Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005.
ABSTRACT The rising temperature of the world's oceans has become a major threat to coral reefs globally as the severity and frequency of mass coral bleaching and mortality events increase. In 2005, high ocean temperatures in the tropical Atlantic and Caribbean resulted in the most severe bleaching event ever recorded in the basin.
Satellite-based tools provided warnings for coral reef managers and scientists, guiding both the timing and location of researchers' field observations as anomalously warm conditions developed and spread across the greater Caribbean region from June to October 2005. Field surveys of bleaching and mortality exceeded prior efforts in detail and extent, and provided a new standard for documenting the effects of bleaching and for testing nowcast and forecast products. Collaborators from 22 countries undertook the most comprehensive documentation of basin-scale bleaching to date and found that over 80% of corals bleached and over 40% died at many sites. The most severe bleaching coincided with waters nearest a western Atlantic warm pool that was centered off the northern end of the Lesser Antilles.
Thermal stress during the 2005 event exceeded any observed from the Caribbean in the prior 20 years, and regionally-averaged temperatures were the warmest in over 150 years. Comparison of satellite data against field surveys demonstrated a significant predictive relationship between accumulated heat stress (measured using NOAA Coral Reef Watch's Degree Heating Weeks) and bleaching intensity. This severe, widespread bleaching and mortality will undoubtedly have long-term consequences for reef ecosystems and suggests a troubled future for tropical marine ecosystems under a warming climate.
- SourceAvailable from: coralations.org[show abstract] [hide abstract]
ABSTRACT: It has been over 10 years since the phenomenon of extensive coral bleaching was first described. In most cases bleaching has been attributed to elevated temperature, but other instances involving high solar irradiance, and sometimes disease, have also been documented. It is timely, in view of our concern about worldwide reef condition, to review knowledge of physical and biological factors involved in bleaching, the mechanisms of zooxanthellae and pigment loss, and the ecological consequences for coral communities. Here we evaluate recently acquired data on temperature and irradiance-induced bleaching, including long-term data sets which suggest that repeated bleaching events may be the consequence of a steadily rising background sea temperature that will in the future expose corals to an increasingly hostile environment. Cellular mechanisms of bleaching involve a variety of processes that include the degeneration of zooxanthellae in situ, release of zooxanthellae from mesenterial filaments and release of algae within host cells which become detached from the endoderm. Photo-protective defences (particularly carotenoid pigments) in zooxanthellae are likely to play an important role in limiting the bleaching response which is probably elicited by a combination of elevated temperature and irradiance in the field. The ability of corals to respond adaptively to recurrent bleaching episodes is not known, but preliminary evidence suggests that phenotypic responses of both corals and zooxanthellae may be significant.Coral Reefs 01/1997; 16:S129-S138. · 3.66 Impact Factor
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ABSTRACT: Detailed mapping of coral bleaching events provides an opportunity to examine spatial patterns in bleaching over scales of 10s to 1,000s of km and the spatial correlation between sea surface temperature (SST) and bleaching. We present data for two large-scale (2,000km) bleaching events on the Great Barrier Reef (GBR): one from 1998 and another from 2002, both mapped by aerial survey methods. We examined a wide range of satellite-derived SST variables to determine which one best correlated with the observed bleaching patterns. We found that the maximum SST occurring over any 3-day period (max3d) during the bleaching season predicted bleaching better than anomaly-based SST variables and that short averaging periods (3–6days) predicted bleaching better than longer averaging periods. Short periods of high temperature are therefore highly stressful to corals and result in highly predictable bleaching patterns. Max3d SST predicted the presence/absence of bleaching with an accuracy of 73.2%. Large-scale (GBR-wide) spatial patterns of bleaching were similar between 1998 and 2002 with more inshore reefs bleached compared to offshore reefs. Spatial change in patterns of bleaching occurred at scales of ~10skm, indicating that reefs bleach (or not) in spatial clusters, possibly due to local weather patterns, oceanographic conditions, or both. Approximately 42% of reefs bleached to some extent in 1998 with ~18% strongly bleached, while in 2002, ~54% of reefs bleached to some extent with ~18% strongly bleached. These statistics and the fact that nearly twice as many offshore reefs bleached in 2002 compared to 1998 (41 vs. 21%, respectively) makes the 2002 event the worst bleaching event on record for the GBR. Modeling of the relationship between bleaching and max3d SST indicates that a 1C increase would increase the bleaching occurrence of reefs from 50% (approximate occurrence in 1998 and 2002) to 82%, while a 2C increase would increase the occurrence to 97% and a 3C increase to 100%. These results suggest that coral reefs are profoundly sensitive to even modest increases in temperature and, in the absence of acclimatization/adaptation, are likely to suffer large declines under mid-range International Panel for Climate Change predictions by 2050.Coral Reefs 03/2004; 23(1):74-83. · 3.66 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: Temperature tolerance in the reef coral Montipora verrucosa (Lamarck) is affected by salinity and light. Low salinity reduces ability of the coral to survive shortterm exposure to elevated temperature. High natural light intensity aggravates damage sustained by corals at high temperature. In long-term growth experiments, high light intensity caused substantial loss of zooxanthellar pigment, higher mortality rates, reduced carbon fixation and lowered growth rate at both upper and lower sublethal temperatures Effects of light at optimal temperature were less dramatic. Interactions between physical environmental factors appear to be most important near the limits of tolerance for a given factor. Acclimation capability was indicated, and was influenced by both thermal history and pigmentation state of stressed corals.Marine Biology 01/1978; 49(3):187-195. · 2.47 Impact Factor
Caribbean Corals in Crisis: Record Thermal Stress,
Bleaching, and Mortality in 2005
C. Mark Eakin1*, Jessica A. Morgan2, Scott F. Heron3,4, Tyler B. Smith5, Gang Liu2, Lorenzo Alvarez-
Filip6,7, Bart Baca8, Erich Bartels9, Carolina Bastidas10, Claude Bouchon11, Marilyn Brandt5, Andrew W.
Bruckner12, Lucy Bunkley-Williams13, Andrew Cameron14, Billy D. Causey15, Mark Chiappone16, Tyler R. L.
Christensen2, M. James C. Crabbe17, Owen Day18, Elena de la Guardia19, Guillermo Dı ´az-Pulido20,21,
Daniel DiResta22, Diego L. Gil-Agudelo23, David S. Gilliam24, Robert N. Ginsburg25, Shannon Gore26,
He ´ctor M. Guzma ´n27, James C. Hendee28, Edwin A. Herna ´ndez-Delgado29, Ellen Husain30,
Christopher F. G. Jeffrey31, Ross J. Jones32, Eric Jorda ´n-Dahlgren33, Les S. Kaufman34, David I. Kline35,27,
Philip A. Kramer36, Judith C. Lang37, Diego Lirman25, Jennie Mallela38,39, Carrie Manfrino40, Jean-
Philippe Mare ´chal41, Ken Marks37, Jennifer Mihaly42, W. Jeff Miller43, Erich M. Mueller44, Erinn M.
Muller45, Carlos A. Orozco Toro46, Hazel A. Oxenford47, Daniel Ponce-Taylor14, Norman Quinn48, Kim B.
Ritchie9, Sebastia ´n Rodrı ´guez10, Alberto Rodrı ´guez Ramı ´rez23, Sandra Romano5, Jameal F. Samhouri49,
Juan A. Sa ´nchez50, George P. Schmahl51, Burton V. Shank52, William J. Skirving3, Sascha C. C. Steiner53,
Estrella Villamizar54, Sheila M. Walsh55, Cory Walter9, Ernesto Weil13, Ernest H. Williams13, Kimberly
Woody Roberson31, Yusri Yusuf56
1Coral Reef Watch, National Oceanic and Atmospheric Administration, Silver Spring, Maryland, United States of America, 2NOAA Coral Reef Watch, IM Systems Group,
Silver Spring, Maryland, United States of America, 3NOAA Coral Reef Watch, ReefSense Pty. Ltd., Townsville, Queensland, Australia, 4School of Engineering and Physical
Sciences, James Cook University, Townsville, Queensland, Australia, 5Center for Marine and Environmental Studies, University of the Virgin Islands, St. Thomas, United
States Virgin Islands, United States of America, 6Parque Nacional Arrecifes de Cozumel, Cozumel, Me ´xico, 7School of Environmental Sciences, University of East Anglia,
Norwich, United Kingdom, 8CSA South, Inc., Dania Beach, Florida, United States of America, 9Center for Coral Reef Research, Mote Marine Laboratory, Summerland Key,
Florida, United States of America, 10Instituto de Tecnologı ´a y Ciencias Marinas, Universidad Simo ´n Bolı ´var, Caracas, Venezuela, 11Laboratoire de Biologie Marine,
Universite ´ des Antilles et de la Guyane, Pointe-a `-Pitre, Guadeloupe, France, 12Khaled bin Sultan Living Oceans Foundation, Landover, Maryland, United States of America,
13Department of Biology, University of Puerto Rico, Mayagu ¨ez, Puerto Rico, United States of America, 14Global Vision International and Amigos de Sian Ka’an Asociacio ´n
Civil, Playa del Carmen, Quintana Roo, Me ´xico, 15Office of National Marine Sanctuaries, National Oceanic and Atmospheric Administration, Key West, Florida, United
States of America, 16Center for Marine Science, University of North Carolina at Wilmington, Key Largo, Florida, United States of America, 17Luton Institute for Research in
the Applied Natural Sciences, University of Bedfordshire, Luton, United Kingdom, 18Buccoo Reef Trust, Carnbee, Trinidad and Tobago, 19Centro de Investigaciones
Marinas, Universidad de la Habana, Habana, Cuba, 20Universidad del Magdalena, Santa Marta, Colombia, 21Griffith School of Environment and Australian Rivers Institute,
Griffith University, Nathan, Queensland, Australia, 22Marine and Atmospheric Science Program, University of Miami, Coral Gables, Florida, United States of America,
23Insituto de Investigaciones Marinas y Costeras (INVEMAR), Santa Marta, Colombia, 24National Coral Reef Institute, Nova Southeastern University, Dania Beach, Florida,
United States of America, 25Rosenstiel School of Marine and Atmospheric Science, University of Miami, Virginia Key, Florida, United States of America, 26Conservation
and Fisheries Department, Road Town, Tortola, British Virgin Islands, United Kingdom, 27Smithsonian Tropical Research Institute, Balboa, Panama ´, 28Atlantic
Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, Miami, Florida, United States of America, 29Center for Applied
Tropical Ecology and Conservation, University of Puerto Rico, San Juan, Puerto Rico, 30Marine Spatial Ecology Lab, University of Exeter, Exeter, United Kingdom,
31Center for Coastal Monitoring and Assessment, National Oceanic and Atmospheric Administration, Silver Spring, Maryland, United States of America, 32Bermuda
Institute of Ocean Sciences, St George’s, Bermuda, 33Instituto de Ciencias del Mar y Limnologı ´a, Universidad Nacional Auto ´noma de Me ´xico, Cancu ´n, Quintana Roo,
Me ´xico, 34Biology Department, Boston University, Boston, Massachusetts, United States of America, 35Global Change Institute, University of Queensland, Brisbane,
Queensland, Australia, 36The Nature Conservancy, Sugarloaf Key, Florida, United States of America, 37Ocean Research and Education Foundation Inc., Coral Gables,
Florida, United States of America, 38Department of Life Sciences, University of the West Indies, St. Augustine, Trinidad and Tobago, 39Research School of Earth Science,
Australian National University, Canberra, Australian Capital Territory, Australia, 40Central Caribbean Marine Institute and Kean University, Union, New Jersey, United States
of America, 41Observatoire du Milieu Marin Martiniquais, Fort de France, Martinique, France, 42Reef Check, Pacific Palisades, California, United States of America,
43South Florida/Caribbean Network, Virgin Islands National Park, St. John, United States Virgin Islands, United States of America, 44Perry Institute for Marine Science,
Jupiter, Florida, United States of America, 45Biological Sciences Department, Florida Institute of Technology, Melbourne, Florida, United States of America,
46Corporacio ´n para el Desarrollo Sostenible del Archipie ´lago de San Andre ´s, Providencia y Santa Catalina (CORALINA), San Andre ´s Isla, Colombia, 47Centre for Resource
Management and Environmental Studies, University of the West Indies, Cave Hill, Barbados, 48St. Croix East End Marine Park, Department of Planning and Natural
Resources, Christiansted, United States Virgin Islands, United States of America, 49Department of Ecology and Evolutionary Biology, University of California Los Angeles,
Los Angeles, California, United States of America, 50Departamento Ciencias Biologicas, Universidad de los Andes, Bogota ´, Colombia, 51Flower Garden Banks National
Marine Sanctuary, National Oceanic and Atmospheric Administration, Galveston, Texas, United States of America, 52Northeast Fisheries Science Center, National Oceanic
and Atmospheric Administration, Woods Hole, Massachusetts, United States of America, 53Institute for Tropical Marine Ecology Inc., Roseau, Dominica, 54Instituto de
Zoologı ´a Tropical, Universidad Central de Venezuela, Caracas, Venezuela, 55Environmental Change Initiative, Brown University, Providence, Rhode Island, United States of
America, 56ReefBase and Institute of Oceanography, Universiti Malaysia Terengganu, Kuala Terengganu, Malaysia
PLoS ONE | www.plosone.org1November 2010 | Volume 5 | Issue 11 | e13969
Background: The rising temperature of the world’s oceans has become a major threat to coral reefs globally as the severity
and frequency of mass coral bleaching and mortality events increase. In 2005, high ocean temperatures in the tropical
Atlantic and Caribbean resulted in the most severe bleaching event ever recorded in the basin.
Methodology/Principal Findings: Satellite-based tools provided warnings for coral reef managers and scientists, guiding
both the timing and location of researchers’ field observations as anomalously warm conditions developed and spread
across the greater Caribbean region from June to October 2005. Field surveys of bleaching and mortality exceeded prior
efforts in detail and extent, and provided a new standard for documenting the effects of bleaching and for testing nowcast
and forecast products. Collaborators from 22 countries undertook the most comprehensive documentation of basin-scale
bleaching to date and found that over 80% of corals bleached and over 40% died at many sites. The most severe bleaching
coincided with waters nearest a western Atlantic warm pool that was centered off the northern end of the Lesser Antilles.
Conclusions/Significance: Thermal stress during the 2005 event exceeded any observed from the Caribbean in the prior 20
years, and regionally-averaged temperatures were the warmest in over 150 years. Comparison of satellite data against field
surveys demonstrated a significant predictive relationship between accumulated heat stress (measured using NOAA Coral
Reef Watch’s Degree Heating Weeks) and bleaching intensity. This severe, widespread bleaching and mortality will
undoubtedly have long-term consequences for reef ecosystems and suggests a troubled future for tropical marine
ecosystems under a warming climate.
Citation: Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, et al. (2010) Caribbean Corals in Crisis: Record Thermal Stress, Bleaching, and Mortality in 2005. PLoS
ONE 5(11): e13969. doi:10.1371/journal.pone.0013969
Editor: Tamara Natasha Romanuk, Dalhousie University, Canada
Received March 2, 2010; Accepted October 4, 2010; Published November 15, 2010
This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public
domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Funding: This work was partially supported by salaries from the NOAA Coral Reef Conservation Program to the NOAA Coral Reef Conservation Program authors.
NOAA provided funding to Caribbean ReefCheck investigators to undertake surveys of bleaching and mortality. Otherwise, no funding from outside authors’
institutions was necessary for the undertaking of this study. The funders had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: email@example.com
Coral bleaching has become a major threat to coral reef
ecosystems worldwide . Bleaching occurs when stress to the
coral-algal symbiosis causes coralsto expel their endosymbiotic algae
(zooxanthellae) and, if prolonged or particularly severe, may result in
partial or complete coral mortality . While many sources of stress
have caused corals to bleach, ‘‘mass’’ coral bleaching (at scales of
100 km or more) has only occurred when anomalously warm ocean
temperatures, typically coupled with high subsurface light levels,
exceeded corals’ physiological tolerances. This was observed during
recent major El Nin ˜o-Southern Oscillation events (e.g., 1982–83 ,
1997–98 , and 2002 ) and verified by laboratory experiments
[6,7]. These bleaching events caused coral death at numerous sites
around the world, with impacts on reef habitats, structures, and
biodiversity that lasted a decade or more [8,9].
From June to October 2005, a warm-water anomaly developed
across the tropical Atlantic Ocean and greater Caribbean Sea
region. Satellite-based sea surface temperature (SST) observations
from the U.S. National Oceanic and Atmospheric Administration
(NOAA)  detected a large region of warming ocean
temperatures that reached a maximum anomaly of +1.2uC vs.
the long-term mean when averaged across all Caribbean reef sites.
Elevated temperatures persisted for many weeks and helped fuel
the most active Atlantic hurricane season on record  and the
most severe and extensive mass coral bleaching event observed in
NOAA’s Coral Reef Watch (CRW) developed and maintains a
suite of operational satellite sea surface temperature (SST)-based
products that provide coral bleaching nowcasts and alerts .
HotSpots are positive SST anomalies beyond coral’s tolerance
level that reflect instantaneous thermal stress and Degree Heating
Weeks (DHWs) providing a a measure of sustained thermal stress
during a 12-week period. In 2005, NOAA warned coral reef
managers and scientists of anomalously warm conditions as they
developed and spread across the greater Caribbean region. The
maps of sustained thermal stress indicated levels that could cause
mass coral bleaching and significant mortality, and guided both
the timing and location of researchers’ field observations. As a
result, collaborators from 22 countries undertook the most
comprehensive documentation of basin-scale bleaching to date.
NOAA measured sustained thermal stress in 2005 that exceeded
16uC-weeks in some regions, far greater than the thresholds that
have usually been associated with the onset of mass coral bleaching
(DHW =4uC-weeks) and mortality (DHW =8uC-weeks) 
(Figure 1A). As the event developed, water temperatures rose
across the basin to levels well above normal (i.e., long-term
average condition, Figure 2A) and remained above normal for
more than 7 months, resulting in especially severe thermal stress at
the northern end of the Lesser Antilles (Figures 1A, S1, S2).
Analysis of retrospective satellite data showed that the sustained
thermal stress in the Caribbean during 2005 was more intense
than any of the previous 20 years (Figure 2B).
The timeline for the geographic spread of the 2005 Caribbean
thermal stress was decomposed into seven major phases as
Caribbean Corals in Crisis
PLoS ONE | www.plosone.org2November 2010 | Volume 5 | Issue 11 | e13969
identified in Figure 2A: in late-May (i), thermal stress was observed
off South America; by mid-June (ii), the Caribbean coast from
Colombia to Nicaragua experienced elevated temperatures. In
July (iii), the western Caribbean warm anomalies persisted from
Panama to Nicaragua and the extreme western Atlantic east of the
Lesser Antilles began to warm. Through August (iv), reefs in the
Gulf of Mexico, Florida, the Bahamas, and the Lesser Antilles
experienced high levels of stress, while low-level stress was present
across most of the Caribbean. In September (v), the center of
warming progressed along Cuba, Hispaniola, and Puerto Rico to
the Leeward and Windward Islands while low-level stress persisted
throughout the Caribbean. By October (vi), thermal stress
subsided in the Gulf of Mexico; however, warm anomalies
intensified in the Windward Islands and expanded into the
southern Caribbean. As the region of maximum warming moved
southward during November (vii), waters around the northern
Antilles cooled; low-level heat stress affected the northern coast of
South America until it mostly dissipated around the end of
December 2005 .
After initial reports of bleaching in Colombia in June, CRW
distributed alerts via the Internet as the thermal stress spread and
intensified. Teams (represented by the many co-authors on this
paper) deployed throughout the region to monitor the bleaching
event as it developed, and subsequently to monitor coral mortality.
Coral bleaching, other disease conditions, and mortality extended
across the entire Caribbean – bleaching was especially intense
along the Antilles (Figure 1B), and was observed in most
Caribbean coral species in depths to 40 m. Over 3600 field
surveys were recorded from 28 jurisdictions (i.e., states, territories)
in 22 countries (Figure S3). After quality control, data from 2575
field surveys were used in the bleaching analysis and 1077 were
used in mortality studies. Surveys were grouped by 0.5-degree
pixel at twice-weekly time intervals to allow satellite data and field
surveys to be analyzed at comparable scales.
Figure 1. Thermal stress and bleaching during the 2005 Caribbean bleaching event. (A) Maximum NOAA Coral Reef Watch Degree
Heating Week (DHW) values showing the highest thermal stress recorded at each 0.5-degree pixel during 2005. Values $4uC-weeks typically resulted
in significant bleaching; $8uC-weeks typically resulted in widespread bleaching and significant mortality. (B) Jurisdictional means of coral bleached;
marker color and size denote the severity measured as either percent live coral colonies (circles) or cover (diamonds).
Figure 2. Temporal patterns of thermal stress in the Caribbean. Average of satellite-derived anomaly and thermal stress indices from the 0.5-
degree pixels containing or nearest to reefs in the Caribbean (bounded by 35uN, 55uW, and the coast of the Americas). (A) NOAA coral bleaching
HotSpots (purple) and DHW (red) in 2005. See results for explanations of (i)–(vii). Letters D–W refer to the major hurricanes of 2005: Dennis, Emily,
Katrina, Rita and Wilma. (B) Average of annual maximum thermal stress (DHW) values during 1985–2006. Significant coral bleaching was reported
during periods with average thermal stress above 0.5uC-weeks, and was especially widespread in 1995, 1998, and 2005.
Caribbean Corals in Crisis
PLoS ONE | www.plosone.org3 November 2010 | Volume 5 | Issue 11 | e13969
Several species and sites were reported to bleach for the first
time, including: the first known bleaching at Saba; the first
documented mass bleaching of the Flower Garden Banks,
including at least partial bleaching of all Millepora alcicornis and
Montastraea cavernosa colonies; and the first reported mass bleaching
of Acropora palmata in Virgin Islands National Park (VINP), a
species listed as threatened under the US Endangered Species Act
(ESA) since 2006 .
Surveys conducted from the peak of thermal stress through
January 2007 were analyzed to assess coral mortality. Detailed and
repeated monitoring revealed that a combination of bleaching and
other disease outbreaks killed coral colonies stressed by high
temperatures [12,14,15]. Some researchers identified continued
mortality as late as October 2007 , beyond which it was difficult
to attribute further mortalities to this bleaching event with sufficient
certainty. In parts of the Caribbean, temperatures remained
anomalously high during the boreal winter-spring and into mid-
2006, although remaining below the bleaching threshold. Many
corals remained bleached, and disease and mortality continued
through much of 2006. Mortality exceeded 50% in several locations
and made this the worst case of thermal stress-related mortality
documented in the Caribbean to date, and one of the worst cases
globally . The pattern of high thermal stress followed by
subsequent mortality across much of the Caribbean was consistent
with the pattern seen since the 1980s and 1990s in the Florida Keys,
where outbreaks ofother diseases have frequently been seen in years
that followed thermal stress and bleaching .
In the Florida Keys in 2005, bleaching was less severe than in
the Caribbean proper. However, increased temperatures were
quickly followed by a loss of resistance to pathogenic disease and
an increased abundance of microbial pathogens in A. palmata ,
perhaps explaining the high incidence of disease following the
thermal stress by either contagious or opportunistic pathogens
. A longitudinal study of cohorts of corals in this region also
revealed that more extensively bleached corals were more
susceptible to disease outbreaks . In VINP, video surveys of
permanent transects revealed that mortality occurred in colonies
due to bleaching, and in colonies that showed disease symptoms
either during bleaching, after recovery from bleaching, or even
without visible bleaching . Frequent monitoring of A. palmata
also revealed that bleached corals suffered greater disease-
associated mortality than unbleached colonies, indicating that
disease severity was dependent on host susceptibility . In
Barbados, corals remained bleached for 8 months or longer before
dying [20,21]; even a year after temperatures dropped below
bleaching thresholds, some corals remained bleached or pale at
many sites, particularly within the important reef-builders of the
Montastraea annularis species complex, which are now under
consideration for ESA protection . Fortunately, thermal stress
was lower off Venezuela (including Los Roques, Aruba, Bonaire,
and Curac ¸ao) and bleaching, disease, and mortality were limited
with no long-term community decline .
Comparison of satellite data with field surveys demonstrated a
strong coherence between thermal stress (Figure 1A) and
widespread bleaching (Figure 1B, 3A) and mortality (Figure 3B).
However, significant variability was seen in the severity of coral
bleaching among reefs within each 0.5-degree satellite pixel,
presumably due to variations in local conditions (e.g., hydrody-
Figure 3. Mean coral bleaching and mortality versus thermal stress. (A) Small squares represent mean percent coral bleached (by area or
colony) for each 0.5-degree pixel and twice-weekly time period plotted against observed DHW value. Solid line indicates significant linear regression
(slope =3.41, intercept =26.94, DF =359, p,0.0001, r2=0.24). Colored bars indicate mean (gray bar) and standard deviation of all surveys binned at
1uC-week intervals; colors correspond to low bleaching risk (DHW ,4, blue), moderate risk (DHW $4, green), high bleaching and mortality risk (DHW
$8, yellow), and very high risk (DHW $12, purple). (B) Triangles represent mean percent coral mortality (6 standard deviation) reported during 25-
Jul-2005 to 20-Jan-2007, plotted against the 2005 maximum DHW value recorded for each 0.5-degree pixel. Yellow and white areas correspond to the
inset box where values indicate number of data points in each quadrant (quadrants defined as 0# DHW ,8 and 0# mortality ,8%; 0# DHW ,8 and
8%# mortality; 8# DHW and 0# mortality ,8%; 8# DHW and 8%# mortality).
Caribbean Corals in Crisis
PLoS ONE | www.plosone.org4 November 2010 | Volume 5 | Issue 11 | e13969
namics, light, community composition). Consistent with CRW’s
previously established bleaching levels, significant coral bleaching
began near 4uC-weeks (Alert Level 1, Figure 3A), with widespread
mass bleaching and significant mortality occurring above 8uC-
weeks (Alert Level 2, Figure 3B) . However, bleaching also
occurred at sites experiencing maximum stress levels below 4uC-
weeks, indicating that either the 4uC-weeks threshold may have
been conservative or the 0.5-degree spatial resolution failed to
detect localized high temperatures. Bleaching has been reported to
depend on numerous local factors, including light level, temper-
ature variability, and past thermal stress history . These could
have influenced bleaching variability within and among reefs in
each 0.5-degree pixel as well. Coral mortality in 2005 was highest
in jurisdictions in the northern and central Lesser Antilles where
stress exceeded 10uC-weeks (Figure 1A).
In the areas where thermal stress levels were less than 8uC-
weeks, significant mortality was rare (2 of 143 surveys, ,1.5%;
Figure 3B). Above this threshold, significant mortality was
observed in 31% of events. It was likely that local conditions at
scales finer than those detected by satellite observations increased
or decreased the effect of the thermal stress within and among
reefs at the sub-pixel scale (e.g., coral community structure, small-
scale hydrodynamics, past bleaching; the analysis of which were
beyond the scope of this study). Despite local variability, thermal
stress values exceeding approximately 8uC-weeks successfully
predicted significant mortality. Thermal stress of this magnitude
should be weighed carefully by reef managers. In 2005, little
mortality was seen below 8uC-weeks of thermal stress while above
it there was an ecologically important 1-in-3 risk of mortality. The
slow rate of recovery seen in Caribbean reefs [16,24,25] suggests
that such high levels of mortality may determine the fate of coral
reef ecosystems in this region for decades to come.
Unlike many past Caribbean bleaching years, strong tropical
climate forcing was only a minor driver of Caribbean SSTs in 2005.
In their analysis of temperature anomalies across the tropical North
Atlantic in 2005, Trenberth and Shea  indicated that half of the
warming (0.45uC of the 0.9uC anomaly vs. a 1901–1970 baseline)
was attributable to monotonic climate change, while only 0.2uC was
attributable to the weak 2004–05 El Nin ˜o, and even less to the
Atlantic Multi-decadal Oscillation (,0.1uC). Despite the lack of
strongtropical forcing,2005fellamongthewarmest yearsonrecord
. NOAA’s Extended Reconstructed SST product [27,28]
showed that average ocean temperatures during the July-October
period for the Caribbean exceeded temperatures seen at any time
during the prior 150 years (Figure 4). Anticipated future warming of
ocean waters  is expected to increase the likelihood of future
Caribbean bleaching events .
High ocean temperature also contributed to the record 2005
hurricane season  that damaged coral reefs in Jamaica, Cuba,
the Yucatan, Flower Garden Banks, and the Florida Keys  as
well as causing major damage to communities and loss of human
life. Hurricanes have been observed to cause mechanical damage
to coral reefs, including damaging coral tissue and dislodging
colonies, weakening corals in ways than could slow recovery
following bleaching, and contributing to long-term ecosystem
decline . However, hurricanes that pass within several
hundred kilometers of coral reefs have been shown to cool
anomalously warm SSTs below bleaching thresholds, and were
probably significant in reducing thermal stress and preventing
more severe bleaching in the Florida Keys in 2005 [12,31]. The
absence of such cooling by tropical cyclones in the Leeward
Islands (Figure 5) most likely contributed to the extreme warming,
bleaching, and mortality seen there. The major hurricanes that
cooled waters around the Florida Keys in 2005 (Dennis, Emily,
Katrina, Rita, Wilma) were strong enough to reduce the
Caribbean-average HotSpots (Figure 2A).
Many Caribbean reefs have changed dramatically since the
early 20thcentury as a result of a wide array of human
disturbances [32,33]. It is unlikely that natural climate variability
was the cause of declines in Caribbean reefs during recent decades,
as coral reef community composition had remained remarkably
stable for the prior 220,000 years . While bleaching is far from
the only cause of reef decline in the Caribbean, the repeated coral
bleaching events since the 1980s have been strongly attributed to
anthropogenic climate change . The mass bleaching and
mortality from the 2005 warming further disturbed Caribbean
ecosystems that were already under assault [12,33]. Coral
bleaching is expected to be an even greater threat to coral reefs
in the future [30,35].
Figure 4. Long-term temperature record in the Caribbean. Temperature anomalies for 2.0-degree reef pixels in the tropical Caribbean
computed using the NOAA Extended Reconstructed Sea Surface Temperature (ERSST) dataset. Anomalies were plotted relative to 1901–2000. The
dashed line indicates the 2005 value.
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Mass coral bleaching from thermal stress, followed by outbreaks
of contagious or opportunistic diseases [18,36,37], have become a
threat common to coral reefs globally. Bleaching and mortality such
as that seen in the Caribbean in 2005 will undoubtedly have long-
term consequences for Caribbean coral reefs, as these corals have
shown very slow rates of recovery to mortality from mass bleaching
. This means that any future bleaching is likely to add to the
damage causedin2005, just as the 2005 event continued the decline
of reefs that have suffered past mortality from bleaching, disease,
and local stressors. As this paper went to press in 2010, major
bleaching was again striking reefs in the Caribbean, in some places
worse than in 2005. Major bleaching events have returned to the
Caribbean every five years or less, and with growing intensity
(Figure 2B). With no real sign of recovery after bleaching in
Caribbean reefs , these repeated events are likely to have caused
reef decline that will extend beyond our lifetimes.
The data presented here will aid researchers and resource
managers as they develop actions to protect reefs against the
thermal stress anticipated in coming decades , especially as
new studies identify ways in which reductions of other sources of
stress can increase reef resilience to climate change [24,39,40,41].
As global ocean temperatures continue to rise, policy makers will
need to address anthropogenic climate change, and managers will
have to take concerted efforts to enhance the resilience of coral
reefs for us to have hope of preventing dramatic losses of valuable
coral reef resources.
Materials and Methods
NOAA Coral Reef Watch (CRW) thermal stress products used
in this study were based on nighttime-only Advanced Very High
Resolution Radiometer (AVHRR) sea surface temperature (SST)
data from sensors aboard operational NOAA Polar-Orbiting
Environmental Satellites (POES), produced in near-real-time at
0.5-degree (50-km) spatial resolution. SST anomalies compared
the measured temperature with the expected value at that time of
year for each pixel. HotSpots were computed as positive anomalies
above the mean temperature of the climatologically warmest
month at each satellite data pixel, based on the NOAA operational
climatology from years 1985–1990 and 1993. Degree Heating
Weeks (DHWs) for any given time accumulated HotSpot values
$1uC over the preceding 12-week period . The satellite-
derived quantities calculated for this paper (Table S1) at each reef
pixel surveyed included: the date of first issuance of Bleaching
Watch alert (HotSpot .0uC); the value of maximum DHW (uC-
weeks) experienced during the event; and the date when
temperatures dropped below stressful levels (HotSpot =0).
The DHW map (Figure 1A) included values in coastal regions
that were masked as land in the operational CRW products. For
the purpose of this figure only, the coastal values were inferred
using kriging, a common statistical technique . However, all
data used for the subsequent analyses (Figure 2A) and comparison
with field data (Figure 3) were retrieved from NOAA operational
products. Spatial averaging of satellite metrics (Figure 2A, S1) was
performed using the original operational data from the greater
Caribbean pixels containing, or nearest to, coral reef locations
within the region [100W-55W, 5N-35N].
CRW operational products were first made available on 12-
Sep-2000. The 22-year time series of annual maximum DHW
(Figure 2B) was produced from a retrospective suite of products
that emulated the CRW near-real-time operational product  for
the period 1985–2006 using data from the Pathfinder Version 5.0
SST dataset . Spatial averaging was undertaken using the
same pixels used for the operational data.
Field surveys of coral bleaching and mortality included at least
the following quantitative data: 1) measures of coral bleaching as
Figure 5. Thermal stress and hurricanes during the 2005 Caribbean bleaching event. Minimum observed SST anomaly for May-December
2005, overlaid with storm tracks (solid: hurricane, thickness denotes strength category; dotted: tropical storm; red: June-August; gray: September;
black: October-December). Dates indicate initial date of hurricane formation. The large yellow region in the eastern Caribbean remained warmer than
usual throughout this period.
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coral cover bleached (%), number of coral colonies bleached (n)
and total number of colonies surveyed (N), or both; and/or 2)
measures of coral mortality as coral cover dead (%), number of
coral colonies dead (n) and total number of colonies surveyed (N),
or both; 3) average observation depth (m); 4) observation date; and
5) observation location, including latitude, longitude, and reef site
any of the following criteria: 1) bleaching observations taken before
the onset of thermal stress (first issuance of Bleaching Watch alert);
2) bleaching observations taken after subsidence of thermal stress,
defined as the 90thday following the date of the last No Stress alert
in 2005; and 3) mortality observations taken before the maximum
DHW value occurred in 2005. Multiple observations (quadrats or
transects) taken at any reef site on the same date and depth (65 m)
were combined into a single survey of either means of percent cover
data or proportion of the number of colonies surveyed. The 2575
bleaching surveys used in this analysis (Table S1, Figures 1b, 3a)
spanned the period 3-Jun-2005 through 13-Feb-2006. The 1077
mortality surveys used to estimate mortality associated with the
thermal stress event (Table S1, Figure 3b) were conducted during
25-Jul-2005 to 20-Jan-2007. In some cases, multiple surveys from
within 0.5-degree pixels were conducted on multiple dates during
the period between the onset of thermal stress and 90 days after
thermal stress subsided. However, these were almost always either
new surveys at different sites or different, random sets of
observations within transects. There were insufficient cases of
repeated surveys of the same transect to analyze how bleaching
changed through time either during the warming or cooling phases
of the event. However, a few resurveyed sites did show some degree
of recovery after the peak of bleaching. Reports detailing change
throughtimeat individualsiteshavebeen publishedandcontinueto
be published elsewhere [15,20,21,22].
As the multiple researchers who took part in this paper used a
variety of methods, the work presented here was a meta-analysis of
surveys conducted by numerous research institutions during the
2005 bleaching event. The techniques used were all highly
comparable, well-accepted field methods. The authors assumed
that differences among techniques were randomly distributed with
respect to thermal stress. Past comparisons among coral reef
survey methods have demonstrated that while there are some
biases among methods, most provide comparable results when
comparing among similar types of observation such as percent
coral cover or disturbance [44,45]. It is important to note that the
percentage of colonies bleached was often higher than the
percentage of cover bleached because (1) small colonies bleached
more often than large colonies; and/or (2) both partially- and
wholly-bleached colonies were counted as bleached in some survey
methodologies. However, a statistical comparison of the linear
regressions of percent cover bleached and percent colonies
bleached vs. thermal stress (Figure S4) found no significant
differences between the slopes of the two parameters (cover =
3.9160.89 vs. colonies =3.4360.70, expressed as slope 695% con-
fidence interval). This supported the assumption that the different
observation methods provided comparable results for this meta-
analysis. Also, because any visible bleaching probably indicated
a loss of most of the zooxanthellae originally present , it was
appropriate to include any degree of bleaching, from pale and
partially bleached to fully bleached colonies, as an indicator of
significant stress in the corals. The same applies to partial and
complete mortality as either indicated a thermal stress response
resulting in mortality due to bleaching or various other diseases.
Therefore, partial and complete bleaching and partial and
complete mortality of corals were combined as observations of
bleaching and mortality, respectively.
Mortality data included only corals that expert observers
determined had recently died; however, the actual cause of
mortality typically was not identifiable. An analysis of reefs in the
region showed that 4% recent mortality normally existed as a
background level during surveys in years lacking any major
disturbance . This 4% background level of mortality was then
considered in establishing the level of mortality considered
significant in Figure 3B. As was expected for an accumulated
variable such as mortality, total percent coral mortality did rise
slowly with time after the thermal stress. The observers did not feel
that they could accurately separate mortality due to the 2005
bleaching event from other causes beyond 20-Jan-2007, thus
determining the end date of the data used. Finally, the data density
and non-random distribution of data submissions did not permit the
standardization of mortality as a function of time since observation.
Operational satellite products from the co-located (or next-
nearest) satellite pixel were compared with all field observations
(Figure S3). A linear regression was used to compare mean coral
bleaching (combined cover and colonies datasets) with thermal
stress (observed DHW at the time of the survey). For surveys that
occurred after the peak of thermal stress, the observed DHW may
have declined from the maximum thermal stressexperienced at that
location. This could have resulted in a level of bleaching greater
than that expected from the observed DHW against which it was
compared. Each data point represented the average of all surveys
for a given 0.5-degree pixel conducted during the twice-weekly time
period (temporal resolution) of the satellite data, plotted against the
DHW value observed for that pixel and time period. The
relationship between observed DHW and percent coral bleached
was highly significant (slope =3.41, intercept =26.94, DF =359,
p,0.0001, r2=0.24). Given the variability of monitoring techniques
employed, sampling errors within each technique, and local factors
at individual reef sites (e.g., shading, ponding), the explicative power
of the satellite metric (r2=0.24 for percent coral bleached)
supported the predictive relationship between the thermal stress
monitored by CRW satellite products and the observed bleaching
during this event. However, it was clear that inclusion of other
information, including higher spatial resolution SST-based prod-
ucts, may further refine bleaching predictions in the future.
For consistency, mortality data were considered only for
observations after the peak of the thermal stress event (i.e., the
maximum DHW) within a pixel and were analyzed against the
maximum thermal stress (Figure 3B). For this study, the threshold
for significant mortality was defined where the observed value was
twice the regional baseline mortality; i.e., 8%. The nature of this
analysis was very broad, combining field datasets across time,
space, and survey methodology. No attempt was made to separate
mortality induced by bleaching from that resulting by other
diseases as both were related to thermal stress [14,48]. The results
showed strong predictive power. However, thermal stress was far
from a perfect predictor of mortality as local variability in the
response of corals at and within individual reef sites likely played a
critical role due to differences in circulation, shading, past thermal
stress, and other factors that may have conferred local resilience.
Hurricanes extract heat from the upper ocean and induce
vertical mixing. Both mechanisms have been shown to reduce the
high temperatures of surface waters that cause coral bleaching
[12,31]. While 2005 was a record hurricane season, none passed
near the Lesser Antilles where some of the highest bleaching and
mortality were observed. This can be seen in hurricane tracks
(Figure 5) acquired from the National Hurricane Center (www.
nhc.noaa.gov). Surface temperatures in this region remained
above climatological values throughout the May-December
period, with no respite from thermal stress (Figures 1A, S2).
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The NOAA Extended Reconstructed SST data [27,28] used in
Figure 4 were averaged across reef-containing pixels (2-degree
resolution) within the region [91W-55W, 5N-35N] and are
presented as anomalies relative to the 1901-2000 mean.
bleaching event. Sea surface temperature (SST) averaged across
the 0.5-degree pixels that contained or were nearest Caribbean
reef locations (bounded by 35uN, 55uW, 5uN and the coast of the
Americas). The ‘+’ symbols indicate the average climatological
temperature during each month and the dashed line shows the
maximum of these, an indication of the expected warmest (usually
summer) temperature. The SST trace shows that, on average,
temperatures around Caribbean reefs exceeded climatological
values by close to 1uC for a period of more than four months. The
magnitude and extended duration of the basin-wide thermal
anomaly resulted in widespread coral bleaching and lowered the
ability of corals to resist other disease conditions.
Found at: doi:10.1371/journal.pone.0013969.s001 (0.69 MB ZIP)
Sea surface temperature during the 2005 Caribbean
during the 2005 Caribbean bleaching event, measured using
NOAA Coral Reef Watch Degree Heating Week product from 4
June 2005 to 14 February 2006 with a pause during the peak of
the event at 28 October 2005.
Found at: doi:10.1371/journal.pone.0013969.s002 (5.54 MB
Animation of the development of thermal stress
sites across the greater Caribbean region. Colors denote number
of surveys at each of the 1212 sites. See Table S1 for location
Found at: doi:10.1371/journal.pone.0013969.s003 (0.18 MB TIF)
Locations of 2575 bleaching surveys submitted from
observations of percent coral colonies (gray circles) and cover
(black diamonds) are plotted versus observed Degree Heating
Week (DHW). Linear regressions for colonies (gray line) and cover
(black line) were highly significant (cover slope =3.91, intercept
=19.99, df =212, p,0.0001, r2=0.26; colonies slope =3.43,
intercept =29.46, df =304, p,0.0001, r2=0.24) and indicated
no difference in slopes, suggesting comparable results.
Found at: doi:10.1371/journal.pone.0013969.s004 (0.08 MB TIF)
Comparison of bleaching survey methods. All
analyses. Multiple observations from the same reef site, date and
depth (65 m) were combined as either means of percent cover
data or proportion of the number of colonies surveyed to provide
2575 bleaching surveys and 1077 mortality surveys.
Found at: doi:10.1371/journal.pone.0013969.s005 (0.17 MB PDF)
Complete data record for all survey data used in the
We thank the many researchers who contributed their data to NOAA
Coral Reef Watch, ReefBase, and Coral-List to document this event. For
each author, there are many more individuals in the various laboratories
who were critical to the success of this work. The manuscript contents are
solely the opinions of the authors and do not constitute a statement of
policy, decision, or position on behalf of NOAA or the U.S. Government.
Contribution 1053 of INVEMAR.
Conceived and designed the experiments: CME JAM SFH TBS GL
TRLC WS. Performed the experiments: TBS LAF BB EB CB CB MB AB
LBW AC BC MC MJCC OD EdlG GDP DD DLGA DSG RG SG HMG
JH EAHD EH CFGJ RJJ EJD LK DK PK JCL DL JM CM JPM KM JM
WJM EMM EM CAOT HAO DPT NQ SR ARR SR JFS JAS GPS BS
SCCS EV SMW CW EW EHW KWR YbY. Analyzed the data: CME
JAM SFH GL KBR. Wrote the paper: CME JAM SFH TBS.
1. Eakin CM, Lough JM, Heron SF (2009) Climate variability and change:
monitoring data and evidence for increased coral bleaching stress. In: Van
Oppen MH, Lough JM, eds. Coral Bleaching: Patterns, processes, causes and
consequences. Berlin: Springer. pp 41–67.
2. Brown BE (1997) Coral bleaching: Causes and consequences. Coral Reefs 16(5):
3. Glynn PW (1990) Coral mortality and disturbances to coral reefs in the tropical
eastern Pacific. In: Glynn PW, ed. Global Ecological Consequences of the 1982-
83 El Nin ˜o-Southern Oscillation. Amsterdam: Elsevier. pp 55–126.
4. Wilkinson CR (2000) Status of Coral Reefs of the World: 2000. Townsville,
Australia: Australian Institute of Marine Science. 363 p.
5. Berkelmans R, De’ath G, Kininmonth S, Skirving WJ (2004) A comparison of
the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial
correlation, patterns, and predictions. Coral Reefs 23(1): 74–83.
6. Coles SL, Jokiel PL (1978) Synergistic Effects of Temperature, Salinity and
Light on Hermatypic Coral Montipora-Verrucosa. Marine Biology 49(3):
7. Glynn PW, 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.
8. Eakin CM (2001) A tale of two ENSO events: Carbonate budgets and the
influence of two warming events and intervening variability, Uva Island,
Panama. Bulletin of Marine Science 69(1): 171–186.
9. Graham NAJ, Wilson SK, Jennings S, Polunin NVC, Bijoux JP, et al. (2006)
Dynamic fragility of oceanic coral reef ecosystems. Proceedings of the National
Academy of Science, USA 103: 8425–8429.
10. Liu G, Strong AE, Skirving WJ, Arzayus LF (2006) Overview of NOAA Coral
Reef Watch Program’s near-real-time satellite global coral bleaching monitoring
activities. Proceedings of the 10th International Coral Reef Symposium:
Okinawa. pp 1783–1793.
11. Shein KA (2006) State of the Climate in 2005. Bulletin of the American
Meteorological Society 87(6): s1–s102.
12. Wilkinson C, Souter D, eds (2008) Status of Caribbean Coral Reefs after
Bleaching and Hurricanes in 2005. Townsville, Australia: Global Coral Reef
Monitoring Network, and Reef and Rainforest Research Centre. 152 p.
13. Muller E, Rogers C, Spitzack A, van Woesik R (2008) Bleaching increases
likelihood of disease on Acropora palmata (Lamarck) in Hawksnest Bay, St John,
US Virgin Islands. Coral Reefs 27(1): 191–195.
14. Whelan KRT, Miller J, Sanchez O, Patterson M (2007) Impact of the 2005 coral
bleaching event on Porites porites and Colpophyllia natans at Tektite Reef, US Virgin
Islands. Coral Reefs 26(3): 689–693.
15. Miller J, Muller E, Rogers C, Waara R, Atkinson A, et al. (2009) Coral disease
following massive bleaching in 2005 causes 60% decline in coral cover on reefs
in the US Virgin Islands. Coral Reefs 28(4): 925–937.
16. Baker AC, Glynn PW, Riegl B (2008) Climate change and coral reef bleaching:
An ecological assessment of long-term impacts, recovery trends and future
outlook Estuarine, Coastal and Shelf Science 80(4): 435–471.
17. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus
and mucus-associated bacteria. Marine Ecology Progress Series 322: 1–14.
18. Lesser MP, Bythell JC, Gates RD, Johnstone RW, 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(1-2): 36–44.
19. Brandt ME, McManus JW (2009) Disease incidence is related to bleaching
extent in reef-building corals. Ecology 90(10): 2859–2867.
20. Oxenford H, Roach R, Brathwaite A, Nurse L, Goodridge R, et al. (2008)
Quantitative observations of a major coral bleaching event in Barbados,
Southeastern Caribbean. Climatic Change 87(3): 435–449.
21. Oxenford HA, Roach R, Brathwaite A (2010) Large scale coral mortality in
Barbados: a delayed response to the 2005 bleaching episode. Proceedings of the
11th International Coral Reef Symposium Ft. Lauderdale: Florida, 7-11 July
22. Rodrı ´guez S, Cro ´quer A, Bone D, Bastidas C (2010) Severity of the 1998 and
2005 bleaching events in Venezuela, southern Caribbean. Revista de Biologı ´a
Tropical 58(Suppl. 3): 189–196.
23. Mumby PJ, Chisholm JRM, Edwards AJ, Andrefouet S, Jaubert J (2001) Cloudy
weather may have saved Society Island reef corals during the 1998 ENSO event.
Marine Ecology Progress Series 222: 209–216.
24. Carilli JE, Norris RD, Black BA, Walsh SM, McField M (2009) Local Stressors
Reduce Coral Resilience to Bleaching. PLoS ONE 4(7): e6324.
25. Mallela J, Crabbe MJC (2009) Hurricanes and coral bleaching linked to changes
in coral recruitment in Tobago. Marine Environmental Research 68(4):
26. Trenberth KE, Shea DJ (2006) Atlantic hurricanes and natural variability in
2005. Geophysical Research Letters 33(12): L12704.
Caribbean Corals in Crisis
PLoS ONE | www.plosone.org8November 2010 | Volume 5 | Issue 11 | e13969
27. Smith TM, Reynolds RW (2004) Improved Extended Reconstruction of SST
(1854-1997). Journal of Climate 17: 2466–2477.
28. NOAA National Climatic Data Center (2009) NOAA Extended Reconstructed
Sea Surface Temperature (ERSST.v3b). Accessed 29 August 2007. Available at:
29. Solomon S, Qin D, Manning M, Chen Z, Marquis M, et al., eds. (2007) Climate
Change 2007: The Physical Science Basis. Cambridge, UK: Cambridge
University Press. 996 p.
30. Donner SD, Knutson TR, Oppenheimer M (2007) Model-based assessment of
the role of human-induced climate change in the 2005 Caribbean coral
bleaching event. Proceedings of the National Academy of Sciences 104(13):
31. Manzello DP, Brandt M, Smith TB, Lirman D, Hendee JC, et al. (2007)
Hurricanes benefit bleached corals. Proceedings of the National Academy of
Sciences 104(29): 12035–12039.
32. Pandolfi JM, Jackson JBC, Baron N, Bradbury RH, Guzman HM, et al. (2005)
ECOLOGY: Enhanced: Are U.S. Coral Reefs on the Slippery Slope to Slime?
Science 307(5716): 1725–1726.
33. Mora C (2008) A clear human footprint in the coral reefs of the Caribbean.
Proceedings of the Royal Society B: Biological Sciences 275(1636): 767–773.
34. Pandolfi JM, Jackson JBC (2006) Ecological persistence interrupted in
Caribbean coral reefs. Ecology Letters 9(7): 818–826.
35. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, et al.
(2007) Coral reefs under rapid climate change and ocean acidification. Science
36. Bruno JF, Selig ER, Casey KS, Page CA, Willis BL, et al. (2007) Thermal Stress
and Coral Cover as Drivers of Coral Disease Outbreaks. PLoS Biol 5(6): e124.
37. Heron SF, Willis BL, Skirving WJ, Eakin CM, Page CA, et al. (2010) Summer
Hot Snaps and Winter Conditions: Modelling White Syndrome Outbreaks on
Great Barrier Reef Corals. PLoS ONE 5(8): e12210.
38. Marshall P, Schuttenberg H (2006) A Reef Manager’s Guide to Coral Bleaching.
Townsville, Australia: Great Barrier Reef Marine Park Authority. 163 p.
39. Carilli JE, Norris RD, Black B, Walsh SM, McField M (2009) Century-scale
records of coral growth rates indicate that local stressors reduce coral thermal
tolerance threshold. Global Change Biology 16(4): 1247–1257.
40. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008)
Ocean acidification causes bleaching and productivity loss in coral reef builders.
Proceedings of the National Academy of Sciences 105(45): 17442–17446.
41. Wooldridge SA (2009) Water quality and coral bleaching thresholds:
Formalising the linkage for the inshore reefs of the Great Barrier Reef,
Australia. Marine Pollution Bulletin 58(5): 745–751.
42. Isaaks EH, Srivastava RM (1989) An Introduction to Applied Geostatistics.
Oxford: Oxford University Press. 561 p.
43. NOAA National Oceanographic Data Center (2009) NODC 4 km Pathfinder
Version 5. Accessed 29 August 2007. Available at: http://www.nodc.noaa.gov/
44. Hill J, Wilkinson C (2004) Methods for Ecological Monitoring of Coral Reefs,
Version 1. Townsville, Australia: Australian Institute of Marine Science. 117 p.
45. Leujak W, Ormond RFG (2007) Comparative accuracy and efficiency of six
coral community survey methods. Journal of Experimental Marine Biology and
Ecology 351(1-2): 168–187.
46. Hoegh-Guldberg O, Lesser MP, Iglesias Prieto R (2005) Bleaching and
physical/chemical stress on coral reefs. In: Hoegh-Guldberg O, ed. Under-
standing the Stress Response of Corals and Symbiodinium in a rapidly changing
environment. Mexico: Universidad Nacional Auto ´noma de Me ´xico, Instituto de
Ciencias del Mar y Limnologı ´a, Unidad Acade ´mica Puerto Morelos. pp
47. Kramer PA (2003) Synthesis of Coral Reef Health Indicators for the Western
Atlantic: Results of the AGRRA Program (1997-2000). Atoll Research Bulletin
48. Bruno JF, Petes LE, Harvell CD, Hettinger A (2003) Nutrient enrichment can
increase the severity of coral diseases. Ecology Letters 6(12): 1056–1061.
Caribbean Corals in Crisis
PLoS ONE | www.plosone.org9November 2010 | Volume 5 | Issue 11 | e13969