coral bleaching and mortality thresholds in the se gulf, highest in the world - riegl et al 2012

7/31/2019 Coral Bleaching and Mortality Thresholds in the SE Gulf, Highest in the World - Riegl Et Al 2012

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95B.M. Riegl and S.J. Purkis (eds.), Coral Reefs of the Gulf: Adaptation to Climatic Extremes,Coral Reefs of the World 3, DOI 10.1007/978-94-007-3008-3_6,

Springer Science+Business Media B.V. 2012

6.1 Introduction

Bleaching is a stress reaction in corals, during which the

symbiosis between corals and the algae (zooxanthellae) living

in the coral cells breaks down. As a result, zooxanthellae are

expelled, and the coral appears pale or even white (Fig. 6.1;

Baker et al. 2008). The link between environmental variables

and coral bleaching has been well-established in a variety of

studies and synthesized in several places (Phinney et al.

2006; Baker et al. 2008; van Oppen and Lough 2009). Large-

scale and region-wide bleaching events, such as occur in the

Gulf, have been clearly linked to unusually high tempera-

tures and the accumulation of heat stress in corals. Other

drivers, such as UV and water acidity can have compounding

effects (Baker et al. 2008) and bleaching can also be caused

by these factors alone, or other local drivers such as unusu-

ally cold temperatures (Saxby et al. 2003; Lajeunesse et al.

2007). However, it is heat stress that has been demonstrated

as the most reliable predictor and defined time-integrated

bleaching thresholds exist for various regions of the Indo-

Pacific and the Caribbean (Berkelmans 2002b; Manzello

et al. 2007; Berkelmans 2009).

Since corals adapt to their local environment, bleaching

thresholds vary within and among regions (Berkelmans

2002a, 2009; Manzello et al. 2007; Baker et al. 2008). As

previous chapters in this book have demonstrated, Gulf cor-

als exist in a uniquely extreme environment both with regards

to extreme highs and lows, the regularly recurring long-time

summertime highs (Chap. 4), however, unsurpassed among

any region in the world. Corals do exist in other areas of the

world in very hot environments, for example in the well-

demonstrated case of tide-pools in Samoa (Birkeland et al.

2009) where temperatures can also reach 34.5C but only for

few hours. Gulf corals are unique in being able to survive

daily mean summertime temperatures in excess of 34 or even

35C for months (Chap. 4). Thus the question becomes just

how much heat is necessary to bleach, or even kill these

apparently uniquely adapted corals. Such information has

much practical value, since it demonstrates just how much

corals can acclimatize in a heating world (Sheppard 2003).

During 2010, a major, region wide bleaching event

occurred in the SE Gulf. While some previous region-wide

beaching and mass mortality events (1996, 1998, 2002) are

well-documented with regards to their effects on coral popu-

lations and communities (George and John 1999, 2000; Riegl

1999, 2001, 2002, 2003; Sheppard and Loughland 2002;

Purkis and Riegl 2005; Burt et al. 2008; Riegl and Purkis

2009; Chap. 5), associated temperature data have been spo-

radic and coarse in resolution (Riegl 2002; Sheppard and

Loughland 2002). During 2010, we had available both locally

continuous temperature and coral monitoring data through-

out the bleaching event which now allows the construction of

bleaching threshold curves and estimates of differential

impacts on all involved coral taxa.

6.2 Study Area and Methods

Study locations were situated in the SE Gulf, in the UAE and

Qatar and are part of a routine monitoring program estab-

lished over 2006/2007. Some of the sites are described in

Chap. 4. For the present contribution, local bleaching thresh-

olds were derived at Bu Tinah in the UAE from where an

Coral Bleaching and MortalityThresholds in the SE Gulf: Highestin the World

Bernhard M. Riegl, Sam J. Purkis, Ashraf S. Al-Cibahy,Suaad Al-Harthi, Edwin Grandcourt, Khalifa Al-Sulaiti,James Baldwin, and Alaa M. Abdel-Moati

6

B.M. Riegl (*) S.J. Purkis

National Coral Reef Institute, Nova Southeastern University,

Dania Beach, FL, USA

e-mail: [email protected]; [email protected]

A.S. Al-Cibahy S. Al-Harthi E. Grandcourt

Environment Agency-Abu Dhabi, Abu Dhabi,

United Arab Emirates

e-mail: [email protected]; [email protected]; [email protected]

K. Al-Sulaiti J. Baldwin

Qatar Gas, Ras Laffan Industrial City, Qatar

e-mail: [email protected];

[email protected]

A.M. Abdel-Moati

Ministry of Environment, Doha, Qatar

e-mail: [email protected]


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96 B.M. Riegl et al.

almost complete temperature timeseries exists from 2007

through the end of 2010 (HoboTemp loggers recording

hourly temperatures at 4 m depth) and at Fasht el Hurabi in

Qatar from where a continuous temperature time series exists

also from 2007 to 2010 (HoboTemp loggers recording at

hourly intervals in 2007 and 2008, VEMCO Miniloggers

recording at half hourly or hourly intervals in 2009 and 2010

at 5 m depth). Large-scale temperature records for the entire

Gulf and world-wide, in order to evaluate the severity and

extent of the thermal anomaly, were obtained from the Met

Office, UK. For Gulf-wide analysis we employed the

HadISST 11 gridded dataset, and for worldwide analysis

the HadISST and HadISST2 55 gridded products offered

at www.hadobs.org(Rayner et al. 2003, 2006). Graphs were

produced using the Erddap mapping facility (http://coast-

watch.pfeg.noaa.gov/erddap/). Air temperature data for

Sharjah airport were obtained from http://climexp.knmi.nl/.

MODIS global SST data were obtained from http://neo.sci.

gsfc.nasa.gov.

Additionally, detailed information about coral mortality

existed at both sites and in the general region from monitoring

programs maintained in Qatar and the UAE. While obvi-

ously local variability exists in temperature among sites

within the SE Gulf, the overall pattern is very similar (Chap. 4).

Fig. 6.1 Bleached corals in Qatar, October 2010. (a) A blanchedPlesiastrea versipora. Blanching is a stress state that occurs prior to

bleaching and is detected by an overall paling of the corals color.

(b) A partially bleached Cyphastrea microphthalma at the height of the

2010 bleaching event. Only a part of the coral is visibly bleached.

(c) A partially bleached Porites harrisoni, (d) a completely bleached

Porites harrisoni not far from the specimen shown in (c) at the same

time. Differences in clades of zooxanthellae, resulting in differential

heat-susceptibility of the algae seem to be responsible (Baker et al.

2004). (e) A completely bleached Coscinarea columna. (f) A com-

pletely bleached Platygyra daedalea. All photographs from the same

area and same time
http://www.hadobs.org/http://www.hadobs.org/http://coastwatch.pfeg.noaa.gov/erddap/http://coastwatch.pfeg.noaa.gov/erddap/http://coastwatch.pfeg.noaa.gov/erddap/http://coastwatch.pfeg.noaa.gov/erddap/http://climexp.knmi.nl/http://climexp.knmi.nl/http://climexp.knmi.nl/http://neo.sci.gsfc.nasa.gov/http://neo.sci.gsfc.nasa.gov/http://neo.sci.gsfc.nasa.gov/http://neo.sci.gsfc.nasa.gov/http://neo.sci.gsfc.nasa.gov/http://neo.sci.gsfc.nasa.gov/http://climexp.knmi.nl/http://coastwatch.pfeg.noaa.gov/erddap/http://coastwatch.pfeg.noaa.gov/erddap/http://www.hadobs.org/


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976 Coral Bleaching and Mortality Thresholds in the SE Gulf: Highest in the World

We therefore investigated coral bleaching and mortality at

several sites in order to detect any commonalities or differ-

ences in local population responses. Sites were at Ras

Ghanada, Al Heel, Dalma and Bu Tina in Abu Dhabi and

Fasht el Hurabi in Qatar. At these sites, phototransects were

taken during and after the bleaching event and compared to

similar transects taken earlier (Ras Ghanada; transect time

series dating back to 2000, regular annual data since 2007).At Al Heel, and Dalma, phototransects exist dating back to

2007. Also at Fasht el Hurabi in Qatar, phototransects, as

well as tagged coral colonies existed for the evaluation of

bleaching. All coral monitoring took place at the end of the

bleaching event, in the last week of September or the first

2 weeks in October 2010.

Thermal bleaching and mortality thresholds were derived

according to Berkelmans (2002a, b, 2009) and Dunne (2002).

At each location, the cumulative time (in days) at each tem-

perature between 30C and 36C (average daily temperature,

since either 24 or 48 daily readings were available) was

calculated. It is known from previous bleaching events in the

Gulf that temperatures need to exceed 35.5C for significant

mortality to occur (Riegl 2002). Bleaching thresholds were

derived using Berkelmans corrected (2002b) equation:

(6.1)

Where bcis the predicted temperature value for the bleach-

ing curve, s is a non-dimensional weighting factor that scales

bleaching severity on a scale from 1 to 4 (we used 4 in this

paper; 1 is mild bleaching, 4 the most severe), Tb

is the tem-

perature distribution in the coolest bleaching year (in our case,

since only one bleaching event was captured, the temperature

curve for 2010), and Tn

is the temperature distribution in the

warmest non-bleaching year. Tb

and Tn

are obtained by com-

paring graphed or tabulated values of the cumulative times

spent at 30C or higher (see above). Ttis the threshold tempera-

ture, i.e. the highest temperature at which no bleaching occurs.

Mortality curves were derived using Berkelmans (2009)

method. These mortality curves are specific to the most

susceptible genus, Acropora, which suffered almost 100%

mortality (see below) in western Abu Dhabi (Dalma, Bu

Tinah, Al Heel), and overall 6080% mortality in eastern

Abu Dhabi (Ras Ghanada). We therefore followed Berkelmans

(2009) in the assumption that TL50

, the temperature value at

which 50% mortality occurs in the indicator corals, is situ-

ated halfway between the bleaching threshold and the value

causing 100% mortality.

We also calculated degree heating days (DHD) and heating

rate (HR), which Maynard et al. (2008a) have shown to be a

useful stress indicators.

(6.2)

where LMST is long-term mean summer temperature (July,

August, September) and Theating

is the daily average tempera-

ture during bleaching. We did not have a long-term record

available, since comparison of in-situ temperature records

with remotely-sensed records did not coincide (see results).

As closest proxy to a long-term record, we used the mean

daily temperatures from 1 July to 30 September over the

three non-bleaching years (2007, 2008, 2009) compared withthe bleaching year (2010). The period 1 July-30 September

encompasses peak temperatures (Fig. 6.9). Heating rate was

calculated as

(6.3)

6.3 The 2010 Bleaching Event in the SE Gulf

Coral bleaching was observed, depending on locality from

August through October 2010. The event was comparable in

severity with the 2002 bleaching event, when almost all cor-

als bleached at least to some extent, but no wide-spread mass

mortality was observed (Riegl 2003). Comparable data for

Qatar are missing, since the 2002 event was not witnessed

there, but presumably similar dynamics occurred.

Depending on locality, the onset of bleaching occurred in

the early to latter half of August and abated by mid September

in eastern Abu Dhabi and in October in Qatar and western

Abu Dhabi with colonies regaining color and no new bleach-

ing observed. At all sites, at least some bleached corals per-

sisted into October 2010. At Fasht el Hurabi, Qatar, most

corals remained bleached until the third week of October

(Figs. 6.1 and 6.2). At Ras Ghanada, most corals had regained

color by the last week of September 2010. At all sites in Abu

Dhabi, significant mortality in Acropora was observed. At

least at Ras Ghanada, this mortality was not uniquely due to

bleaching but to a large extent, if not predominantly, to an

outbreak of diseases, so-called white syndromes (Chap. 7) in

the immediate aftermath of the bleaching. Many Acropora

were able to recuperate from bleaching and coral diseases

did not kill the entire local population. While some patches

ofAcropora escaped unscathed, much of the area suffered

~90% loss ofAcropora tables of all sizes (recruits similarly

affected as large colonies) (Fig. 6.2). At Ras Ghanada, an

estimated 60% of the overallAcropora population was lost.

Also at Al Heel and Dalma,Acropora was the worst-affected

genus, with all colonies in the sampling sites suffering mor-

tality (Fig. 6.2). At Bu Tinah and Fasht el HurabiAcropora

does not occur. Porites harrisoni, a dominant coral through-

out the area, bleached heavily. At Ras Ghanada most colo-

nies had regained most of their color by late September, with

[ ]( )= + - >c n b n b tb T s / 5 T T , for T T

( )= S -heatingDHD T LMST

( )= S >days heatingHR DHD / T LMST


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about 50% remaining blanched (i.e. somewhat paler than

usual), at Al Heel and Dalma about half of the colonies

remained bleached to various extents and at Fasht el Hurabi,

Qatar, most colonies remained bleached white into the sec-

ond week of October. Among the faviids, the genera Favia

and Favites bleached less than Platygyra. Most Platygyra

colonies still showed signs of bleaching (white, whitish or

pale tissue patches as well as increased signs of recent mor-

tality) and subsequent partial mortality.

A clear gradation of bleaching recovery was observed

from W to E, with the least impact and the most rapid regen-

eration at Ras Ghanada in the E, and the longest duration of

the event at Fasht el Hurabi in Qatar, at the western extreme

of the study area.

6.4 Temperature Regime During the 2010Bleaching

6.4.1 Gulf-Wide Pattern

2010 was an overall hot year in the Gulf region. In September

2010, the Gulf was one of the warmest places in the worlds

ocean (Fig. 6.3). A significant positive temperature anomaly

existed over most of the NW Indian Ocean, Red Sea and

Gulf region that persisted throughout the bleaching months

of September and October well into December 2010

(Fig. 6.4). The Gulf showed a positive anomaly between 1

and 3C over this period. The warm temperatures extended

both over land and sea (HadISST and HadISST2 data; Rayner

31

30

29

28

27

26

25

24

23

46 48 50 52 54 56 58Degrees longitude

United ArabEmirates

SaudiArabia

Qatar

Iraq

Kuwait

Degreeslatitude Iran

d

b a

c,e

Fig. 6.2 Taxon-specific bleaching levels during the 2010 event atselected sites in Abu Dhabi and Qatar, SE Gulf (locations detailed in

inset map). (a, b) Relative frequency of taxa along point-intercept

transects in Abu Dhabi and the bleached proportion. (c) Space cover in

phototransects in Abu Dhabi and the bleached proportion. (d) Bleached

proportion of tagged experimental colonies in Qatar. (e) Space cover in

phototransects and proportion of colonies that died in the period from

the onset of bleaching to the monitoring period. The mortality value

thus includes bleaching mortality and subsequent disease attacks

(Chap. 7 )


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Fig. 6.3 Composite image of mean MODIS SST between Sep. 1 and Sep. 30, 2010. During this month and during the bleaching event, the Gulfwas the warmest sea worldwide

Fig. 6.4 World-wide sea surface temperature anomalies during the2010 Gulf bleaching (October, November 11 HadISST data) and

shortly thereafter (November, December 55 HadISST2 data).

Composite images courtesy The MetOffice (http://www.hadobs.org,

crown copyright). The anomalously warm temperatures in the Gulf

region are clearly visible. The anomaly is defined as deviance from the

monthly means in the period 19611990
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Fig. 6.6 Peak hourly temperatures observed in situ at temperaturemonitoring sites at (a) Bu Tinah (c) Fasht el Hurabi. Peak temperatures

are circled red. (b, d) Deviation of mean daily temperatures in 2010

(red) from the mean daily temperatures 20072009 (blue). The in situ

temperature record shows more detail than the 11 gridded HadISST

data (Fig. 6.4). Local temperatures are higher than in the 11 cell and

the cooling trend observed in September in Fig.6.4 did not correspond

to all local data

Table 6.1 Degree heating days (DHD) and heating rate (HR) at sites in Abu Dhabi and Qatar. The peak in DHD in August suggests onset ofbleaching in that month

DHD July HR July DHD August HR August DHD September HR September

Fasht el Hurabi 21.4 0.9 74.3 2.4 40.7 1.35Bu Tinah 12.8 0.6 36.1 1.2 25.6 1.34

Fig. 6.7 Bleaching and mortality thresholds from Abu Dhabi and Qatar. Each datapoint represents the number of days spent at or above the tem-perature on the x-axis


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determinant whether bleaching occurs or not, rather than

the maximum temperatures.

Although local variability is obvious in our dataset and

has been demonstrated from many regions (Berkelmans

2002a, 2009; Manzello et al.2007), we also evaluated a mean

bleaching curve, which takes the average of the observations

at Bu Tinah and Fasht el Hurabi. These mean values would

suggest that, as a rule of thumb, Gulf corals are likely to

bleach if they are exposed to more than 3 weeks at daily

mean temperatures at or above 35C and between 8 and

9 weeks at or above 34C. Such a situation is only likely to

occur in hot summers with heat wave conditions.

6.6 Discussion

Bleaching thresholds in the Gulf are the highest recorded in

the world, and far exceed those recorded from the Great

Barier Reef (Berkelmans 2002a, 2009), Galapagos (Podesta

and Glynn 1997, 2001) and Caribbean (Manzello et al.

2007; Baker et al. 2008). This is clearly selected by the Gulf

being in summer maybe the hottest place on earth support-

ing significant coral growth (Fig. 6.3) forcing Gulf corals to

have higher absolute temperature tolerance than anywhere

else. Daily maximum temperatures survived by corals in

lagoons in American Samoa can exceed 34C (Birkeland et

al. 2009), however, only on an hourly basis, while in the

Gulf daily mean temperatures, peaking sometimes above

36C , can be above 34C for over a month. From nowhere

else have similar long-term warm temperature extremes

been recorded. On Australias Great Barrier Reef and in the

Caribbean, bleaching thresholds are mostly anchored

around maximum temperatures ~30C.

While we fully appreciate that much local variability

exists with regard to the onset of bleaching, and this is also

shown in our dataset (Figs. 6.5 and 6.6), we nonetheless

find a mean bleaching curve, as we show in Fig. 6.8, very

instructive. It suggests that a severe Gulf bleaching event of

the type that causes severeAcropora die back, as treated in

Chap. 5, requires about 3 weeks of exposure to >35C aver-

age daily temperatures. This agrees with findings of Riegl

(2002) for the 1996 and 1998 Acropora mass mortalities.

Our findings also correspond well with those of Manzello et

al. (2007) who found that a combination of maximum SST,

and the number of days spent above a certain threshold

(30.5C in the Caribbean, 35C in the Gulf) are the most

significant determinants for the onset of a bleaching event.

By varying parameter s in Eq. 6.1 (methods section), we

can obtain some insight into the temperature loading required

for milder bleaching to develop (Fig. 6.9). These results

would suggest that, given previous heat-stress accumulation,

about 1 week of average daily temperature means above

35C will cause mild symptoms of bleaching, while about

3 weeks of exposure will cause a severe bleaching event.

Table 6.2 Bleaching table and bleaching thresholds. Values in columns refer to the numbers of days spent at, or above the indicated temperature.Thus, the values of each higher temperature are included in those of the lower temperature. To obtain time spent at each temperature, the sum of

all values of time spent at higher temperatures in the same line must be subtracted. Temperature data exist from 7 July 2010 to 31 December 2010,

thus the time spent at temperatures 30C >31C >32C >33C >34C >35C >36C

Bu Tinah

2007 79* 67* 56* 53* 38* 20* 0

2008 156 130 98 67 43 2 0

2009 161 135 114 67 24 1 0

2010 108 108 100 91 67 23 0

Fasht el Hurabi

2007 136 119 101 76 53 27 0

2008 121 105 78 57 38 4 0

2009 125 105 78 22 8 0 0

2010 136 115 104 93 57 33 0

Bleaching Thresholds

Fasht el Hurabi 134 113 99 79 47 26 0

BuTinah 113 110 101 86 58 18 0

Mean 124 112 100 83 53 22 0

Mortality Thresholds

Fasht el Hurabi 136 115 104 93 57 33 0

BuTinah 119 113 102 89 62 21 0

Mean 127 114 103 91 60 27 0


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While local differences exist with regards to stress-loading

at lower temperatures (3032C), the pattern is very simi-

lar at the higher temperatures (3335C) that are respon-

sible for the onset of bleaching (Berkelmans 2009). Thus,

Gulf corals can support approximately 5C more heat than

their relatives on the Great Barrier Reef and in the

Caribbean.

We also followed Berkelmans (2009) in developing

mortality curves (Table 6.2). We find that in the Gulf, mor-

tality thresholds are close to the bleaching threshold

(Table 6.2) but still exceed those known from any other

region. Gulf corals are probably the most robust corals any-

where in the world with regards to bleaching, and mortality

from bleaching.

The question arises whether the observed very high

bleaching thresholds are already the result of acclimatiza-

tion in response to rapidly recurring heat events (Maynard et

al. 2008a, b; Riegl and Purkis 2009; Chap. 5). Riegl (2003)

observed during the 2002 bleaching event that Acropora,

which during the 1996 and 1998 events had bleached prior

to and suffered more mortality than other taxa, locally (at

Sir Abu Nuair) bleached later and to a lesser extent than

other corals. Maynard et al. (2008a) observed that bleaching

events indeed can lead to increased thermal tolerance. This

may suggest a phenotypic shift in bleaching resistance in

the surviving Gulf coral population. Temperatures in the

Gulf region are indeed getting warmer and atmospheric

temperatures in the region show more, and more closely

Fig. 6.8 Bleaching thresholds derived for a variety of Caribbean andGreat Barrier Reef locations by Berkelmans (2002a, b) and Manzello et

al. (2007) compared to the mean bleaching threshold from the SE Gulf.

The overall tolerance envelope for the comparative areas is shown in

grey. The differential between the curve and the bleaching threshold is

directly related to the physiological capability of corals to adapt to heat

Fig. 6.9 Theoretical bleaching curves derived from Berkelmans (2002b) equation if the bleaching severity is altered while all other parametersare held equal. The value on the curve is parameters of equation 6.1


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spaced, positive anomalies since the 1980s. This has been

interpreted as a global warming signature (Nasrallah et al.

2004; Al-Rashidi et al. 2009) and may therefore have con-

tributed to raising bleaching thresholds over the past decade

due to selection caused by closely-spaced bleaching events

(Fig. 6.10).

The remarkable temperature tolerance of Gulf corals sug-

gests that coral physiology is indeed capable of adapting to

high temperatures and that some hope may exists that coral

adaptation can track continuously increasing temperatures.

If corals are not subjected to a host of other stressors, reason-

able hope may exist that at least a subset of todays coral

fauna may adapt to a heated world.

Acknowledgements Early phases of the monitoring project were

funded by the WWF/EWF/Dolphin project and then sponsored by Abu

Dhabi EAD, Qatar Gas, Qatar Ministry of Environment and NCRI at

NSU. We thank R. Al-Mubarak, F. Launay, M. Chandler for support

during that project.

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