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Beyond peak summer temperatures, branching corals in the Gulf of Aqaba are resilient to thermal stress but sensitive to high light


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Despite rapidly rising sea surface temperatures and recurrent positive temperature anomalies, corals in the Gulf of Aqaba (GoA) rarely experience thermal bleaching. Elsewhere, mass coral bleaching has been observed in corals when the water temperature exceeds 1–2 °C above the local maximum monthly mean (MMM). This threshold value or “bleaching rule” has been used to create predictive models of bleaching from satellite sea surface temperature observations, namely the “degree heating week” index. This study aimed to characterize the physiological changes of dominant reef building corals from the GoA in response to a temperature and light stress gradient. Coral collection and experiments began after a period of 14 consecutive days above MMM in the field. Stylophora pistillata showed negligible changes in symbiont and host physiology parameters after accumulating up to 9.4 degree heating weeks during peak summer temperatures, for which the index predicts widespread bleaching and some mortality.
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Beyond peak summer temperatures, branching corals in the Gulf
of Aqaba are resilient to thermal stress but sensitive to high light
Jessica Bellworthy
Maoz Fine
Received: 31 January 2017 / Accepted: 29 May 2017
ÓSpringer-Verlag Berlin Heidelberg 2017
Abstract Despite rapidly rising sea surface temperatures
and recurrent positive temperature anomalies, corals in the
Gulf of Aqaba (GoA) rarely experience thermal bleaching.
Elsewhere, mass coral bleaching has been observed in
corals when the water temperature exceeds 1–2 °C above
the local maximum monthly mean (MMM). This threshold
value or ‘‘bleaching rule’’ has been used to create predic-
tive models of bleaching from satellite sea surface tem-
perature observations, namely the ‘‘degree heating week’
index. This study aimed to characterize the physiological
changes of dominant reef building corals from the GoA in
response to a temperature and light stress gradient. Coral
collection and experiments began after a period of 14
consecutive days above MMM in the field. Stylophora
pistillata showed negligible changes in symbiont and host
physiology parameters after accumulating up to 9.4 degree
heating weeks during peak summer temperatures, for
which the index predicts widespread bleaching and some
mortality. This result demonstrates acute thermal tolerance
in S. pistillata from the GoA and deviation from the
bleaching rule. In a second experiment after 4 weeks at
4°C above peak summer temperatures, S. pistillata and
Acropora eurystoma in the high-light treatment visibly
paled and suffered greater midday and afternoon photoin-
hibition compared to corals under low-light conditions
(35% of high-light treatment). However, light, not
temperature (alone or in synergy with light), was the
dominant factor in causing paling and the effective quan-
tum yield of corals at 4 °C above ambient was indistin-
guishable from those in the ambient control. This result
highlights the exceptional, atypical thermal tolerance of
dominant GoA branching corals. Concomitantly, it vali-
dates the efficacy of protecting GoA reefs from local
stressors if they are to serve as a coral refuge in the face of
global sea temperature rise.
Keywords Coral Degree heating weeks Gulf of Aqaba
Thermotolerance Refugia Resilience
The recent global coral bleaching event, the longest on
record (NOAA 2016), is a clear cause for concern. In the
wake of the third global mass bleaching event, it becomes
increasingly important to identify reefs resilient to global
change to support conservation efforts. High light in
combination with heat enhances the likelihood of bleaching
(Fitt et al. 2001; Bhagooli and Hidaka 2004; Lesser and
Farrell 2004; Hill et al. 2005). Both stressors reduce pho-
tosynthetic yield of the Symbiodinium symbionts, primarily
through accumulation of reactive oxygen species. Yield
may be impaired via damage to the D1 protein of photo-
system II (Warner et al. 1996), inhibition of de novo D1
protein synthesis (Warner et al. 1999; Takahashi et al.
2013), disrupted thylakoid membrane integrity (Tchernov
et al. 2004), or the light harvesting complexes (Takahashi
et al. 2008). Chlorophyll fluorescence parameters are often
used to indicate the degree of thermal and light stress
experienced by photosystem II within the coral’s symbiotic
dinoflagellates (Warner et al. 1999; Hill et al. 2004;
Communicated by Biology Editor Dr. Anastazia Banaszak
&Jessica Bellworthy
The Mina and Everard Goodman Faculty of Life Sciences,
Bar-Ilan University, Ramat Gan, Israel
The Interuniversity Institute for Marine Sciences, Eilat, Israel
Coral Reefs
DOI 10.1007/s00338-017-1598-1
Rodrigues et al. 2008; Schrameyer et al. 2016). In a variety
of photosynthetic organisms, including corals, midday
depressions in effective quantum yield (DF/F
0) are
observed (Brown et al. 1999a; Sorek and Levy 2012). The
magnitude of diurnal change and recovery of this param-
eter can be used to assess photoinhibition and the degree of
adaptation to the prevailing light environment (Brown et al.
1999b; Jones and Hoegh-Guldberg 2001; Winters et al.
2003; Hill and Ralph 2005).
Temperatures 1–2 °C above the local annual maximum
temperature are often cited as the level of thermal stress
which initiates bleaching, otherwise referred to as the
‘bleaching rule’’, which defines ‘‘hot spots’’ as used by the
United States National Oceanic and Atmospheric Admin-
istration (NOAA). Since the extent of coral bleaching is
influenced by the cumulative effect of sustained hot spots,
these are used to calculate NOAA’s degree heating week
(DHW) index (Wellington et al. 2001; Liu et al. 2006). The
DHW index represents the intensity and duration for which
the night time sea surface temperature (SST) has been
C1°C higher than the climatological (20 yr) maximum
monthly mean (MMM) over the preceding 12-week period
in a given location. Four DHW has resulted in significant
bleaching (Liu et al. 2006), and coral mortality is expected
to occur above 8 DHW. Hot spot and DHW theory are
supported primarily by observations from the Great Barrier
Reef (Berkelmans and Willis 1999; Liu et al. 2003) and the
Caribbean (Montgomery and Strong 1994), and yet the
theory is applied to coral reefs worldwide without con-
sideration for regional differences in bleaching thresholds
(Maina et al. 2008; Donner et al. 2009).
Annual SST in the northern Gulf of Aqaba (GoA) has
been increasing at an average rate of 0.034 °Cyr
the past 25 yr, with summer (August) temperatures
increasing at a faster rate than the winter (February; Fine
et al. 2013). Despite repeated episodes of temperatures
beyond the predicted local bleaching threshold, only neg-
ligible paling has been observed on the reefs of Eilat
(Shaked and Genin 2014) and mass bleaching has not been
recorded. For example, during the summer of 2012, the
water temperature exceeded the MMM on 42 out of
52 days. Despite this, the national monitoring program did
not detect any bleaching and in fact reported an increase in
the coral live tissue index reversing the trend of previous
years (Shaked and Genin 2014). In addition, experimental
work using multiple species common at Eilat report no
visual signs of bleaching or significant changes in chloro-
phyll concentration per zooxanthella cell, even when corals
experienced 4 weeks of sustained temperatures up to 7 °C
above MMM (Fine et al. 2013).
While thermotolerance has been putatively identified in
this region, experiments have not specifically been directed
to examine the physiological response of corals to
temperatures beyond the peak summer maximum follow-
ing seasonal summer warming (i.e., DHW model). It is
hypothesized that dominant GoA coral holobionts exhibit
minimal physiological changes when exposed to thermal
stress and therefore the 1–2 °C bleaching rule does not
apply to corals in the GoA. Furthermore, the GoA is typ-
ically oligotrophic and non-turbid. Very low attenuation
coefficients (K
(PAR) =0.04–0.06 m
; Stambler 2006)
together with the desert-associated cloudless skies, result in
exceptionally high irradiance on the reef flat
(*1200 lmol m
; Veal et al. 2010). The interaction
of light and thermal stress, although extremely relevant,
has seldom been investigated with corals from this region
(but see Veal et al. 2010) and is not accounted for in the
global DHW model. Stylophora pistillata was employed as
a model species. This species, considered thermally sen-
sitive in some regions (Stat et al. 2009; Sampayo et al.
2016), is a dominant and ecologically important sclerac-
tinian in the GoA. Acropora eurystoma was used as a
comparative species in a follow-up experiment since
acroporids have the greatest percentage cover on contem-
porary GoA reefs (Shaked and Genin 2014) and have also
been described as unable to recover from thermal bleaching
elsewhere such as in Okinawa (Loya et al. 2001) and the
Gulf of Thailand (Yeemin et al. 2013). The experiments
were designed to empirically test thermal and light stress
levels that have led to significant damage in corals from
other regions.
Materials and methods
Experimental system
Experiments were conducted at the Interuniversity Institute
for Marine Science (IUI) in Eilat (Gulf of Aqaba, Red Sea,
29°300N, 34°550E), Israel. Experiments were conducted
using the Red Sea Simulator (RSS) system. The system
consists of 80, 40-L experimental tanks supplied with fil-
tered (500 lM) seawater pumped from the adjacent sea.
Flow rate of seawater into the experimental tanks was 40 L
. Temperature was manipulated in each experimental
tank individually using chillers/heaters and a titanium heat
exchanger per tank. Temperature was set as a delta from
incoming reef water temperature (0.2 °C tolerance),
ensuring corals experienced natural diurnal fluctuations
and seasonal trends in temperature. Temperature was
controlled and monitored by custom-made Crystal-OPC
software (Crystal Vision, Samar, Israel) which stores real-
time data on the IUI server. A two-armed robot, equipped
with temperature (PT100, Hamilton, Switzerland), dis-
solved oxygen (VisiFerm DO Arc 120, Hamilton,
Switzerland) and pH (Polilyte Plus Arc 120, Hamilton,
Coral Reefs
Switzerland) probes on each arm, monitors every aquar-
ium. The robot completes a monitoring cycle of every
aquarium within 30 min (*1 min in each aquarium, 24/7).
The system is located outdoors. To avoid direct sunlight on
the corals, wave generator pumps break the water’s surface
and a shade cloth covers the whole facility. This results in
photosynthetically active radiation (PAR) of approximately
350 lmol quanta m
at midday at the surface.
Accumulated thermal stress
Maximum monthly mean in Eilat
To investigate how the bleaching rule relates to the GoA, S.
pistillata was exposed to different warming rates and
accumulated thermal stress levels (time of exposure to
higher than ambient seawater temperature) during the peak
seawater temperature period in the GoA. MMM was cal-
culated specifically for Eilat according to NOAA’s DHW
method, using the daily minimum sea temperature obtained
from continuous (10-min interval) recordings at the IUI
(ca. 2 m depth).
The experiment was initiated in August 2014. The
monthly mean surface water temperature at this time was
27.26 °C, the third highest since recordings began in 1988
(after August 2012: 27.62 °C, and August 2007: 27.38 °C;
methods in Fine et al. 2013). Coral fragments were pro-
duced from 12 different colonies (brown morph) growing
on the IUI nursery at 8 m depth. At this depth, adult S.
pistillata contain primarily clade A Symbiodinium (Byler
et al. 2013; Borell et al. 2016). Four days before the
experimental phase, fragments were distributed into the
RSS experimental tanks. Each temperature treatment con-
sisted of three replicate tanks containing four fragments,
each originating from known parental colonies (n=12
fragments per temperature treatment). On day zero, tem-
perature was ramped at different rates: 0, 0.3, 0.4, 0.6 or
0.7 °Cd
(Table 1). After 7 d of thermal ramping, the
maximal temperature (relative to ambient) was reached in
all treatments, namely –0.5 (control), ?2.0, ?3.0, ?4.0 and
?5.0 °C. Corals were incubated at these temperatures
(±0.5 °C) for a further 8 d (Fig. 1a).
Biological examination
Coral physiology was examined at five time points during
the experimental period: day 0 (just prior to the onset of
temperature ramping) and days 7, 10, 13 and 16. On each
sampling day, dark-adapted (20 min; Murchie and Lawson
2013) maximum quantum efficiency of photosystem II (F
) was measured on every fragment using an imaging
pulse amplitude modulated fluorometer (I-PAM, Walz
GmbH, Effeltrich, Germany). In addition, temperature-
controlled metabolic chambers (300 mL volume) were
used to measure the rate of dark respiration (Rd) followed
by net photosynthesis (Pn) for an hour each. A consistent
subset of selected fragments (n=3) from each treatment
were used at each time point. Chambers were filled with
filtered seawater (0.2 lM) and placed on a magnetic stirrer.
Light was provided by overhead fluorescent lights (Tension
Laag–Dunn, 36 W) emitting ca. 100 lmol photons
to the surface of the chamber. Oxygen concen-
tration was measured using probes connected to an OXY-4
mini (PreSens, Germany) and logged at 30-s intervals using
Presens software.
Chlorophyll concentration, total protein, zooxanthellae cell
counts and surface area
At the end of the experiment, all experimental fragments
were examined biologically as outlined in Horwitz and
Fine (2014). Briefly, after removal of the tissue, the surface
area of coral skeletons was determined using the paraffin
wax dip method of Stimson and Kinzie (1991) as modified
by Holmes (2008). The Bradford method was used to
analyze total protein content of the tissue homogenate
(Bradford 1976) with a multiscan spectrum spectropho-
tometer (595 nm, Biotek HT Synergy plate reader).
Zooxanthellae were counted using a hemocytometer (Im-
proved Neubauer). Chlorophyll was extracted in 90% (v:v)
acetone for 20 h at 4 °C before being measured spec-
trophotometrically (Ultrospec 2100 pro) according to Jef-
frey and Humphrey (1975). These data were later
normalized to total protein or surface area of each
Table 1 Experimental heating rates and total degree heating week (DHW) accumulation after one and two weeks’ incubation
Treatment (Dambient °C) Heating rate (°Cd
) Experimental temperature (°C) DHW week 1 DHW week 2
-0.5 27 0 0
?2?0.3 29 1.6 3.6
?3?0.4 30 2.4 5.4
?4?0.6 31 3.2 7.2
?5?0.7 32 4.4 9.4
Coral Reefs
Light and temperature stress interaction
When S. pistillata demonstrated high thermotolerance, A.
eurystoma, from a typically ‘‘sensitive’’ genus (Loya et al.
2001; Yeemin et al. 2013), was added in a follow-up
experiment. Since the consensus is that the mechanism of
coral bleaching involves elevated temperature in addition
to photodamage (Lesser and Farrell 2004; Lesser 2011),
but light is not a factor in the DHW model, the focus for
this experiment was the combined effect of temperature
and high light intensity.
Experimental setup
In July 2015, fragments (2–4 cm high) of S. pistillata and
A. eurystoma were sourced from the IUI coral nursery.
After 4 d of recovery, fragments were assigned to experi-
mental tanks. Three fragments from known different par-
ental colonies of each species were placed on each of three
light tiers duplicated into a total of six separate tanks (total
n=108 fragments). Light tiers were constructed from a
plastic grid covered by neutral density filters (Lee Filters,
UK) to achieve three light levels during the initial accli-
mation period: ca. 230 (high light, HL), 150 (medium light,
ML) and 80 (low light, LL) lmol photons m
the shade cloth at midday. Initial experiments indicated
short-term resilience to 3–4 °C above MMM, but that at
?5°C some signs of stress could be observed. Addition-
ally, even at the highest previous temperature ramping rate
(0.7 °Cd
) no immediate signs of physiological decline
were observed. Therefore, in half of the tanks, temperature
was increased at a higher rate of 1 °Cd
to 4 °C above
ambient and maintained for 4 weeks to imitate prolonged
thermal stress (high temperature treatment, HT; Fig. 1b).
The remaining tanks were used as the ambient control
(control temperature, CT). After 4 weeks (on day one; see
below), primary diurnal PAM measurements were taken to
assess effective quantum yield of chlorophyll fluorescence
(YII). The following day, the shade cloth over the RSS was
opened, to induce light stress [ca. 1200 (HL), 825 (ML) and
500 (LL) lmol photons m
at midday, equivalent to
1 m reef depth, 5, and 13 m, respectively; Dishon et al.
Diurnal pulse amplitude modulation fluorometry
The impact of treatment conditions on the diurnal YII was
measured on each sampling day at five times between dawn
and dusk (0600, 0900, 1200, 1500 and 1800 hrs). A single
saturation pulse was delivered to every coral fragment
under ambient light, but shaded equally to avoid sunspots
on the water’s surface and even actinic illumination
(Murchie and Lawson 2013). All fragments were assessed
within 30–40 min at each time point. Diurnal PAM mea-
surements were repeated at 3-d intervals on days 4, 7 and
10 after opening the shade cloth. Ten days has been shown
to be adequate time to induce changes in the photosynthetic
apparatus in response to new irradiances (Lesser and Shick
1989; Iglesias-Prieto and Trench 1997; Fujise et al. 2014)
and to result in measurable and significant symbiont and
host changes, e.g., in protein and chl aconcentration
(Lesser and Farrell 2004).
Fig. 1 a Schematic representation of water temperature in each
treatment during acclimation and experimental periods. The initial
tank acclimation period ran from day -3 to day 0 (23–26 August).
Temperatures were ramped until maximum experimental tempera-
tures were reached on day 7 (2 September). Temperatures were
maintained at a delta above ambient water in the control tank (circles)
until termination of the experiment on day 15 (10 September). Final
treatment temperatures were 2 °C(downward triangles), 3 °C
(squares), 4 °C(diamonds) and 5 °C(upward triangles) above
ambient. The insert displays ambient sea surface temperature (°C,
10-min interval) during the weeks surrounding and during (gray
shading) the experiment. Experimental tanks experienced the same
diurnal fluctuations. Dashed line represents 8-yr maximum monthly
mean for Eilat. bLight and temperature interaction experimental
design; shading indicates period before light intensity increase.
Asterisks indicate sampling days in both figures
Coral Reefs
Statistical analysis
Analyses of individual coral fragments were normalized
as follows before analysis: zooxanthellae cell number
protein, zooxanthellae cell number cm
area, chl azooxanthella cell
and protein cm
area. Endpoint differences between treatments were
assessed using one-way ANOVA with SigmaPlot (V. 13).
The majority (70%) of data groups (treatment 9param-
eter measured) passed the Shapiro–Wilk normality test,
normally distributed. Taken together and considering the
robustness of parametric tests, it was deemed accept-
able to use parametric ANOVAs. Changes in oxygen
evolution rate and maximal photochemical efficiency
were calculated as the change in slope of individual
treatments over time. Every data group within the oxygen
evolution analyses passed the Shapiro–Wilk normality
test. One-way ANOVAs were used to assess differences
between treatments in these slopes. In addition, the effect
of time in each individual treatment was tested using a
regression analysis. Three-way ANOVAs were used to
assess the interactions between time of day, temperature
and light level in the second experiment. Holm–Sidak
post hoc pairwise multiple comparison tests were used to
distinguish where significant interactions occurred for
each species separately. In all cases, results were accepted
as significant when pB0.05.
Accumulated thermal stress
The highest mean water temperature typically occurs in
August in the GoA. The 8-yr MMM for Eilat was 26.75 °C
(Fig. 1), and therefore, the control treatment of the thermal
stress experiment at 27.3 ±0.8 °C (mean ±standard
deviation of experimental period) is considered to be rep-
resentative of the MMM temperature for this region. The
high temperature treatments—?2.0, ?3.0, ?4.0 and
?5.0 °C—were equivalent to 3.6, 5.4, 7.2 and 9.4 DHW,
respectively, by the end of the experiment (Table 1).
ANOVAs confirmed that there were no significant initial
physiological differences (oxygen evolution or F
among fragments in different treatments at the first sam-
pling time point. There were no significant endpoint dif-
ferences among the temperature treatments in any of the
coral biological parameters (chlorophyll content, zooxan-
thellae count, total protein; one-way ANOVA, p[0.05 in
all cases; Fig. 2). Although not statistically different, the
two highest temperature treatments showed a 64% decrease
in the number of zooxanthellae cells mg
total protein,
and fewer zooxanthellae cells cm
(Fig. 2a–c), compen-
sated by a near equal increase (66%) in average chlorophyll
azooxanthella cell
. Respiration rates, however, consis-
tently increased over time in all treatments (i.e., there was a
positive slope in oxygen consumption rates normalized to
coral surface area), net photosynthesis decreased (a nega-
tive slope in net oxygen production over time), and F
generally decreased with time in all treatments. However,
the regression of these slopes was only significant in a few
cases. Net photosynthesis significantly decreased with time
at ?4°C(R
=0.94, F=43.22, p\0.01), ?5°C
=0.93, F=38.53, p\0.01), and ambient
=0.86, F=17.79, p=0.02). Respiration rate was
highest in the ?5°C treatment at all time points
(0.2 ±0.04 lmol h
). However, respiration rate in
the ?5°C treatment significantly decreased with time
=0.81, F=12.11, p=0.04) to values closer to the
other treatments indicating some degree of thermal accli-
mation. No significant differences in F
were recorded
within a treatment throughout the experiment. Typically,
treatments were not significantly different, with the
exception of significantly lower F
at ?5°C at all
sampling points (with the exclusion of the initial mea-
surement before the temperature ramping; Fig. 3).
Light and temperature stress interaction
At the end of the experiment, corals in the high temperature
treatment had accumulated 21.5 DHW, while the control
remained at 0 DHW. While there was an interaction of PAR
with effective quantum yield (DF/F
0) of chlorophyll
afluorescence (YII), there was typically a delayed response
so that highest PAR did not always coincide with lowest
YII, which often occurred mid-afternoon. As expected,
corals of both species under HL had statistically significant
lower YII than under the ML and LL treatments at every
sampling point even prior to the shade opening (Fig. 4). The
influence of the time of day was also significant in all cases
(p\0.001). Multiple comparisons tests indicated that at
0600 hrs, YII was typically significantly higher than sub-
sequent daytime measurements. There were significant
disordinal interactions between the tested parameters in
some instances. For example, recovery to dawn levels at the
end of the day was less likely in HL treatments (e.g., A.
eurystoma, HL, day 4, 0600 hrs YII significantly higher
than all other times of day) or in the initial days after the
shade opening [e.g., S. pistillata, day 4, 0600 hrs YII sig-
nificantly higher (0.45 ±0.014) than all other times of day
(0.362 ±0.016)]. Temperature did not significantly influ-
ence S. pistillata on any day, but there was a single signif-
icant interaction between temperature and time of day on
day one (CT significantly higher YII than HT at 1600 hrs,
Coral Reefs
F=3.295, p=0.017). In A. eurystoma, YII at HT was
significantly higher than CT, but only as a main effect on
day one (F=18.066, p\0.001). On days 4 and 7, the light
level significantly interacted with the effect of temperature
on A. eurystoma (day 4: F=5.387, p=0.007; day 7:
F=4.432, p=0.016); YII was only significantly higher at
HT under ML on day 4 (yield =0.524 ±0.042), and only
significant under HL and ML, but not LL on day 7.
This study investigated the physiological response of
dominant GoA branching corals to thermal and light stress
beyond peak summer water temperatures. The exposure
period of 2–6 weeks means that the results represent the
effects of acute stress events that result in a high DHW
index and are likely to induce bleaching events. In an initial
Fig. 2 Endpoint measures of coral physiological parameters (a
d) and change over experimental time in biological functioning (e,f).
Treatments on the horizontal axis represent ambient, ?2, ?3, ?4 and
?5°C, respectively. Data are mean ±standard deviation. aNumber
of zooxanthellae cells mg
protein. bpg chlorophyll azooxanthella
.cNumber of zooxanthellae cells cm
surface area. dmg total
protein cm
surface area. eChange in net photosynthesis (gray bars)
and dark respiration rate (black bars) from day 1 to day 16. fChange
in F
from day 1 to day 16
Coral Reefs
experiment, graduated treatments exposed corals to tem-
peratures 2, 3, 4 and 5 °C above MMM for 2 weeks to
relate the commonly cited 1–2 °C bleaching threshold to
this region. The experiment was initiated following a per-
iod of 14 d when daily minimum ambient water tempera-
ture was already above GoA MMM (27.1 ±0.25 °C).
Stylophora pistillata experienced the equivalent of up to
9.4 DHW; this degree of heating is predicted to result in
widespread bleaching and likely mortality (Liu et al. 2006).
However, no statistically significant effects of sustained
increased temperature up to ?3°C were observed for the
analyzed parameters and only few significant changes were
observed at ?4 and ?5°C. A total of 60 fragments were
used between five temperature treatments. Setting the
required significance value (a) to 0.05, an effect size of 0.5,
and a sample size of 60, the statistical power is high at a
value of 0.86 (G*Power software), reflecting the robustness
of the results obtained.
This result contrasts with the thermal stress response
previously observed of S. pistillata in other regions. For
example, when seawater temperatures exceeded the MMM
on the GBR in 2002, all monitored intertidal S. pistillata
colonies bleached (Stat et al. 2009). Of the ten species in
the study, S. pistillata was among the worst afflicted by
bleaching. Similarly, during the 2006 bleaching event on
Heron Island (GBR), S. pistillata was the only species
(symbiont clade C79 and C35a) of those examined to
exhibit significant bleaching (Sampayo et al. 2016). Trop-
ical corals such as those on the GBR are likely to be more
vulnerable to warming, whereas corals living in variable
temperature regimes exhibit thermotolerance (Oliver and
Palumbi 2011). Ex situ positive thermal experiments have
also been conducted with high-latitude S. pistillata from
Lord Howe Island, Australia (i.e., that naturally experience
a wide range in sea temperature). While this species
retained initial symbiont density, F
declined signifi-
cantly by 22% after just 5 d at 29 °C, 4 °C above MMM
(Pontasch et al. 2017). Under cold stress, the same authors
found that S. pistillata lost 68% of symbionts and F
decreased by 79.8% (Pontasch et al. 2017). So, while S.
pistillata on some of the world’s high-latitude reefs exhibit
improved acute thermotolerance compared to the tropics,
the tolerance of GoA corals to relatively long-term heating
(this study) still appears exceptional.
The DHW system, which predicts bleaching from
temperature stress alone as in the initial experiment here,
has been shown to match well to field observations on
Australian, tropical Atlantic, and Caribbean reefs (Liu
et al. 2003,2008; Eakin et al. 2010). However, GoA
corals did not display significant bleaching after temper-
ature stress alone, indicating that corals from this site
exhibit greater thermotolerance than the DHW model
predicts. Therefore, the DHW model should be modified
if applied to GoA corals. This conclusion is similar to a
few other studies that indicated the 1 °C bleaching
threshold does not apply to all reefs (e.g., Maina et al.
2008; Donner et al. 2009) because of regional and local
differences in temperature sensitivity. Such differences
can arise from the range in annual or daily temperature,
for example (McClanahan et al. 2007).
Fig. 3 Dark-adapted F
each sampling time point
(numbers 1–5 on the xaxis
represent experimental days 0,
7, 10, 13 and 16, respectively).
Mean F
of corals (n=12)
in each treatment is represented
at each sampling time point.
Bars (dark to light and left to
right within each group)
represent ambient, ?2, ?3, ?4
and ?5°C treatments,
respectively. Bars marked with
different letters are significantly
different from one another
within each group (one-way
ANOVA, p\0.05)
Coral Reefs
Fig. 4 Diurnal maximal photochemical yield (YII, left axis) and PAR
intensity (lmol m
,right axis) at five time points throughout the
day (0600, 0900, 1200, 1500, 1800 hrs) of control (blue) and high
temperature (red) fragments under high-light (circles), medium-light
(triangles) and low-light (squares) conditions for S. pistillata (a,c,
e) and A. eurystoma (b,d,f). Figures are chronologically ordered top
to bottom a,bday before shade opening; c,d3 d post-opening; e,f6
d post-opening; g,h9 d post-opening the shade. Actual PAR intensity
for each day displayed with solid black line
Coral Reefs
Combined thermal and light stress
Subsequently, as a result of this striking thermotolerance,
the effect of high light stress on corals from the GoA was
tested. Since typical signs of thermal stress (decreased
and net photosynthesis, increased respiration) began
to appear at ?4°C in the initial shorter-term experiment
(Figs. 2,3), corals were exposed to temperatures 4 °C
above ambient summer temperatures (ca. 31 °C) for
4 weeks before being subjected to additional light stress.
Despite this relatively long thermal stress at 4 °C above
MMM (compared to many other studies and the DHW
theory), there was little observed effect upon YII between
HT and CT treatments at the first sampling time point
(Fig. 4a, b). In fact, A. eurystoma displayed higher morning
and midday YII in the HT rather than the CT treatments.
As expected, when light stress was combined with elevated
temperature, the midday YII decreased with greatest affect
at the HL level. Midday photoinhibition with afternoon
hysteresis has been reported before in this region for S.
pistillata at 2 m depth on the reef flat (Winters et al. 2003).
However, the effect of high temperature was photosyn-
thetically stimulating under high light rather than con-
founding as indicated in that high temperature–high light
combinations displayed much less change in YII compared
to the control temperature—high-light corals (Fig. 4).
Similarly, Veal et al. (2010) reported the highest number of
zooxanthellae cells normalized to mg protein or surface
area, in addition to an ability to maintain total protein
content and chl aconcentrations at 4 °C above ambient in
S. pistillata from the GoA under high light and high tem-
perature compared to ambient conditions.
In French Polynesia, the lack of bleaching during the
anomalously high sea water temperatures of the 1998 El
˜o event was attributed to concomitant cloud cover
reducing the light stress received on the reefs (Mumby
et al. 2001). This observation can be related to the current
study in that no bleaching was observed in response to
temperature stress alone (both experiments). However, in
contrast to this study, the combination of light and tem-
perature stress is typically reported to be additive (Bha-
gooli and Hidaka 2004; Lesser and Farrell 2004). Despite
up to 6 weeks’ exposure to high temperatures (21.5 DHW),
temperature alone did not significantly alter the YII of S.
pistillata or A. eurystoma. In fact, corals incubated at the
higher temperatures outperformed those in ambient con-
ditions. This suggests that, even during summer, corals in
the GoA are currently living below rather than at optimum
temperature for photosynthesis.
An experimental design comparable to the thermal and
light stress interaction in this study is that of Lesser and
Farrell (2004). These authors tested the photophysiological
response of Montastraea faveolata collected from a reef
8 m deep in the Bahamas. Corals were abruptly exposed to
a light increase from ca. 500 to 2000 lmol m
and visibly bleached within 3–4 d. This exposure is similar
to the opening of the shade in the current experiment.
Lesser and Farrell (2004) reported that exposure to thermal
stress under high light significantly lowered early morning,
midday and end of day F
and increased daytime non-
photochemical quenching. Despite the similar rates and
magnitudes of heat and light stress, the more striking
changes in coral physiology reported by Lesser and Farrell
(2004) and the significant role of temperature are likely due
to the additive effect that temperature and light stress has
on corals from regions other than the GoA.
Thermal tolerance of GoA corals
This study emphasizes that while light stress can evoke
photosynthetic stress in GoA corals similar to other
regions, the effect of ecologically relevant temperature
alone is low. These results support the ‘‘reef refuge’
hypothesis of Fine et al. (2013) which proposes that corals
of the Red Sea are evolutionarily selected for thermal
tolerance. They also suggest that GoA corals currently live
below their thermal maximum. This notion is supported by
the conclusions of Sawall et al. (2015), who reported that
calcification rates of another Pocilloporid coral, Pocillo-
pora verrucosa, were maximal at 28–29 °C, independent of
season or latitude in the Red Sea. In addition, photo-
chemical efficiency of P. verrucosa was maximal at
26–28 °C in this region (Sawall et al. 2014) and, with
improved photochemistry and increased chlorophyll
acontent, S. pistillata from the GoA increased primary
productivity by 51% after 6 weeks at 1–2 °C above MMM
(Krueger et al. 2017). These studies that found improved
performance at temperatures above the current MMM in
the GoA imply that GoA corals may prosper with rising
SST. Furthermore, retention of thermal phenotypic plas-
ticity and the absence of local adaptation (Sawall et al.
2015) further elevate the likelihood of Red Sea corals being
resistant to warming. Whether higher temperatures stimu-
late the physiology of GoA corals or whether the lower
temperatures are actively inhibiting remains to be clarified.
The heat-tolerant symbiont, Symbiodinium ther-
mophilum from the Persian Gulf (Hume et al. 2015), is not
present in the GoA (Hume et al. 2016). In the GoA, S.
pistillata has only been found to host clade A and/or clade
CSymbiodinium throughout all life stages (Byler et al.
2013; Borell et al. 2016). These clades are typically gen-
eralists and not especially thermally tolerant (Lajeunesse
2005). However, genetically distinct corals can have wide-
ranging physiological and gene expression responses to
thermal stress even when hosting the same Symbiodinium
clade (Parkinson et al. 2015), indicating that symbiont
Coral Reefs
identity does not always confer a distinct thermal tolerance.
In addition, thermotolerance of the coral holobiont may be
afforded by host or holobiont adaptation/selection rather
than the symbiont alone in the GoA. Host and symbiont
thermal tolerance are not necessarily mutually exclusive
and together may in fact result in the observed local resi-
lience. High variability in corals’ physiological response
(reflected in a high standard deviation) further points to
genotypic differences in thermotolerance. All fragments
were of the same color morph, reef origin and (presumed)
zooxanthella clade. However, differences in host constitu-
tive gene expression (Barshis et al. 2013) or previous stress
exposure, for example, can result in inter-colony variation
in the stress response of coral conspecifics (Brown et al.
Due to its abundance on the reef, especially on the high-
light reef flat, S. pistillata is thought to be a relatively fast
colonizer of and survivor in unstable environments (Loya
1976). Acropora eurystoma also demonstrated resilience
and maintained high YII when exposed to 4 weeks of
elevated temperatures. This, together with work on addi-
tional species by Fine et al. (2013), suggests that resilience
to positive temperature anomalies is likely a generalized
trait in GoA corals. However, thermal stress impacts on
other life-history stages, and biological functions such as
reproduction and energy balance have seldom been inves-
tigated in this region and may well alter the long-term
viability of the GoA as a refuge. In the GoA in recent
decades, anthropogenic local stressors such as eutrophica-
tion from fish farming and coastal development have
caused a decline in hard coral cover and may increase
corals’ sensitivity to elevated temperature and/or reduce
local bleaching thresholds (Loya 2004). Therefore,
although GoA corals may be resilient to SST rise, local
scale impacts still require stringent management.
Acknowledgements The research was funded in part by an Israel
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Coral Reefs
... The present study examined the energetic state of Stylophora pistillata in the GoA following a 9-d incubation at moderate to extreme seawater temperature, to determine the effect on energy reserves, ATP concentration, and survival. It was hypothesized based on previous studies (Bellworthy and Fine 2017;Krueger et al. 2017) that elevation of seawater temperature by 1-3°C will not harm the energetic state of S. pistillata, while an elevation of 5-7°C will impair it, leading to bleaching and reducing the survival of corals. ...
... After acclimation, eight of the 16 tanks remained at ambient temperature, and 8 were used for temperature ramping. Of the latter, two adjacent tanks (40L, flowthrough rate = 40L h -1 ) were assigned to each treatment, and these were heated by 1°C a day, a rate that did not have physiological effects on the corals in previous studies (Bellworthy and Fine 2017). The temperature (mean ± SD) was set to ? ...
... 3°C treatment; Krueger et al. 2017), on the verge of bleaching during prolong heat stress (the ? 5°C treatment; Maor-Landaw et al. 2014;Bellworthy and Fine 2017;Grottoli et al. 2017) and the bleaching threshold of Stylophora pistillata (the ? 7°C treatment; Fine et al. 2013;Voolstra et al. 2020;Evensen et al. 2021;Savary et al. 2021 (in press)). ...
Full-text available
Coral reefs are on the brink of collapse from global warming and associated coral bleaching. Coral bleaching is the loss of algal symbionts from the coral tissue. The reduction in photosynthates produced by the symbionts makes the survival of the coral dependent on heterotrophy and stored resources, which are catabolized into available energy, i.e., Adenosine Triphosphate (ATP). The present study examined how an increase in water temperature affects energetic reserves and available ATP in the Red Sea coral Stylophora pistillata. Following a 9-d hold at 1, 3, 5 °C above ambient summer temperature (~ 26 °C), ATP levels in the coral tissue remained constant. Similarly, no significant differences in the stored energy (proteins, carbohydrates, and lipids) of the holobiont were measured. However, half of the coral nubbins in the + 7 °C treatment experienced tissue dissociation, while the remaining nubbins bleached with a 34% decline in stored energy and a decline in respiration and photosynthesis rates by 69 and 72%, respectively. The + 7 °C treated coral nubbins had 75% lower carbohydrates compared to nubbins at ambient conditions and the lowest carbohydrates to lipid and protein ratio. This study demonstrates that exceeding the high bleaching threshold of S. pistillata in the Gulf of Aqaba is associated with a catabolic response to maintain ATP levels and highlights the energetic cost of thermal stress. Understanding anabolic and catabolic processes in corals under environmental stress is key to understanding their capacity to survive future thermal stress scenarios.
... Corals from the GoA display high thermal resistance [high thermal threshold relative to their local maximum monthly mean (MMM)] in response to experimental heat stress (Bellworthy and Fine, 2017;Evensen et al., 2021;Fine et al., 2013;Savary et al., 2021;Voolstra et al., 2021) and increased primary productivity when exposed to 11 degree heating weeks (DHWs) (Krueger et al., 2017), conditions that would typically incur severe bleaching and mortality . This suggests that GoA corals live much below their upper bleaching threshold as opposed to corals in the central and southern Red Sea (Fine et al., 2013;Osman et al., 2018). ...
... adaptation) to the cooler waters of the GoA and may be subsequently losing its high thermal resistance compared to other common reefbuilding species. This finding is particularly of importance as (i) S. pistillata, widely distributed across the Indo-Pacific region (Veron, 2000), is the most abundant coral of the shallow fraction of the northern GoA (10.6% of all species between 0 and30 m deep; Kramer et al., 2020) and (ii) it is commonly considered a 'laboratory rat' (Sawall and Al-sofyani, 2015), used extensively as a model organism in laboratory experiments simulating temperature stress (Banc-Prandi and Fine, 2019;Bellworthy and Fine, 2017;Krueger et al., 2017;Savary et al., 2021;Voolstra et al., 2020 et al., 2021). We therefore question the relevance of using this species in heat stress experiments in the future to assess the thermal resistance of coral species from the Red Sea. ...
Full-text available
Rising ocean temperatures are pushing reef-building corals beyond their temperature optima (Topt), resulting in reduced physiological performances and increased risk of bleaching. Identifying refugia with thermally resistant corals and understanding their thermal adaptation strategy is therefore urgent to guide conservation actions. The Gulf of Aqaba (GoA, northern Red Sea) is considered a climate refuge, hosting corals that may originate from populations selected for thermal resistance in the warmer waters of the Gulf of Tadjoura (GoT, entrance to the Red Sea and 2000 km south of the GoA). To better understand the thermal adaptation strategy of GoA corals, we compared the temperature optima (Topt) of six common reef-building coral species from the GoA and the GoT by measuring oxygen production and consumption rates as well as photophysiological performance (i.e. chlorophyll fluorescence) in response to a short heat stress. Most species displayed similar Topt between the two locations, highlighting an exceptional continuity in their respective physiological performances across such a large latitudinal range, supporting the GoA refuge theory. Stylophora pistillata showed a significantly lower Topt in the GoA, which may suggest an ongoing population-level selection (i.e. adaptation) to the cooler waters of the GoA and subsequent loss of thermal resistance. Interestingly, all Topt were significantly above the local maximum monthly mean seawater temperatures in the GoA (27.1°C) and close or below in the GoT (30.9°C), indicating that GoA corals, unlike those in the GoT, may survive ocean warming in the next few decades. Finally, Acropora muricata and Porites lobata displayed higher photophysiological performance than most species, which may translate to dominance in local reef communities under future thermal scenarios. Overall, this study is the first to compare the Topt of common reef-building coral species over such a latitudinal range and provides insights into their thermal adaptation in the Red Sea.
... The Gulf of Aqaba (GoA), located in the northern Red Sea, has been reported to constitute a coral refuge from climate change (Fine et al., 2013), harboring corals with high thermal tolerance despite elevated warming rates (0.4 -0.5 • C per decade; Bellworthy and Fine 2017;Krueger et al., 2017). With rapid urbanization of the coastlines (Kleinhaus et al., 2020), corals from the GoA are increasingly exposed to various pollutants (Al-Taani et al., 2020), including heavy metals and Cu, with dissolved Cu concentrations ranging from 2.1 μg L − 1 in Dahab (GoA) to 5.2 μg L − 1 in El-Ain Al-Sukhna (Ali et al., 2011). ...
... Used extensively as a model organism (Sawall and Al-sofyani, 2015) for heat stress (e.g. Bellworthy and Fine, 2017;Krueger et al., 2017) and ecotoxicology studies (e.g. Banc-Prandi and Fine, 2019;Hall et al., 2018), S. pistillata from the GoA was reported to (1) withstand elevated temperatures of up to 7 • C above the local current long-term maximum monthly mean (MMM) of 27.1 • C (Krueger et al., 2017), (2) accumulate high amount of Cu compared to other species, ranging from 1.77 to 3 µg g − 1 dry weight (Ali et al., 2011), and (3) recover from prolonged Cu contamination after depuration (Banc--Prandi et al., 2021). ...
Copper (Cu) is a common marine pollutant of coastal environments and can cause severe impacts on coral organisms. To date, only a few studies assessed the effects of Cu contamination in combination with elevated seawater temperatures on corals. Furthermore, experiments focusing on coral recovery during a depuration phase, and under thermal stress, are lacking. The present study investigated the physiological response of the common and thermally tolerant scleractinian coral Stylophora pistillata from the northern Red Sea to Cu contamination (2.5, 5 or 10 µg L⁻¹) in combination with thermal stress (5°C above local ambient temperatures (26°C)) for 23 days, and assessed the impact of elevated temperatures on its ability to recover from such pollution during a one-week depuration period. Variation in coral photo-physiological biomarkers including antioxidant defense capacity, were dose, time and temperature-dependent, and revealed additive effects of elevated temperatures. Successful recovery was achieved in ambient temperature only and was mediated by antioxidant defenses. Elevation of temperature altered the recovery dynamics during depuration, causing reduced Cu bioaccumulation and photosynthetic yield. The present study provides novel information on the effects of elevated temperature on the resilience (resistance and recovery processes) of a scleractinian coral exposed to a common marine pollutant. Our findings suggest that ocean warming may alter the resilience strategies of corals when exposed to local pollution, an impact that might have long-term consequences on the chances of survival of reefs in increasingly populated and warming coastal environments.
... Counter to previous work suggesting that the extraordinary thermal tolerance from corals of the Gulf of Aqaba might equal that of southern/central Red Sea populations (Fine et al., 2013;Osman et al., 2018), we could demonstrate that while corals throughout the Red Sea harbor consistent thermal tolerance thresholds exceeding +7℃ above their regional maximum monthly mean (MMM) temperature, absolute thermal limits differed according to the prevailing MMM temperature. Although it is unclear at present how ED50-derived thermal thresholds relate to natural bleaching thresholds, our determined thermal limits correspond very well with the exceptional thermal tolerance of S. pistillata from the Gulf of Aqaba that was found to sustain temperatures of +5℃ above MMM for a period of two weeks, equivalent to 9.4 DHW (Bellworthy & Fine, 2017;Krueger et al., 2017;Savary et al., 2021). Importantly, the experimentally determined ED50 of 34.08℃ for the ICN population is 3.28℃ higher than the maximum temperature ever recorded for this site over the last decade (based on data from The Israel National Monitoring Program at the Gulf of Eilat). ...
... Transcriptional response patterns differed substantially between GoA and CRS corals with a strong response to the thermal stress in GoA corals vs. a muted/static response in CRS corals (up to 2,766 vs. up to 22 differentially expressed genes between temperature treatments in GoA and CRS corals, respectively). Notably, transcriptional differences in GoA corals were minor between the 30℃ control and the 33℃ heat stress temperature (105 DEGs), corroborating the notion that 33℃ is below the critical thermal threshold of GoA corals (Bellworthy & Fine, 2017;Evensen et al., 2021;Krueger et al., 2017). Conversely, differences were most pronounced between 30℃ and 36℃, but we also found substantial gene expression differences between 33℃ and 36℃. ...
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Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching >5℃ above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during recolonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus central Red Sea (CRS) Stylophora pistillata corals using multi-temperature acute thermal stress assays to determine thermal thresholds. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7℃ above MMM). However, absolute thermal thresholds of CRS corals were on average 3℃ above those of GoA corals. To explore the molecular underpinnings, we determined gene expression and microbiome response of the coral holobiont. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals and their symbiotic algae versus a remarkably muted response in CRS colonies. Concomitant to this, coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression (front-loading) in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed stable assemblages. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that may affect the response of coral populations to ocean warming.
... Recent research is finding positive effects of reduced light habitats (e.g., corals growing under mangrove shade) (Yates et al., 2014;Kellogg et al., 2020;Stewart et al., 2021) and other shading sources (e.g., also including turbidity, clouds and artificial shades). A number of authors suggest that such natural shading could help conserve corals under climate change scenarios (Cacciapaglia and van Woesik, 2016;Bellworthy and Fine, 2017;Coelho et al., 2017;Gonzalez-Espinosa and Donner, 2021), but the percentage cover of such natural shading only impacts a tiny fraction of coral reefs around the world. However, some other research is investigating and reporting negative effects of reduced light (e.g., turbidity) in coral reefs (Juhi et al., 2021;López-Londoño et al., 2021). ...
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The current coral reefs crisis is motivating a number of innovative projects attempting to leverage new mechanisms to avoid coral bleaching, reduce coral mortality and restore damaged reefs. Shading the reef, through seawater atomised fogging, is one tool in development to reduce levels of irradiance and temperature. To evaluate the potential viability of this concept, here we review 91 years (1930–2021) of published research looking at the effects of different levels of shade and light on coral reefs. We summarised the types of studies, places, coral species used, common responses variable measured, and types of shades used among studies. We discuss issues related to reef scale shading applicability, different methods used to measure light, standardisation methods and most importantly the positive and negative effects of shading corals.
... It is possible that the mass bleaching in MCEs of the northern Red Sea are due to their longer exposure to thermal stress (Table 1) or faster increases in temperature at depth (Fig. 2). However, our aquaria experiments and other studies have revealed multiple shallow specialist coral species with exceptional thermal tolerance under experimental conditions (Fine et al., 2013, Bellworthy and Fine, 2017, Krueger et al., 2017. ...
Climate change is degrading coral reefs around the world. Mass coral bleaching events have become more frequent in recent decades, leading to dramatic declines in coral cover. Mesophotic coral ecosystems (30-150 m depth) comprise an estimated 50-80 % of global coral reef area. The potential for these to act as refuges from climate change is unresolved. Here, we report three mesophotic-specific coral bleaching events in the northern Red Sea over the course of eight years. Over the last decade, faster temperature increases at mesophotic depths resulted in ~50 % decline in coral populations, while the adjacent shallow coral reefs remained intact. Further, community structure shifted from hard coral dominated to turf algae dominated throughout these recurrent bleaching events. Our results do not falsify the notion of the northern Red Sea as a thermal refuge for shallow coral reefs, but question the capacity of mesophotic ecosystems to act as a universal tropical refuge.
... Coral communities in the Gulf of Aqaba exhibit high temperature resistance (Krueger et al. 2017;Grattoli et al. 2017;Bellworthy and Fine 2017;Bellworthy and Fine 2021;Hammerman et al. 2021), to the point that the Gulf has been pitched as possessing the potential to become a coral refugia in the coming decades (Osman et al. 2018;Bellworthy et al. 2019; and others). Fine et al. (2013), for instance, hypothesized that the elevated heat tolerances of Gulf of Aqaba corals are the result of "selective filtering" during invasion from the Indian ocean. ...
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Coral reefs are in global decline and anomalously hot temperatures shoulder the blame. Foraminferal bioindicators are important because they record historical reef stress over periods of centuries to millennia, as compared to the few decades offered by diver surveys. For a region lacking systematic long-term reef monitoring programs, the use of bioindicators in the Red Sea is compelling. Whereas foraminfera-based indices exist to reconstruct histories of nutrient stress on reefs, there is a paucity of equivalent bioindicators that respond to temperature. Capitalizing on a portfolio of surficial sediment samples collected along the eastern margin of the N. Red Sea and Gulf of Aqaba, this study shows that the relative abundance of Amphisteginidae foraminifera—specifically Amphistegina lobifera—closely track heat stress, as has recently been reported for this family in the S. Pacific. This result is consequential for at least three reasons. First, the Red Sea hosts some of the most northerly coral reefs on Earth. Establishment of a thermal bioindicator here confirms the strategy can be deployed on high latitudes reefs, which are disproportionally afflicted with heat extremes. Second, the considered reefs, and the foraminifera they host, are famed for their thermal resilience. Foraminiferal bioindicators have not previously been trialed on reefs that have adapted in this way. Finally, as a restricted offshoot of the Indian Ocean, the level of endemism in the Red Sea is especially high. The bioindicator that we propose is apparently not compromised by endemism. Our findings advocate for an expanded deployment of Amphistegina-based reef bioindicators.
... The term 'hotspot' has frequented coral literature most often in relation to biodiversity [50,51] or thermal stress [52,53], but also in a diversity of other applications, e.g. artificial spawning hotspots [54] and coral architectural complexity hotspots [55]. ...
Reducing the global reliance on fossil fuels is essential to ensure the long-term survival of coral reefs, but until this happens, alternative tools are required to safeguard their future. One emerging tool is to locate areas where corals are surviving well despite the changing climate. Such locations include refuges, refugia, hotspots of resilience, bright spots, contemporary near-pristine reefs, and hope spots that are collectively named reef ‘safe havens' in this mini-review. Safe havens have intrinsic value for reefs through services such as environmental buffering, maintaining near-pristine reef conditions, or housing corals naturally adapted to future environmental conditions. Spatial and temporal variance in physicochemical conditions and exposure to stress however preclude certainty over the ubiquitous long-term capacity of reef safe havens to maintain protective service provision. To effectively integrate reef safe havens into proactive reef management and contingency planning for climate change scenarios, thus requires an understanding of their differences, potential values, and predispositions to stress. To this purpose, I provide a high-level review on the defining characteristics of different coral reef safe havens, how they are being utilised in proactive reef management and what risk and susceptibilities they inherently have. The mini-review concludes with an outline of the potential for reef safe haven habitats to support contingency planning of coral reefs under an uncertain future from intensifying climate change.
... In some locations, such as the Northern Red Sea (Gulf of Aqaba, GoA), mass coral bleaching was never recorded, suggesting that reefs in this region may serve as coral refugia, and may persist through climate change . Red Sea corals, such as Stylophora pistillata, appear to be living at least 5 °C below their bleaching threshold in the GoA and can resist heat exposure of 11 degree-heating weeks (DHW) compared to 4 DHW for this species in other regions, such as the Great Barrier Reef (Bellworthy & Fine, 2017;Krueger et al., 2017). Such physiological resistance to ocean warming is partly explained by evolutionary selection, as corals passed through the warmer Southern Red Sea during re-colonization from the Arabian Sea Savary et al., 2021). ...
Climate change-related increase in seawater temperature has become a leading cause of coral bleaching and mortality. However, corals from the northern Red Sea show high thermal tolerance and no recorded massive bleaching event. This specific region is frequently subjected to intense dust storms, coming from the surrounding arid deserts, which are expected to increase in frequency and intensity in the future. The aerial dust deposition supplies essential bioelements to the water column. Here, we investigated the effect of dust deposition on the physiology of a Red Sea coral, Stylophora pistillata. We measured the modifications in coral and Symbiodiniaceae metallome (cellular metal content), as well as the changes in photosynthesis and oxidative stress status of colonies exposed during few weeks to dust deposition. Our results show that 1 mg L⁻¹ of dust supplied nanomolar amounts of nitrate and other essential bioelements, such as iron, manganese, zinc, and copper, rapidly assimilated by the symbionts. At 25 °C, metal bioaccumulation enhanced the chlorophyll concentration and photosynthesis of dust-exposed corals compared to control corals. These results suggest that primary production was limited by metal availability in seawater. A 5 °C increase in seawater temperature enhanced iron assimilation in both control and dust-enriched corals. Temperature rise increased the photosynthesis of control corals only, dust-exposed ones having already reached maximal photosynthesis rates at 25 °C. Finally, we observed a combined effect of temperature and bioelement concentration on the assimilation of molybdenum, cadmium, manganese, and copper, which were in higher concentrations in symbionts of dust-exposed corals maintained at 30 °C. All together these observations highlight the importance of dust deposition in the supply of essential bioelements, such as iron, to corals and its role in sustaining coral productivity in Red Sea reefs.
... A decrease in photosynthesis and an increase in respiration are already observed when corals are exposed to PAR 250 μmol photons m −2 s −1 (Hoogenboom et al., 2012). This seems to be a consistent finding in all experiments (Bhagooli and Hidaka, 2003;Ferrier-Pagès et al., 2007;Hoogenboom et al., 2012;Hawkins et al., 2015;Bellworthy and Fine, 2017;Nakamura et al., 2017;Tilstra et al., 2017;Levy et al., 2020;Tamir et al., 2020). At higher light levels (PAR 400 to 1200 μmol photons m −2 s −1 and PAR 0 95% to 100%), chlorophyll a concentration and symbiont density decrease (Titlyanov et al., 2002;Hawkins et al., 2015;Tilstra et al., 2017) and bleaching is observed (Hoegh-Guldberg and Smith, 1989;Bhagooli and Hidaka, 2003;Hawkins et al., 2015). ...
Sometimes called the “lab rat” of coral research, Stylophora pistillata (Esper, 1797) has been extensively used in coral biology in studies ranging from reef ecology to coral metabolic processes, and has been used as a model for investigations into molecular and cellular biology. Previously thought to be a common species spanning a wide distribution through the Indo-Pacific region, “S. pistillata” is in fact four genetically distinct lineages (clades) with different evolutionary histories and geographical distributions. Here, we review the studies of stress responses of S. pistillata sensus lato (clades 1–4) and highlight research trends and knowledge gaps. We identify 126 studies on stress responses including effects of temperature, acidification, eutrophication, pollutants, and other local impacts. We find that most studies have focused on the effect of single stressors, especially increased temperature, and have neglected the combined effects of multiple stressors. Roughly 61% of studies on S. pistillata come from the northern Red Sea (clade 4), at the extreme limit of its current distribution; clades 2 and 3 are virtually unstudied. The overwhelming majority of studies were conducted in laboratory or mesocosm conditions, with field experiments constituting only 2% of studies. We also note that a variety of experimental designs and treatment conditions makes it difficult to draw general conclusions about the effects of particular stressors on S. pistillata. Given those knowledge gaps and limitations in the published research, we suggest a more standardized approach to compare responses across geographically disparate populations and more accurately anticipate responses to predicted future climate conditions.
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Coral reefs are currently experiencing substantial ecological impoverishment as a result of anthropogenic stressors, and the majority of reefs are facing immediate risk. Increasing ocean surface temperatures induce frequent coral mass bleaching events—the breakdown of the nutritional photo-symbiosis with intracellular algae (genus: Symbiodinium). Here, we report that Stylophora pistillata from a highly diverse reef in the Gulf of Aqaba showed no signs of bleaching despite spending 1.5 months at 1–2°C above their long-term summer maximum (amounting to 11 degree heating weeks) and a seawater pH of 7.8. Instead, their symbiotic dinoflagellates exhibited improved photochemistry, higher pigmentation and a doubling in net oxygen production, leading to a 51% increase in primary productivity. Nanoscale secondary ion mass spectrometry imaging revealed subtle cellular-level shifts in carbon and nitrogen metabolism under elevated temperatures, but overall host and symbiont biomass proxies were not significantly affected. Now living well below their thermal threshold in the Gulf of Aqaba, these corals have been evolutionarily selected for heat tolerance during their migration through the warm Southern Red Sea after the last ice age. This may allow them to withstand future warming for a longer period of time, provided that successful environmental conservation measures are enacted across national boundaries in the region.
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Corals at the world's southernmost coral reef of Lord Howe Island (LHI) experience large temperature and light fluctuations and need to deal with periods of cold temperature (< 18 °C), but few studies have investigated how corals are able to cope with these conditions. Our study characterized the response of key photophysiological parameters, as well as photoacclimatory and photoprotective pigments (chlorophylls, xanthophylls and β-carotene), to short-term (5-day) cold stress (~ 15 °C; 7 °C below control) in three LHI coral species hosting distinct Symbiodinium ITS2 types, and compared the coral-symbiont response to that under elevated temperature (~ 29 °C; 7 °C above control). Under cold stress, Stylophora sp. hosting Symbiodinium C118 showed the strongest effects with regards to losses of photochemical performance and symbionts. Pocillopora damicornis hosting Symbiodinium C100/C118 showed less severe bleaching responses to reduced temperature than to elevated temperature, while Porites heronensis hosting Symbiodinium C111* withstood both reduced and elevated temperature. Under cold stress, photoprotection in the form of xanthophyll de-epoxidation increased in unbleached P. heronensis (by 178%) and bleached Stylophora sp. (by 225%), while under heat stress this parameter increased in unbleached P. heronensis (by 182%) and in bleached P. damicornis (by 286%). The xanthophyll pool size was stable in all species at all temperatures. Our comparative study demonstrates high variability in the bleaching vulnerability of these coral species to low and high thermal extremes, and shows that this variability is not solely determined by the ability to activate xanthophyll de-epoxidation.
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The in hospite Symbiodinium symbiont of corals on shallow reefs relies on photoprotection and photorepair during periods of exposure to short-term high light and/or temperature stress. A coral’s susceptibility to bleaching is species specific and determined not only by Symbiodinium type, size and physiology, but also by coral host features. Here, photoprotective, photorepair, photochemical and non-photochemical efficiency parameters of Symbiodinium harboured in two morphologically different coral species were examined on Heron Island (23.4420°S, 151.9140°E) in July 2011. The two coral species were exposed to high light stress for 96 h, with or without inhibition of photosystem (PS) II repair by lincomycin. Symbiodinium harboured in Pocillopora damicornis showed an increase in xanthophyll de-epoxidation under high light exposure, whereas algal symbionts in Pavona decussata showed constant levels of xanthophyll de-epoxidation. High light-treated specimens of P. damicornis maintained steady PsbA protein (D1 protein) content throughout the experiment, but P. decussata showed a peak in PsbA protein content after 48 h of exposure. In hospite Symbiodinium in P. damicornis had greater content of PsbA protein fragments, suggesting higher accumulation of photodamaged products, compared to Symbiodinium in P. decussata, where both maintained steady PSII photochemical capacity over 96 h of exposure. Under inhibition of PSII repair, both species lost PsbA protein content and PSII photochemical capacity. Both species showed increased heat dissipation under inhibition of PSII repair, but differed in photoprotective strategies and photorepair activity. Our results suggest that, as well as any differences in the symbiont, characteristics of the coral host can alter important physiological responses in Symbiodinium.
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Scleractinian corals are prolific producers of dimethylsulphoniopropionate (DMSP), but ecophysiological mechanisms influencing cellular concentrations are uncertain. While DMSP is often proposed to function as an antioxidant, interactions between specific host–symbiont genotype associations, plasticity in DMSP concentrations and environmental conditions that can either exert or alleviate oxidative stress are unclear. We used long-term (6 months) reciprocal transplantation of Stylophora pistillata hosting two distinct symbiont phylotypes along a depth gradient, clades A (<20 m) and C (>20 m), to assess the effect of change in depth (light intensity) on DMSP concentrations in relation to symbiont genotype and photoacclimation in corals between 3 and 50 m in the Gulf of Aqaba. Bathymetric distribution of total DMSP (DMSPt) per cell varied significantly while particulate DMSP (DMSPp) appeared to be unaffected by depth. Highest DMSPt concentrations in control corals occurred at 20 m. While 3-m transplants showed a significant increase in DMSPt concentration at 20 m and became affiliated with an additional genotype (C72), 50-m transplants largely persisted with their original genotype and exhibited no significant changes in DMSPt concentrations. DMSPt concentrations in transplants at both 3 and 50 m, on the other hand, increased significantly while all corals maintained their original symbiont genotypes. Photoacclimation differed significantly with transplantation direction relative to the controls. Symbionts in 3-m transplants at 20 m exhibited no changes in chlorophyll a (chl a) concentration, cell density or cell diameter while symbiont densities decreased and chl a concentrations increased significantly at 50 m. In contrast, symbiont densities in 50-m transplants remained unaffected across depths while symbiont diameters decreased. Chl a concentrations decreased at 20 m and increased at 3 m. Our results indicate that DMSPt concentrations following changes in depth are not only a function of symbiont genotype but result from different acclimation abilities of both symbiotic partners.
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Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ∼35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only <6,000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world's warmest reefs are symbioses with a newly discovered alga,Symbiodinium thermophilum Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across >5,000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show thatS. thermophilumis a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general.
Episodes of mass coral bleaching across the world since the 1980s have led to widespread coral mortality and concern about the viability of warm water coral reef ecosystems during a period of rapid climate warming. A number of recent studies have used the output of global climate models to estimate the effects of ocean warming and, to a lesser extent, ocean acidification on future likelihood of coral bleaching and the fate of coral reef ecosystems. These studies generally conclude that mass coral bleaching could become an annual event by mid-century at many of the world’s coral reefs, without any adaptation of corals and their symbionts. The fidelity of such future projections depends on issues including model resolution, model ability to simulate modes of climate variability such as the El Niño-Southern Oscillation, and the representation of the role of past climate experience and possible means of acclimatisation and adaptation on coral susceptibility to bleaching. This chapter includes an introduction to global climate modelling, a review of the efforts to date to simulate the effects of climate change on coral bleaching, a case study on the Great Barrier Reef, and a discussion of future research needs.
New equations are presented for spectrophotometric determination of chlorophylls, based on revised extinction coefficients of chlorophylls a, b, c1 and c2. These equations may be used for determining chlorophylls a and b in higher plants and green algae, chlorophylls a and c1 + c2 in brown algae, diatoms and chrysomonads, chlorophylls a and c2 in dinoflagellates and cryptomonads, and chlorophylls a, b, and c1 + c2 in natural phytoplankton.
As climate change progresses, understanding the long-term response of corals and their endosymbionts (Symbiodinium) to prolonged environmental change is of immediate importance. Here, a total of 1152 fragments from 72 colonies of three common coral species (Stylophora pistillata, Pocillopora damicornis, Seriatopora hystrix) underwent a 32-month reciprocal depth transplantation. Genetic analysis showed that while S. hystrix maintained its generalist symbiont, some S. pistillata and P. damicornis underwent temporary changes in resident symbionts immediately after stress (transplantation; natural bleaching). These temporary changes were phylogenetically constrained to ‘host-compatible’ symbionts only and reversion to original symbionts occurred within 7 to 12 months, indicating long-term fidelity and stability of adult symbioses. Measurements of symbiont photo-physiology (dark adapted yield, pressure over photosystem II) and coral health (host protein, bleaching status, mortality) indicated a broad acclimatory capacity. However, this came at an apparent energetic expense as disproportionate mortality amongst symbioses that persisted outside their distribution range was observed following a natural bleaching event. As environmental changes due to climate change become more continuous in nature, sub-lethal effects linked to the existence near tolerance range limits coupled with the inability of adult coral colonies to change resident symbionts makes corals particularly susceptible to additional environmental fluctuations or stress events and reduces the resilience of coral populations.