Marine Pollution Bulletin 105 (2016) 654659

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Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Local bleaching thresholds established by remote sensing techniques

vary among reefs with deviating bleaching patterns during the 2012
event in the Arabian/Persian Gulf
Dawood Shuail a, Jrg Wiedenmann a, Cecilia D'Angelo a, Andrew H. Baird b, Morgan S. Pratchett b,
Bernhard Riegl c, John A. Burt d, Peter Petrov e, Carl Amos a
a
Coral Reef Laboratory, Ocean and Earth Science, University of Southampton, SO143ZH Southampton, UK
b
ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia
c
National Coral Reef Institute, Nova Southeastern University, Fort Lauderdale, Florida 33314-7796, USA
d
Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates
e
Regional Organization for the Protection of the Marine Environment (ROPME), 13124 Safat, Kuwait

a r t i c l e i n f o a b s t r a c t

Article history: A severe bleaching event affected coral communities off the coast of Abu Dhabi, UAE in August/September, 2012.
Received 18 December 2015 In Saadiyat and Ras Ghanada reefs ~40% of the corals showed signs of bleaching. In contrast, only 15% of the corals
Received in revised form 6 February 2016 were affected on Delma reef. Bleaching threshold temperatures for these sites were established using remotely
Accepted 1 March 2016
sensed sea surface temperature (SST) data recorded by MODIS-Aqua. The calculated threshold temperatures var-
Available online 10 March 2016
ied between locations (34.48 C, 34.55 C, 35.05 C), resulting in site-specic deviations in the numbers of days
Keywords:
during which these thresholds were exceeded. Hence, the less severe bleaching of Delma reef might be explained
Coral bleaching by the lower relative heat stress experienced by this coral community. However, the dominance of Porites spp.
Threshold temperature that is associated with the long-term exposure of Delma reef to elevated temperatures, as well as the more pris-
Extreme environment tine setting may have additionally contributed to the higher coral bleaching threshold for this site.
Coral reefs Crown Copyright 2016 Published by Elsevier Ltd. This is an open access article under the CC BY license
Zooxanthellae (http://creativecommons.org/licenses/by/4.0/).
Symbiodinium
Global change

1. Introduction cooling by winds (Thoppil and Hogan, 2010; Cavalcante et al., 2016) or
preferential heating/cooling in shallow areas or regions protected by
Warm water coral reefs are among the most productive and biologi- headlands is common (Riegl and Purkis, 2012). Correspondingly, small-
cally diverse ecosystems on Earth. Many of these reefs are in decline due scale excursions of thermal stress with consequent variation in the se-
to the impact of a variety of global and local stressors (Sheppard, 2003, verity of coral bleaching and mortality events have been observed. A se-
Baker et al., 2008, Logan et al., 2014, van Hooidonk et al., 2013, vere bleaching event recorded in 2007 off the Iranian coast (Baker et al.,
D'Angelo and Wiedenmann, 2014). Among them are heat stress episodes 2008) was absent or had negligible impact in the south-eastern IRSA.
during which temperatures exceed a regional threshold and induce the Bleaching was observed in 2013 in Qatar, but not in eastern Abu Dhabi
often fatal breakdown of the coral/alga symbiosis which manifests as (B. Riegl pers. obs.). In general, coral stress events in the northern IRSA
coral bleaching (Baker et al., 2008, Goreau and Hayes, 1994). The globally (Iran) often do not coincide with those in the southern IRSA, and the
highest bleaching thresholds are found among corals of the southern Western IRSA (Kuwait, KSA, Bahrain) appears to have suffered fewer,
Arabian/Persian Gulf, hereafter IRSA (Inner ROPME Sea Area) where or at least differently-timed, events than the south-eastern IRSA.
they survive peak temperatures above 35 C (Coles, 2003; Sheppard Hence, strong regional variability in the frequency and severity of
et al., 1992). However, also these corals can fall victim to bleaching and bleaching events seem to be characteristic for the region.
coral bleaching linked to unusually warm temperatures has been Bleaching events are frequently characterized by high variability. On
shown to affect the IRSA at least since 1996 contributing to a substantial an individual level, the within-colony bleaching response can strongly
loss of coral cover (Riegl and Purkis, 2015; Riegl, 2002). The variability of vary depending on light exposure (Coles and Jokiel, 1978; Brown
bleaching susceptibility observed among different species resulted in et al., 1994; Hoegh-Guldberg, 1999). Further variability can also arise
shifts of the coral community structure in the aftermath of bleaching from the bleaching susceptibility of different zooxanthellae clades/spe-
events in the IRSA (Riegl and Purkis, 2015). cies (Baker, 2001; Pettay et al., 2015). Among them, the year-round
The IRSA is a shallow basin at high latitude and therefore, the thermal prevalent algal partner of corals in the southern IRSA, Symbiodinium
properties of the waterbody, respond quickly to local factors. Rapid thermophilum, can be considered to be one of the most thermo-

http://dx.doi.org/10.1016/j.marpolbul.2016.03.001
0025-326X/Crown Copyright 2016 Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
 D. Shuail et al. / Marine Pollution Bulletin 105 (2016) 654659 655

tolerant symbionts (D'Angelo et al., 2015; Hume et al., 2015). Marked tools to reconstruct environmental conditions prevailing during coral
regional variability is commonly encountered during bleaching events reef disturbance events (Andrfout et al., 2014), we used satellite
and may be caused by small-scale water-dynamics and ow patterns data to establish the local bleaching thresholds in the study sites.
(Nakamura and Van Woesik, 2001; Davis et al., 2011), by greater adap-
tation/acclimatization due to previous stress episodes (Brown et al., 2. Material and methods
2002; Guest et al., 2012) or by differences in the species assemblage of
the affected sites (Marshall and Baird, 2000). The onset of bleaching is 2.1. Measuring SST using remote sensing products
often not synchronous across several, even nearby, reefs and neither is
the severity or the effects of bleaching (Baker et al., 2008). Additional The SST (C) data was extracted from the Aqua\Terra Ocean Color 3
stressors, such as the disturbance of the nutrient environment, can (OC3) Moderate Resolution Imaging Spectroradiometer (MODIS) imag-
have signicant impacts on bleaching susceptibility (Wiedenmann ery downloaded from the NASA ocean color data website (http://
et al., 2012; D'Angelo and Wiedenmann, 2014). In this context, the oceancolor.gsfc.nasa.gov/) and by the Regional Organization for the
mean water column productivity, besides mean temperatures, was the Protection of the Marine Environment (ROPME) archived in Kuwait.
best predictor of the variability of coral reef recovery across the Indo- MODIS data are recorded by two instruments. The rst is integrated in
Pacic (Riegl et al., 2015). Also, local adaptions to environmental factors the Terra satellite (MODIS-Terra) and launched in December, 1999.
other than temperature can have strong inuences on the temperature The second instrument is installed on the Aqua satellite (MODIS-
tolerance of corals. D'Angelo et al. have shown that IRSA corals are char- Aqua), and was launched in May, 2002. Both satellites are in sun-
acterized by a pronounced local adaptation to the high salinity of their synchronous orbits: Terra crosses the equator in a descending node at
habitat and that their superior heat tolerance is lost when they are 10:00, and Aqua crosses in an ascending node at 12:00 noon. Satellite
exposed to normal oceanic salinity levels (D'Angelo et al., 2015). Global imagery was used for the periods between February, 2000 to December,
warming will expose the world's reef to positive temperature anomalies 2014 (MODIS Terra) and from July, 2002 to December, 2014. (MODIS
with increasing frequency (Logan et al., 2014). The prerequisite for Aqua). Level-2 images were used for which the sensors were calibrated,
knowledge-based coral reef management that aims to regionally miti- geo-located with atmospheric corrections and bio-optical algorithms
gate the effects of climate change is a thorough understanding of how had been applied. Temperatures were determined for 1 km2 areas cov-
local factors modulate the response to temperature stress. Therefore, ering the study sites, the highest spatial resolution provided by the
we set out to identify the causes for local differences in bleaching sever- MODIS product. Images were analyzed using the SeaWiFS Data Analysis
ity observed among coral communities in the southern IRSA off the System (SeaDAS) software program Version 7.2 and VISAT BEAM soft-
coast of Abu Dhabi. Since remote sensing platforms offer valuable ware Version 4.10.3. Images in which the SST signal was affected by

Fig. 1. Bathymetric map of the southern IRSA. Numbers identify the three study sites: (1) Delma, (2) Saadiyat and (3) Ras Ghanada. The Map was constructed using Sea-viewing Wide
Field-of-view Sensor (SeaWiFS) Ocean Color Data provided by NASA Ocean Biology (OB.DAAC). Gray-level scale denes the depth in meters.
656 D. Shuail et al. / Marine Pollution Bulletin 105 (2016) 654659

Table 1 2.4. Calculation of bleaching threshold temperatures

Calculated bleaching threshold temperatures for the hottest weeks of the year.

Delma Saadiyat Ras Ghanadah The MODIS-Aqua SST data set was used to calculate the local thresh-
Bleaching threshold temp.
old temperature of coral bleaching, dened as the temperature 1 C
34.99 34.55a 34.37 higher than the highest monthly mean temperature (Glynn and
(0131 Aug. 20022014)
Bleaching threshold temp. D'Croz, 1990). Since the SST peaks are mostly in August in the southern
35.05 34.53 34.48
(15 Aug.15 Sept. 20022014) IRSA (Supplementary Fig. 2), we used this period to determine the
a
Highest values for each site are underlined. highest 4-weekly mean temperature using the Aqua data set for the
years 2002 to 2014. However, since temperatures are also high in the
rst two weeks of September, the period from 15th August to 15th Sep-
cloud cover or high amounts of dust in the air were excluded from the tember was analyzed for comparison.
analysis. The time of recording of the respective imagery was extracted
from le names. 2.5. Field surveys

2.2. Reconstruction of daily temperature maxima in situ Coral communities were surveyed at three sites in the southern IRSA
in UAE, Delma (latitude 24.5208/longitude 52.2781), Saadiyat (lat.
In situ water temperature timeseries were recorded at ~7 m depth 24.599/long. 54.4215) and Ras Ghanada (lat. 24.8481/long. 54.6903)
for the Saadiyat and Delma sites using Hobo temperature loggers (Fig. 1). At each of these sites, bleaching was recorded along three rep-
(Tempcon, UK) at hourly intervals from January to December, 2013. licate transects during the period from 17th to 19th September, 2012.
Using this data set and data from August 2014, typical daily temperature Transects were arranged radially around a central origin, extending for
variations were calculated by averaging the corresponding hourly 10 m with 120 degrees separating each transect. Corals were classied
values for the last week of August, commonly one of the hottest to genus level on the basis of Veron (2000), with taxonomic updates
weeks of the year. This temperature record revealed considerable vari- from Budd et al. (2012). The genus of juvenile corals (b 5 cm diameter)
ations of the temperature over the course of the day with temperatures within a 1 m wide band were included in the dataset. The analysis of
differing by N0.25 C between the early morning hours and the daily adult corals was restricted to Platygyra spp. and Porites spp. as these
temperature maximum at ~17:00 (Supplementary Fig. 1). corals were represented in large numbers in all sites. Porites spp. were
represented by species with massive growth forms (Porites cf. lutea,
2.3. Reconstruction of daily temperature maxima using remote sensing data lobata and harrisoni). Underwater color scales were used to assign the
degree of bleaching to three categories: 1) Bleached: The whole colony
The recording times of the analyzed MODIS Terra and Aqua imagery was white, 2) Partially bleached: Larger parts of the colony (N20%) lost
show considerable deviations due to the different ight paths of the sat- their normal color and 3) Unbleached: The colonies showed their typi-
ellites. Terra data were recorded between 09:3011:45 (median 10:50) cal variety of colors.
whereas Aqua images were taken in the period 12:0514:20 (median Chi-square statistic (2) was used to test whether the percentage of
13:50). The Terra data provide values that can be ~ 0.15 C below the bleached, partially bleached and non-bleached coral colonies recorded
daily SST maximum due to their early recording time. By contrast, in August 2012 in Delma, Saadiyat and Ras Ghanada was region-specic.
MODIS Aqua records close to the in situ temperature maximum and its
data are therefore best suited to reconstruct the SST of the IRSA. To 3. Results
verify this method, we selected N250 pairs of MODIS-Aqua values and
corresponding in situ measurements (14:00 data points), from days 3.1. Local temperature thresholds of coral bleaching
distributed over all seasons of 2013. Then, the corresponding tempera-
ture values were plotted against each other and the coefcient of deter- Using the MODIS Aqua data, the local threshold temperatures for
mination (R2) for a linear regression t was calculated (Supplementary coral bleaching (dened as 1 C above the long-term average of the
Fig. 2bc). mean temperature of the 4 hottest weeks of each year) was calculated

Fig. 2. Variations in heat stress exposure during the 2012 bleaching event in the southern IRSA reconstructed from MODIS-Aqua imagery. a) Number of days during which the site-specic
bleaching threshold temperatures (Delma: 35.05 C, Saadiyat 34.55 C, Ras Ghanada: 34.8 C) were exceeded in each of the study sites. b) Days at which the site-specic local bleaching
threshold was exceeded in the corresponding study sites, indicating also the length of the positive temperature anomaly.
 D. Shuail et al. / Marine Pollution Bulletin 105 (2016) 654659 657

Fig. 3. Site-specic composition of the coral community. a) Total number of juvenile (species indicated in the panel legend) and b) adult (Porites spp. and Platygyra spp.) corals recorded
along the transects in the three study sites.

for the time period 20022014. Comparably high threshold tempera- time over which IRSA corals are exposed to elevated temperatures
tures were obtained for the 4 weeks of August and for the period from (Table 1). Our analysis revealed marked differences in the local temper-
the 15th of August to the 15th of September, signifying the length of ature history of the study sites which are reected in bleaching

Fig. 4. Representative photographs of corals from the bleaching categories used in this study. (Image credits: J. Wiedenmann).
658 D. Shuail et al. / Marine Pollution Bulletin 105 (2016) 654659

threshold temperatures ranging from 34.48 C (Ras Ghanada) over lost their pigmentation often in the upper, most light-exposed parts of
34.55 C (Saadiyat) to 35.05 C (Delma) (Supplementary Fig. 2, Table 1). the colonies.
In summer 2012, the number of days during which temperatures In Ras Ghanada and Saadiyat reefs, N40% of the analyzed corals
exceeded 35.05 C was comparable for the three sites (Fig. 2a). Around (juvenile and adult Porites, adult Platygyra) were affected by bleaching
Delma reef, temperatures above 34.48 and 34.55 C were recorded more (Fig. 5). An exception were juvenile Porites among which no partially
frequently than for the other two sites within the same time period. bleached individuals were encountered in Ras Ghanada and the overall
However, due to the site-specic deviations of the bleaching threshold percentage of colonies showing signs of bleaching was accordingly
temperatures, the three locations showed considerable differences in lower. In all analyzed groups, between 20 and ~30% of the corals were
the number of days during which their regional thresholds were completely bleached in Saadiyat and Ras Ghanada. By contrast, the
exceeded (Fig. 2b). Specically, coral communities had to endure corals in the Delma site were less affected and no more than 15% of
above-threshold temperatures for 16 days in Ras Ghanada reefs and the corresponding groups showed signs of bleaching. For both species,
for 15 days in Saadiyat reefs. In contrast, in Delma Island reefs, the tem- statistical analysis identied the lower bleaching severity in Delma as
peratures were higher than the local bleaching threshold for only a signicant site-specic effect (Supplementary Table 3).
10 days (Fig. 2). Also, the period of time between the rst and the last Similar bleaching levels were observed for the combined numbers of
day at which the threshold temperatures were exceeded was longer recorded juveniles from other species (Supplementary Fig. 3). It has to
in Saadiyat and Ras Ghanada compared to Delma. These data suggest be noted, however, that the data for Delma reef need to be considered
that similar relative heat stress levels were experienced by corals in with caution due to low number of non-Porites spp. juveniles encoun-
Saadiyat and Ras Ghanada and that these were higher than in Delma. tered in this site.

3.2. Site-specic severity of the 2012 bleaching event 4. Discussion

We surveyed three coral reef sites in the southern IRSA to document We studied three sites in the IRSA that experienced different levels
the bleaching event that took place in August/September 2012. The of bleaching during the 2012 bleaching event with the purpose to estab-
three sites revealed pronounced differences in the abundance of genera lish potential causes for the patchiness of bleaching that is frequently
and genus richness of juvenile corals (Fig. 3a). The overall abundance of observed during mass bleaching events. Bleaching levels for two com-
juveniles was similar in Saadiyat and Ras Ghanada and numbers were mon taxa, Porites spp. and Platygyra spp., were analyzed. Additionally,
higher than in Delma. Species richness of juvenile corals decreased we recorded the site-specic degree of bleaching among juvenile Porites
from Ras Ghanada to Saadiyat and Delma, with Porites spp. becoming in- spp. and other less abundant corals.
creasingly dominant. Similarly, the number of adult Porites spp. and Reefs in Saadiyat and Ras Ghanada were severely affected by
Platygyra spp. recorded along the transects was higher in Ras Ghanada bleaching whereas corals in Delma showed little or no signs of bleaching
and Saadiyat than in Delma (Fig. 3b). despite their relatively close geographic proximity and exposure to a
Within the sites, corals of the same taxonomic group were affected comparable temperature regime in AugustSeptember, 2012. This
to variable degrees by bleaching, ranging from unaffected to partially trend was comparable for all the monitored species and developmental
bleached and completely bleached (Fig. 4). Partially bleached corals stages.
Since light exposure is known to promote heat-stress mediated
bleaching (Coles and Jokiel, 1978; Brown et al., 1994, 2002;
Hoegh-Guldberg, 1999; Fitt et al., 2001), the observation, that partial
bleaching of adult colonies was frequently found in the upper part of
the colonies, suggests that light stress was also inuential in 2012
bleaching event.
In Ras Ghanada, a higher percentage of adult Porites spp. showed
signs of bleaching compared to juveniles from the same taxon. This ob-
servation is in line with previous studies that found that juvenile corals
were less affected by bleaching than adults (Mumby, 1999; Nakamura
and Van Woesik, 2001; Loya et al., 2001). However, this trend was not
observed in the other sites where comparable numbers of adults and
juveniles suffered from bleaching.
A possible explanation for the different bleaching susceptibility
across the three study sites is that the local bleaching threshold of
~ 35 C at Delma reef is ~ 0.5 C higher than in the other sites. Conse-
quently, the corals experienced less relative heat stress, indicated by
the smaller number of days during which the local bleaching threshold
was exceeded. Still, the threshold temperature was exceeded for
10 days at Delma with little effect on the corals, setting this site
among the most temperature tolerant reefs of the world (Riegl et al.,
2011, 2012). The resilience of Delma reef is further underlined by the fe-
cundity of its corals in the aftermath of the 2012 bleaching event which
was signicantly higher compared to those from Saadiyat and Ras
Ghanada reefs (Howells et al., 2016). Previous observations from else-
where found massive Porites spp. to be among the taxa with a high
survival rate after bleaching events (Loya et al., 2001; Sheppard and
Loughland, 2002). Therefore, the dominance of massive Porites spp. at
Delma (Burt et al., 2011) that is reected by the species composition
of juvenile corals presented in this study, may be considered as an addi-
Fig. 5. Site-specic severity of bleaching. Comparison of the percentage of the total tional potential reason for the exceptional heat tolerance of this reef site
numbers of juvenile and adult Porites spp. colonies and other species affected by bleaching. (Marshall and Baird, 2000; Loya et al., 2001). Also, the history of
 D. Shuail et al. / Marine Pollution Bulletin 105 (2016) 654659 659

increased temperature stress levels in Delma may have increased the D'Angelo, C., Wiedenmann, J., 2014. Impacts of nutrient enrichment on coral reefs: new
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et al., 2002). Furthermore, Delma reef is situated ~50 km off the coast Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium
from the Persian/Arabian Gulf. ISME J. 110.
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cause of El Nio-coincident coral mortality. Coral Reefs 8, 181191.
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the coral communities at the study sites offer likely explanations for Species-specic trends in the reproductive output of corals across environmental gra-
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other parameters such as the water quality and light stress should also Symbiodinium thermophilum sp. nov., a thermotolerant symbiotic alga prevalent in
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Logan, C., Dunne, J.P., Eakin, C.M., Donner, S.D., 2014. Incorporating adaptive responses
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verse Saadiyat and Ras Ghanada sites. Hence, a long-term increase of the Loya, Y., Sakai, K., Nakano, Y., Woesik, R. Van, 2001. Coral Bleaching: The Winners and The
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Acknowledgment in Belize. Mar. Ecol. Prog. Ser. 190, 2735.
Nakamura, T., Van Woesik, R., 2001. Water-ow rates and passive diffusion partially ex-
plain differential survival of corals during the 1998 bleaching event. Mar. Ecol. Prog.
The study was funded by NERC (Grant no. NE/K00641X/1 to JW) and Ser. 212, 301304.
the European Research Council under the European Union's Seventh Pettay, D.T., Wham, D.C., Smith, R.T., Iglesias-Prieto, R., LaJeunesse, T.C., 2015. Microbial in-
vasion of the Caribbean by an Indo-Pacic coral zooxanthella. Proc. Natl. Acad. Sci. U.
Framework Program (FP/20072013) ERC Grant Agreement no.
S. A. 112, 75137518.
311179 to JW and a scholarship by the Public Authority for Education Riegl, B., 2002. Effects of the 1996 and 1998 positive sea-surface temperature anomalies
and Training of the State of Kuwait to DS. We are grateful to NYU Abu on corals, coral diseases and sh in the Arabian Gulf (Dubai, UAE). Mar. Biol. 140,
Dhabi Institute for supporting the 2012/2013 eld workshops during 2940.
Riegl, B.M., Purkis, S.J., 2012. Coral reefs of the gulf: Adaptation to climatic extremes in the
which data for this study were collected. We also thank Tropical Marine world's hottest sea. Coral Reefs of the Gulf, pp. 14.
Centre (London) and Tropic Marin (Wartenberg) for sponsoring the Riegl, B., Purkis, S., 2015. Coral population dynamics across consecutive mass mortality
NOCS Coral Reef Laboratory and acknowledge NASA Ocean Biology events. Glob. Chang. Biol. 21, 39954005.
Riegl, B., Glynn, P.W., Wieters, E., Purkis, S., d'Angelo, C., Wiedenmann, J., 2015. Water col-
(OB.DAAC) for Sea-viewing Wide Field-of-view Sensor (SeaWiFS) umn productivity and temperature predict coral reef regeneration across the Indo-
Ocean Color Data. We extend our appreciation to ROPME for the access Pacic. Sci. Rep. 5, 8273.
to their remote sensing database. Riegl, B.M., Purkis, S.J., Al-Cibahy, A.S., Abdel-Moati, M.A., Hoegh-Guldberg, O., 2011. Pres-
ent limits to heat-adaptability in corals and population-level responses to climate ex-
tremes. PLoS One 6, e24802.
Appendix A. Supplementary data Riegl, B.M., Purkis, S.J., Al-Cibahy, A.S., Al-Harthi, S., Grandcourt, E., Al-Sulaiti, K., Baldwin,
J., Abdel-Moati, A.M., 2012. Coral bleaching and mortality thresholds in the SE Gulf:
highest in the world. Coral Reefs of the Gulf. Springer, pp. 95105.
Supplementary data to this article can be found online at http://dx. Sale, P.F., Feary, D.a., Burt, J.a., Bauman, A.G., Cavalcante, G.H., Drouillard, K.G., Kjerfve, B.,
doi.org/10.1016/j.marpolbul.2016.03.001. Marquis, E., Trick, C.G., Usseglio, P., Van Lavieren, H., 2011. The growing need for sus-
tainable ecological management of marine communities of the Persian Gulf. Ambio
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