropora from the SE Arabian Gulf after the 1996 mass bleaching
event. Burt et al. (2008) demonstrated local recovery of these
species a decade later. In contrast, Lambo and Ormond (2006)
observed continuous decline in coral cover and generic richness on
a Kenyan coral reef.
Size can also play a role in determining patterns of mortality on
bleached reefs. As discussed in Section 4.2.1, small juvenile colonies
of some species can survive better than large, mature colonies
(Mumby, 1999; Loya et al., 2001; Riegl, 2002; van Woesik et al.,
2004). Consequently, repetitive bleaching events might shift the
stable age distribution toward smaller colonies with lower fecun-
dities (Done, 1999), in turn hindering the recovery of these reefs.
However, this may not be true of all sites and species, and may vary
according to how other environmental stressors interact with
bleaching: Bak and Meesters (1999) suggested that large colonies
might be more resistant than small colonies to environmental
disturbances, such as nutrients and sedimentation, with greater
potential for continued gamete output and reproductive success
post-disturbance.
4.2.3. Changes in algal symbiont communities
Coral bleaching is characteristically patchy, and may uniformly
affect entire colonies or only certain areas, such as the sides,
summits or terminal branches (Fig. 8). In some cases this has been
shown to be the result of the interaction between environmental
stressors and the patchy distribution and/or zonation of different
Symbiodinium within and among coral species (Rowan and
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3712
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Knowlton, 1995; Rowan et al., 1997). Because different types of
symbiont can respond differently to environmental stressors, the
distribution of symbiont diversity within and among coral colonies
and species can influence patterns of bleaching and result in
changes in these communities following a bleaching event. For
example, Symbiodinium in clade D (particularly D1a) are resistant to
elevated temperature conditions (Rowan, 2004) and may remain in
coral host tissues when other symbiont clades are depleted or
disappear (e.g., Baker, 2001; Glynn et al., 2001; Baker at al., 2004;
Berkelmans and van Oppen, 2006; Jones et al., 2008). The processes
by which these residual symbionts recover in bleached coral
tissues, and the potential for succession within these communities
during recovery, have not been widely investigated (but see Toller
et al., 2001;Thornhill et al., 2006a,b). These processes are of critical
importance to understanding how reef coral symbioses respond to
bleaching events.
Buddemeier and Fautin (1993) were the first to explicitly
suggest that changes in algal symbiont communities (Symbiodi-
nium spp.) following bleaching might be a mechanism which helps
corals adapt to environmental change (but see earlier speculation
by Gladfelter (1988) and Sandeman (1988) on the role of symbiont
diversity in explaining within-colony bleaching variability). Since
that time, studies of symbiont shifts occurring in response to
bleaching have reached different conclusions, with some studies
documenting changes and others not.
For example, Goulet and Coffroth (2003) in a study of eight
colonies of the gorgonian coral Plexaura kuna following a bleaching
event in 1995 found no evidence of symbiont change, and Iglesias-
Prieto et al. (2004), transplanting two species of scleractinian corals
between different depths on eastern Pacific reefs also found no
change in symbionts as a result of the transplantation (although no
bleaching or heat stress was involved). A number of other single
observations of stable symbiont distributions over long-term time
scales have also been interpreted as supporting the notion that the
coral species in question are incapable of changing symbiont types.
For example, LaJeunesse et al. (2004) found one colony of Porites
compressa in Hawaii that, 10 years after transplantation from deep to
shallow water, contained the same symbiont type as its conspecifics
at shallow sites, and also found one colony of Fungia scutaria that
continued to host an exclusively Pacific symbiont 35 years after its
transplantation to a Jamaican reef (LaJeunesse et al., 2005).
Nevertheless, a growing number of larger studies involving
important reef coral species support the idea that changes in
symbiont communities can and do occur in response to environ-
mental variation, particularly that which causes coral bleaching. For
example, Baker (2001) recorded shifts in symbiont communities in
several common species of Caribbean coral following bleaching due
to irradiance stress, and showed that corals which changed their
symbiont communities as a result of bleaching experienced less
mortality. Glynn et al. (2001) showed that colonies of Pocillopora in
Panama
´containing Symbiodinium in clade D did not bleach during
the 1997–98 bleaching event, whereas colonies that contained
Symbiodinium in clade C bleached severely.
Baker et al. (2004), monitoring the same Panamanian Pocillopora
between 1995 and 2001, showed that Symbiodinium in clade D had
become more common in these corals after the 1997–98 bleaching
event. They also found that these symbionts were common on reefs
recently devastated by coral bleaching (Kenya) and on reefs
routinely exposed to high temperatures (Arabian Gulf), but that
they were relatively rare on reefs not exposed to high temperatures
(Red Sea), or without a history of recent severe bleaching (Maur-
itius). Taking this evidence jointly, they concluded that bleaching
can result in adaptive shifts in symbiont communities to favor the
dominance of more heat tolerant Symbiodinium in clade D.
Berkelmans and van Oppen (2006) found that transplanting
Acropora millepora from cooler to warmer sites on the Great Barrier
Reef resulted in a change in their symbiont communities to favor
Symbiodinium in clade D, and that this transition increased their
thermal tolerance by up to 1.5

C. Jones et al. (2008), in a study of
460 colonies of A. millepora during a bleaching event, showed that
71% of these colonies changed their symbiont communities to favor
more heat tolerant types following a natural bleaching event, with
many corals shuffling pre-existing symbiont communities at the
colony level to achieve this.
It is clear that not all stressors result in changes in symbiont
communities, and that different taxa vary in their likelihood of
Fig. 8. (a, b) Colonies of Caribbean Montastraea faveolata at 4–6 m depth in the San
Blas Islands, Panama
´, in February 1996, 4–5 months after initial bleaching in late 1995.
Clear within-colony variability in bleaching is visible; with most bleached tissue still
alive after this extended period. Red arrows show areas of partial mortality caused by
bleaching. Yellow arrows indicate areas of tissue that are regaining pigmentation faster
than surrounding areas. The patchy recovery of Symbiodinium communities in
bleached tissues is commonly observed, but processes of symbiont community
assembly and succession have not been widely investigated.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 13
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

exhibiting changes Thornhill et al., 2006b;(Baker and Romanski,
2007; but see also Goulet, 2006, 2007). Nonetheless, the growing
number of studies documenting these changes in response to
bleaching events, and the increasing number of reef coral species
found to be capable of hosting Symbiodinium in clade D (Mieog et al.,
2007) indicate that these changes do indeed occur and are likely to
be important response mechanisms for many coral species. We
discuss the adaptive significance of these changes in Section 7.1.2.
4.2.4. Corallivores
Coral community structure can also be influenced by the
changing abundance of other reef associates affected during
bleaching events. Such effects may begin soon after coral
mortalities and continue for several years. While many reef-
associated species die during the disturbance event (see above),
others are unaffected, and some appear to increase in numbers.
For example, in Panama
´, an area highly impacted in 1982–83,
warming increased mortality of a gastropod corallivore (Jenneria
pustulata)byw94% but did not alter the mortality of a coral-
eating echinoderm (Acanthaster planci)andfish(Arothron
meleagris)(Glynn, 1985a). These differences in survivorship
reduced coral predation by Jenneria, but increased predation by
Acanthaster and Arothron, due to the lower abundances of their
prey. In the Indo-Pacific, Drupella spp., obligate gastropod cor-
allivores, have a strong preference for acroporid corals (Turner,
1994). The abundance of this gastropod is unaffected by high
temperatures that cause coral bleaching. It typically aggregates
around corals damaged by cyclones, diseases and elevated
temperature events (Ayling and Ayling, 1992; Antonius and Riegl,
1997; Baird, 1999). Morton et al. (2002) suggested that the
increased release of mucus and other cellular products by injured
corals may attract the predatory snails, causing concentrated
feeding resulting in high local coral mortality.
Perhaps of greater concern is the asteroid sea star Acanthaster
planci, which has undergone population outbreaks (unrelated to
coral reef bleaching) on numerous reefs in the Indo-Pacific region
since at least the 1950s (Moran, 1986; Birkeland and Lucas, 1990).
Acanthaster is much larger than Drupella, and individuals have been
estimated to consume 5–13 m
2
of coral per year in different
regions. Some of these outbreaks have involved hundreds of
thousands of sea stars that greatly reduce coral cover on entire reefs
and across large reef tracts, such as in the Ryukyus Islands, Palau,
and along the Great Barrier Reef. Like Drupella, this sea star pred-
ator feeds preferentially on several coral species that are highly
susceptible to bleaching. Declines in coral cover after bleaching
result in reduced prey abundances for populations of both
Acanthaster and Drupella spp., whose numbers remain steady
through disturbance events. Therefore, the feeding effects of these
corallivores become more concentrated on the remaining corals.
Such delayed predation has been reported in the eastern Pacific
(Glynn, 1985b; Guzma
´n and Corte
´s, 2001), the central and western
Pacific (van Woesik et al., 2004; Wilkinson, 2004) and Indian Ocean
(McClanahan et al., 2000).
4.2.5. Reef fishes
The responses of reef fishes to coral bleaching are highly varied,
depending in large part on the particular resources affected. The
effects are dominantly indirect, since moderate SST increases
appear to have little or no direct impact on adult fish mortality.
Instead, sublethal physiological effects can reduce fitness, such as
growth rate, body size at maturity, competitive ability, and fecun-
dity (Pratchett et al., 2004; Berumen et al., 2005). Bellwood et al.
(2006) have emphasized the importance of considering individual
species responses because variations in fish community metrics
such as abundance, species richness and diversity, may give poor
indications of impacts on particular taxa and guilds. Fish responses
to bleaching depend upon specific resource use and the coral taxa
affected. Reef fish communities are made up of corallivores, coral
dwellers, herbivores, omnivores, invertivores, piscivores and
planktivores, all with different resource requirements. We consider
first the responses of fish corallivores, which feed directly on coral
tissues.
Obligate corallivores, species in the families Gobiidae, Poma-
centridae, Monacanthidae and Chaetodontidae, generally die
within weeks of the disappearance of their coral prey and habitat
niche (Spalding and Jarvis, 1998; Shibuno et al., 1999, 2002; Kokita
and Nakazono, 2001; Sano, 2004). For example, a study reef at
Iriomote Island (Ryukyu Islands) that experienced severe coral
bleaching in August 1998 had lost five species of fish corallivores
when sampled in October (Sano, 2004). Fish abundances in other
trophic categories at Iriomote (herbivores, omnivores, and benthic
animal feeders) did not show statistically significant differences
over pre- and post-bleaching sampling periods. Some corallivore
species do not experience declines in abundance during and
following bleaching events that deplete their usual coral prey. Such
species are facultative corallivores and are capable of switching
their diets to include other coral species and/or non-coral prey
(Guzma
´n and Robertson, 1989; Pratchett et al., 2008). In addition,
coral associated fishes that require coral structure for shelter,
reproduction or larval settlement sites have shown marked
declines following habitat loss (Bellwood et al., 2006).
Some studies have reported increases in fish herbivore abun-
dance after bleaching events, and such responses would be
expected with increases in algae that colonize dead coral substrates
(Lindahl et al., 2001). Fish herbivore abundance responses are not
straightforward due to the different functional feeding groups
present, the type of algae replacing live coral, the mobility of
schooling herbivores, and the disconnect between planktonic larval
stages and juvenile and adult stages. An additional factor is the loss
of live coral, which is used by parrotfishes as shelter when inactive
at night (Randall et al., 1990). Two meta-analyses have concluded
that about one-half of reef fish herbivores, including species of
parrotfish, surgeonfish and damselfish, actually decline signifi-
cantly in abundance following coral bleaching (Wilson et al., 2006;
Pratchett et al., 2008). Declines in abundance may occur if frondose
macroalgae become more abundant than filamentous algal turfs,
which are typically preferred by fish herbivores (Ledlie et al., 2007).
Also, large herbivores may move away from disturbed sites in
search of more favorable feeding areas. Non-specialist fishes that
feed on a wide range of prey, e.g. invertivores, detritivores and
planktivores, may show short-lived post-disturbance increases in
abundance (Wilson et al., 2006).
More subtle than changes in adult fish abundances are the
negative effects on recruits in the aftermath of bleaching (Booth
and Beretta, 2002; Feary et al., 2007a,b; Ledlie et al., 2007). Fish
recruits that do not depend critically on live or dead coral cover as
adults were found to decline in abundance in reef areas of degraded
coral (Jones et al., 2004; Feary et al., 2007b). On Indo-Pacific reefs,
about 60% of early developmental stages associate with live coral
(Jones et al., 2004). This emphasizes the importance of the struc-
tural integrity of coral habitats following bleaching disturbances.
Suitable settlement sites are necessary to replenish the diverse
feeding guilds that are characteristic of healthy, pre-disturbance
reef fish communities. It is clear, from these studies, that responses
of numerous fish species following bleaching are dependent on
whether the structural integrity of coral reefs remains intact
following a bleaching event (Wilson et al., 2006; Munday et al.,
2007; Pratchett et al., 2008, 2009).
4.2.6. Bioerosion
Bioerosion, the biological breakdown of limestone skeletons and
reef frameworks, is a result of activity by a suite of taxonomically
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3714
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

diverse endolithic borers (such as photosynthetic algae, hetero-
trophic fungi and bacteria, sponges, polychaete worms, mollusks
and crustaceans), and epibenthic metazoans (such as mollusks,
echinoids and fishes) (Steneck, 1983; Hutchings, 1986; Perry and
Hepburn, 2008). Bioerosion is commonly in close balance with reef
accretion (Highsmith, 1980; Hallock and Schlager, 1986; Glynn,
1997; Hubbard, 1997). Calcification in healthy coral reefs outpaces
bioerosion and thus maintains positive reef accretion. Reefs subject
to a variety of disturbances that cause significant declines in live
coral cover, such as eutrophication, sedimentation, epizootics and
bleaching, can quickly transition to an erosional state resulting in
a loss of structural integrity and topographic relief. Following are
examples of coral reef bioerosion resulting from coral mortality due
to high temperature bleaching.
Detailed studies in the Gala
´pagos Islands have demonstrated the
effects of rapid bioerosion on coral after bleaching-related death
(Table 1). External bioerosion, mainly by the sea urchin (Eucidaris
galapagensis) grazing on algal-coated dead coral skeletons, was
responsible for 70–80% of a mean total erosion of 34 kg m
2
y
1
of
pocilloporid corals (Glynn, 1988), and for 90% of the mean total
erosion of 25 kg m
2
y
1
of poritid corals (Reaka-Kudla et al., 1996).
Mean sea urchin abundances were between 40 and 60 ind m
2
at
the sites investigated. Once incorporated with estimates of CaCO
3
production and sediment retention, these data can be used to
calculate the erosional loss of reef frameworks. In the central and
southern Gala
´pagos Islands, rates of bioerosion exceeded net
carbonate production rates, resulting in the loss of reef framework
structures over a w10 year period (Glynn,1994, 2003). Eakin (1996)
studied whole reef erosion post-bleaching in Pacific Panama
´, and
showed that Diadema mexicanum, the main sea urchin bioeroder,
was responsible for w17% of the total bioerosion. Fishes and
internal borers (sponges and bivalve mollusks) caused w11% and
w72% of the remaining bioerosion respectively. The presence of
damselfish and their aggressive defense of algal lawns, helped to
alleviate sea urchin and fish abrasion. A reef that had been
depositional (0.34 kg m
2
y
1
) prior to the 1982–83 bleaching
event, subsequently became erosional (0.19 kg m
2
y
1
). Re-
analysis after the 1997–98 El Nin
˜o bleaching event again demon-
strated that the reef continued in an erosional state, with net
erosion ¼0.36 kg m
2
y
1
(Eakin, 2001).
Contributing significantly to the more recent erosion were low
tidal exposures events in 1989 and 1993, which resulted in high
coral mortality on the reef flat. Other reefs in the equatorial eastern
Pacific that experienced high levels of bioerosion after the 1982–83
El Nin
˜o were those along the mainland of Costa Rica (Scott et al.,
1988; Corte
´s and Jime
´nez, 2003), Cocos Island (Macintyre et al.,
1992; Guzma
´n and Corte
´s, 2007), and mainland Ecuador (Glynn,
2003). Mean internal bioerosion rates were similar in Panama
´and
Costa Rica, 8.6 and 9.0 kg m
2
y
1
respectively (Table 1). Several
eastern Pacific areas have not experienced significant reef frame-
work erosion, e.g., Colombia (Zapata and Vargas-A
´ngel, 2003) and
Mexico (Reyes-Bonilla, 2001, 2003). Those areas that experienced
severe framework degradation or loss were subject to intense sea
urchin grazing and low rates of coral recruitment. This led Colgan
(1990) to hypothesize that El Nin
˜o warming events causing coral
mortality followed by the loss of reef structures through bioerosion,
are responsible for the paucity of structural reefs in much of the
eastern Pacific region.
Other reported reefs that experienced significant bioerosion
following climate-related bleaching have been identified in the
Indian Ocean and adjacent areas. Riegl (2001, 2002, 2007)
demonstrated the breakdown sequence of Arabian Gulf Acropora
frameworks killed in 1996 and by earlier disturbances, and found
complete removal of frameworks in 10–15 years. The sequence of
events, similar to many other regions, was one of erosion of
superficial structures in the first year after death, then moderate
carbonate accretion due to the settlement of bivalves, calcareous
algae and other corals, but finally breakdown due largely to
mechanical weakening caused by boring sponges, bivalves, and
other endolithic organisms.
In the Seychelles, bleaching in 1998 reduced live coral cover by up
to 90% over large areas. By 2005 these reef areas had been trans-
formed into rubble and algal-dominated communities, with struc-
tural complexity diminished by 10 to 50% (Graham et al., 2006). Coral
bleaching in the Maldives in 1998 caused high mortality (w97%) of
branching species (Schuhmacher et al., 2005). This resulted in the
transformation of the three-dimensional structure of reef flat and
upper reef slope zones into a rubble field in 6 years. Acropora colo-
nies with spreading, table-like branches were among the abundant
affected species, and by 2004 all of these had collapsed. Bioerosion
caused the weakening of their pedestal supports, and the weight of
coral recruits that settled and grew on the dead branches exacer-
bated their weakened condition. Williams et al. (1999) predicted the
loss of Acropora-built ramparts in the Atlantic and Pacific based on
Table 1
Bioerosion rates of coral skeletons following the 1982–83 El Nin
˜o bleaching/mortality event in the equatorial eastern Pacific. Predominant reef-building corals are listed under
‘‘Site characteristics’’ as well as coral mortality associated with the 1982–83 El Nin
˜o disturbance. Champion Island coral mortality from Wellington and Glynn (2007). Coral
mortality on Uva Island reef is based on overall (n¼21 sampling sites) mortality in the Gulf of Chiriquı
´(Glynn et al., 1988)
Location Authority Study
period
Site characteristics Bioerosion (kg m
2
y
1
)
Internal External Total Bioeroding taxa
Gala
´pagos Iss.,
Onslow
Island
Glynn
(1988)
1975–
1987
1.2 ha patch reef; 1–3 m depth; Pocillopora elegans,
Porites lobata, 99% mortality
16.0 2.7 18.1 2.6 34.1 2.6 Internal: Lithophaga spp., clionid sponges
(n¼4,
SEM)
(n¼10,
SEM)
External: Eucidaris galapagensis (25 ind m
2
),
scarid and acanthurid fishes
Gala
´pagos Iss.,
Champion
Island
Reaka-Kudla
et al. (1996)
1989–
90
0.5 km long fringing reef; 5–6 m depth, Pavona clavus,
Pavona gigantea,Porites lobata w100% mortality
2.6 0.1 22.8 2.4 25.4 2.4 Internal: Lithophaga spp., polychaete worms
(n¼18,
SEM)
(n¼18,
SEM)
External: Eucidaris galapagensis
(22–61 ind m
2
), scarid and acanthurid fishes
Panama
´,Uva
Island
Eakin (1996,
2001)
1986–
1995
2.5 ha patch reef, 1–3 m depth, Pocillopora damicornis,
P. elegans,766.5% mortality
23.9 1.9 9.2 1.7 33.2 6.0 Internal: Lithophaga spp., clionid sponges
(n¼21, SEM)
(n¼127,
0.95% CI)
a
(n¼36,
0.95% CI)
a
External: Diadema mexicanum (17.1 ind m
2
),
Arothron meleagris, scarid and acanthurid fishes
Panama
´,Uva
Island
Glynn
(1988)
1975–
1987
2.5 ha patch reef, 1–3 m depth, Pocillopora damicornis,
P. elegans,766.5% mortality
8.6 2.2 1.46 0.5 10.1 1.4 Internal: Lithophaga spp., clionid sponges
(n¼21, SEM)
(n¼23,
SEM)
(n¼54,
SEM)
External: Diadema mexicanum (20 ind m
2
),
Arothron meleagris, scarid and acanthurid fishes
Costa Rica, Can
˜o
Island
Scott et al.
(1988)
1986 1–2 ha patch reefs, 5–10 m depth, Pocillopora
damicornis,P. elegans,Porites lobata,51.210.5%
mortality
92.0 – – Internal: Lithophaga spp. (202 ind kg
1
), clionid
sponges
(n¼12, SEM)
(n¼7,
SD)
a
Internal bioerosion included the infauna and Diadema. External bioerosion included fishes and other non-echinoid motile species. These estimates are also based on 23
community composition surveys, each of which included 20 1-m
2
quadrats.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 15
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

observations that skeletons were weakened after mass mortality and
easily removed by storms. They considered this process an important
physical sign. Just how widespread this loss of coral reef structures is
awaits further study. What is known, however, is that loose coral
rubble, for example from dynamiting (Fox and Caldwell, 2006),
impedes recovery processes.
In addition to the effects of coral bleaching and mortality on reef
bioerosion, an important corollary of climate change is the acidi-
fication of surface waters as a result of increased atmospheric pCO
2
.
The associated decrease in coral calcification rate, as a result of
lower aragonite saturation state (Kleypas et al., 1999; Langdon et al.,
2000), is likely to reduce the ability of reef-builders to prevent and/
or repair damage caused by bioeroders. Consequently, the effects of
coral bleaching and mortality on bioerosional rates and processes
are likely to be magnified as a result of interacting climate change
stressors, which further decrease reef framework strength and
depress reef accumulation rates. To date, these impacts have yet to
be investigated.
5. Coral reef recovery
To date there have been no detailed global assessments of coral
reef recovery from bleaching. Wilkinson’s (2004) synopsis in the
Status of Coral Reefs of the World: 2004 summarized reports on coral
reef health by 240 contributors in 98 countries, stating that 40% of
reefs that were seriously damaged by bleaching in 1998 had either
‘‘recovered’’ or were ‘‘recovering well’’, but no further additional
quantitative assessments have yet been undertaken. Here we
attempt to synthesize the available information with the goal of
refining this assessment and comparing rates, degree and pattern
of recovery.
Previous quantitative studies of coral reef recovery from
disturbance have not focused specifically on recovery from
bleaching events. Pearson’s (1981) review of coral reef recovery and
recolonization examined several kinds of disturbance, but made no
mention of elevated sea water temperatures. Connell (1997)
examined 77 examples of recovery of coral cover worldwide from
various disturbances (e.g. predation, storms, reduction of herbivore
populations, epizootics, and bleaching). Coral bleaching, accom-
panied by high mortality, was classified as an acute disturbance
with indirect effects on the environment. Connell found that these
kinds of disturbances resulted in greater recoveryof live coral cover
compared to chronic disturbances with long-term direct effects on
the environment. Given the predicted increase in the frequency and
severity of coral reef bleaching (Hoegh-Guldberg, 1999; Lough,
2000; Buddemeier et al., 2004; Hoegh-Guldberg et al., 2007;
Kleypas, 2007), it is likely that bleaching can now be considered
a chronic disturbance in many reef regions.
In Connell’s bleaching examples, the longest recovery intervals
examined were 13 years. Here we review extended recovery periods
up to 20–25 years, and examine patterns and rates of recovery, as
well as community changes in some more recent studies. Since
recovery to pre-disturbance states (with statistically equal levels of
live coral cover, species diversity and topographic relief) may require
decades (to restore former levels of coral cover and species diversity)
to centuries (to reconstruct lost reef frameworks), we emphasize
that recovery is still ongoing in many areas. We also recognize that,
due to the chronic nature of bleaching, it is now becoming difficult to
distinguish the individual recovery trajectories of reefs exposed to
multiple sequential bleaching events.
5.1. Biogeographic differences in recovery response
The longest-running datasets on the effects of mass coral reef
bleaching begin in 1982–83 (>25 years), when the first such
episodes were documented in the eastern Pacific. Most coral
bleaching events have occurred more recently and thus have
significantly shorter recovery periods. For our synthesis, we used
datasets with recovery periods extending at least 4 years past the
bleaching event, although in some cases we included short-term
datasets (1 year and longer) that demonstrated rapid recovery. We
also only used datasets for which coral reef bleaching was associ-
ated with anomalously high sea surface temperatures, implying
thermal stress was the principal driver of bleaching. In determining
the percent live coral cover lost as a result of coral bleaching, we
only used data collected relatively soon after the bleaching
disturbance, in order to exclude mortality from other secondary
factors, such as predation by Acanthaster.
Tables 2 and 3 and Figs. 9 and 10 show the recovery trajectories
of reefs meeting these criteria. Bleaching severity and recovery
were both highly variable across a variety of spatial scales. Not
unlike the high variability observed in bioerosion, all regions
showed some degree of heterogeneity in recovery response. In the
Maldive Islands, for example, coral recovery was modest in the
northern and central islands, but pronounced in the southern
islands. This variability was sometimes observed even over small
geographic scales, with some locations on the same island or reef
(e.g. the Hithadhoo reef, Fig. 10: 6e, 6f) recovering, while adjacent
sites declined. Despite this variability, some large scale biogeo-
graphic patterns in recovery from bleaching were apparent. We
found a significant overall recovery trend in the Indian Ocean, with
46 of 58 sites (79.3%) increasing coral cover by 0.2–42.6% (mean:
8.3%) after 4.7 years (standard deviation 1.8 years). A decrease in
coral cover of 0.5–41.0% (mean: 15.0%) occurred at 12 of 58 sites
(20.7%) after 7.3 years (standard deviation 5.4 years).
In contrast, in the western Atlantic, we found a reverse trend of
continuing decline. Sixteen of 17 sites (94.1%), for which appro-
priate datasets exist, show a continuing decline in coral cover
following bleaching of 0.5–16.5% (mean: 6.6%) after 4.9 years
(standard deviation 1.8 years). One site recovered by 0.5% after
7.0 years. No clear trends in coral recovery or decline were apparent
in the eastern Pacific, the central-southern-western Pacific or the
Arabian Gulf, where some reefs declined, while others showed
evidence of recovery.
5.1.1. Recovering reefs
We found that rate of recovery among sites was variable, but
in some cases was high enough to be detected within as little as
2 years (e.g., reefs at 10 m in Hithadoo, Maldives, which recov-
ered from 40.9% coral cover after the 1998 bleaching to 51.7%
coral cover by 2000; Table 2). In other locations, recovery was
totally absent even over 20 years (Gala
´pagos, several sites,
Table 2). Surprisingly, rate of recovery did not appear to be
related to the severity of the bleaching disturbance, and the
degree of recovery was also not related to the amount of coral
cover remaining after the disturbance. Many reefs with high
coral cover continued to decline (e.g., Rarotonga in the south
Pacific declined in coral cover from 41% to 15% in 3 years; in
Costa Rica, Can
˜o island declined from 32% to 10.5% in 16 years,
while Manuel Antonio declined from 52% to 30% in 9 years; reefs
in the U.S. Virgin Islands declined from 17.2% to 8.6% in the
2000s). Other reefs with low cover regenerated notably (e.g.,
Dubai in the Arabian Gulf recovered from 0% to 42% in 9 years;
Tutuila in American Samoa in the south Pacific, recovered from
6% to 40% in 4 years).
Wellington and Glynn (2007) tabulated recovery and losses
for several eastern Pacific sites that were tracked over periods of
10–28 years. Changes in coral cover varied from total elimination
(100%), to total recovery (þ100%). Guzma
´n and Corte
´s (2007)
observed notable, but variable, recovery at Cocos Island (Costa
Rica) 20 years after the 1982–83 disturbance. Live coral cover
increased from 4% in 1987 to 23% in 2002, with the main
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3716
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Table 2
Change in percent live coral cover worldwide after major coral reef bleaching events
Region/site Authority Pre-bleaching
coral cover
Post-bleaching
coral cover
Period (years) % change Absolute magnitude
(post/pre cover)
Absolute change as
% of pre-disturbance
cover
Dominant recovering
taxa
Additional impacts
INDIAN OCEAN
Reunion Wilkinson et al., 2004
1 Planche Alizees ? 21 /61 1998–2004 (6) þ40 2.9 ? Montipora
circumvallata,Pavona
spp.
Overfishing, coastal
development, pollution
2 Trois Chamois ? 32 /28 1998–2004 (6) 4 0.9 ? Montipora circumvallata Overfishing, coastal
development, pollution
3 Corne Nord ? 57 /38 1998–2004 (6) 19 0.7 ? Acropora spp.; non-
acroporid species
Overfishing, coastal
development, pollution
Maldives Wilkinson et al., 2004
4 Northern atolls pooled (mean values)
a
? 0.8 /2.2 5–6 years þ1.4 4.6 ? Acropora spp.,
Pocillopora spp.
4a Hondaafushi (N) ? 1.6 /3.1 1998–2003 (5) þ1.5 1.9 ? As above Anchor damage, coastal
development,
eutrophication, solid
waste disposal
4b Finey (N) ? 0.7 /2.5 1998–2003 (5) þ1.8 3.6 ? As above
4c Hirimaradhoo (N) ? 0.7 /1.1 1998–2003 (5) þ0.4 1.6 ? As above
4d Velidhoo (N) ? 0.2 /2.3 1998–2004 (6) þ2.1 11.5 ? As above
5 Central atolls pooled (mean values)
a
? 2.2 /7.9 4–6 years þ5.7 3.8 ? Acropora spp.
Pocillopora spp.
5a Fesdhoo (C) ? 3.3 /27.2 1998–2004 (6) þ23.9 8.2 ? As above
5b Mayaafushi (C) ? 0.6 /4.8 1998–2004 (6) þ4.2 8.0 ? As above
5c Ambaraa (C) ? 1.2 /4.8 1998–2003 (5) þ3.6 4.0 ? As above
5d Wattaru (C) ? 2.8 /5.0 1998–2003 (5) þ2.2 1.8 ? As above
5e Foththeyo (C) ? 5.0 /9.7 1998–2003 (5) þ4.7 1.9 ? As above
5f Feydhoofinolhu (C) ? 1.7 /1.9 1998–2002 (4) þ0.2 1.1 ? As above
5g Bandos (C) ? 1.9 /6.9 1998–2002 (4) þ5.0 3.6 ? As above
5h Eydhafushi (C) ¼Udhafushi ? 1.3 /2.9 1998–2002 (4) þ1.6 2.2 ? As above
6 Southern atolls pooled (mean values)
a
26.01 /30.2 2–6 years þ4.2 1.2 Acropora spp.
Pocillopora spp.
6a Gan (S) ? 4.0 /17.0 1998–2004 (6) þ13.0 4.2 ? As above
6b Villingili (S) ? 4.3 /13.2 1998–2002 (4) þ8.9 3.1 ? As above
6c Villingili (reef slope, 10 m) ? 54.3 /61.4 2002–2004 (2) þ7.1 1.1 ? As above
6d Kooddoo (S) ? 1.0 /6.0 1998–2002 (4) þ5.0 6.0 ? As above
6e Hithadhoo (reef flat, 3 m) (S) ? 51.6 /32.0 2002–2004 (2) 19.6 0.6 ? As above
6f Hithaddoo (reef slope, 10 m) ? 40.9 /51.7 2002–2004 (2) þ10.8 1.3 ? As above
7 Maldives pooled McClanahan, 2000b 64.8 (1958) 27.5 /8.3 1992–1999 (7) 19.2 0.3 12.8 As above
East Africa McClanahan et al., 2005c
8 Mombasa 43.5 (1995) 13.5 /24.5 1999–2002 (4) þ11.0 1.8 56.3 Millepora spp.,
branching Porites,
Pavona,Montipora,
Galaxea
9 Malindi 39 9 /17 1999–2002 (4) þ8.0 1.9 43.6 Millepora, branching
Porites,Pavona
10 Watamu 38 10 /13 1999–2002 (4) þ3.0 1.3 34.2 Montipora,Galaxea
11 Vipingo 27 11 /23 1999–2002 (4) þ12.0 2.1 85.2 Branching Porites
12 Kanamai 21 17 /23 1999–2002 (4) þ6.0 1.4 109.5 Branching Porites
13 Ras Iwatine 10 3 /5 1999–2002 (4) þ2.0 1.7 50 Branching Porites
14 Diani McClanahan and Maina,
2003
?12/13 1995–2001 (6) þ1 1.1 ? Branching Porites
15 Malindi Lambo and Ormond,
2006
?46/5 1994–2004 (10) 41 0 .1 ? Galaxea,Pocillopora,
Gardineroseris,Fungia
(continued on next page)
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 17
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Table 2 (continued)
Region/site Authority Pre-bleaching
coral cover
Post-bleaching
coral cover
Period (years) % change Absolute magnitude
(post/pre cover)
Absolute change as
% of pre-disturbance
cover
Dominant recovering
taxa
Additional impacts
Madagascar Wilkinson et al., 2004
16 Reef slope ? 45 /40.5 1998–2004 (6) 4.5 0.9 ? ? Damage from
Acanthaster
17 Reef flat ? 42.5 /54 1998–2004 (6) þ11.5 1.3 ? ?
Southern Africa
18 Sodwana Bay, South Africa Celliers and Schleyer,
2002; Floros et al.,
2004; Schleyer et al.,
2008
49.7 47 /44.2 1993–2006 (13) 2.8 0.94 88.9 Some damage from
Acanthaster
19 Lighthouse Reef, Bazaruto (Mozambique) Schleyer and Maggs,
2008
?41.3/43.4 2000–2007 (7) þ2.1 1.05 ? ?
20 Coral garden, Bazaruto Schleyer and Maggs,
2008
?41.1/27.0 2000–2007 (7) 14.4 0.65 ? ?
21 Inner Two-Mile Reef, Bazaruto Schleyer and Maggs,
2008
? 39.5 /42.7 2000–2007 (7) þ3.2 1.14 ? ?
22 Ponta Maunhana, Pemba (Mozambique) Rodrigues et al., 2000;
Pereira et al., 2003
? 69.7 /80.0 2000–2002 (2) þ10.3 1.14 ? ?
23 Sete Paus Islands (Mozambique) Rodrigues et al., 2000;
Pereira et al., 2003
?37.2/42.0 2000–2002 (2) þ4.8 1.13 ? ?
24 Goa Island (Mozambique) Rodrigues et al., 2000;
Pereira et al., 2003
?27.7/44.3 2000–2002 (2) þ16.6 1.15 ? ?
Chagos
25 Northern Atolls Sheppard et al., 2002 45 45 /9 1978–2001 (23) 36 0.2 20 Acropora,Montipora,
Pavona
Lakshadweep Wilkinson et al., 2004
26 Agatti-E ? 4.5 /11.5 2000–2003 (3) þ7 2.6 ? ? E-side reefs ‘‘unstable,
collapsing coral
settlement sites causing
high recruitment
mortality’’
27 Agatti-W ? 13.5 /34.5 2000–2003 (3) þ21 2.6 ? Acropora
28 Kadmat-E ? 4 /7.5 2000–2003 (3) þ3.5 1.9 ? ?
29 Kadmat-W ? 5 /20.0 2000–2003 (3) þ15.0 4.0 ? Acropora
30 Kavaratti-E ? 20 /19.5 2001–2003 (2) 0.5 0.98 ? ?
31 Kavaratti-W ? 18 /27.5 2001–2003 (2) þ9.5 1.5 ? Acropora
Seychelles
32 Cousin M1 Ledley et al., 2007 49 (1994) 17 /1 1998–2005 (7) 16 0.06 2.04 ? MPA since 1968,
disturbances minimal
33 Cousin M2 23 (1994) 6 /2 1998–2005 (7) 4 0.3 8.7 ?
34 Cousin M3 39 (1994) ? /0.5 1998–2005 (7) ? ? 1.3 ?
Aldabra Stobart et al., 2005;
Stobart, pers. commun.
Pocillopora spp.,
Acropora branching,
Porites branching
35 10 m ? 11.3 /11.6 1999–2003 (5) þ0.3 1.03 ? ?
36 20 m ? 20.3 /18.8 1999–2003 (5) 1.5 0.9 ? ?
37 Alphonse Hagan and Spencer,
2006;Hagan et al.,
2008
>30 (pre-1998) 14.8 /21.2 1998–2007 (9) þ6.4 1.43 70.6 Pocillopora spp., few
Acropora, massive
Porites
Sri Lanka Wilkinson et al., 2004
38 Pigeon Island National Park. ? 51.3 /54.4 1999–2004 (5) þ3.1 1.1 ? ?
39 Bar Reef Marine Sanctuary 78.5 (pre-1998) 1 /17.7 1998–2004 (6) þ16.7 17.7 22.6 Pocillopora damicornis,
Acropora cytherea
Sedimentation, coral
mining, destructive
fishing, pollution
40 Hikkaduwa National Park 92 7.0 /10.1 1998–2004 (6) þ3.1 1.4 11.0 Foliose Montipora
41 Weligama Reef 92 28.0 /70.6 1998–2004 (6) þ42.6 2.5 76.7 Acropora
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3718
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Western Australia Smith et al., 2006
42 Scott Reef L1 8.1 (1994) 0.1 /2.9 1998–2003 (5) þ2.8 29 35.8 Acropora,
Pocilloporidae
No other kinds of
disturbances noted by
Smith et al. (2006)
43 Scott Reef L2 23.0 (1994) 0 /5.1 1998–2003 (5) þ5.1 – 22.2 Acropora,
Pocilloporidae
44 Scott Reef L3 25.0 (1994) 0 /1.6 1998–2003 (5) þ1.6 – 6.4 Acropora,
Pocilloporidae
Arabian Gulf Riegl, 1999; Burt et al., 2008
Dubai, Saih al Shaib, Jebel Ali Multiple bleaching
events (1996, 1998,
2002), development,
land reclamation,
desalination effluents,
sedimentation
1 Group 2 28 (1996) 28 /26 1998–2007 (9) 2 0.9 92.9 Porites lutea
2 Group 3 72 (1996) 0 /41.9 1998–2007 (9) þ41.9 – 58.2 Acropora downingi,
Platygyra daedalea
Leptastrea transversa
3 Group 4 51.2 51.2 /37.7 1998–2007 (9) 13.5 0.74 73.6 Porites harrisoni
4 Group 5 16 16 /34 1998–2007 (9) þ18.0 2.1 212.5 Favia spp., Porites spp.
PACIFIC OCEAN
American Samoa Acanthaster predation,
destructive fishing,
tropical cyclones,
bleaching in 2002,
2003; coral diseases
1 Tutuila, general, 3 m Craig et al., 2005,
c
25 (1982) 13 /47 1995–2001 (6) þ34 3.6 188.0 Acropora spp. (4
species), Montipora
grisea,Pavona varians,
Porites rus
1994 bleaching,
frequent cyclones,
Acanthaster outbreak
1978
2 Tutuila, general, 6 m 11 (1982) 4 /47 1995–2001 (6) þ43 11.8 427.3 As above As above
3 Fagatele Bay, reef flat Craig et al., 2005,
c
47 (1985) 40 /12 1995–2002 (7) 28 0.3 25 Porites rus,Montipora
grisea,M. efflorescens,
Galaxea fascicularis,
Acropora (2 spp.)
1994 bleaching,
frequent cyclones,
Acanthaster outbreak
1978, extreme low tidal
exposure
4 Fagatele Bay, 3 m Craig et al., 2005,
c
19 (1985) 17 /43 1995–2002 (7) þ25 2.5 226.3 As above As above
5 Fagatele Bay, 6 m Craig et al., 2005,
c
7 (1985) 12 /64 1995–2002 (7) þ52 5.3 914.3 As above As above
6 Fagatele Bay, 9 m Craig et al., 2005,
c
26 (1985) 3 /92 1995–2002 (7) þ89 30.7 353.8 As above As above
7 Aunu’u Birkeland et al., 2008 ?16/70 1996–2002 (6) þ54 4.3 Bleaching in 1994 and
2002, two cyclones
8 Olosega, reef slope Birkeland et al., 2008 ?15/12 1996–2002 (6) 3 0.8
9 Ta’u Birkeland et al., 2008 ?15/17 1996–2002 (6) þ21.1
10 Ofu Birkeland et al., 2008 ?25/42 1996–2002 (6) þ17 1.7
French Polynesia Wilkinson et al., 2004
11 Marutea S 37 (1994) 54 /45 1994–2003 (9) 9 0.8 121.62 ? 5 bleaching events
(1991, 1994, 1997, 2001,
2003)
12 Moorea 24.5 (1992) 42 /45 1992–2003 (11) þ3 1.1 183.7 ?
13 Tahiti 10.4 (1993) 37 /29 1993–2003 (10) 8 0.8 278.8
14 Mataiva 25 (1992) 5 /22 1992–2003 (11) þ17 4.4 88 Cyclone in 1998
15 Tiahura (Moorea) Adjeroud et al., 2002 ?51/37.5 1991–1997 (7) 13.5 0.7 ? Pocillopora Repeated bleaching
(1991, 1994)
16 Tiahura (Moorea) Berumen and Pratchett,
2006
?37.4/37.6 1979–2003 (24) þ0.2 ? Both bleaching and
Acanthaster
(continued on next page)
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 19
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Table 2 (continued)
Region/site Authority Pre-bleaching
coral cover
Post-bleaching
coral cover
Period (years) % change Absolute magnitude
(post/pre cover)
Absolute change as
% of pre-disturbance
cover
Dominant recovering
taxa
Additional impacts
South Ryukyu Islands Wilkinson et al., 2004
17 Ishigaki Island ? 18.5 /28.0 1998–2003 (5) þ9.5 1.5 ? Acropora Repeated bleaching,
Acanthaster predation,
localized sedimentation
18 Sekisei Lagoon ? 33.5 /46.5 1998–2003 (5) þ13.0 1.4 ? ?
Cook Islands Wilkinson et al., 20 04
19 Rarotonga ? 41 /15 2000–2003 (3) 26 0.4 ? ? Acanthaster predation
Great Barrier Reef
20 Lizard Island Wakeford et al., 2008 25 (1981) 10 /19 1981–2003 (23) þ91.9 76 Pocillopora damicornis,
Acropora hyacinthus
1982-mortality caused
by bleaching and
Acanthaster; 1990 by
cyclone; 1996 by
Acanthaster
21 Fitzroy Island Sweatman et al., 20 03,
b
33.0 (1998) 7 /7 200 0–2003 (3) 0 1.0 21.2 Poritidae Flooding in 1989/1990
22 Havannah Island Sweatman et al., 2003,
b
42 (1997) 21 /7 1998–2003 (5) 14 0.3 16.7 Acropora,Montipora Decline in coral cover
after 1998 due to
Acanthaster and storm
23 Middle Reef Sweatman et al., 2003,
b
26 (1993) 34 /29 1998–2003 (5) 5 0.85 111.5 Poritidae, Montipora Slight decline in 1998
due to bleaching,
additional bleaching in
2002
24 Myrmidon Reef Sweatman et al., 2003,
b
26 (1993) 33 /22 20 02–2003 (1) 11 0.67 84.6 Acroporidae, Faviidae Decline due to
bleaching
25 Pandora Reef Sweatman et al., 2003,
b
58 (1997) 52 /40 1998–2003 (5) 12 0.77 69.0 Poritidae Flooding prevented
recovery after 1998
26 Fantome Island Sweatman et al., 2003,
b
20.6 (1990) 3 /3 200 0–2003 (3) 0 1.0 14.6 ? Acanthaster not
observed on this reef
Keppel Bay Berkelmans, pers.
commun.
c
27 Halfway Island 83 (1996) 82 /92 1998–2006 (8) þ10 1.1 110.8 Acropora spp., tabulate
and arborescent species
Most recent flood
impact 1991 caused 30–
90% coral mortality at
shallow depth; mass
bleaching in 1998,
2002, 2006
28 Middle Island 68 (1993) 33 /58 1998–2002 (4) þ25 1.8 85.3 Acropora spp., tabulate
and arborescent species
29 North Keppel Island 39 (1995) 32 /30 1998–2006 (8) 2 0.9 76.9 Acropora spp., tabulate
and arborescent species
E-Pacific
Costa Rica
1 Can
˜o Island Guzma
´n and Corte
´s
(2001)
64.0 (1982)
d
32.0 /10.5 1984–1999 (16) 21.5 0.33 16.4 Porites lobata,
Pocillopora spp.
Dinoflagellate blooms,
ENSO bleaching 1987,
1990–5, 1997/1998
Cocos Island Guzm
´n and Corte
´s
(2007)
2 Presidio 79.7 (pre-1982) 3.5 /25.7 1984–2002 (19) þ22.2 7.3 32.2 Porites lobata,Pavona
varians
Physical and biotic
disturbances slight
3 Chatham 89.6 (pre-1982) 2.9 /16.7 1984–2002 (19) þ13.8 5.8 18.6 Porites lobata Physical and biotic
disturbances slight
4 Pacheco 91.3 (pre-1982) 2.6 /2.4 1984–2002 (19) 0.2 0.9 2.6 Porites lobata Physical and biotic
disturbances slight
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3720
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Costa Rica Mainland Jime
´nez and Corte
´s (2003)
5 M. Antonio 34 (1992) 52 /30 1993–2001 (9) 22 0.6 88.2 Porites lobata,
Psammocora stellata
2 bleaching events
5 years apart; started to
recover, but 2nd
bleaching event
interfered
6 Cambutal 22 (1992) 24 /20 1993–2001 (9) 4 0.8 90.9 Porites lobata
7 Ballena 19.5 (1992) 26 /13 1993–2001 (9) 13 0.5 66.7 Porites lobata
Panama
´
8 Saboga Reef Wellington and Glynn,
2007; unpublished data
50 (1982) 4 /49.5 1984–2002 (19) þ45.5 12.4 99 Pocillopora damicornis,
P. elegans
Repeated low water
exposures
9 Uva Reef – deep reef base Wellington and Glynn,
2007
34.7 (1974) 0.7 /12.1 1984–2002 (19) þ11.4 17.3 34.9 Pocillopora spp.,
Psammocora stellata
10 Uva Reef – reef flat 39.2 (1974) 6.4 /2.5 1984–2000 (17) 3.9 0.4 6.4 Pocillopora damicornis
11 Secas Reef 10.6 (1971) 6.1 /7.6 1984–2002 (19) þ1.5 1.2 71.7 Pocillopora damicornis
Colombia Wilkinson, 2000
12 Gorgona Island (shallow) Zapata, pers. commun.;
Zapata et al., in press
23.6 /61 1998–2007 (9) 46.2 0.2 62.7 Pocillopora spp. Repeated low water
exposures
13 Gorgona Island (deep) Glynn et al., 1982 70 (pre-1982) 72.7 /67.9 1984–1998 (16) 4.8 0.9 131.6 Pocillopora spp.
14 Malpelo Island Birkeland et al., 1975;
Garzo
´n-Ferreira and
Pinzo
´n, 1999
65.0 (1972) 14
e
/45 1984–1999 (17) þ31 3.2 69.2 Porites lobata,Pavona
gigantea,Pocillopora
spp.
White Band Disease in
1999
Gala
´pagos Glynn and Wellington,
1983 ; Glynn, 2003;
Wellington and Glynn,
2007; Glynn,
unpublished data
15 Santa Fe 48.0 (1976) 0 /0 1984–2002 (19) 0 0 0 n.a.
16 Espan
˜ola 37.0 (1975) 0 /0.096 1984–2002 (19) þ0.096 – 0.26 Psammocora
superficialis
17 Onslow 37.1 (1975) 0 /0.3 1984–2002 (19) þ0.3 – 0.8 Pocillopora spp., Porites
lobata,Psammocora
stellata
18 Bartolome
´24.0 (1975) 0 /0 1984–2003 (20) 0 0 0 n.a.
19 Punta Pitt 27.0 (1975) 0 /0 1984–2003 (20) 0 0 0 n.a.
20 Bassa Point E 15.0 (1975) 0 /0 1984–2003 (20) 0 0 0 n.a.
21 Bassa Point W 18.0 (1975) 0 /0 1984–2003 (20) 0 0 0 n.a.
W ATLANTIC
Belize Wilkinson and
Souter, 2008
1 Reef 1 29 (1997) 12 /10 1998–2005 (7) 2 0.8 34.5 ?
2 Reef 2 27 (1997) 12 /12.5 1998–2005 (7) þ0.5 1.04 46.3 ?
Florida Keys Wilkinson and
Souter, 2008
3 Site 1 patch 20 (1996) 15.5 /15 1999–2005 (6) 0.5 1.0 75 Bleaching in 1997,1998;
hurricanes 1998, 1999
4 Site 2 shallow 12.5 (1996) 5.5 /4 1999–2005 (6) 1.5 0.7 32
5 Site 3 deep 7 (1996) 4 /3.5 1999–2005 (6) 0.5 0.9 50
6 Site 4 hardbottom 2 (1996) 2 /1.5 1999–2005 (6) 0.5 0.8 75
US Virgin Islands Rogers et al., 2008;
Rogers, pers. commun.
7 Newfound ? 13.3 /6.2 1999–2006 (7) 7.1 0.47 ? Montastraea annularis
species complex
f
Bleaching in 2005,
followed by white
plague disease
8 Mennebeck ? 26.7 /10.2 2000–2006 (6) 16.5 0.38 ? Porites porites
9 Haulover ? 22.5 /12.4 2003–2006 (3) 10.1 0.55 ? Montastraea annularis
species complex
f
10 Tektite ? 24.7 /11.1 20 05–2006 (1) 13.6 0.45 ? ?
(continued on next page)
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 21
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Table 2 (continued)
Region/site Authority Pre-bleaching
coral cover
Post-bleaching
coral cover
Period (years) % change Absolute magnitude
(post/pre cover)
Absolute change as
% of pre-disturbance
cover
Dominant recovering
taxa
Additional impacts
11 South Fore Reef ? 19.8 /11.4 2002–2006 (4) 8.4 0.58 ? ?
12 Yawzi ? 8.5 /5.6 1999–2006 (7) 2.9 0.66 ? Porites porites
13 W. Spur and Groove ? 5.1 /3.1 2000–2006 (6) 2 0.61 ? ?
Puerto Rico Garcı
´a-Sais et al., 2005
14 Media Luna 42.5 (1994) 45 /40 1998–2000 (2) 5 0.9 94.1 ? 1998 and 1999
bleaching events
Luis Pen
˜a channel marine fishery reserve 1998 and 1999
bleaching events
15 <4 m 50 (1997) 43 /34 1999–2003 (4) 9 0.8 68.0 ?
16 4–8 m 75 (1997) 53 /43 1999–2003 (4) 10 0.8 57.3 ?
17 >8 m 60 (1997) 50 /34 1999–2003 (4) 16 0.7 56.7 ?
a
Data in ‘‘pooled’’ section are means for sites marked (N), (C), (S).
b
Long-term monitoring sites and manta-tows all from NE aspects (outer rim) of reefs; bleaching impacts more prevalent inside lagoons.
c
Recovery data from different survey than original assessment.
d
Overall 50% coral mortality in 1982/83, therefore, 32% coral cover in 1984 is equal to approximately 64% live cover in 1982.
e
Assuming about 79% mortality as observed at Gorgona Island in 1983.
f
The Montastraea annularis species complex includes M. annularis,M. faveolata and M. franksi.
Tabl e 3
Summary of mean percent change (coral recovery or decline) following bleaching mortality events in five major coral reef regions.
Region Number of sites recovering/
declining/no change
Mean (SD) % change in coral cover Median
(range) % change in coral cover
Mean (SD) number of years after
bleaching mortality
Recovering Declining No change Recovering Declining No change
Indian Ocean 46/12/0 +8.3 9.1 -15.0 1 3.2 – 4.7 1. 8 7. 3 5.4 –
+5.0 (0.2–42.6) -17.5 (0.5-41.0) –
Arabian Gulf 2/2/0 +30.0 -7.8 – 9.0 9.0 –
+30.0 (18–41.9) -7.8 (2.0–13.5) –
Central/Southern/Western
Pacific Ocean
16/11/2 +25.2 24.1 -12.0 8.4 0 8.9 6.0 6.0 2.6 3.0
+17.0 (0.2–89.0) -11.5 (2.0–28.0) –
Eastern Pacific 9/6/5 +19.0 18.1 -10.8 9.5 0 18.4 1.1 13.2 4.7 16.6 7.6
+13.8 (<0.1–45.5) -8.5 (0.2–22.0) –
Western Atlantic 1/16/0 +0.5 -6.6 5.6 – 7.0 4.9 1. 8 –
-6.0 (0.5–16.5) –
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3722
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

reef-building species similar to those in the pre-disturbance
community. This suggests that, at Cocos Island, at least 20 years
were required for the regeneration of live cover following
a major mortality event. Glynn et al. (in press) observed
recovery to comparable pre-bleaching coral cover (w22%) at
Darwin Island in the northern Gala
´pagos Islands after 23 years.
Here, asexual regeneration predominated, but was limited
primarily to Porites lobata, whereas at Cocos Island sexual
recovery appeared to be the norm. Glynn and Fong (2006)
observed almost exclusively asexual regeneration of Pocillopora
elegans and Pavona clavus in Panama
´, while Acropora recovery
was entirely sexual in the Arabian Gulf (Riegl, 2002). Fong and
Glynn (2000) modeled recovery of Gardineroseris planulata in
Panama
´and found that populations could recover based almost
entirely on the asexual regrowth of surviving patches.
Increases in live coral cover after disturbance can occur by the
asexual regeneration of surviving colony tissues as well as by the
sexual recruitment of larvae (Harrison and Wallace, 1990; Rich-
mond, 1997). Among the essential physical conditions for coral re-
growth are light, and stable, firm, and relatively sediment-free
substrates. Additionally, substrates should be free of other taxa that
might outcompete young coral recruits. Heavy fish predation and
sea urchin grazing may also impede coral recovery (Bellwood et al.,
2003; McClanahan et al., 2005c).
5.1.2. Declining reefs
Reasons for continuous declines were frequently not related to
bleaching, but to Acanthaster predation (e.g., Rarotonga in the south
Pacific), and coral diseases subsequent to the bleaching disturbance
(US Virgin Islands; Table 2 and Rogers et al., 2008). Repeated
bleaching events, however, caused continuous declines at many
sites (e.g., Can
˜o Island, Pacific Costa Rica, Table 2), particularly in the
western Atlantic (Caribbean).
Since the catastrophic coral mortality at the Onslow Island
(Gala
´pagos) coral reef in 1983, pocilloporid colony abundances and
live tissue area are now increasing at an accelerating rate (Figs. 11
and 12). Nevertheless, the pre-El Nin
˜o total reef area is much
diminished, showing a change from w1ha to 400m
2
, a 96%
reduction. This loss was largely a result of intense internal and
external bioerosion (Table 1). Almost the entire pre-existing reef
framework has been reduced to unstable rubble and sand,
substrates unfavorable for coral recruitment and renewed reef
building. Thus, despite the fact that coral cover on a per-square-
meter basis may soon approach pre-disturbance levels at some
sites (after 25–30 years), a much longer time will probably be
necessary to regain the full extent of the former reef area.
5.2. Recovering species
Where recovery was observed, the dominant recruiting taxa
tended to be Acropora,Pocillopora and branching Porites. Massive
Porites spp. were frequently mentioned as survivors. Within the
Indo-Pacific, many of the reef communities that showed rapid
recovery consisted of acroporid, pocilloporid and faviid species, with
typically high rates of recruitment and growth, as well as a capacity
for asexual propagation. It may be that the continued presence of
these taxa on impacted reefs is important for the regeneration of
coral cover. In the western Atlantic, acroporids and faviids (especially
small-polyped Montastraea) have been heavily depleted by
a combination of bleaching and disease outbreaks (Rogers et al.,
2008). Their increasing rarity may be connected to the presently
observed paucity of regenerative settlement after bleaching events.
Recovery of reefs spanning the longest study periods in Indo-
nesia and the equatorial eastern Pacific have demonstrated marked
differences in the species composition of coral communities that
regained pre-disturbance live cover. In the Java Sea, recovery from
larval settlement at two sites resulted in the replacement of
formerly dominant Acropora spp. with Porites spp. (Brown, 1997a).
In contrast, at several eastern Pacific sites in Ecuador, Colombia,
Panama
´and Costa Rica, where recovery of live coral cover has been
observed, the relative abundance of species post-disturbance was
similar to the original community structure (Corte
´s and Jime
´nez,
2003; Glynn, 2003; Mate
´, 2003; Zapata and Vargas-A
´ngel, 2003;
Guzma
´n and Corte
´s, 2007; Wellington and Glynn, 2007; Glynn
et al., in press). These taxa are predominantly Porites lobata and
Pavona spp., which have recovered by both regeneration of
surviving live patches and sexual recruitment. At Cocos Island,
Costa Rica, the formerly rare Leptoseris scabra is now abundant
20 years after the 1982–83 El Nin
˜o disturbance (Guzma
´n and
Corte
´s, 2007). In contrast, the recruitment of Pocillopora spp., via
the settlement of sexually produced larvae, has been low to nil. The
principal recovery of Pocillopora reefs in the eastern Pacific has been
by the asexual regeneration of surviving branches (Glynn and Fong,
2006). In contrast, McClanahan et al. (2007b) showed Pocillopora
and Pavona to be among the fastest recruiters after bleaching
events. Compared with pre-disturbance coral communities of the
1970s and earlier, many coral communities in the Caribbean are
now dominated by brooding species, due to replacement of
broadcast spawning species following storms, diseases and
bleaching events (Hughes, 1994; Aronson et al., 1998; Aronson and
Precht, 2001; Kramer, 2003). Our global analysis of recovering taxa,
however, shows that corals with a broadcasting mode of repro-
duction, such as species of Acropora,Montipora,Porites and faviids,
are the predominant recovering corals in most regions (Table 2).
5.3. Sources of coral recovery
An important question is whether recruitment is local or distant
and/or from deep or shallow populations (Hughes et al., 1999), and
whether availability of recruits determines whether reefs recover
by sexual or asexual means. Glynn et al. (2001) suggested that the
sexual recruitment of Millepora intricata in Panama
´likely occurred
from surviving deep populations (12–20 m depth). Molecular
evidence for Acropora cervicornis shows the importance of local
recruitment (Vollmer and Palumbi, 2007). Baums et al. (2006) have
shown that the population density of survivors is important in
determining the relative importance of sexual vs. asexual recruit-
ment in recovery. The taxa observed in Table 2 to be the most
prolific regenerating species are mostly broadcast spawners (Har-
rison and Wallace, 1990; Wallace, 1999). Since their larvae tend to
spend more time in the water column than those of brooding
species, they conceivably have higher dispersal potential which
would be expected to increase their capacity to colonize impacted
reefs and contribute to regeneration.
While recruitment is important, maintaining reef framework
integrity is equally important in the recovery process. Loch et al.
(2004) observed that high recruitment success in the Maldives was
neutralized by the recruitment substrate (dead Acropora tables),
which collapsed and killed newly-settled corals. The secondary
effects of bioerosion continued to degrade potential settlement
substrates, an observation also made by Sheppard et al. (2002) in
the Chagos Archipelago. Originally noted by Endean (1976) but
negated by Pearson (1981), this is obviously an important process,
and one which we have emphasized in this review.
6. Conservation of reefs in an era of continued
coral bleaching
6.1. Managing for coral bleaching
The management of coral reefs for bleaching, once considered
somewhat of an oxymoron, has now become a central feature of
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 23
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

coral reef conservation strategy worldwide. Contemporary
approaches to managing bleaching now involve, either implicitly or
explicitly, a variety of strategies to minimize bleaching risk or
impact (Salm and Coles, 2001;Salm et al., 2001; Hughes et al., 2003;
West and Salm, 2003; Wells, 2006; Hoegh-Guldberg et al., 2007).
Initial strategies tended to assume that management actions were
unlikely to have direct effects on the incidence and severity of
bleaching and instead focused on identifying habitats that might be
Fig. 9. Percent change in coral cover at sites that experienced elevated SST bleaching/mortality in five major coral reef regions. The numbered sites in each region correspond to the
sequence of sites in Table 2. Wilcoxon matched-pairs signed-ranks test results are noted for four regions of sufficiently large sample sizes.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3724
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

naturally protected from bleaching (Salm and Coles, 2001; Salm et
al., 2001; West and Salm, 2003). These habitats could then be
prioritized for conservation activities designed to prevent degra-
dation as a result of direct anthropogenic stresses, such as overf-
ishing and nutrient pollution.
More recently, these strategies have been incorporated into an
emerging Ecosystem-Based Management (EBM) approach to
marine conservation. This approach suggests that removing local
stressors from coral reefs, including those at threat from climate
change, will improve coral health and increase ecosystem resilience
(Marshall and Schuttenberg, 2006a,b; McCook et al., 2007). This
idea, although compelling from the point of view of ecosystem
structure and function, has yet to be rigorously tested from a coral
reef bleaching perspective (but see McClanahan, 2008). Maxi-
mizing coral reef ecosystem resilience by removing secondary
stressors implicitly assumes that organismal health of reef corals
increases once secondary stresses are removed, a hypothesis which
is still lacking direct support.
Even if the removal of secondary stressors does improve the
ability of corals to resist or recover from bleaching, efforts to
remove these stressors must still be prioritized geographically to
maximize conservation outcomes. Since not all reefs can be pro-
tected from all threats, attempts to safeguard reefs must be stra-
tegically allocated to areas where they can have the greatest impact
(Salm and Coles, 2001;Salm et al., 2001). Consequently, most
strategies to manage bleaching by restoring ecosystem resilience
still emphasize identifying areas likely to be subject to less
bleaching, so that conservation efforts have the greatest chance of
success. Efforts to identify areas of least bleaching fall broadly into
two categories: (1) identifying local physical or environmental
conditions that characterize reef areas that are naturally protected
from bleaching (see Section 3.2.2); and (2) using climate models to
identify coral reef areas or regions most likely to escape the worst
effects of warming.
6.2. Prioritizing reef conservation in geographic regions projected
to suffer the least from climate change
Prioritizing conservation activities in coral reef regions pro-
jected to be most likely to survive the worst effects of climate
change is a relatively new approach that, by definition, takes an
international perspective and a longer-term view. This strategy
attempts to forecast which regions have the best chance to survive
climate change, and use this information to help set international
priorities. Typically, this approach uses coupled ocean–atmosphere
climate models to forecast bleaching stress on reefs (Hoegh-
Guldberg, 1999; Donner et al., 2005) but other approaches to
estimate bleaching susceptibility have also been undertaken
(McClanahan et al., 2007a; Kleypas et al., 2008), including attempts
to use the relative abundance of heat tolerant Symbiodinium in
corals to help identify ‘‘Reefs of Hope’ that might be less bleaching
susceptible (Baker, 2003, 2004).
These large-scale forecasting efforts are not substitutes for local
scale management efforts, and should not undermine the priority-
setting activities undertaken by coral reef managers with
a mandate to protect their local reefs. Rather, these efforts should
be used as a tool to study global ecosystem response and to
galvanize scientific action in the appropriate geographic areas to
understand survival trajectories and adaptive responses.
6.3. Intervention strategies to mitigate the impacts
of bleaching on reefs
Despite the global scale of the climate change problem, localized
attempts to mitigate the effects of bleaching may prove beneficial
in reducing mortality over restricted geographic areas. Pilot
projects to assess the potential conservation utility of these
methodologies may be justified in some cases, since these efforts
would secondarily advance our understanding of coral biology,
physiology and/or reef hydrodynamics. The direct intervention
strategies discussed here (reef shading, polyp feeding, electro-
chemical stimulation, symbiont inoculation, and wave-powered
artificial upwelling) are logistically challenging in natural reef
situations and require some degree of environmental manipula-
tion. Despite these considerations, we discuss them briefly because
they have received little attention in the scientific literature, but
may nevertheless be of future conservation interest.
Fig. 10. Percent change in coral cover at northern (4a–c), central (5a–i), and southern
(6a–f) sites in the Maldive Islands. See Table 2 for further details.
Fig. 11. Healthy, normally-pigmented Pocillopora spp. colonies at 2–3 m depth, Onslow Island, north of Floreana Island, Gala
´pagos Islands. (a) View of pre-El Nin
˜o 1982–83 patch
reef (11 January 1975, photograph by C. Birkeland). (b) Initiation of reef recovery, recently recruited colonies on basalt basement rock (10 June 2007, photograph by J.S. Feingold).
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 25
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

The use of reef shading to mitigate coral bleaching relies on the
fact that high solar irradiance acts in combination with high
temperature to cause photoinhibition, oxidative stress, cellular
damage, and eventual expulsion of symbionts (Iglesias-Prieto et al.,
1992; Lesser, 1997; Warner et al., 1999). Natural bleaching events
often exhibit strong light-related patterns of severity, with corals
(or parts of corals) that are exposed to lower light levels typically
exhibiting less bleaching. Consequently, attempts to artificially
shade sections of reef, using buoyant shadecloth, are expected to
reduce incident irradiance (typically by >50%) and decrease
bleaching if deployed in advance of, or during, a protracted elevated
temperature anomaly. Smart solar powered sprinkler devices,
operating only when bleaching conditions threaten, may also
replace shadecloth as an inexpensive way of reducing irradiance by
reflecting and scattering sunlight, as well as potentially increasing
evaporative cooling (M. Fine, pers. commun.). Currently, attempts
to run pilot experiments are underway on the Great Barrier Reef
(O. Hoegh-Guldberg, pers. commun.).
Feeding corals may also help mitigate the effects of coral bleach-
ing by providing an alternative energy source for corals that might
otherwise starve from lack of autotrophic inputs. Increased hetero-
trophy has been shown to benefit bleached corals (Grottoli et al.,
2006), and the use of artificial light sources to attract and concentrate
zooplankters on coral surfaces at night may be a cost-effective
method of achieving this. Controlled experiments to investigate the
survivorship of bleached corals exposed to strong night-time illu-
mination, in natural reef environments, would be worthwhile.
The electrical stimulation of corals using low voltage direct
current applied to a metallic reef substrate has also been suggested
as a way to mitigate coral bleaching (Goreau et al., 2004). To date,
electrically-stimulated reefs have been implemented in the Mal-
dives, Mexico, Panama
´, Indonesia, Thailand and Papua New Guinea.
It has been reported that this technique increases survivorship of
massive corals following bleaching (Goreau et al., 2000), but pub-
lished data confirming this report are currently lacking and
a hypothesized mechanism for this process would likely be of great
research interest.
Boosting the abundance of heat-tolerant Symbiodinium in corals,
either before or during a bleaching event, is another potential
means of reducing bleaching impacts over local scales. Certain
symbionts (notably those in Symbiodinium clade D) have been
shown to be thermally tolerant, and corals that contain these
symbionts at high abundance are more resistant to bleaching than
those corals which do not (Glynn et al., 2001; Baker, 2004; Baker
et al., 2004; Rowan, 2004; Berkelmans and van Oppen, 2006). Many
coral species have been shown to flexibly associate with a variety of
symbionts, including those in clade D (Baker, 2003; Mieog et al.,
2007). but debate exists over whether this is a general rule (Goulet,
2006, 2007; Baird et al., 2007; Baker and Romanski, 2007). It is not
yet known whether adult scleractinian corals can acquire symbi-
onts from environmental sources (but see Lewis and Coffroth,
2004; Coffroth et al., 2006, for evidence in octocorals), nor what the
tradeoffs or longevity of these heat-tolerant associations might be.
Consequently, further research in this area is needed.
0
5,000
10,000
15,000
20,000
25,000
30,000
35,000
40,000
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007
0
20
40
60
80
100
120
140
160
Number of colonies
Number of colonies
Colony surface area
no data
no data
1400
1200
1000
800
600
400
200
0
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007
a
b
Live tissue colony-1 (cm2) Colony surface area cm2
no data
no data
no data
no data
Fig. 12. Recovery of Pocillopora spp. over a 1 ha area, 2–3 m depth, Onslow Island, north of Floreana Island, Gala
´pagos Islands (1995–2007). (a) Number of colonies and planar colony
surface area. (b) Mean ( SD) annual live tissue planar surface area per colony.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3726
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Finally, wave-powered artificial upwelling devices have been
proposed (Kirke, 2003) to bring cool, nutrient-rich deep water to
the surface and mitigate bleaching by reducing thermal stress (and
potentially also increasing heterotrophy). Although there are
natural analogs to this approach, such as hurricanes, that have been
shown to help mitigate bleaching (Manzello et al., 2007b), similar
techniques proposed to sequester carbon have met with scientific
skepticism and environmental concern. Nevertheless a small-scale
test project might be justified given the current bleaching crisis.
7. Outlook: Predicted trends
7.1. Adaptation and acclimatization of reef corals
to high temperatures
The ability of corals to respond to warming temperatures by
adapting or acclimatizing to changing conditions has been a central
topic of debate for over a decade (Smith and Buddemeier, 1992;
Buddemeier and Smith, 1999; Gates and Edmunds, 1999; Hoegh-
Guldberg, 1999; Pittock, 1999;Coles and Brown, 2003; Hughes et
al., 2005; Hoegh-Guldberg et al., 2007; Edmunds and Gates, 2008).
When studied over biogeographic scales, many coral species can be
found under conditions that far exceed the thermal tolerances of
the same coral species at other locations (Coles et al., 1976; Hughes
et al., 2003). Bleaching temperature thresholds vary locally, and
conditions that result in coral mortality in some regions can have
no effect on corals in others. For example, while 30.5

C and 30.8

C
represent bleaching thresholds for at least some regions of the
Caribbean and Great Barrier Reef, respectively (Berkelmans et al.,
2004; Manzello et al., 2007a), temperatures as high as 35.5

Cdo
not affect corals in the Arabian Gulf or in the Samoan Manu’a
Islands (Craig et al., 2001; Riegl, 2002; Birkeland et al., 2008).
Indeed, individual corals have been reported surviving in Abu
Dhabi at temperatures up to 40

C(Kinsman, 1964), although
mortality did occur in this region in 1996 when temperatures
remained above 35

C for 3 weeks (Riegl, 1999, 2002).
These differences indicate that, over long time scales, adaptive
processes operate that can increase the thermal tolerance of these
organisms. The critical question is not, therefore, whether reef
corals can live at higher temperatures, but whether they can
respond to warmer conditions quickly enough to keep up with
increases caused by anthropogenic climate change. Secondary
questions center on whether climate change will lead to extinction,
range contraction, loss of coral cover and/or loss of biodiversity, and
what the consequences of these impacts will be for ecosystem
function.
The increasing frequency of bleaching events worldwide, and
the mortality that often accompanies them, are often seen as
compelling prima facie evidence that corals are unable to adapt or
acclimatize quickly enough to compensate for climate changes
(Jones, 2008). Moreover, the temperature anomalies that typically
cause mass bleaching are, by definition, temporary and sporadic.
Their magnitude and duration is determined by seasonal patterns
as well as ocean–atmosphere phenomena, such as the El Nin
˜o-
Southern Oscillation. Consequently, adaptation or acclimatization
must respond to unpredictable and dramatic spikes in temperature
that may challenge adaptive mechanisms suited to gradual and
continuous increases in baseline or average temperatures (Hoegh-
Guldberg, 1999). Both of these reasons suggest that adaptive
mechanisms will fail to operate over the ecological timescales
necessary to avoid large-scale irreversible loss of coral cover.
Nonetheless, the short generation times of algal symbionts
(Symbiodinium) suggest that the capacity for rapid adaptation may
be much greater than has been assumed for their long-lived coral
hosts. Although sexual reproduction has not yet been directly
observed in Symbiodinium, molecular evidence suggests that it does
occur (Baillie et al., 2000; Rodriguez-Lanetty, 2003; Santos and
Coffroth, 2003; Santos et al., 2003), also potentially favoring rapid
evolution. Similarly, selection pressure and heritability of thermal
tolerance traits are dynamic entities that greatly increase at higher
temperatures, again suggesting that adaptive capacity of these
systems may easily have been underestimated (Day et al., 2008).
Assuming adaptive capacity cannot operate rapidly enough is no
substitute for testing for its existence and studying coral response
to repeated stress events. This has proved challenging because,
although bleaching reports worldwide are on the rise and some
reef regions have experienced multiple bleaching events (Brown,
1997a,b;Berkelmans and Oliver, 1999; Hoegh-Guldberg, 1999;
Glynn et al., 2001), testing whether adaptation or acclimatization is
operating requires comparing bleaching temperature thresholds of
coral species across multiple events. This is difficult either because
repeat bleaching events have not been studied in sufficiently
quantitative ways, or because the same reefs within the same
region have not been affected. Consequently, relatively few
scenarios for testing adaptive response have actually been appro-
priately investigated. Podesta
´and Glynn (2001) compared the
effects of the 1997–98 El Nin
˜o with those of the 1982–83 event, and
concluded that, despite the fact that the 1997–98 event was at least
as strong as the former event, coral bleaching and mortality were
significantly less during the second event (Baker, 2002). Berkel-
mans et al. (2004) compared the 1998 and 2002 bleaching events
on the Great Barrier Reef, but did not test for potential acclimati-
zation or adaptation in response to the two events. An updated
analysis, however, indicates that bleaching temperature thresholds
on some reefs in the central GBR have indeed increased over time,
and suggests that acclimatization is the most likely mechanism for
these changes (Berkelmans, 2009).
7.1.1. Mechanisms of acclimatization
By what mechanisms can individual corals respond to
increasing temperatures? A number of physiological mechanisms
may be responsible for the ability of corals to compensate for
warmer conditions and/or recover from bleaching events, and
a comprehensive discussion of these mechanisms is beyond the
scope of this ecological review (see Brown, 1997b; Gates and
Edmunds, 1999; Coles and Brown, 2003;Lesser, 2006 for details). It
is worthwhile noting that corals, as symbioses between inverte-
brate metazoans, dinoflagellate algae, and an assemblage of diverse
microbial associates, have access to a wider variety of mechanisms
than might ordinarily be found in non-symbiotic equivalents
(Reshef et al., 2006). Corals, as symbioses, might acclimatize or
adapt to environmental changes by altering the physiology of the
individual partners (the coral host, the algal symbionts, and the
microbial associates) and also by varying the identities and/or
composition of the algal and microbial communities, a mechanism
we consider in Section 7.1.2 . Mechanisms for changing coral host
physiology include inducible changes in the expression of heat
shock proteins (Sharp et al., 1997), and the production of fluores-
cent proteins to dissipate excess energy (Salih et al., 1998, 2000;
Hoegh-Guldberg and Jones, 1999). Tissue characteristics may also
be expanded or contracted to increase photoprotective capacity and
regulate radiant flux to the zooxanthellae (Brown, 1997b; Hoegh-
Guldberg, 1999). Heterotrophic plasticity may also help corals
survive bleaching, and studies in Hawaii have shown that a coral
species (Montipora capitata) capable of increasing heterotrophic
feeding when bleached survives high temperature stress better
than a species that relies on photosynthetically fixed carbon
(Grottoli et al., 2006; Rodrigues and Grottoli, 2007). Mechanisms
for changing symbiont physiology to accommodate high temper-
ature stress include increases in oxidative enzymes, and the ability
to photoacclimatize by regulating accessory pigments such as
xanthophylls (Brown, 1997a; Brown et al., 1999; Gates and
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 27
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Edmunds, 1999; Hoegh-Guldberg and Jones, 1999). Similar physi-
ological mechanisms are likely present in the microbial associates,
but have not yet been investigated.
7.1.2. Adaptive shifts in symbiont communities
Changes in Symbiodinium communities have been demon-
strated in response to environmental change, including bleaching
(see Section 4.2.1), and similar changes have also been proposed for
microbial associates (Reshef et al., 2006). The ability to compensate
in this way is different from the physiological acclimatization
mechanisms outlined above, and the degree of physiological
change is potentially greater, because it involves diverse algal
partners with extremely different physiological capacities (Bud-
demeier and Fautin, 1993; Baker, 2004; Buddemeier et al., 2004).
Some researchers (e.g., Hoegh-Guldberg et al., 2002) have sug-
gested that genotypic shifts in symbiont communities cannot be
considered truly ‘‘adaptive’’ because they simply reflect changes in
the relative abundance of existing symbionts within a coral colony
(a process referred to as symbiont ‘‘shuffling’’: by Baker, 2003).
Furthermore, even if coral colonies can acquire additional symbi-
onts from the environment (symbiont ‘‘switching’’: Baker, 2003),
this does not represent true ‘‘adaptation’’ unless these symbionts
are truly novel to the coral species in question (Hoegh-Guldberg,
2006). Hoegh-Guldberg (2006) considers the genotypic changes in
symbiont communities documented to date (e.g., Baker et al., 2004;
Berkelmans and van Oppen, 2006; Jones et al., 2008) to be changes
in symbiotic partnerships that already exist in nature. Because
these changes do not involve ‘‘evolutionarily novel’’ symbionts, he
suggests they do not represent ‘‘adaptation’’ and are instead just
one of many mechanisms by which corals acclimatize to environ-
mental change, with clear physiological limits. This paradigm leads
to the conclusion that ‘‘evidence that corals and their symbionts
can adapt rapidly to coral bleaching is equivocal or nonexistent’’
(Hoegh-Guldberg et al., 2007).
We challenge this conclusion, and suggest that any genotypic
change in response to natural selection on corals, or their symbi-
onts, can be described as ‘‘adaptation’’ (Edmunds and Gates, 2008).
Restricting the use of the term ‘‘adaptation’’ to the appearance of
‘‘evolutionarily novel’’ genotypes is not in keeping with accepted
theory, which recognizes adaptation as a process rather than an
event. It is also untestable because it requires, in this case,
a complete understanding of symbiotic associations across both
space and time. We suggest that, in reef corals (and other diverse
microbial symbioses), adaptation involves natural selection acting,
at the level of the coral colony, on the diverse metacommunity of
symbionts already present on reefs. These symbiont meta-
communities exhibit the properties of Complex Adaptive Systems
(Levin, 1998; Leibold and Norberg, 2004), leading to the emergence
of coral colonies, dominated by very unusual symbionts, with novel
physiological capabilities. Applying this definition of adaptation to
reef corals (and other microbial symbioses) is not only in keeping
with evolutionary theory, but leads to new perspectives that
promote, rather than suppress, further research. Although the
extent to which this phenomenon might enhance coral survival in
an era of rapid climate change remains to be fully determined,
corals that are capable of hosting diverse symbiont communities
are not mere ecological curiosities; indeed flexibility in coral–algal
symbiosis is likely to be a principal factor underlying the evolu-
tionary success of these organisms (Baker, 2003).
7.1.3. Reef-scale ecological predictions
Numerous projections have been offered over the past three
decades forecasting likely changes due to climate-induced global
warming and coral reef bleaching. It seems appropriate now to
assess the general accuracy of these various forecasts to help
establish a basis for future assessments. While many of these
predictions (Buddemeier and Smith, 1999; Done, 1999; Kleypas
et al., 2001; Knowlton, 2001; McClanahan et al., 2007c) are too
recent to evaluate at present, it is of interest to revisit some of the
older projections.
Glynn (1984,1993) suggested that an increase in global warming
would result in an increase in the frequency, severity and scale of
coral reef bleaching. This simple prediction proved to be correct and
was further developed by Hoegh-Guldberg (1999) and Sheppard
(2003), among several others. The unprecedented coral mortality of
1997–98 was also anticipated by Williams and Bunkley-Williams
(1990) and Glynn (1993) who predicted high rates of mortality soon
after mass bleaching. The 1997–98 bleaching event also heralded
a change in reef scientists’ appreciation of the importance of
bleaching as a threat to the persistence of coral reefs in general
(compare Wilkinson, 2000 to Wilkinson and Buddemeier, 1994).
Hoegh-Guldberg (1999) further projected the likelihood of
bleaching-recurrence and drew clear attention to the perils. The
predicted declines in coral populations (Glynn, 1996; Knowlton,
2001) have also been observed. What has not yet occurred are
extinctions of any coral species, even those in small, isolated pop-
ulations. Thus far, only local extirpations, many of these just
temporary, have been observed (see Section 4.2.2 above).
Secondary effects that follow coral bleaching and mortality, such as
corallivore concentrations on surviving corals, bioerosion, desta-
bilization of reef substrata and loss of coral frameworks have all
been observed (Glynn, 1993, 1994; Eakin, 1996, 2001; Reaka-Kudla
et al., 1996; Riegl, 2001; Loch et al., 2002; Schuhmacher et al.,
2005).
7.2. Other impacts of climate change
Perhaps the most significant impact of climate change on coral
reefs, aside from coral bleaching, is the effect of ocean acidification
resulting from higher atmospheric pCO
2
. Increased pCO
2
equili-
brates with the ocean to result in seawater with a lower pH whose
aragonite saturation state (
U
arag
) is consequently also lower (Cal-
deira and Wickett, 2003; Feely et al., 2004). This results in lower
calcification rates for corals and other calcifying reef associates
(Gattuso et al., 1998; Kleypas et al., 1999; Langdon et al., 2000).
Recent reviews have addressed the uncertainties underlying how
increasing temperatures and decreasing pH might interact to affect
corals (Kleypas et al., 2001; Hoegh-Guldberg et al., 2007), and we
will not explore these uncertainties further in this review on
bleaching. We note that if warming temperatures lead to range
expansions of corals into higher latitudes (see below), these
expansions will likely be tempered by declines in
U
arag
, which are
expected to occur sooner at higher latitudes.
Shifts of coral diversity and reef growth to higher latitudes were
predicted by Veron (1992) on the basis of high coral diversity in
Numa (Boso Peninsula, central Japan) bed fossils at 5000–6000 yr
BP when sea temperatures were significantly higher than today.
Precht and Aronson (2004) claim recent range extensions of
acroporid corals and the azooxanthellate coral Tubastraea coccinea
in the western subtropical Atlantic are a result of recent ocean
warming in this region. However, T. coccinea was introduced
recently in the Caribbean, likely in the late 1930s to early 1940s
(Cairns, 2000), and it is probable that the migration of this species
to higher latitudes is a result of its expansion into favorable
previously unoccupied habitats. Also, temporary range extensions
of many scleractinian genera into higher latitudes have been
observed in southern Africa (Boshoff, 1981) long before global
warming became an issue. Recently, Greenstein and Pandolfi
(2008) used Pleistocene coral records from Western Australia to
show that corals routinely expanded and contracted their ranges in
response to climate changes, and predicted that certain species will
expand their ranges southwards in response to the current crisis.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3728
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Migration of reefs to higher latitudes is not only contingent on
favorable temperature conditions, but also on substrate availability
and aragonite saturation states.
Sea levels, rising at rates of 1–3 mm per year since the 1960s
(Leuliette et al., 2004; IPCC, 2007) and projected to be a further 18–
59 cm higher by 2100 (IPCC, 2007), have been predicted to stimu-
late reef flat coral growth (Buddemeier and Smith, 1988; Hopley
and Kinsey, 1988). Particularly if rising more rapidly thanprojected,
sea levels could drown deeper reefs and increase sedimentation,
light attenuation, and nutrient loading (Hallock and Schlager, 1986;
Graus and Macintyre, 1988) all of which would likely be detri-
mental to coral health. Since a warming climate drives rising sea
levels, concomitant coral bleaching and mortality can be expected,
combined with lower growth rates as a result of decreased arago-
nite saturation states, which would disadvantage the shallow coral
communities needed to keep pace with sea level rise. Furthermore,
flooding of coastal sedimentary basins as a result of increased storm
activity (Emanuel, 2005; Hoyos et al., 2006) could result in
increased turbidity and nutrient loading, potentially ‘‘shooting the
reefs in the back’’, i.e., negatively impacting near-shore reef zones
(Neumann and Macintyre, 1985). In addition, corals might be
stressed by corallivores, benthic competitors (algae, sponges, etc.),
and bioeroders that would not be subject to the thermal limitations
of zooxanthellate corals.
7.3. Forecasting future bleaching from climate models
Since the 1980s, when elevated temperatures were first recog-
nized as the driving factor underlying episodes of mass coral
bleaching and mortality, concern has grown over the likely fate of
reefs in an era of continued climate change (Hayes and Goreau,
1991). Hoegh-Guldberg (1999) was the first to explicitly forecast the
frequency and severity of bleaching events from climate models. By
synthesizing field data on bleaching temperature thresholds with
coupled atmosphere-ocean general circulation models (GCMs) from
the 2nd assessment (1996) of the Intergovernmental Panel on
Climate Change (IPCC, 1996) Hoegh-Guldberg concluded that severe
bleaching events were likely to become ‘‘commonplace’’ worldwide
by 2020. This simple model assumed a single bleaching threshold at
any given site, and no capacity for acclimatization or adaptation of
corals over time. Although only semi-quantitative, this startling
prediction, combined with the devastating events of the next
decade, placed coral bleaching and climate change squarely at the
center of the coral reef conservation debate.
Despite significant advances in climate modeling, surprisingly
few studies have updated these early predictions of bleaching
frequency or intensity, or attempted to explore spatial trends in
these models that might lend insight into the potential response of
reefs globally. This is surprising given the potentially critical
importance of climate models in predicting reef futures. Sheppard
(2003) used bleaching data from the severe 1998 bleaching event in
the Indian Ocean, as well as data on temperature variability and
outputs from the 3rd assessment of the IPCC (2001), to predict the
likely recurrence of similar episodes of regional mass coral
mortality in the twenty-first century. His analysis of the western
Indian Ocean showed that many reef sites within a relatively
narrow equatorial band reached an ‘‘extinction date’’ (a 20% annual
probability of a month as warm as 1998) by the mid-2010s. He also
found that numerous sites outside this latitudinal band did not
reach this date for several more decades, and that even a ‘‘modest’’
adaptation or acclimatization of 2

C might prolong coral survival
for nearly a century.
Donner et al. (2005), in the first comprehensive global assess-
ment of future bleaching under climate change, used models from
the 3rd IPCC (2001) and incorporated a bleaching prediction algo-
rithm developed and ground-truthed by NOAA’s Coral Reef Watch
program. They found that, without an increase in thermal tolerance
of 0.2– 1.0

C per decade, the majority of the world’s reefs were at
risk of annual or semi-annual bleaching by the 2050s. Although
recognizing that advances in modeling and monitoring would
likely impact forecasts for individual reefs, they concluded that the
global prognosis was unlikely to change without an accelerated
political effort to stabilize atmospheric greenhouse gas
concentrations.
It is now clear from model outputs that coral bleaching will be
a severe threat to continued coral survival for the next 30–50 years
even under the most optimistic climate scenarios. Recent studies by
McClanahan et al. (2007c) and Kleypas et al. (2008) have revealed
considerable potential for continued coral survival even under
relatively harsh scenarios. These studies related observed patterns of
bleaching to historical temperature variability in the western Indian
Ocean and the western Pacific warm pool, respectively. McClanahan
et al. (2007c) showed that corals that experience the greatest
temperature variability, usuallyat higher latitudes, are also the corals
most capable of surviving bleaching events. These findings support
the notion that past experience plays a significant role in deter-
mining the susceptibility of corals to bleaching (Brown et al., 2002),
but are also particularly relevant to predicting climate change
futures because the more temperate sites that are highly variable are
also those predicted to warm the fastest. These findings also suggest
that coral reefs at equatorial sites that are already among the
warmest might be doomed to extinction since they show relatively
little variability and have already been severely affected by past
bleaching events. Kleypas et al. (2008) provided evidence for an
‘‘ocean thermostat’’ in the warmest parts of the tropical Pacific that
may limit future temperature rise in this region, and showed that
corals in this warm pool have experienced the least historical
warming, and the fewest reported bleaching events. Consequently,
an upper temperature limitmay exist for reefs in the tropical central-
west Pacific that may provide some potential for continued coral
survival in this region. Nevertheless, habitat heterogeneity may limit
the influence of this thermostat to specific oceanic reefs; shallow
coastal reefs, particularly in restricted embayments and poorly
flushed areas, are unlikely to benefit from this phenomenon.
Acknowledgments
We wish to thank A. Campbell and A. Clark of the Rosenstiel
School of Marine and Atmospheric Science (RSMAS) library, for
obtaining literature. S. Andre
´foue
¨t, R. Berkelmans, C. Birkeland,
I.M. Co
ˆte
´, J.S. Feingold, and G. Rowlands provided us with images.
W. Allison, R. Berkelmans, L. Bigot, C. Birkeland, C.M. Eakin,
D. Fenner, N. Graham, A. Hagan, M. Ledlie, C. Rogers, M. Schleyer, B.
Stobart, and F. Zapata gave us access to published and unpublished
data and information for Tables 1 and 2. Critical editorial advice by
I. Valiela greatly improved this review. We also thank I. Enochs for
help with multiple technical tasks. P.W.G. received support from
NSF grant OCE-0526361 and earlier awards, A.C.B. was supported
by NSF OCE-0527184 and grants from the Pew Institute for Ocean
Science and the Wildlife Conservation Society, B.R. was supported
by NOAA grant NA160A1443 to the National Coral Reef Institute
(NCRI) at Nova Southeastern University and the Dolphin Energy/
World Wildlife Foundation coral reef project. This is a contribution
from the University of Miami’s Rosenstiel School (RSMAS), and
NCRI publication #102.
References
Adjeroud, M., Augustinm, D., Galzin, R., Salvat, B., 2002. Natural disturbances and
interannual variability of coral reef communities on the outer slope of Tiahura
(Moorea, French Polynesia): 1991–1997. Marine Ecology Progress Series 237,
121–131.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 29
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Andre
´foue
¨t, S., Berkelmans, R., Odriozola, L., Done, T., Oliver, J., Muller-Karger, F.E.,
2002. Choosing the appropriate spatial resolution for monitoring coral
bleaching events using remote sensing. Coral Reefs 21, 147–154.
Andre
´foue
¨t, S., Muller-Karger, F.E., Hochberg, E.J., Hu, C., Carder, K.L., 2001. Change
detection in shallow coral reef environments using Landsat 7 ETMþdata.
Remote Sensing of Environment 78, 150–162.
Andre
´foue
¨t, S., Payri, C., Hochberg, E.J., Hu, C., Atkinson, M.J., Muller-Karger, F.E.,
2004. Use of in situ and airborne reflectance for scaling-up spectral discrimi-
nation of coral reef macroalgae from species to communities. Marine Ecology
Progress Series 283, 161–177.
Antonius, A., Riegl, B., 1997. A possible link between coral diseases and a cor-
allivorous snail (Drupella cornus) outbreak in the Red Sea. Atoll Research
Bulletin 447, 1–9.
Aronson,R.B., Bruno, J.F.,Precht, W.F., Glynn, P.W., Harvell,C.D., Kaufman,L., Rogers, C.S.,
Shinn, E.A., Valentine, J.F., 2003. Causes of reef degradation. Science 302,1502.
Aronson, R.B., Macintyre, I.G., Precht, W.F., Murdoch, T.J.T., Wapnick, C.M., 2002. The
expanding scale of species turnover events on coral reefs in Belize. Ecological
Monographs 72, 233–249.
Aronson, R.B., Macintyre, I.G., Wapnick, C.M., O’Neill, M.W., 20 04. Phase-shifts,
alternative states, and the unprecedented convergence of two reef systems.
Ecology 85, 1876–1891.
Aronson, R.B., Precht, W.F., 2001. Evolutionary paleoecology of Caribbean coral
reefs. In: Allmon, W.D., Bottjer, D.J. (Eds.), Evolutionary Paleoecology: The
Ecological Context of Macroevolutionary Change. Columbia University Press,
New York, pp. 171–233.
Aronson, R.B., Precht, W.F., 2006. Conservation, precaution and Caribbean reefs.
Coral Reefs 25, 441–450.
Aronson, R.B., Precht, W.F., Macintyre, I.G., 1998. Extrinsic control of species
replacement on a Holocene reef in Belize: the role of coral disease. Coral Reefs
17, 223–230.
Ayling, A.M., Ayling, A.L., 1992. Preliminary information on the effects of Drupella
spp. grazing on the Great Barrier Reef. In: Turner, S. (Ed.), Drupella cornus:
a symposium. Department of Conservation and Land Management, western
Australia CALM Occasional Paper 3/92.
Baillie, B.K., Belda-Baillie, C.A., Silvestre, V., Sison, M., Gomez, A.V., Gomez, E.D.,
Monje, V., 2000. Genetic variation in Symbiodinium isolates from giant clams
based on random-amplified-polymorphic DNA (RAPD) patterns. Marine Biology
136, 829–836.
Baird, A., 1999. A large aggregation of Drupella rugosa following the mass bleaching
of corals on the Great Barrier Reef. Reef Research 9, 6–7.
Baird, A.H., Cumbo, V.R., Leggat, W., Rodriguez-Lanetty, M., 2007. Fidelity and
flexibility in coral symbioses. Marine Ecology Progress Series 347, 307–309.
Bak, R.P.M., Meesters, E.H., 1999. Population structure as a response of coral
communities to global change. American Zoologist 39, 56–65.
Baker, A.C., 2001. Reef corals bleach to survive change. Nature 411, 765–766.
Baker, A.C., 2002. Is coral bleaching really adaptive? Reply to Hoegh-Guldberg, et al.
Nature 415, 602.
Baker, A.C., 2003. Flexibility and specificity in coral-algal symbiosis: diversity,
ecology and biogeography of Symbiodinium. Annual Review of Ecology and
Systematics 34, 661–689.
Baker, A.C., 2004. Symbiont diversity on coral reefs and its relationship to bleaching
resistance and resilience. In: Rosenberg, E., Loya, Y. (Eds.), Coral Health and
Disease, pp. 177–194.
Baker, A.C., Jones, S.H.I.V., Lee, T.S., Abuzinada, A.H., Joubert, E., Krupp, F., 2005.
Symbiont diversity in Arabian corals and its relation to patterns of contempo-
rary and historical environmental stress. Proceedings of an International
Symposium on the Extent and Impact of Coral Bleaching in the Arabian Region:
Riyadh (5–9 February 2000) Kingdom of Saudi Arabia, 24–36.
Baker, A.C., Romanski, A.M., 2007. Multiple symbiotic partnerships are common in
scleractinian corals, but not in octocorals: comment on Goulet (2006. Marine
Ecology Progress Series 335, 237–242.
Baker, A.C., Starger, C.J., McClanahan, T.R., Glynn, P.W., 20 04. Corals’ adaptive
response to climate change. Nature 430, 741.
Barton, A.D., Casey, K.S., 2005. Climatological context for large-scale coral bleaching.
Coral Reefs 24, 536–554.
Bassim, K.M., Sammarco, P.W., Snell, T.L., 2002. Effects of temperature on success of
(self and non-self) fertilization and embryogenesis in Diploria strigosa (Cnidaria,
Scleractinia). Marine Biology 140, 479–488.
Baums, I.B., Miller, M.W., Hellberg, M.E., 2006. Geographic variation in clonal
structure in a reef-building Caribbean coral, Acropora palmata. Ecological
Monographs 76, 503–519.
Bellwood, D.R., Hoey, A.S., Ackerman, J.L., Depczynski, M., 2006. Coral bleaching,
reef fish community phase shifts and the resilience of coral reefs. Global Change
Biology 12, 1587–1594.
Bellwood, D.R., Hoey, A.S., Choat, J.H., 2003. Limited functional redundancy in high
diversity systems: resilience and ecosystem function on coral reefs. Ecology
Letters 6, 281–285.
Ben-Haim, Y., Thompson, F.L., Thompson, C.C., Cnockaert, M.C., Hoste, B., Swings, J.,
Rosenberg, E., 2003. Vibrio coralliilyticus sp nov., a temperature-dependent
pathogen of the coral Pocillopora damicornis. International Journal of Systematic
and Evolutionary Microbiology 53, 309–315.
Berkelmans,R., 2002a. Time-integrated thermalbleaching thresholdsof reefs and their
variation on the Great Barrier Reef. Marine Ecology Progress Series 229, 73–82.
Berkelmans, R., 2002b. Reply comment: Time-integrated thermal bleaching
thresholds of reefs and their variation on the Great Barrier Reef. Marine Ecology
Progress Series 237, 309–310.
Berkelmans, R., 2009. Bleaching and mortality thresholds: How much is too much?
In: van Oppen, M.J.H., Lough, J.M. (Eds.), Coral Bleaching: Patterns and
Processes, Causes and Consequences. Ecological Studies, vol. 205. Springer, New
York, pp. 103–120.
Berkelmans, R., De’ath, G., Kinnimonth, S., Skirving, W.J., 2004. A comparison of the
1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial
correlation, patterns, and predictions. Coral Reefs 23, 74–83.
Berkelmans, R., Oliver, J.K.,1999. Large-scale bleaching of corals on the Great Barrier
Reef. Coral Reefs 18, 55–60.
Berkelmans, R., van Oppen, M.J.H., 2006. The role of zooxanthellae in the thermal
tolerance of corals: a ‘‘nugget of hope’’ for coral reefs in an era of climate
change. Proceedings of the Royal Society B 273, 2305–2312.
Berumen, M.L., Pratchett, M.S., 2006. Recovery without resilience: persistent
disturbance and long-term shifts in the structure of fish and coral communities
at Tiahura Reef, Moorea. Coral Reefs 25, 647–653.
Berumen, M.L., Pratchett, M.S., McCormick, M.I., 2005. Within reef variation in the
diet and condition of two coral feeding butterflyfish (Pisces: Chaetodontidae).
Marine Ecology Progress Series 287, 217–227.
Birkeland, C., Craig, P., Fenner, D., Smith, L., Kiene, W.E., Riegl, B., 2008. Geologic
setting and ecological functioning of coral reefs in American Samoa. In: Riegl, B.,
Dodge, R.E. (Eds.), Coral Reefs of the USA. Coral Reefs of the World, vol. 1.
Springer, pp. 737–761.
Birkeland, C., Lucas, J.S., 1990. Acanthaster planci: Major Management Problem of
Coral Reefs. CRC Press, Boca Raton, 257 pp.
Birkeland, C., Meyer, D.L., Stames, J.P., Buford, C.L., 1975. Subtidal communities of
Malpelo Island. In: Graham, J.B. (Ed.), The Biological Investigation of Malpelo
Island, Colombia. Smithsonian Contributions to Zoology, 176, pp. 55–68.
Booth, D.J., Beretta, G.A., 2002. Changes in a fish assemblage after a coral bleaching
event. Marine Ecology Progress Series 245, 205–212.
Boshoff, P.H., 1981. An annotated checklist of Southern African Scleractinia.
Oceanographic Research Institute Investigational Reports, Durban, 45.
Brock, J.C., Wright, C.W., Clayton, T.D., Nayegandhi, A., 2004. LIDAR optical rugosity
of coral reefs in Biscayne National Park, Florida. Coral Reefs 23, 48–60.
Brown, B.E., 1987. Worldwide death of coralsdnatural cyclical events or man-made
pollution? Marine Pollution Bulletin 18, 9–13.
Brown, B.E., 1997a. Coral bleaching: causes and consequences. Coral Reefs 16,
129–138.
Brown, B.E., 1997b. Adaptations of reef corals to physical environmental stress.
Advances in Marine Biology 31, 221–299.
Brown, B.E., Ambarsari, I., Warner, M.E., Fitt, W.K., Dunne, R.P., Gibb, S.W.,
Cummings, D.G., 1999. Diurnal changes in photochemical efficiency and
xanthophyll concentrations in shallow water reef corals: evidence for photo-
inhibition and photoprotection. Coral Reefs 18, 99–105.
Brown, B.E., Dunne, R.P., Chansang, H., 1996. Coral bleaching relative to elevated
seawater temperature in the Andaman Sea (Indian Ocean) over the last 50
years. Coral Reefs 15, 151–152.
Brown, B.E., Dunne, R.P., Goodson, M.S., Douglas, A.E., 2000. Bleaching patterns in
reef corals. Nature 404, 142–143.
Brown, B.E., Dunne, R.P., Goodson, M.S., Douglas, A.E., 2002. Experience shapes the
susceptibility of a reef coral to bleaching. Coral Reefs 21, 119–126.
Brown, B.E., Le Tissier, M.D.A., Dunne, R.P., 1994. Tissue retraction in the scler-
actinian coral Coeloseris mayeri, its effect upon coral pigmentation and
preliminary implications for heat balance. Marine Ecology Progress Series 105,
209–218.
Brown, B.E., Suharsono, 1990. Damage and recovery of coral reefs affected by El
Nin
˜o related seawater warming in the Thousand Islands, Indonesia. Coral Reefs
8, 163–170.
Bruce, A.J., 1976. Shrimps and prawns of coral reefs, with special reference to
commensalism. In: Jones, O.A., Endean, R. (Eds.), Biology and Geology of Coral
Reefs. Biol. 2, vol. 3. Academic Press, New York, pp. 37–94.
Bruckner, A.W. (Ed.), 2003. Proceedings of the Caribbean Acroporaworkshop:
potential application of the US Endangered Species Act as a conservation
strategy. NOAA Technical Memorandum NMFS-OPR-24, p. 206. Silver Spring,
Maryland.
Bruno, J.F., Selig, E.R., 2007. Regional decline of coral cover in the Indo-Pacific:
timing, extent, and subregional comparisons. PLoS ONE 2 (8), e711, doi:10.1371/
journal.pone.0000711.
Bruno, J.F., Selig, E.R., Casey, K.S., Page, C.A., Willis, B.L., Harvell, C.D., Sweatman, H.,
Melendy, A.M., 2007. PLoS Biology 5, 1220–1227.
Bruno, J.F., Siddon, C.E., Witman, J.D., Colin, P.I., Toscano, M.A., 2001. El Nin
˜o related
coral bleaching in Palau, Western Caroline Islands. Coral Reefs 20, 127–136.
Buddemeier, R.W., Fautin, D.G., 1993. Coral bleaching as an adaptive mechanismda
testable hypothesis. Bioscience 43, 320–326.
Buddemeier, R.W., Kleypas, J.A., Aronson, R., 2004. Coral reefs and global climate
change. Potential contributions of climate change to stresses on coral reef
ecosystems, prepared for the Pew Center for Global Climate Change, 42. www.
pewclimate.org/global-warming-in-depth/all_reports/coral_reefs/index.cfm.
Buddemeier, R.W., Smith, S.V.,1988. Coral reef growth in an era of rapidly rising sea
level: predictions and suggestions for long-term research. Coral Reefs 7, 51–56.
Buddemeier, R.W., Smith, S.V., 1999. Coral adaptation and acclimatization: A most
ingenious paradox. American Zoologist 39, 1–9.
Burt, J., Bartholomew, A., Usseglio, P., 2008. Recovery of corals a decade after
a bleaching event in Dubai, United Arab Emirates. Marine Biology, doi:10.1007/
s00227-0892-9.
Cairns, S.D., 2000. A revision of the shallow-water azooxanthellate Scleractinia of
the Western Atlantic. Studies of the Natural History of the Caribbean 75, 1–231.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3730
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Caldeira, K., Wickett, M.E., 2003. Anthropogenic carbon and ocean pH. Nature 425,
365.
Castro, P., 1978. Movements between coral colonies in Trapezia ferruginea (Crus-
tacea: Brachyura), an obligate symbiont of scleractinian corals. Marine Biology
46, 237–245.
Castro, P.,1988. Animal symbioses in coral reef communities: a review. Symbiosis 5,
161–184.
Celliers, L., Schleyer, M.H., 2002. Coral bleaching on high-latitude marginal reefs at
Sodwana Bay, South Africa. Marine Pollution Bulletin 44, 1380–1387.
Cerrano, C., Bavastrello, G., Bianchi, C.M., Cattaneo-Vietti, R., Bava, S., Morganti, C.,
Morri, C., Picco, P., Sara, G., Schiaparelli, S., Siccardi, A., Sponga, F., 2000. A
catastrophic mass-mortality episode of gorgonians and other organisms in the
Ligurian Sea (North-western Mediterranean), summer 1999. Ecology Letters 3,
284–293.
Clark, C.D., Mumby, P.J., Chisholm, J., Jaubert, J., Andre
´foue
¨t, S., 2000. Spectral
discrimination of coral mortality states following a severe bleaching event.
International Journal of Remote Sensing 21, 2321–2327.
Coffroth, M.A., Lewis, C.F., Santos, S.R., Weaver, J.L., 2006. Environmental pop-
ulations of symbiotic dinoflagellates in the genus Symbiodinium can initiate
symbioses with reef cnidarians. Current Biology 16, R985–R987.
Coles, S.L., Brown, B.E., 2003. Coral bleachingdcapacity for acclimatization and
adaptation. Advances in Marine Biology 46, 183–223.
Coles, S.L., Fadlallah, Y.H., 1991. Reef coral survival and mortality at low tempera-
tures in the Arabian Gulf: new species-specific lower temperature limits. Coral
Reefs 9, 231–237.
Coles, S.L., Jokiel, P.L., 1977. Effects of temperature on photosynthesis and respira-
tion in hermatypic corals. Marine Biology 43, 209–216.
Coles, S.L., Jokiel, P.L., 1978. Synergistic effects of temperature, salinity and light on
the hermatypic coral Montipora verrucosa. Marine Biology 49, 187–195.
Coles, S.L., Jokiel, P.L., Lewis, C.R., 1976. Thermal tolerance in tropical versus
subtropical Pacific reef corals. Pacific Science 30, 159–166.
Coles, S.L., Seapy, D.G., 1998. Ultra-violet absorbing compounds and tumorous
growths on acroporid corals from Bandar Khayran, Gulf of Oman, Indian Ocean.
Coral Reefs 17, 195–198.
Colgan, M.W., 1990. El Nin
˜o and the history of eastern Pacific reef building. In:
Glynn, P.W. (Ed.), Global Ecological Consequences of the 1982–83 El Nin
˜o-
Southern Oscillation. Elsevier Oceanography Series 52, Elsevier, Amsterdam, pp.
183–232.
Colley, S.B., Glynn, P.W., May, A.S., Mate
´, J.L., 2004. Species-dependent reproductive
responses of eastern Pacific corals to the 1997–1998 ENSO event. Proceedings of
the 10th International Coral Reef Symposium, Okinawa, 61–70. session 1-2-A.
Collier, J.S., Humber, S.R., 2007. Time-lapse side-scan sonar imaging of bleached
coral reefs: a case study from the Seychelles. Remote Sensing of Environment
108, 339–356.
Connell, J.H., 1997. Disturbance and recovery of coral assemblages. Coral Reefs 16
(suppl.), S101–S113.
Corte
´s, J., Jime
´nez, C., 2003. Corals and coral reefs of the Pacific of Costa Rica. In:
Corte
´s, J. (Ed.), Latin American Coral Reefs. Elsevier, Amsterdam, pp. 361–385.
Corte
´s, J., Murillo, M.M., Guzma
´n, H.M., Acun
˜a, J., 1984. Pe
´rdida de zooxantelas y
muerte de corales y otros organismos arrecifales en el Caribe y Pacı
´fico de Costa
Rica. Revista de Biologı
´a Tropical 32, 227–231.
Co
ˆte
´, I.M., Gardner, T.A., Gill, J.A., Hutchinson, D.J., Watkinson, A.R., 2006. New
approaches to estimating recent ecological changes on coral reefs. Conservation
Biology Series (Cambridge) 13, 293–313.
Co
ˆte
´, I.M., Gill, J.A., Gardner, T.A., Watkinson, A.R., 2005. Measuring coral reef
decline through meta-analyses. Philosophical Transactions of the Royal Society
B 360, 385–395.
Cox, E.F., 2007. Continuation of sexual reproduction in Montipora capitata following
bleaching. Coral Reefs 26, 721–724.
Craig, P., Birkeland, C., Belliveau, S., 2001. High temperatures tolerated by a diverse
assemblage of shallow-water corals in American Samoa. Coral Reefs 20, 185–189.
Craig, P., DiDonato, E.M., Fenner, D., Hawkins, C., 2005. The state of coral reef
ecosystems of American Samoa . In: Waddell, J.E. (Ed.), The State of Coral Reef
Ecosystems of the United States and Pacific Freely Associated States: 2005.
NOAA Technical Memorandum NOS NCCOS 11. NOAA/NCCOS Center for
Coastal Monitoring and Assessment’s Biogeography Team, Silver Spring, MD,
pp. 312–337.
Curran, H.A., Smith, D.P., Meigs, L.C., Pufall, A.E., Greer, M.L., 1994. The health and
short-term change of two coral patch reefs, Fernandez Bay, San Salvador Island,
Bahamas. In: Ginsburg, R.N. (Ed.), Proceedings of the Colloquium on Global
Aspects of Coral Reefs: HealthHazards and History. Rosenstiel School of Marine
and Atmospheric Science, University of Miami, pp. 147–153.
Day, T., Nagel, L., van Oppen, M.J.H., Caley, M.J., 2008. Factors affecting the evolution
of bleaching resistance in corals. American Naturalist 171, E72–E88.
Done, T.J., 1999. Coral community adaptability to environmental change at the
scales of regions, reefs and reef zones. American Zoologist 39, 66–79.
Done, T.J., Jones, R., 2006. Tropical coastal ecosystems and climate change predic-
tion: global and local risks. In: Phinney, J.T., Hoegh-Guldberg, O., Kleypas, J.,
Skirving, W., Strong, A. (Eds.), Coral Reefs and Climate Change: Science and
Management. Coastal and Estuarine Studies 61. American Geophysical Union,
pp. 5–32.
Donner, S.D., Skirving, W.J., Little, C.M., Oppenheimer, M., Hoegh-Guldberg, O.,
2005. Global assessment of coral bleaching and required rates of adaptation
under climate change. Global Change Biology 11, 2251–2265.
Douglas, A.E., 2003. Coral bleaching – how and why? Marine Pollution Bulletin 46,
385–392.
Downs, C.A., Fauth, J.E., Halas, J.C., Dustan, P., Bemiss, J., Woodley, C.M., 2002.
Oxidative stress and seasonal coral bleaching. Free Radical Biology and Medi-
cine 33, 533–543.
Dunn, S.R., Bythell, J.C., Le Tissier, M.D.A., Burnett, W.J., Thomason, J.C., 2002. Pro-
grammed cell death and cell necrosis activity during hyperthermic stress-
induced bleaching of the symbiotic sea anemone Aiptasia sp. Journal of
Experimental Marine Biology and Ecology 272, 29–53.
Dunne, R.P., 2002. Comment on Berkelmans (2002) ‘‘Time-integrated thermal
bleaching thresholds of reefs and their variation on the Great Barrier Reef’’.
Marine Ecology Progress Series 237, 307–308.
Dunne, R.P.,Brown, B.E., 2001. The influence of solar radiation on bleaching of shallow
water reef corals in the Andaman Sea, 1993–1998. Coral Reefs 20, 201–210.
Dustan, P., Dobson, E., Nelson, G., 2001. Landsat Thematic Mapper: detection of shifts
in community composition of coral reefs. Conservation Biology 15, 892–902.
Eakin, C.M., 1996. Where have all the carbonates gone? A model comparison of
calcium carbonate budgets before and after the 1982–1983 El Nin
˜oatUva
Island in the eastern Pacific. Coral Reefs 15, 109–119.
Eakin, C.M., 2001. A tale of two ENSO events: carbonate budgets and the influence
of two warming disturbances and intervening variability, Uva Island, Panama
´.
Bulletin of Marine Science 69, 171–186.
Eakin, C.M., Smith, D.B., Glynn, P.W., D’Croz, L., Gil, J., 1989. Extreme tidal exposures,
cool upwelling and coral mortality in the eastern Pacific (Panama
´). Association
of Marine Laboratories of the Caribbean 22, insert.
Edmunds, P.J., Gates, R.D., 2008. Acclimatization in tropical reef corals. Marine
Ecology Progress Series 361, 307–310.
Edmunds, P.J., Gates, R.D., Gleason, D.F., 2003. The tissue composition of Montastrea
franksi during a natural bleaching event in the Florida Keys. Coral Reefs 22, 54–
62.
Elvidge, C.D., Dietz, J.B., Berkelmans, R., Andrefouet, S., Skirving, W., Strong, A.,
Tuttle, B.T., 2004. Satellite observation of Keppel Islands (Great Barrier Reef)
2002 coral bleaching using Ikonos data. Coral Reefs 23, 123–132.
Emanuel, K., 2005. Increasing destructiveness of tropical cyclones over the past 30
years. Nature 436, 686–688.
Endean, R., 1976. Destruction and recovery of coral reef communities. In: Jones, O.A.,
Endean, R. (Eds.), Biology and Geology of Coral Reefs, Vol. 3. Academic Press,
London, pp. 215–255.
English, S., Wilkinson, C., Baker, V., 1997. Survey Manual for Tropical Marine
Resources. Australian Institute of Marine Science,, 390.
Fabricius, K.E., 2006. Effects of irradiance, flow, and colony pigmentation on the
temperature microenvironment around corals: implications for coral bleach-
ing? Limnology and Oceanography 51, 30–37.
Fadlallah, Y.H., 1996. Synchronous spawning of Acropora clathrata coral colonies
from the western Arabian Gulf (Saudi Arabia). Bulletin of Marine Science 59,
209–216.
Fadlallah, Y.H., Lindo, R.T., Lennon, D.J., 1992. Annual synchronous spawning event
in Acropora species for the western Arabian Gulf. Proceedings of the 7th
International Coral Reef Symposium. Guam 1, 501 (single page).
Feary, D.A., Almany, G.R., Jones, G.P., McCormick, M.I., 2007a. Coral degradation and
the structure of tropical reef fish communities. Marine Ecology Progress Series
333, 243–248.
Feary, D.A., Almany, G.R., McCormick, M.I., Jones, G.P., 2007b. Habitat choice,
recruitment and the response of coral reef fishes to coral degradation. Oeco-
logia 153, 727–737.
Feely, R.A., Sabine, C.L., Lee, K., Berelson, W., Kleypas, J., Fabry, V.J., Millero, F.J., 2004.
Impact of anthropogenic CO
2
on the CaCO
3
system in the oceans. Science 305,
362–366.
Fitt, W.K., Brown, B.E., Warner, M.E., Dunne, R.P., 2001. Coral bleaching: interpre-
tation of thermal tolerance limits and thermal thresholds in tropical corals.
Coral Reefs 20, 51–65.
Fitt, W.K., McFarland, F.K., Warner, M.E., Chilcoat, G.C., 2000. Seasonal patterns of
tissue biomass and densities of symbiotic dinoflagellates in reef corals and
relation to coral bleaching. Limnology and Oceanography 45, 677–685.
Fitt, W.K., Spero, H.J., Halas, J., White, M.W., Porter, J.W., 1993. Recovery of the coral
Montastrea annularis in the Florida Keys after the 1987 Caribbean ‘‘bleaching
event’’. Coral Reefs 12, 57–64.
Fitt, W.K., Warner, M.E., 1995. Bleaching patterns of four species of Caribbean reef
corals. Biological Bulletin 189, 298–307.
Floros, C.D., Samways, M.J., Armstrong, B., 2004. Taxonomic patterns of bleaching
within a South African coral assemblage. Biodiversity and Conservation 13,
1175–1194.
Fong, P., Glynn, P.W., 2000. A regional model to predict coral population
dynamics in response to El Nin
˜o-Southern Oscillation. Ecological Applications
10, 842–854.
Fox, H.E., Caldwell, R.L., 2006. Recovery of blast fishing on coral reefs: a tale of two
scales. Ecological Applications 16, 1631–1635.
Franklin, D.J.P., Hoegh-Guldberg, O., Jones, R.J., Berges, J.A., 2004. Cell death and
degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata
during bleaching. Marine Ecology Progress Series 272, 117–130.
Fujioka, Y., 1999. Mass destruction of the hermatypic corals during a bleaching
event in Ishigaki Island, southwestern Japan. Galaxea. Journal of the Japanese
Coral Reef Society 1, 41–50.
Garcı
´a-Sais, J.R., Appeldoorn, R., Bruckner, A., Caldow, C., Christensen, J.D.,
Lilyestrom, C., Monaco, M.E., Sabater, J., Williams, E., Diaz, E., 2005. The state of
coral reef ecosystems of the Commonwealth of Puerto Rico. In: Waddell, J.E.
(Ed.), The State of Coral Reef Ecosystems of the United States and Pacific Freely
Associated States: 2005. NOAA Technical Memorandum NOS NCCOS 11. NOAA/
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 31
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

NCCOS Center for Coastal Monitoring and Assessment’s Biogeography Team,
Silver Spring, MD, pp. 91–131.
Garzo
´n-Ferreira, J., Pinzo
´n, J., 1999. Evaluacio
´nra
´pida de estructura y salud de las
formaciones coralinas de la Isla de Malpelo (Pacı
´fico colombiano). Boletı
´nde
Investigaciones Marinas y Costeras INVEMAR 28, 137–154.
Gardner, T.A., Co
ˆte
´, I.M., Gill, J.A., Grant, A., Watkinson, A.R., 2003. Long-term
region-wide declines in Caribbean corals. Science 301, 958–960.
Gardner, T.A., Co
ˆte
´, I.M., Gill, J.A., Grant, A., Watkinson, A.R., 2005. Hurricanes and
Caribbean coral reefs: impacts, recovery patterns, and role in long-term decline.
Ecology 86, 174–184.
Gates, R.D., 1990. Seawater temperature and sublethal coral bleaching in Jamaica.
Coral Reefs 8, 193–197.
Gates, R.D., Baghdasarian, G., Muscatine, L., 1992. Temperature stress causes host-
cell detachment in symbiotic cnidariansdimplications for coral bleaching.
Biological Bulletin 182, 324–332.
Gates, R.D., Edmunds, P.J.,1999. The physiological mechanisms of acclimatization in
tropical reef corals. American Zoologist 39, 30–43.
Gill, J.A., Watkinson, A.R., McWilliams, J.P., Co
ˆte
´, I.M., 2006. Opposing forces of
aerosol cooling and El Nin
˜o drive coral bleaching on Caribbean reefs.
Proceedings of the National Academy of Sciences USA 103, 18870–18873.
Gattuso, J.P., Frankignoulle, M., Bourge, I., Romaine, S., Buddemeier, R.W., 1998.
Effect of calcium carbonate saturation of seawater on coral calcification. Global
and Planetary Change 18, 37–46.
Gladfelter, E.H., 1988. The physiological basis of coral bleaching. In: Ogden, J.,
Wicklund, R. (Eds.), Mass Bleaching of Coral Reefs in the Caribbean: A Research
Strategy. National Undersea Research Program, Research Report 88-2. National
Oceanic and Atmospheric Administration, U.S. Department of Commerce,
Washington, DC, pp. 15–18.
Gleason, M.G., 1993. Effects of disturbance on coral reef communities: bleaching in
Moorea, French Polynesia. Coral Reefs 12, 193–201.
Gleeson, M.W., Strong, A.E.,1995. Applying MCSST to coral reef bleaching. Advances
in Space Research 16, 151–154.
Glynn, P.W., 1983. Extensive ‘‘bleaching’’ and death of reef corals on the Pacific coast
of Panama
´. Environmental Conservation 10, 149–154.
Glynn, P.W., 1984. Widespread coral mortality and the 1982/83 El Nin
˜o warming
event. Environmental Conservation 11, 133–146.
Glynn, P.W., 1985a. Corallivore population sizes and feeding effects following El
Nin
˜o (1982-1983) associated coral mortality in Panama
´. Proceedings of the Fifth
International Coral Reef Congress. Tahiti 4, 183–188.
Glynn, P.W.,1985b. El Nin
˜o-associated disturbance to coral reefs and postdisturbance
mortality by Acanthaster planci. Marine Ecology Progress Series 26, 295–300.
Glynn, P.W.,1988. El Nin
˜o warming, coral mortality and reef framework destruction
by echinoid bioerosion in the eastern Pacific. Galaxea 7, 129–160.
Glynn, P.W., 1990a. Coral mortality and disturbances to coral reefs in the tropical
eastern Pacific. In: Glynn, P.W. (Ed.), Global Ecological Consequences of the
1982–83 El Nin
˜o-Southern Oscillation. Elsevier Oceanography Series 52, pp. 55–
126. Amsterdam.
Glynn, P.W. (Ed.), 1990b. Global Ecological Consequences of the 1982–83 El Nin
˜o-
Southern Oscillation. Elsevier Oceanography Series 52. Elsevier, Amsterdam,
563 pp.
Glynn, P.W., 1991. Coral reef bleaching in the 1980s and possible connections with
global warming. Trends in Ecology and Evolution 6, 175–179.
Glynn, P.W., 1993. Coral reef bleaching: ecological perspectives. Coral Reefs 12, 1–17.
Glynn, P.W., 1994. State of coral reefs in the Gala
´pagos Islands: natural vs anthro-
pogenic impacts. Marine Pollution Bulletin 29, 131–140.
Glynn, P.W., 1996. Coral reef bleaching: facts, hypotheses and implications. Global
Change Biology 2, 495–509.
Glynn, P.W., 1997. Bioerosion and coral reef growth: a dynamic balance. In: Bir-
keland, C. (Ed.), Life and Death of Coral Reefs. Chapman & Hall, New York, pp.
68–95.
Glynn, P.W., 2003. Coral communities and coral reefs of Ecuador. In: Corte
´s, J. (Ed.),
Latin American Coral Reefs. Elsevier, Amsterdam, pp. 449–472.
Glynn, P.W., Colley, S.B. (Eds.), 2001. A collection of studies on the effects of the
1997–98 El Nin
˜o-Southern Oscillation event on corals and coral reefs in the
eastern tropical Pacific. Bulletin of Marine Science, 69, pp. 1–288.
Glynn, P.W., Colley, S.B., Ting, J.H., Mate
´, J.L., Guzma
´n, H.M., 2000. Reef coral
reproduction in the eastern Pacific: Costa Rica, Panama
´and Gala
´pagos Islands
(Ecuador). IV. Agariciidae, recruitment and recovery of Pavona varians and
Pavona sp.a. Marine Biology 136, 785–805.
Glynn, P.W., Corte
´s, J., Guzma
´n, H.M., Richmond, R.H., 1988. El Nin
˜o (1982–83)
associated coral mortality and relationship to sea surface temperature devia-
tions in the tropical eastern Pacific. Proceedings of the 6th International Coral
Reef Symposium. Australia 3, 237–243.
Glynn, P.W., D’Croz, L., 1990. Experimental evidence for high temperature stress as
the cause of El Nin
˜o-coincident coral mortality. Coral Reefs 8, 181–191.
Glynn, P.W., de Weerdt, W.H., 1991. Elimination of two reef-building hydrocorals
following the 1982-83 El Nin
˜o warming event. Science 253, 69–71.
Glynn, P.W., Feingold, J.S., 1992. Hydrocoral species not extinct. Science 257, 1845.
Glynn, P.W., Fong, P., 2006. Patterns of reef coral recovery by the regrowth of
surviving tissues following the 1997-98 El Nin
˜o warming and 2000, 2001
upwelling cool events in Panama
´, eastern Pacific. Proceedings of the 10th
International Coral Reef Symposium, Okinawa, 624-630.
Glynn, P.W., Mate
´, J.L., Baker, A.C., Caldero
´n, M.O., 2001. Coral bleaching and
mortality in Panama
´and Ecuador during the 1997–1998 El Nin
˜o-Southern
Oscillation event: spatial/temporal patterns and comparisons with the 1982–
1983 event. Bulletin of Marine Science 69, 79–101.
Glynn, P.W., Perez, M., Gilchrist, S.L., 1985. Lipid decline in stressed corals and their
crustacean symbionts. Biological Bulletin 168, 276–284.
Glynn, P.W., Riegl, B., Correa, A.M.S., Baums, I.B., in press. Rapid recovery of a coral
reef at Darwin Island, Gala
´pagos Islands. Gala
´pagos Research.
Glynn, P.W., von Prahl, H., Guhl, F., 1982. Coral reefs of Gorgona Island, Colombia,
with special reference to corallivores and their influence on community
structure and reef development. Anales del Instituto de Investigaciones Marinas
de Punta de Betı
´n 12, 185–214.
Goreau, T.F., 1964. Mass expulsion of zooxanthellae from Jamaican reef communi-
ties after Hurricane Flora. Science 145, 383–386.
Goreau, T.J., Cervino, J.M., Pollina, R., 2004. Increased zooxanthellae numbers and
mitotic index in electrically stimulated corals. Symbiosis 37, 107–120.
Goreau, T.J., Hayes, R.L.,1994. Coral bleaching and ocean ‘‘hot spots’’. Ambio 23,176–
180.
Goreau, T.J., Hayes, R.L., Clark, J.W., Basta, D.J., Robertson, C.R., 1993. Elevated sea
surface temperatures correlate with Caribbean coral reef bleaching. In:
Geyer, R.A. (Ed.), Global Warming Forum, Scientific, Economic and Legal Over-
view. CRC Press, Boca Raton, FL, pp. 225–255.
Goreau, T.J., Hayes, R.M., Strong, A.E., 1997. Tracking South Pacific coral reef
bleaching by satellite and field observations. Proceedings of the 8th Interna-
tional Coral Reef Symposium. Panama
´2, 1491–1494.
Goreau, T.J., Hilbertz, W., Azeez Hakeem, A., 2000. Increased coral and fish survival
on mineral accretion reef structures in the Maldives after the 1998 bleaching
event. 9th International Coral Reef Symposium, Bali Abstracts, p. 263.
Goreau, T.J., Macfarlane, A.H., 1990. Reduced growth rate of Montastrea annularis
following the 1987–1988 coral-bleaching event. Coral Reefs 8, 211–215.
Goulet, T.L., 2006. Most corals may not change their symbionts. Marine Ecology
ProgressSeries 321, 1–7.
Goulet, T.L., 2007. Most scleractinian corals and octocorals host a single symbiotic
zooxanthella clade. Marine Ecology Progress Series 335, 243–248.
Goulet, T.L., Coffroth, M.A., 2003. Stability of an octocoral-algal symbiosis over time
and space. Marine Ecology Progress Series 250, 117–124.
Graus, R.R., Macintyre, I.G., 1988. Model predictions of the effects of future sea level
rise on the growth of Caribbean coral reefs. Proceedings of the 6th International
Coral Reef Symposium, Townsville (abstract).
Graham, N.A.J., Wilson, S.K., Jennings, S., Polunin, N.V.C., Bijoux, J.P., Robinson, J.,
2006. Dynamic fragility of oceanic coral reef ecosystems. Proceedings of the
National Academy of Sciences USA 103, 8425–8429.
Grebmeier, J.M., Overland, J.E., Moore, S.E., Farley, E.V., Carmack, E.C., Cooper, L.W.,
Frey, K.E., Helle, J.H., McLaughlin, F.A., McNutt, S.L., 2006. A major ecosystem
shift in the northern Bering Sea. Science 311, 1461–1464.
Greenstein, B.J., 2007. Taphonomy: detecting critical events in fossil reef-coral
assemblages. In: Aronson, R.B. (Ed.), Geological Approaches to Coral Reef
Ecology. Ecological Studies 192, pp. 31–60.
Greenstein, B.J., Pandolfi, J.M., 2008. Escaping the heat: range shifts of reef coral
taxa in coastal Western Australia. Global Change Biology 14, 513–528.
Grotolli, A.G., Rodrigues, L.J., Juarez, C., 2004. Lipids and stable carbon isotopes in
two species of Hawaiian corals, Porites compressa and Montipora verrucosa,
following a bleaching event. Marine Biology 145, 621–631.
Grotolli, A.G., Rodrigues, L.J., Palardy, J.E., 2006. Heterotrophic plasticity and resil-
ience in bleached corals. Nature, London 440, 1186–1189.
Guzma
´n, H.M., Corte
´s, J., 1992. Cocos Island (Pacific of Costa Rica) coral reefs after
the 1982–83 El Nin
˜o disturbance. Revista de Biologı
´a Tropical 40, 309–324.
Guzma
´n, H.M., Corte
´s, J., 2001. Changes in reef community structure after fifteen
years of natural disturbances in the eastern Pacific (Costa Rica). Bulletin of
Marine Science 69, 133–149.
Guzma
´n, H.M., Corte
´s, J., 2007. Reef recovery 20 years after the 1982–1983 El Nin
˜o
massive mortality. Marine Biology 151, 401–411.
Guzma
´n, H.M., Robertson, D.R., 1989. Population and feeding responses of the
corallivorous pufferfish Arothron meleagris to coral mortality in the eastern
Pacific. Marine Ecology Progress Series 55, 121–131.
Hagan, A.B., Hamylton, S.M., Spencer, T., 2008. Status of carbonate reefs of the
Amirantes and Alphonse groups, southern Seychelles. In: Obura, D.O., Tame-
lander, J., Linden, O. (Eds.), Ten years after bleaching, facing the consequences of
climate change in the Indian Ocean. CORDIO Status Report, pp. 71–82.
Hagan, A.B., Spencer, T., 2006. Reef recovery at Alphonse Atoll, western Indian
Ocean, following the 1997-98 ocean warming event. Proceedings of the 10th
International Coral Reef Symposium, pp. 676–682.
Halley, R.B., Hudson, J.H., 2007. Fidelity of annual growth in Montastraea faveolata
and the recentness of coral bleaching in Florida. In: Aronson, R.B. (Ed.),
Geological Approaches to Coral Reef Ecology.Ecological Studies 192, pp. 161–178.
Hallock, P., Schlager, W., 1986. Nutrient excess and the demise of coral reefs and
carbonate platforms. Palaios 1, 389–398.
Hallock, P., Williams, D.E., Fisher, E.M., Toler, S.K., 2006. Bleaching in foraminifera
with algal symbionts: implications for reef monitoring and risk assessment.
Anuario do Instituto de Geosciencias UFRJ 29, 108–128.
Harriott, V.J., 1985. Mortality rates of scleractinian corals before and during a mass
bleaching event. Marine Ecology Progress Series 21, 81–88.
Harrison, P.L., Wallace, C.C., 1990. Reproduction, dispersal and recruitment of
scleractinian corals. In: Dubinsky, Z. (Ed.), Coral Reefs. Ecosystems of the World
25. Elsevier, Amsterdam, pp. 133–207.
Hayes, R.L., Goreau, T.J., 1991. The tropical coral reef ecosystem as a harbinger of
global warming. Proceedings of the 2nd International Conference on Global
Warming. World Resources Review 3, 306–322.
Hedley, J.D., Mumby, P.J., 2002. Biological and remote sensing perspectives of
pigmentation in coral reef organisms. Advances in Marine Biology 43, 277–317.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3732
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Hedley, J.D., Roelfsema, C.M., Phinn, S.R., Mumby, P.J., in press. Environmental and
sensor imitations in optical remote sensing of coral reefs: implications for
monitoring and sensor design. Remote Sensing of Environment.
Heron, S.F., Liu, G., Arzayus, L.F., Skirving, W.J., Strong, A.E., 2004. A benefit from
hurricanes. Pervasive Computing and Communication Security (PERSEC) 2004,
Concepcio
´n, Chile.
Highsmith, R.C., 1980. Geographic patterns of coral bioerosion: a productivity
hypothesis. Journal of Experimental Marine Biology and Ecology 46,
177 –196 .
Hochberg, E.J., Atkinson, M.J., 2003. Capabilities of remote sensors to classify coral,
algae, and sand as pure and mixed spectra. Remote Sensing of Environment 85,
174–189.
Hochberg, E.J., Atkinson, M.J., Apprill, A., Andre
´foue
¨t, S., 2004. Spectral reflectance
of coral. Coral Reefs 23, 84–95.
Hoegh-Guldberg, O., 1999. Coral bleaching, climate change and the future of the
world’s coral reefs. Review. Marine and Freshwater Research 50, 839–866.
Hoegh-Guldberg, O., 2006. Introduction. In: Hoegh-Guldberg, O. (Ed.), Under-
standing the Stress Response of Corals and Symbiodiniumin a Rapidly Changing
Environment Global Environment Facility CRTR Report.
Hoegh-Guldberg, O., Fine, M., Skirving, W., Johnstone, R., Dove, S., Strong, A., 2005.
Coral bleaching following wintry weather. Limnology and Oceanography 50,
265–271.
Hoegh-Guldberg, O., Jones, R.J., 1999. Photoinhibition and photoprotection in
symbiotic dinoflagellates from reef-building corals. Marine Ecology Progress
Series 183, 73–86.
Hoegh-Guldberg, O., Jones, R.J., Ward, S., Loh, W.K., 2002. Is coral bleaching really
adaptive? Nature 415, 601–602.
Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P.,
Gomez, E., Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N.,
Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A.,
Hatziolos, M.E., 2007. Coral reefs under rapid climate change and ocean acidi-
fication. Science 318, 1737–1742.
Hoegh-Guldberg, O., Salvat, B., 1995. Periodic mass-bleaching and elevated sea
temperatures: bleaching of outer reef slope communities in Moorea, French
Polynesia. Marine Ecology Progress Series 121, 181–190.
Hoegh-Guldberg, O., Smith, G.J., 1989. The effects of sudden changes in tempera-
ture, light and salinity on the population density and export of zooxanthellae
from the reef corals Stylophora pistillata Esper and Seriatopora hystrix Dana.
Journal of Experimental Marine Biology and Ecology 129, 279–303.
Holden, H., Derksen, C., LeDrew, E., 2001. An examination of spatial autocorrelation
as a means of monitoring coral reef ecosystems. Geoscience and Remote
Sensing Symposium 2, 622–624.
Holden, H., LeDrew, E., 1998. Spectral discrimination of healthy and non-healthy
corals based on cluster analysis, principal components analysis, and derivative
spectroscopy. Remote Sensing of Environment 65, 217–224.
Holden, H., LeDrew, E., 2001a. Hyperspectral discrimination of healthy versus
stressed corals using in situ reflectance. Journal of Coastal Research 17,850–858.
Holden, H., LeDrew, E., 2001b. Coral reef features: multi- vs. hyper-spectral char-
acteristics. Sea Technology, 63–70. February.
Hopley, D., Kinsey, D.W., 1988. The effects of rapid short-term sea-level rise on the
Great Barrier Reef. In: Pearman, G.I. (Ed.), Greenhouse, Planning for Climate
Change. Brill, Leiden, pp. 189–201.
Hoyos, C.D., Agudelo, P.A., Webster, P.J., Curry, J.A., 2006. Deconvolution of the factors
contributing to the increase in global hurricane intensity. Science 312, 94–97.
Hubbard, D.K., 1997. Reefs as dynamic systems. In: Birkeland, C. (Ed.), Life and Death
of Coral Reefs. Chapman & Hall, New York, pp. 43–67.
Hueerkamp, C., Glynn, P.W., D’Croz, L., Mate
´, J.L., Colley, S.B., 2001. Bleaching and
recovery of five eastern Pacific corals in an El Nin
˜o-related temperature
experiment. Bulletin of Marine Science 69, 215–236.
Hughes, T.P., 1994. Catastrophes, phase shifts, and large-scale degradation of
a Caribbean coral reef. Science 265, 1547–1551.
Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C.,
Grosberg, R., Hoegh-Guldberg, O., Jackson, J.B.C., Kleypas, J., Lough, J.M.,
Marshall, P., Nystro
¨m, M., Palumbi, S.R., Pandolfi, J.M., Rosen, B., Roughgarden, J.,
2003. Climate change, human impacts, and the resilience of coral reefs. Science
301, 929–933.
Hughes, T.P., Baird, A.H., Dinsdale, E.A., Moltschaniwskyi, N.A., Pratchett, M.S.,
Tanner, J.E., Willis, B.L., 1999. Patterns of recruitment and abundance of corals
along the Great Barrier Reef. Nature 397, 59–63.
Hutchings, P.A., 1986. Biological destruction of coral reefs. Coral Reefs 4, 239–252.
Iglesias-Prieto, R., Beltra
´n, V.H., LaJeunesse, T.C., Reyes Bonilla, H., Thome
´, P.E., 2004.
Different algal symbionts explain the vertical distribution of dominant reef
corals in the eastern Pacific. Proceedings of the Royal Society B: Biological
Sciences 271, 1757–1763.
Iglesias-Prieto, R., Matta, J.L., Robins, W.A., Trench, R.K., 1992. Photosynthetic
response to elevated temperature in the symbiotic dinoflagellate Symbiodinium
microadriaticum in culture. Proceedings of the National Academy of Sciences
USA 89, 10302–10305.
Iglesias-Prieto, R., Reyes Bonilla, H., Riosmena Rodriguez, R., 2003. Effects of the
1997–1998 ENSO on coral reef communities in the Gulf of California, Mexico.
Geofisica Internacional 42, 467–471.
Iglesias-Prieto, R., Trench, R.K., 1997. Acclimation and adaptation to irradiance in
symbiotic dinoflagellates. II Response of cholorophyll-protein complexes to
different photon-flux densities. Marine Biology 130, 23–33.
IPCC, 1996. Climate change 1995: The science of climate change. Contribution of
working group I. In: Houghton, J.T., Meira Filho, L.G., Callander, B.A., Harris, N.,
Kattenberg, A., Maskell, K. (Eds.), Second Assessment Report of the Intergov-
ernmental Panel on Climate Change. Cambridge University Press, Cambridge.
IPCC, 2001. Climate change 2001: The scientific basis. Contribution of working
group I.J.T. In: Ding, Y., Griggs, D.J., Noguer, M., van der Linden, P.J., Dai, X.,
Maskell, K., Johnson, C.A. (Eds.), Third Assessment Report of the Intergovern-
mental Panel on Climate Change, Houghton. Cambridge University Press,
Cambridge.
IPCC, 2007. Climate change 2007: The physical science basis. Summary for policy-
makers. Contribution of working group I to the fourth assessment report of the
Intergovernmental Panel on Climate Change. http://www.ipcc.ch Website.
Jackson, J.B.C., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque, B.J.,
Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.A., Hughes, T.P., Kidwell, S.,
Lange, C.B., Lenihan, H.S., Pandolfi, J.M., Peterson, C.H., Steneck, R.S., Tegner, M.J.,
Warner, R.R., 2001. Historical overfishing and the recent collapse of coastal
ecosystems. Science 293, 629–638.
Jime
´nez, C.E., Corte
´s, J., 2003. Coral cover change associated to El Nin
˜o, eastern
Pacific, Costa Rica, 1992–2001. P.S.Z.N. Marine Ecology 24, 179–192.
Jokiel, P.L., Brown, E.K., 2004. Global warming, regional trends and inshore envi-
ronmental conditions influence coral bleaching in Hawaii. Global Change
Biology 10, 1627–1641.
Jokiel, P.L., Coles, S.L., 1974. Effects of heated effluent on hermatypic corals at Kahe
point, Oahu. Pacific Science 28, 1–18.
Jokiel, P.L., Coles, S.L., 1977. Effects of temperature on mortality and growth of
Hawaiian reef corals. Marine Biology 43, 201–208.
Jokiel, P.L., Coles, S.L.,1990. Response of Hawaiian and other Indo-Pacific reef corals
to elevated temperature. Coral Reefs 8, 155–162.
Jones, A.M., Berkelmans, R., van Oppen, M.J.H., Mieog, J.C., Sinclair, W., 2008. A
community change in the algal endosymbionts of a scleractinian coral following
a natural bleaching event: field evidence of acclimatization. Proceedings of the
Royal Society B: Biological Sciences 275, 1359–1365.
Jones, G.P., McCormick, M.I., Srinivasan, M., Eagle, J.V., 2004. Coral decline threatens
fish biodiversity in marine reserves. Proceedings of the National Academy of
Sciences USA 101, 8251–8253.
Jones, R.J., 2008. Coral bleaching, bleaching-induced mortality, and the adaptive
significance of the bleaching response. Marine Biology 154, 65–80.
Jones, R.J., Hoegh-Guldberg, O., Larkum, A.W.D., Schreiber, U., 1998. Temperature
induced bleaching of corals begins with impairment of the CO
2
fixation
mechanism in zooxanthellae. Plant, Cell and Environment 21, 1219–1230.
Jones, R.J., Kildea, T., Hoegh-Guldberg, O., 1999. PAM chlorophyll fluorometry: A
new in situ technique for stress assessment in scleractinian corals, used to
examine the effects of cyanide from cyanide fishing. Marine Pollution Bulletin
38, 864–874.
Jordan, I.E., Samways, M.E., 2001. Recent changes in coral assemblages of a South
African coral reef, with recommendations for long-term monitoring. Biodiver-
sity and Conservation 10, 1027–1037.
Kenyon, J.C., Brainard, R.E., Hoeke, R.K., Parrish, F.A., Wilkinson, C.B., 20 06. Towed-
diver surveys, a method for mesoscale spatial assessment of benthic reef
habitat: a case study at Midway Atoll in the Hawaiian Archipelago. Environ-
mental Management 34, 339–349.
Kinsman, D.J.J., 1964. Reef coral tolerance of high temperature and salinities. Nature
202, 1280–1282.
Kirke, B., 2003. Enhancing fish stocks with wave-powered artificial upwelling.
Ocean and Coastal Management 46, 901–915.
Kleypas, J.A., 2007. Constraints on predicting coral reef response to climate change.
In: Aronson, R.B. (Ed.), Geological Approaches to Coral Reef Ecology. Ecological
Studies 192. Springer, pp. 386–424.
Kleypas, J.A., Buddemeier, R.W., Archer, D., Gattuso, J.P., Langdon, C., Opdyke, B.N.,
1999. Geochemical consequences of increased atmospheric carbon dioxide on
coral reefs. Science 284, 118–120.
Kleypas, J.A., Buddemeier, R.W., Gattuso, J.-P., 2001. The future of coral reefs in an
age of global change. International Journal of Earth Science (Geologischen
Rundschau) 90, 426–437.
Kleypas, J.A., Danabasoglu, G., Lough, J.M., 2008. Potential role of the ocean ther-
mostat in determining regional differences in coral reef bleaching events.
Geophysical Research Letters 35, L03613, doi:10.1029/2007GL032257.
Kleypas, J.A., Langdon, C., 2006. Coral reefs and changing seawater carbonate chem-
istry. In: Phinney, J.T., Hoegh-Guldberg, O., Kleypas, J., Skirving, W., Strong, A.
(Eds.), Coral Reefs and Climate Change: Science and Management. Coastal and
Estuarine Studies 61. American Geophysical Union, Washington, DC, pp. 73–110.
Knowlton, N., 2001. The future of coral reefs. Proceedings of the National Academy
of Sciences USA 98, 5419–5425.
Knowlton, N., Rohwer, F., 2003. Multispecies microbial mutualisms on coral reefs:
the host as a habitat. American Naturalist 162, S51–S62.
Kokita, T., Nakazono, A., 2001. Rapid response of an obligately corallivorous filefish
Oxymonacanthus longirostris (Monacanthidae) to a mass coral bleaching event.
Coral Reefs 20, 155–158.
Kramer, P.A., 2003. Synthesis of coral reef health indicators for the western Atlantic:
results of the AGRAA program (1997-2000). In: Lang, J.C. (Ed.), Status of Coral
Reefs in the Western Atlantic: Results of Initial Surveys, Atlantic and Gulf Rapid
Reef Assessment (AGRAA) Program. Atoll Research Bulletin, 496, pp. 1–57.
Lambo, A.L., Ormond, R.F.G., 2006. Continued post-bleaching decline and changed
benthic community of a Kenyan coral reef. Marine Pollution Bulletin 52, 1617–1624.
Langdon, C., Takahashi, T., Sweeney, C., Chipman, D., Goddard, J., Marubini, F.,
Aceves, H., Barnett, H., Atkinson, M.J., 2000. Effect of calcium carbonate satu-
ration state on the calcification rate of an experimental coral reef. Global
Biogeochemical Cycles 14, 639–654.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 33
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

LaJeunesse, T.C., Lee, S., Bush, S., Bruno, J.F., 2005. Persistence of non-Caribbean algal
symbionts in Indo-Pacific mushroom corals released to Jamaica 35 years ago.
Coral Reefs 24, 157–159.
LaJeunesse, T.C., Reyes-Bonilla, H., Warner, M.E., 2007. Spring ‘‘bleaching’’ among
Pocillopora in the Sea of Cortez, eastern Pacific. Coral Reefs 26, 265–270.
LaJeunesse, T.C., Thornhill, D.J., Cox, E.F., Stanton, F.G., Fitt, W.K., Schmidt, G.W.,
2004. High diversity and host specificity observed among symbiotic dinofla-
gellates in reef coral communities from Hawaii. Coral Reefs 23, 596–603.
Leder, J.J., Szmant, A.M., Swart, P.K., 1991. The effect of prolonged ‘‘bleaching’’ on
skeletal banding and stable isotope composition in Montastrea annularis.
Preliminary observations. Coral Reefs 10, 19–27.
Ledlie, M.H., Graham, N.A.J., Bythell, J.C., Wilson, S.K., Jennings, S., Polunin, N.V.C.,
Hardcastle, J., 2007. Phase shifts and the role of herbivory in the resilience of
coral reefs. Coral Reefs 26, 641–653.
LeDrew, E.F., Holden, H., Wulder, M., Derksen, C., Newman, C., 2004. A spatial
statistical operator applied to multidate satellite imagery for identification of
coral reef stress. Remote Sensing of Environment 91, 271–279.
Leibold, M.A., Norberg, J., 2004. Biodiversity in metacommunities: plankton as
complex adaptive systems? Limnology and Oceanography 49, 1278–1289.
Lesser, M.P., 1996. Exposure of symbiotic dinoflagellates to elevated temperatures
and ultraviolet radiation causes oxidative stress and inhibits photosynthesis.
Limnology and Oceanography 41, 271–283.
Lesser, M.P., 1997. Oxidative stress causes coral bleaching during exposure to
elevated temperatures. Coral Reefs 16, 187–192.
Lesser, M.P., 2004. Experimental biology of coral reef ecosystems. Journal of
Experimental Marine Biology and Ecology 300, 217–252.
Lesser, M.P., 2006. Oxidative stress in marine environments: Biochemistry and
physiological ecology. Annual Review of Physiology 68, 253–278.
Lesser, M.P., Bythell, J.C., Gates, R.D., Johnstone, R.W., Hoegh-Guldberg, O., 2007. Are
infectious diseases really killing corals? Alternative interpretations of the
experimental and ecological data. Journal of Experimental Marine Biology and
Ecology 346, 36–44.
Lesser, M.P., Stochaj, W.R., Tapley, D.W., Shick, J.M., 1990. Bleaching in coral reef
anthozoansdeffects of irradiance, ultraviolet radiation, and temperature on the
activities of protective enzymes against active oxygen. Coral Reefs 8, 225–232.
Leuliette, E.W., Nerem, R.S., Mitchum, G.T., 2004. Calibration of TOPEX/Poseidon and
Jason altimeter data to construct a continuous record of mean sea level change.
Marine Geodesy 27, 79–94.
Levin, S.A., 1998. Ecosystems and the biosphere as complex adaptive systems.
Ecosystems 1, 431–436.
Lewis, C.L., Coffroth, M.A., 2004. The acquisition of exogenous algal symbionts byan
octocoral after bleaching. Science 304, 1490–1492.
Lindahl, U., Ohman, M.C., Schelten, C.K., 2001. The 1997/1998 mass mortality of
corals: effects on fish communities on a Tanzanian coral reef. Marine Pollution
Bulletin 42, 127–131.
Liu, G., Skirving, W., Strong, A.E., 2003. Remote sensing of sea surface temperatures
during 2002 Barrier reef coral bleaching. Eos Transactions 84, 137–144.
Loch, K., Loch, W., Schuhmacher, H., See, W.R., 2002. Coral recruitment and
regeneration on a Maldivian reef 21 months after the coral bleaching event of
1998. P.S.Z.N.: Marine Ecology 23, 219–236.
Loch, K., Loch, W., Schuhmacher, H., See, W.R., 2004. Coral recruitment and
regeneration on a Maldivian reef four years after the coral bleaching event of
1998. Part 2: 2001-2002. P.S.Z.N. Marine Ecololgy 25, 145–154.
Lough, J.M., 2000. 1997–98: unprecedented thermal stress to coral reefs?
Geophysical Research Letters 27, 3901–3904.
Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., van Woesik, R., 2001. Coral
bleaching, the winners and the losers. Ecology Letters 4, 122–131.
Macintyre, I.G., Glynn, P.W., Corte
´s, J., 1992. Holocene reef history in the eastern
Pacific: mainland Costa Rica, Can
˜o Island, Cocos Island, and Gala
´pagos Islands.
Proceedings of the 7th International Coral Reef Symposium, Guam 2,1174–1184.
Manzello, D.P., Berkelmans, R., Hendee, J.C., 2007a. Coral bleaching indices and
thresholds for the Florida reef tract, Bahamas, and St. Croix, US Virgin Islands.
Marine Pollution Bulletin 54, 1923–1931.
Manzello, D.P., Brandt, M., Smith, T.B., Lirman, D., Hendee, J.C., Nemeth, R.S., 2007b.
Hurricanes benefit bleached corals. Proceedings of the National Academy of
Sciences USA 104, 12035–12039.
Marshall, P.A., Baird, A.H., 2000. Bleaching of corals on the Great Barrier Reef:
differential susceptibilities among taxa. Coral Reefs 19, 155–163.
Marshall, P.A., Schuttenberg, H.Z., 2006a. Adapting coral reef management in the
face of climate change. In: Phinney, J.T., Hoegh-Guldberg, O., Kleypas, J.,
Skirving, W., Strong, A. (Eds.), Coastal and Estuarine Studies 61 American
Geophysical Union, Washington, DC, pp. 223–241.
Marshall, P.A., Schuttenberg, H.Z., 2006b. A Reef Manager’s Guide to Coral Bleach-
ing. Great Barrier Reef Marine Park Authority, Townsville, Australia.
Martinez, J.L., Baquero, F., 2002. Interactions among strategies associated with
bacterial infection, pathogenicity, epidemicity, and antibiotic resistance. Clinical
Microbiology Reviews 15, 647–679.
Mascarelli, P., Bunkley-Williams, L., 1999. An experimental field evaluation of
healing in damaged, unbleached and artificially bleached star coral, Montastrea
annularis. Bulletin of Marine Science 65, 577–586.
Mate
´, J.L., 2003. Corals and coral reefs of the Pacific coast of Panama
´. In: Corte
´s, J.
(Ed.), Latin American Coral Reefs. Elsevier, Amsterdam, pp. 387–417.
Mayer, A.G.,1914. The effects of temperature upon marine animals. Papers from the
Tortugas Laboratory of the Carnegie Institution of Washington 6, 3–24.
McClanahan, T.R., 2000a. Bleaching damage and recovery potential of Maldivian
coral reefs. Marine Pollution Bulletin 40, 587–597.
McClanahan, T.R., 2000b. Coral reef use and conservation. In: McClanahan, T.R.,
Sheppard, C.R.C., Obura, D.O. (Eds.), Coral Reefs of the Indian Ocean: Their
Ecology and Conservation. Oxford University Press, Oxford, pp. 39–80.
McClanahan, T.R., 2004. The relationship between bleaching and mortality of
common corals. Marine Biology 144, 1239–1245.
McClanahan, T.R., 2008. Response of the coral reef benthos and herbivory to fishery
closure management and the 1998 ENSO disturbance. Oecologia 155, 169–177.
McClanahan, T.R., Ateweberhan, M., Graham, N.A.J., Wilson, S.K., Ruiz Sebastia
´n, C.,
Guillaume, M.M.M., Bruggemann, J.H., 2007b. Western Indian Ocean coral
communities: bleaching responses and susceptibility to extinction. Marine
Ecology Progress Series 337, 1–13.
McClanahan, T.R., Ateweberhan, M., Muhando, C.A., Maina, J., Mohammed, M.S.,
2007a. Effects of climate and seawater temperature variation on coral bleaching
and mortality. Ecological Monographs 77, 503–525.
McClanahan, T.R., Atweberhan, M., Ruiz Sebastian, C., Graham, N.A.J., Wilson, S.,
Bruggemann,J.H., Guillaume,M.M.M., 2007c. Predictabilityof coral bleachingfrom
synoptic satellite and in situ temperatureobservations. Coral Reefs 26, 695–701.
McClanahan, T.R., Baird, A.H., Marshall, P.A., Toscano, M.A., 2004. Comparing
bleaching and mortality responses of hard corals between southern Kenya and
the Great Barrier Reef, Australia. Marine Pollution Bulletin 48, 327–335.
McClanahan, T.R., Baker, A.C., Atweberhan, M., Maina, J., Moothien-Pillai, K.R.,
2005b. Refining coral bleaching experiments and models through reiterative
field studies. Marine Ecology Progress Series 305, 301–303.
McClanahan, T.R., Maina, J., 2003. Response of coral assemblages to the interaction
between natural temperature variation and rare warm-water events. Ecosys-
tems 6, 551–563.
McClanahan, T.R., Maina, J., Moothien-Pillai, K.R., Baker, A.C., 2005a. Effects of
geography, taxa, water flow, and temperature variation on coral bleaching
intensity in Mauritius. Marine Ecology Progress Series 298, 131–142.
McClanahan, T.R., Maina, J., Starger, C.J., Herron-Perez, P., Dusek, E., 2005c. Detri-
ments to post-bleaching recovery of corals. Coral Reefs 24, 230–246.
McClanahan, T.R., Sheppard, C.R.C., Obura, D.O. (Eds.), 2000. Coral Reefs of the Indian
Ocean: Their Ecology and Conservation. Oxford University Press, 525 pp.
McCook, L.J., Folke, C., Hughes, T., Nystrom, M., Obura, D., Salm, R., 2007. Ecological
resilience, climate change and the Great Barrier Reef. In: Johnson, J.E.,
Marshall, P.A. (Eds.), Climate Change and the Great Barrier Reef. Great Barrier
Reef Marine Park Authority, Townsville, Australia.
McWilliams, J.P., Co
ˆte
´, I.M., Gill, J.A., Sutherland, W.J., Watkinson, A.R., 2005.
Accelerating impacts of temperature-induced coral bleaching in the Caribbean.
Ecology 86, 2055–2060.
Meesters, E.H., Bak, R.P.M., 1993. Effects of coral bleaching on tissue regeneration
potential and colony survival. Marine Ecology Progress Series 96, 189–198.
Mendes, J.M., Woodley, J.D., 2002. Effect of the 1995-1996 bleaching event on polyp
tissue depth, growth, reproduction and skeletal band formation in Montastraea
annularis. Marine Ecology Progress Series 235, 93–102.
Mieog, J.C., van Oppen, M.J.H., Cantin, N.E., Stam, W.T., Olsen, J.L., 2007. Real-time
PCR reveals a high incidence of Symbiodinium clade D at low levels in four
scleractinian corals across the Great Barrier Reef: implications for symbiont
shuffling. Coral Reefs 26, 449–457.
Moran, P.J., 1986. The Acanthaster phenomenon. Oceanography and Marine Biology
Annual Reviews 24, 379–480.
Morton, B., Blackmore, G., Kwok, C.T., 2002. Corallivory and prey choice by Drupella
rugosa (Gastropoda: Muricidae) in Hong Kong. Journal of Molluscan Studies 68,
217–223.
Mumby, P.J., 1999. Bleaching and hurricane disturbances to populations of coral
recruits in Belize. Marine Ecology Progress Series 190, 27–35.
Mumby, P.J., Chisholm, J.R.M., Edwards, A.J., Andrefouet, S., Jaubert, J., 2001a. Cloudy
weather may have saved Society Islands reef corals during the 1998 ENSO
event. Marine Ecology Progress Series 222, 209–216.
Mumby, P.J., Chisholm, J.R.M., Edwards, A.J., Clark, C.D., Roark, E.B., Andre
´foue
¨t, S.,
Jaubert, J., 2001b. Unprecedented bleaching-induced mortality in Porites spp. at
Rangiroa Atoll, French Polynesia. Marine Biology 139, 183–189.
Mumby, P.J., Hedley, J.D., Chisholm, J.R.M., Clark, C.D., Ripley, H., Jaubert, J., 2004.
The cover of living and dead corals from airborne remote sensing. Coral Reefs
23, 171–183.
Munday, P.L., Jones, G.P., Sheaves, M., Williams, A.J., Goby, G., 2007. Vulnerability of
fishes of the Great Barrier Reef to climate change. In: Johnson, J., Marshall, P.
(Eds.), Climate Change and the Great Barrier Reef: A Vulnerability Assessment.
Great Barrier Reef Marine Park Authority, Townsville, Australia, pp. 357–392.
Muscatine, L., Porter, J.W., 1977. Reef corals: mutualistic symbioses adapted to
nutrient-poor environments. BioScience 27, 454–460.
Nakamura, T., van Woesik, R., 2001. Water-flow rates and passive diffusion partially
explain differential survival of corals during the 1998 bleaching event. Marine
Ecology Progress Series 212, 301–304.
Nakamura, T., van Woesik, R., Yamasaki, H., 2005. Photoinhibition of photosynthesis
is reduced by water flow in the reef-building coral Acropora digitifera. Marine
Ecology Progress Series 301, 109–118.
Nakamura, T., Yamasaki, H., van Woesik, R., 2003. Water flow facilitates recovery
from bleaching in the coral Stylophora pistillata. Marine Ecology Progress Series
256, 287–291.
Neumann, A.C., Macintyre, I., 1985. Reef response to sealevel rise: keep-up, catch-
up, or give-up. Proceedings of the Fifth International Coral Reef Congress. Tahiti
3, 105–110.
Omori, M., Fukami, H., Kobinata, H., Hatta, M., 2001. Significant drop of fertilization
of Acropora corals in 1999: an after-effect of heavy coral bleaching? Limnology
and Oceanography 46, 704–706.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3734
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Otis, D.B., Carder, K.L., English, D.C., Ivey, J.E., 2004. CDOM transport from the
Bahamas Banks. Coral Reefs 23, 152–160.
Palandro, D., Andre
´foue
¨t, S., Dustan, P., Muller-Karger, F.E., 2003a. Change detection
in coral reef communities using Ikonos satellite imagery and historic aerial
photographs. International Journal of Remote Sensing 24, 873–878.
Palandro, D., Andre
´foue
¨t, S., Muller-Karger, F.E., Dustan, P., Hu, C., Hallock, P., 20 03b.
Detection of changes in coral reef communities using Landsat-5 TM and
Landsat-7 ETMþdata. Canadian Journal of Remote Sensing 29, 201–209.
Pandolfi, J.M., 1999. Response of Pleistocene coral reefs to environmental change
over long temporal scales. American Zoologist 39, 113–130.
Pandolfi, J.M., Bradbury, R.H., Sala, E., Hughes, T.P., Bjorndal, K.A., Cooke, R.G.,
McArdle, D., McClenachan, L., Newman, M.J.H., Paredes, G., Warner, R.R.,
Jackson, J.B.C., 2003. Global trajectories of the long-term decline of coral reef
ecosystems. Science 301, 955–958.
Pandolfi, J.M., Jackson, J.B.C., 2006. Ecological persistence interrupted in Caribbean
coral reefs. Ecology Letters 9, 818–826.
Pandolfi, J.M., Jackson, J.B.C., Baron, N., Bradbury, R.H., Guzma
´n, H.M., Hughes, T.P.,
Kappel, C.V., Micheli, F., Ogden, J.C., Possingham, H.P., Sala, E., 2005. Are U.S.
coral reefs on the slippery slope to slime? Science 307, 1725–1726.
Parmesan, C., Yohe, G., 2002. A globally coherent fingerprint of climate change
impacts across natural systems. Nature 421, 37–42.
Patton, W.K.,1976. Animal associates of living reef corals. In: Jones, O.A., Endean, R. (Eds.),
Biology and Geology of Coral Reefs.Biol. 2, Vol. 3. Academic Press, New York, pp.1–36.
Pearson, R.G., 1981. Recovery and recolonization of coral reefs. Marine Ecology
Progress Series 4, 105–122.
Pereira, M.A.M., Videira, E.J.S., Motta, H., Louro, C.M.M., Abrantes, G.S.,
Schleyer, M.H., 2003. Coral reef monitoring in Mozambique III: 2002 Report.
MICOA/CORDIO/WWF, Maputo, 16 pp.
Perry, C.T., Hepburn, L.J., 2008. Syn-depositional alteration of coral reef framework
through bioerosion, encrustation and cementation: taphonomic signatures of
reef accretion and reef depositional events. Earth Science Reviews 86,
106–144.
Phinney, J.T., Hoegh-Guldberg, O., Kleypas, J., Skirving, W., Strong, A., 2006. Coral
reefs and climate change: science and management. In: Coastal and Estuarine
Studies 61. American Geophysical Union, Washington, DC.
Pittock, A.B., 1999. Coral reefs and environmental change: Adaptation to what?
American Zoologist 39, 10–29.
Podesta
´, G.P., Glynn, P.W., 1997. Sea surface temperature variability in Panama
´and
Gala
´pagos: extreme temperatures causing coral bleaching. Journal of
Geophysical Research 102 (C7), 15749–15759.
Podesta
´, G.P., Glynn, P.W., 2001. The 1997-98 El Nin
˜o event in Panama
´and Gal-
a
´pagos: an update of thermal stress indices relative to coral bleaching. Bulletin
of Marine Science 69, 43–59.
Porter, J.W., Fitt, W.K., Spero, H.J., Rogers, C.S., White, M.W., 1989. Bleaching in reef
corals: physiological and stable isotopic responses. Proceedings of the. National
Academy of Sciences USA 86, 9342–9346.
Pratchett, M.S., Munday, P.L., Wilson, S.K., Graham, N.A.J., Cinner, J.E., Bellwood, D.R.,
Jones, G.P., Polunin, N.V.C., McClanahan, T.R., 2008. Effects of climate-induced
coral bleaching on coral-reef fishesdecological and economic consequences.
Oceanography and Marine Biology: An Annual Review 46, 251–296.
Pratchett, M.S., Wilson, S.K., Berumen, M.L., McCormick, M.I., 2004. Sub-lethal
effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs
23, 352–356.
Pratchett, M.S., Wilson, S.K., Graham, N.A.J., Munday, P.M., Jones, G.P.,
Polunin, N.V.C., 2009. Coral bleaching and consequences for motile reef
organisms: past, present and uncertain future effects. In: van Oppen, M.J.H.,
Lough, J.M. (Eds.), Coral Bleaching: Patterns and Processes, Causes and Conse-
quences, Ecological Studies,, vol. 205 Springer, New York, pp. 139–158.
Precht, W.F., Aronson, R.B., 2004. Climate flickers and range shifts of reef corals.
Frontiers in Ecology and the Environment 2, 307–314.
Purkis, S.J., 2005. A ‘‘reef-up’’ approach to classifying coral habitats from IKONOS
imagery. IEEE Transactions in Geoscience and Remote Sensing 43, 1375–1390.
Purkis, S.J., Riegl, B., 2005. Spatial and temporal dynamics of Arabian Gulf coral
assemblages quantified from remote-sensing and in situ monitoring data.
Marine Ecology Progress Series 287, 99–113.
Purkis, S.J., Riegl, B., Andre
´foue
¨t, S., 2005. Remote sensing of geomorphology and
facies pattern on a modern carbonate ramp (Arabian Gulf; Dubai, UAE). Journal
of Sedimentary Research 75, 861–876.
Randall, J.E., Allen, G.R., Steene, R., 1990. Fishes of the Great Barrier Reef and Coral
Sea. Crawford House Press, Bathurst, NSW, Australia.
Razak,T.B., Hoeksema,B.W., 2003. Thehydrocoralgenus Millepora(Hydrozoa:Capitata:
Milleporidae) in Indonesia. Zoologische Verhande lingen Leiden 345, 313–336.
Reaka-Kudla, M.L., Feingold, J.S., Glynn, P.W., 1996. Experimental studies of rapid
bioerosion of coral reefs in the Gala
´pagos Islands. Coral Reefs 15, 101–107.
Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I., Rosenberg, E., 2006. The coral
probiotic hypothesis. Environmental Microbiology 8, 2068–2073.
Reyes-Bonilla, H., 2001. Effects of the 1997–1998 El Nin
˜o-Southern Oscillation on
coral communities of the Gulf of California, Me
´xico. Bulletin of Marine Science
69, 251–266.
Reyes-Bonilla, H., 2003. Coral reefs of the Pacific coast of Me
´xico. In: Corte
´s, J. (Ed.),
Latin American Coral Reefs. Elsevier, Amsterdam, pp. 331–349.
Richardson, L.S., 1998. Coral diseases: what is really known? Trends in Ecology and
Evolution 13, 438–443.
Richmond, R.H., 1997. Reproduction and recruitment in corals: critical links in the
persistence of reefs. In: Birkeland, C. (Ed.), Life and Death of Coral Reefs.
Chapman & Hall, New York, pp. 175–197.
Riegl, B., 1999. Corals in a non-reef setting in the southern Arabian Gulf (Dubai,
UAE): fauna and community structure in response to recurrent mass mortality.
Coral Reefs 18, 63–73.
Riegl, B., 2001. Inhibition of reef framework by frequent disturbance: examples
from the Arabian Gulf, South Africa, and the Cayman Islands. Palaeogeography,
Palaeoclimatology. Palaeoecology 175, 79–101.
Riegl, B., 2002. Effects of the 1996 and 1998 positive sea-surface temperature
anomalies on corals, coral diseases and fish in the Arabian Gulf (Dubai, UAE).
Marine Biology 140, 29–40.
Riegl, B., 2003. Global climate change and coral reefs: different effects in two high
latitude areas (Arabian Gulf, South Africa). Coral Reefs 22, 433–446.
Riegl, B., 2007. Extreme climatic events and coral reefs: how much short-term
threat from global change? In: Aronson, R.B. (Ed.), Geological Approaches to
Coral Reef Ecology. Ecological Studies 192. Springer, pp. 315–341.
Riegl, B., Piller, W.E., 2001. Cryptic tissues inside Acropora frameworks: a mecha-
nism to enhance tissue survival in hard times while also enhancing framework
density. Coral Reefs 5, 67–68.
Riegl, B., Purkis, S.J., 2005. Detection of shallow subtidal corals from IKONOS
satellite and QTC View (50, 200 kHz) single-beam sonar data (Arabian Gulf;
Dubai, UAE). Remote Sensing of Environment 95, 96–114.
Riegl, B., Korrubel, J.L., Martin, C., 2001. Mapping and monitoring of coral
communities and their spatial patterns using a surface-based video method
from a vessel. Bulletin of Marine Science 69, 869–880.
Roberts, C.M., McClean, C.J., Veron, J.E.N., Hawkins, J.P., Allen, G.R., McAllister, D.E.,
Mittermeier, C.G., Schueler, F.W., Spalding, M., Wells, F., Vynne, C., Werner, T.B.,
2002. Marine biodiversity hotspots and conservation priorities for tropical
reefs. Science 295, 1280–1284.
Rodolfo-Metalpa, R., Bianchi, C.N., Peirano, A., Morri, C., 2005. Tissue necrosis and
mortality of the temperate coral Cladocora caespitosa. Italian Journal of Zoology
72, 271–276.
Rodolfo-Metalpa, R., Richard, C., Allemand, D., Bianchi, C.N., Morri, C., Ferrier-
Pages, C., 2006. Response of zooxanthellae in symbiosis with the Mediterranean
corals Cladocora caespitosa and Oculina patagonica to elevated temperatures.
Marine Biology 150, 45–55.
Rodrigues, L.J., Grottoli, A.G., 2007. Energy reserves and metabolism as indicators of
coral recovery from bleaching. Limnology and Oceanography 52, 1874–1882.
Rodrigues, M.J., Motta, H., Pereira, M.A.M., Goncalves, M., Carvalho, M., Schleyer,
M.H., 2000. Reef monitoring in Mozambique. I: The monitoring programme and
1999 report. Unpublished report, 65 pp.
Rodriguez-Lanetty, M., 2003. Evolving lineages of Symbiodinium-like dinoflagellates
based on ITS1 rDNA. Molecular Phylogenetics and Evolution 28, 152–168.
Rogers, C.S., Miller, J., Muller, E.M., Edmunds, P., Nemeth, R.S., Beets, J.P.,
Friedlander, A.M., Smith, T.B., Boulon, R., Jeffrey, C.F.G., Menza, C., Caldow, C.,
Idrisi, N., Kojis, B., Monaco, M.E., Spitzack, A., Gladfelter, E.H., Ogden, J.C., Hillis-
Starr, Z., Lundgren, I., Schill, W.B., Kuffner, I.B., Richardson, L.L., Devine, B.E.,
Voss, J.D., 2008. Ecology of coral reefs in the US Virgin Islands. In: Riegl, B.M.,
Dodge, R.E. (Eds.), Coral Reefs of the USA. Springer, Berlin, pp. 303–373.
Rohwer, F., Seguritan, V., Azam, F., Knowlton, N., 2002. Diversity and distribution of
coral-associated bacteria. Marine Ecology Progress Series 243, 1–10.
Rosenberg, E., Ben-Haim, Y., 2002. Microbial diseases of corals and global warming.
Environmental Microbiology 4, 318–326.
Rowan, R., 2004. Thermal adaptation in reef coral symbionts. Nature 430, 742.
Rowan, R., Knowlton, N., 1995. Intraspecific diversity and ecological zonation in
coral-algal symbionts. Proceedings of the National Academy of Sciences USA 92,
2850–2853.
Rowan, R., Knowlton, N., Baker, A.C., Jara, J., 1997. Landscape ecology of algal
symbiont communities explains variation in episodes of coral bleaching. Nature
388, 265–269.
Rowlands, G.P., Purkis, S., Riegl, B., 2008. The 2005 coral-bleaching event Roatan
(Honduras): use of pseudo-invariant features (PIFs) in satellite assessment.
Journal of Spatial Science 53, 99–112.
Salih, A., Hoegh-Guldberg, O., Cox, G., 1998. Bleaching responses of coral zooxan-
thellae: the effects of light and elevated temperature on their morphology and
physiology. In: Greenwood, J.G., Hall, N.J. (Eds.), Proceedings of the Australian
Coral Reef Society Conference 1997. School of Marine Science, University of
Queensland, Brisbane, pp. 206–216.
Salih, A., Larkum, A., Cox, G., Kuhl, M., Hoegh-Guldberg, O., 2000. Fluorescent
pigments in corals are photoprotective. Nature 408, 850–853.
Salm, R., Smith, S.E., Llewelyn, G., 2001. Mitigating the impact of coral bleaching
through marine protected area design. In: Schuttenberg, H.Z. (Ed.), Coral
Bleaching: Causes, Consequences and Response. Papers presented at the 9th
ICRS session on ‘‘Coral Bleaching: Assessing and Linking Ecological and Socio-
economic Impacts, Future Trends and Mitigation Planning’’. Coastal Resources
Center, Narragansett, RI, ISBN 1-885454-40-6, pp. 81–88. Coastal Management
Report #2230.
Sammarco, P.W., Winter, A., Steward, J.C., 2006. Coefficient of variation of sea
surface temperature (SST) as an indicator of coral bleaching. Marine Biology
149, 1337–1344.
Salm, R.V., Coles, S.L. (Eds.), 2001. Coral Bleaching and Marine Protected Areas.
Proceedings of the Workshop on Mitigating Coral Bleaching Impact Through
MPA Design, Bishop Museum, Honolulu, Hawaii, 29-31 May 2001. Asia Pacific
Coastal Marine Program Report #0102, The Nature Conservancy, Honolulu,
Hawaii, U.S.A: 118 pp.
Salvat, B., 1992. Blanchissement et mortalite
´des scle
´ractinaires sur les re
´cifs de
Moorea (archipel de la socie
´te
´) en 1991. Comptes rendus de l’Acade
´mie des
sciences. Se
´rie 3. Sciences de la vie 314, 105–111.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 35
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Sandeman, I.M., 1988. Coral bleaching at Discovery Bay, Jamaica: a possible
mechanism for temperature-related bleaching. In: Ogden, J., Wicklund, R. (Eds.),
Mass Bleaching of Coral Reefs in the Caribbean: A Research Strategy. National
Oceanic and Atmospheric Administration, U.S. Department of Commerce,
Washington DC, pp. 46–48. National Undersea Research Program, Research
Report 88-2.
Sano, M., 2004. Short-term effects of a mass coral bleaching event on a reef fish
assemblage at Iriomote Island, Japan. Fisheries Science 70, 41–46.
Santer, B.D., Mears, C., Wentz, F.J., Taylor, K.E., Gleckler, P.J., Wigley, T.M.L.,
Barnett, T.P., Boyle, J.S., Bruggemann, W., Gillett, N.P., Klein, S.A., Meehl, G.A.,
Nozawa, T., Pierce, D.W., Stott, P.A., Washington, W.M., Wehner, M.F., 2007.
Identification of human-induced changes in atmospheric moisture content.
Proceedings of the National Academy of Sciences USA 104, 15248–15253.
Santos, S.R., Coffroth, M.A., 2003. Molecular genetic evidence that dinoflagel-
lates belonging to the genus Symbiodinium are haploid. Biological Bulletin
204, 10–20.
Santos, S.R., Guiterrez-Rodriguez, C., Lasker, H.R., Coffroth, M.A., 2003. Symbiodi-
nium sp. associations in the gorgonian Pseudopterogorgia elisabethae in the
Bahamas: high levels of genetic variability and population structure in symbi-
otic dinoflagellates. Marine Biology 143, 111–120.
Sarmiento, J.L., Slater, R., Barber, R., Bopp, L., Doney, S.C., Hirst, A.C., Kleypas, J.,
Matear, R., Mikolajewicz, U., Monfray, P., Soldatov, V., Spall, S.A., Stouffer, R.,
2004. Response of ocean ecosystems to climate warming. Global Biogeochem-
ical Cycles 18, GB3003, doi:10.1029/2003GB002134. 2004.
Saxby, T., Dennison, W.C., Hoegh-Guldberg, O., 20 03. Photosynthetic responses of
the coral Montipora digitata to cold temperature stress. Marine Ecology Progress
Series 248, 85–97.
Schleyer, M.H., Kruger, A., Celliers, L., 2008. Long-term community changes on
a high-latitude coral reef in the Greater St. Lucia Wetland Park. South Africa
Marine Pollution Bulletin 56, 493–502.
Schleyer, M.H., Maggs, J.Q., 2008. Surveys of reef benthos conducted in the Bazaruto
Archipelago on behalf of Sasol in 2007. Oceanographic Research Institute,
Durban, Unpublished Report (257): 9 pp.
Schuhmacher, H., Loch, K., Loch, W., See, W.R., 2005. The aftermath of coral
bleaching on a Maldivian reefda quantitative study. Facies 51, 80–92.
Scott, P.J.B., Risk, M.J., Carriquiry, J.D., 1988. El Nin
˜o, bioerosion and the survival of
east Pacific reefs. Proceedings of the 6th International Coral Reef Symposium,
Townsville 2, 517–520.
Selig, E.R., Harvell, C.D., Bruno, J.F., Willis, B.L., Page, C.A., Casey, K.S., Sweatman, H.,
2006. Analyzing the relationship between ocean temperature anomalies and
coral disease outbreaks at broad spatial scales. In: Phinney, J.T., Hoegh-
Guldberg, O., Kleypas, J., Skirving, W., Strong, A. (Eds.), Coral Reefs and Climate
ChangedScience and Management. Coastal and Estuarine Studies 61. American
Geophysical Union, pp. 111–128.
Sharp, V.A., Brown, B.E., Miller, D., 1997. Heat shock protein (hsp70) expression
in the tropical reef coral Goniopoa djiboutiensis. Journal of Thermal Biology
22, 11–19.
Sheppard, C.R.C., 2003. Predicted recurrences of mass coral mortality in the Indian
Ocean. Nature 425, 294–297.
Sheppard, C.R.C., 2006. Longer-term impacts of climate change on coral reefs. In:
Co
ˆte
´, I.M., Reynolds, J.D. (Eds.), Coral Reef Conservation. Cambridge University
Press, Cambridge, UK, pp. 264–290.
Sheppard, C.R.C., Spalding, M., Bradshaw, C., Wilson, S., 2002. Erosion vs. recovery of
coral reefs after 1998 El Nin
˜o: Chagos Reefs, Indian Ocean. Ambio 31, 40–48.
Shibuno, T., Hashimoto, K., Abe, O., Takada, Y., 1999. Short-term changes in the
structure of a fish community following coral bleaching at Ishigaki Island,
Japan. Galaxea JCRS 1, 51–58.
Shibuno, T., Hashimoto, K., Abe, O., Takada, Y., Kawasaki, H., 2002. Disturbed coral
reefs and the effects upon the structure of fish communities at Ishigaki Island,
Japan. Fisheries Science 68 (Suppl. 1), 139–142.
Shick, J.M., Lesser, M.P., Jokiel, P.J.,1996. Effects of ultraviolet radiation on corals and
other coral reef organisms. Global Change Biology 2, 527–545.
Siebeck, U.E., Marshall, N.J., Klueter, A., Hoegh-Guldberg, O., 2006. Monitoring coral
bleaching using a color reference card. Coral Reefs 25, 453–460.
Skirving, W., Heron, M., Heron, S., 2006. The hydrodynamics of a bleaching event:
implications for management and monitoring. In: Phinney, J.T., Hoegh-
Guldberg, O., Kleypas, J., Skirving, W., Strong, A. (Eds.), Coral Reefs and Climate
ChangedScience and Management. Coastal and Estuarine Studies 61. American
Geophysical Union, pp. 145–161.
Smith, D.J., Suggett, D.J., Baker, N.R., 2005. Is photoinhibition of zooxanthellae
photosynthesis the primary cause of thermal bleaching in corals? Global
Change Biology 11, 1–11.
Smith, L.D., Gilmour, J.P., Heyward, A.J., Rees, M., 2006. Mass-bleaching, mortality
and slow recovery of three common groups of scleractinian corals at an iso-
lated reef. Proceedings of the 10th International Coral Reef Symposium 1,
651–656.
Smith, L.W., Wirshing, H.H., Baker, A.C., Birkeland, C., 2008. Environmental versus
genetic influences on growth rates of the corals Pocillopora eydouxi and Porites
lobata (Anthozoa: Scleractinia). Pacific Science 62, 57–69.
Smith, S.V., Buddemeier, R.W., 1992. Global change and coral reef ecosystems.
Annual Review of Ecology and Systematics 23, 89–118.
Spalding, M.D., Jarvis, G.E., 1998. The impact of the 1998 coral mortality on reef fish
communities in the Seychelles. Marine Pollution Bulletin 44, 309–321.
Steneck, R.S.,1983. Quantifying herbivoryon coral reefs: justscratching the surface and
stillbiting off more thanwe can chew. In:Reaka, M.L. (Ed.),The Ecology of Deep and
Shallow Coral Reefs, pp. 103–111. NOAA Symposium Series, Undersea Research.
Stobart, B., Teleki, K., Buckley, R., Downing, N., Callow, M., 2005. Coral recovery at
Aldabra Atoll, Seychelles: five years after the 1998 bleaching event. Philo-
sophical Transactions of the Royal Society: Mathematical. Physical and Engi-
neering Sciences 363, 251–255.
Strong, A.E., Arzayus, F., Skirving, W., Heron, S.F., 2006. Identifying coral bleaching
remotely via coral reef watchdimproved integration and implications for
changing climate. In: Phinney, J.T., Hoegh-Guldberg, O., Kleypas, J., Skirving, W.,
Strong, A. (Eds.), Coral Reefs and Climate ChangedScience and Management.
Coastal and Estuarine Studies 61. American Geophysical Union, pp. 163–180.
Suzuki, A., Kawahata, H., Tanimoto, Y., Tsukamoto, H., Gupta, L.P., Yukino, I., 2000.
Skeletal isotopic record of a Porites coral during the 1998 mass bleaching event.
Geochemical Journal 34, 321–329.
Sweatman, H., Abdo, D., Burgess, S., Cheal, A., Coleman, G., Delean, S., Emslie, M.,
Miller, I., Osborne, K., Oxley, W., Page, C., Thompson, A., 2003. Long-term
Monitoring of the Great Barrier Reef Status Report Number 6. Institute of
Marine Science (CD ROM), Townsville, Australia.
Szmant, A.M., Gassman, N.J., 1990. The effects of prolonged ‘‘bleaching’’ on the
tissue biomass and reproduction of the reef coral Montastraea annularis. Coral
Reefs 8, 217–224.
Tchernov, D., Gorbunov, M.Y., de Vargas, C., Yadav, S.N., Milligan, A.J., Ha
¨ggblom, M.,
Falkowski, P.G., 2004. Membrane lipids of symbiotic algae are diagnostic of
sensitivity to thermal bleaching in corals. Proceedings of the National Academy
of Sciences USA 101, 13531–13535.
Thornhill, D.J., LaJeunesse, T.C., Kemp, D.W., Fitt, W.K., Schmidt, G.W., 2006a. Multi-
year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent
stability or post-bleaching reversion. Marine Biology 148, 711–722.
Thornhill, D.J., Fitt, W.K., Schmidt, G.W., 2006b. Highly stable symbioses among
western Atlantic brooding corals. Coral Reefs 25, 515–519.
Toller, W.W., Rowan, R., Knowlton, N., 2001. Repopulation of zooxanthellae in the
Caribbean corals Montastrea annularis and M. faveolata following experimental
and disease-associated bleaching. Biological Bulletin 201, 360–373.
Trapido-Rosenthal, H., Zielke, S., Owen, R., Buxton, L., Boeing, B., Bhagooli, R.,
Archer, J., 2005. Increased zooxanthellae nitric oxide synthase activity is asso-
ciated with coral bleaching. Biological Bulletin 208, 3–6.
Tsai, F., Philpot, W., 1998. Derivative analysis of hyperspectral data. Remote Sensing
of Environment 66, 41–51.
Tsuchiya, M., 1999. Effect of mass coral bleaching on the community structure of
small animals associated with the hermatypic coral Pocillopora damicornis.
Galaxea. Japanese Coral Reef Society 1, 65–72.
Tsuchiya, M., Yamauchi, Y., Moretzsohn, F., Tsukiji, M., 1992. Species composition
and some population traits of obligate symbiotic xanthid crabs, Trapezia and
Tetralia, associated with bleached corals. Proceedings of the 7th International
Coral Reef Symposium. Guam 1, 56–63.
Tudhope, A.W., Allison, N., Le Tissier, M.D.A., Scoffin, T.P., 1992. Growth character-
istics and susceptibility to bleaching in massive Porites corals, south Thailand.
Proceedings of the 7th International Coral Reef Symposium 1, 64–69.
Turner, S.J., 1994. The biology and population outbreaks of the corallivorous
gastropod Drupella on Indo-Pacific reefs. Oceanography and Marine Biology: An
Annual Review 32, 461–530.
van Woesik, R., Irikawa, A., Loya, Y., 2004. Coral bleaching: signs of change in
southern Japan. In: Rosenberg, E., Loya, Y. (Eds.), Coral Health and Disease.
Springer, Berlin, pp. 119–141.
van Woesik, R., Koksal, S., 2006. A coral population response (CPR) model for
thermal stress. In: Phinney, J.T., Hoegh-Guldberg, O., Kleypas, J., Skirving, W.,
Strong, A. (Eds.), Coral Reefs and Climate ChangedScience and Management.
Coastal and Estuarine Studies 61. American Geophysical Union, pp. 129–144.
van Woesik, R., Nakamura, T., Yamasaki, H., Sheppard, C., 2005. Comment on
‘‘Effects of geography, taxa, water flow, and temperature variation on coral
bleaching intensity in Mauritius’’ (McClanahan et al. 2005). Marine Ecology
Progress Series 305, 297–299.
Veron, J.E.N., 1992. Environmental control of Holocene changes to the world’s most
northern hermatypic coral outcrop. Pacific Science 46, 405–425.
Vollmer, S.V., Palumbi, S.R., 2007. Restricted gene flow in the Caribbean staghorn
coral Acropora cervicornis: implications for the recovery of endangered reefs.
Journal of Heredity 98, 40–50.
Von Prahl, H., 1983. Blanqueo masivo y muerte de corales en la Isla de Gorgona,
Pacı
´fico Colombiano. Cespedesia 12, 125–129.
Von Prahl, H., 1985. Blanqueo masivo y muerte de corales hermatı
´picos en el
Pacı
´fico colombiano atribuidos al feno
´meno de El Nin
˜o 1982–83. Boletı
´n Erfen
12, 22–24.
Wade, B.S., Al-Sabouni, N., Hemleben, C., Kroon, D., 2008. Symbiont bleaching in
fossil planktonic foraminifera. Ecolutionary Ecology 22, 253–265.
Wakeford, M., Done, T.J., Johnson, C.R., 2008. Decadal trends in a coral community
and evidence of changed disturbance regime. Coral Reefs 27, 1–13.
Wallace, C., 1999. Staghorn corals of the world: a revision of the coral genus
Acropora (Scleractinia; Astrocoeniina; Acroporidae) worldwide, with emphasis
on morphology, phylogeny and biogeography. CSIRO Publishing, Collingwood,
Vic., Australia. 421.
Wapnick, C.M., Precht, W.F., Aronson, R.G., 2004. Millennial-scale dynamics of
staghorn corals in Discovery Bay, Jamaica. Ecological Letters 7, 345–361.
Ward, S., Harrison, P., Hoegh-Guldberg, O., 2000. Coral bleaching reduces repro-
duction of scleractinian corals and increases susceptibility to future stress.
Proceedings of the 9th International Coral Reef Symposium 2, 1123–1128.
Warner, M.E., Fitt, W.K., Schmidt, G.W.,1996. The effects of elevated temperature on
the photosynthetic efficiency of zooxanthellae in hospite from four different
species of reef coral: a novel approach. Plant, Cell and Environment 19, 291–299.
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–3736
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003

Warner, M.E., Fitt, W.K., Schmidt, G.W., 1999. Damage to photosystem II in symbiotic
dinoflagellates: a determinant of coral bleaching. Proceedings of the National
Academy of Sciences USA 96, 8007–8012.
Wellington, G.M., Dunbar, R.B., 1995. Stable isotopic signature of El Nin
˜o-Southern
Oscillation events in eastern tropical Pacific reef corals. Coral Reefs 14, 5–25.
Wellington, G.M., Glynn, P.W., 2007. Responses of coral reefs to El Nin
˜o-Southern
Oscillation sea warming events. In: Aronson, R.B. (Ed.), Geological Approaches
to Coral Reef Ecology. Ecological Studies 192, pp. 342–385.
Wells, S., 2006. Assessing the effectiveness of marine protected areas as a tool for
improving coral reef management. Ecological Applications 10. In: Co
ˆte
´, I.M.,
Reynolds, J.D. (Eds.), Coral Reef Conservation. Conservation Biology 13. Cam-
bridge University Press, Cambridge, pp. 314–331.
West, J.M., Salm, R.V., 2003. Resistance and resilience to coral bleaching: implica-
tions for coral reef conservation and management. Conservation Biology 17,
956–967.
Wilkinson,C.R., 1999. Globaland Local Threats to Coral ReefFunctioning and Existence:
Review and Predictions. Marine Freshwater Resources 50, 867–878.
Wilkinson, C.R., 2000. Status of Coral Reefs of the World: 2000. Australian Institute
of Marine Science, Cape Ferguson, Qld., 361.
Wilkinson, C.R., 2004. Status of Coral Reefs of the World: 2004. Australian Institute
of Marine Science, Cape Ferguson, Qld., Volume 1 301 pp.
Wilkinson, C.R., Buddemeier, R.W., 1994. Global climate change and coral reefs:
implications for people and reefs. Report of the UNEP-IOC-ASPEI-IUCN Global
Task Team on Coral Reefs. IUCN, Gland, 124 pp.
Wilkinson, C.R., Souter, D., 2008. Status of Caribbean coral reefs after bleaching and
hurricanes in 2005. Global Coral Reef Monitoring Network, 148.
Williams, D.E., Hallock, P., 2004. Bleaching in Amphistegina gibbosa d’Orbigny (Class
Foraminifera): observations from laboratory experiments using visible and
ultraviolet light. Marine Biology 145, 641–649.
Williams Jr., E.H., Bartels, P.J., Bunkley-Williams, L., 1999. Predicted disappearance of
coral-reef ramparts: a direct result of major ecological disturbances. Gobal
Change Biology 5 (8), 839–845.
Williams Jr., E.H., Bunkley-Williams, L., 1990. The world-wide coral reef
bleaching cycle and related sources of coral mortality. Atoll Research Bulletin
335, 1–71.
Wilson, S.K., Graham, N.A.J., Pratchett, M.S., Jones, G.P., Polunin, N.V.C., 2006.
Multiple disturbances and the global degradation of coral reefs: are reef fishes
at risk or resilient? Global Change Biology 12, 2220–2234.
Winter, A., Appeldoorn, R.S., Bruckner, A., Williams Jr., E.H., Goenaga, C., 1998. Sea
surface temperatures and coral reef bleaching off La Parguera, Puerto Rico
(northeastern Caribbean Sea). Coral Reefs 17, 377–382.
Yamano, H., Tamura, M., 2002. Can satellite sensors detect coral reef bleaching?
A feasibility study using radiative transfer models in air and water. Proceedings
of the 9th International Coral Reef Symposium. Bali 2, 1025–1031.
Yamano, H., Tamura, M., 2004. Detection limits of coral reef bleaching by satellite
remote sensing: simulation and data analysis. Remote Sensing of Environment
90, 86–103.
Yamano, H., Tamura, M., Kunii, Y., Hidaka, M., 2003. Hyperspectral remote sensing
and radiative transfer simulation as a tool for monitoring coral health. Marine
Technology Society Journal 36, 4–13.
Yonge, C.M., Nicholls, A.G., 1931. Studies on the physiology of corals. IV. The
structure, distribution and physiology of the Zooxanthellae. ScientificReports of
the Great Barrier Reef Expedition 1928-29 1, 135–176.
Zahir, H., Clark, S., Agila, R., Saleem, M., 2002. Spatial and temporal patterns of coral
recruitment following a severe bleaching event in the Maldives. In: Linden, O.,
Souter, D., Wilhelmsson, D., Obura, D. (Eds.), Coral Reef Degradation in the
Indian Ocean. CORDIO, Stockholm, pp. 125–134. Status Report 2002.
Zapata, F.A., Vargas-A
´ngel, B., 2003. Corals and coral reefs of the Pacific coast of
Colombia. In: Corte
´s, J. (Ed.), Latin American Coral Reefs. Elsevier, Amsterdam,
pp. 419–447.
Zapata, F.A., Rodrı
´guez-Ramı
´rez, A., Ca ro-Zambrano, C., Garzo
´n-Ferrei ra, J., in
press. Mid-term coral-algal dynamics and conservation status of a Gor-
gona Island (tropical eastern Pacific) coral reef. Revista de Biologia
Tropical (in press).
A.C. Baker et al. / Estuarine, Coastal and Shelf Science xxx (2008) 1–37 37
ARTICLE IN PRESS
Please cite this article in press as: Andrew C. Baker et al., Climate change and coral reef bleaching: An ecological assessment of long-term
impacts, recovery trends and future outlook, Estuar. Coast. Shelf Sci. (2008), doi:10.1016/j.ecss.2008.09.003