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Vol.:(0123456789)
Coral Reefs
https://doi.org/10.1007/s00338-024-02562-0
REPORT
A decade ofbenthic changes oncoral reefs intheSouthern
Persian/Arabian Gulf (2010–2020)
BernhardRieglJr1· AndrewBauman2·
JeneenHadj‑Hamou3· JohnA.Burt3
Received: 23 June 2024 / Accepted: 9 September 2024
© The Author(s), under exclusive licence to International Coral Reef Society (ICRS) 2024
Abstract In recent decades, extensive coral mortality
throughout the Persian/Arabian Gulf (PAG) from thermal
stress events has led to increasing reef degradation and
the loss of biodiversity across the region. To quantify
these dynamics, water temperatures and benthic cover
were monitored on ten reefs spanning about 350km in
the Southeastern PAG (Abu Dhabi) over a 10-year period.
Water temperatures measured on the reefs fell into cooler
(2010–2015) and warmer (2015–2020) periods. 2010–2015
had lower mean winter minimum (19°C vs. 19.56°C) and
lower mean summer maximum (35.3°C vs. 35.8°C, coral
bleaching threshold is 35.7°C). Over the decade, mass
coral bleaching occurred in seven years with four bleaching
years after 2015. Coral cover decreased by 78% while turf
and coralline algae strongly increased (66% and 154%,
respectively), and fleshy macroalgae also collapsed in cover
(− 83%). Cyanobacteria increased by 980% from 2017–20
with concurrent coral bleaching but without becoming
spatially dominant. Despite the decline in coral cover, no
shift into a macroalgae-dominated system occurred.
Keywords Persian/Arabian Gulf· Coral benthos·
Monitoring· Bleaching· Mortality· Climate change
Introduction
In many areas, reef building corals are in crisis. Climate-
driven thermal stress causes widespread mass coral
bleaching, threatening coral reefs globally (Gardner etal.
2003; Bruno and Selig 2007; Hughes etal. 2018a). At local
scales, land-use changes and other human pressures are
widespread and just as damaging (Hoegh-Guldberg etal.
2007; Carpenter etal. 2008; Hughes etal. 2018a; Riegl and
Glynn 2020; Jones and Gilliam 2024). However, different
levels of reef degradation are observed globally (Cinner
etal. 2016). High-latitude reefs were proposed as potential
refugia (Glynn 1996; Riegl and Piller 2003; Beger etal.
2014), and it is also believed that they could serve as a
springboard for coral range expansion in a warmer climate
(Precht etal. 2002; Yamano etal. 2011; Baird etal. 2012).
This highlights the importance of high-latitude reefs. While
relatively healthy in Japan, South Africa, Australia and the
Eastern Pacific (Schleyer etal. 2018; Denis etal. 2013; Abdo
etal. 2012; Glynn etal. 2018), other high-latitude reefs, for
example in the Caribbean and Persian/Arabian Gulf (PAG),
are degraded (Weil 2004; Weil and Rogers 2010; Burt etal.
2011, 2019; Riegl etal. 2018). In general, the health of
tropical reefs is better documented than that of high-latitude
reefs (Abrego etal. 2021).
Some high-latitude reefs are clearly in deep trouble. Coral
cover on high-latitude Caribbean reefs (i.e., Florida) was
decimated by bleaching, disease outbreaks and hurricanes
(Jackson etal. 2014; Lirman etal. 2014; Jones etal. 2020;
Jones and Gilliam 2024). At a similar latitude, reefs in
the Persian/Arabian Gulf (PAG) also have significantly
declined in coral health (Burt etal. 2011; 2019). Since 1996,
bleaching events have recurred with increasing frequency
and impacted reefs throughout the region (Sheppard and
Loughland 2002; Burt etal. 2008, 2019; Riegl etal. 2018).
* Bernhard Riegl Jr
riegl58@gmail.com
1 Department ofBiology, Halmos College ofArts
andSciences, Nova Southeastern University, Davie,
FL33328, USA
2 National Coral Reef Institute, Halmos College ofArts
andSciences, Nova Southeastern University, 8000 N Ocean
Drive, DaniaBeach, FL33004, USA
3 Mubadala Arabian Center forClimate andEnvironmental
Sciences (ACCESS), New York University Abu Dhabi,
AbuDhabi, UnitedArabEmirates
Coral Reefs
Coral cover, fish abundance and biomass have declined,
and changes in the algae flora may have occurred (George
and John 2005; Schils and Wilson 2006; Sheppard etal.
2010; Grandcourt 2012). Seasonal temperature variations
and greater daily fluctuations likely modify the growth
conditions for corals, microalgae and macroalgae, affecting
production efficiency (Ras etal. 2013) and community
composition (Bauman etal. 2013; Burt and Bauman 2020).
Shifts from coral dominance to communities
characterized by other benthos, most frequently algae, have
become increasingly common (Hughes etal. 2003; Gardner
etal. 2003; Hoegh-Guldberg etal. 2007; Wilkinson and
Souter 2008). In the Gulf, severe, recurrent bleaching events
have disadvantaged corals (Sheppard and Loughland 2002;
Bento etal. 2016; Riegl etal. 2018; Burt and Bauman 2020)
but the magnitude of coral decline and trajectories in other
benthic communities remains to be clearly documented.
Since temperatures in PAG are comparable to what can be
expected across the tropics (Riegl and Purkis 2012; Paparella
and Burt 2024), it is important to have a more holistic
understanding of the reaction of entire reef communities to
closely spaced heat events.
In this study, a decade-long time series of benthic
community data recording cover by corals, macro-,
turf- and coralline algae (CCA), sessile invertebrates in
ten monitoring sites within the southern Gulf (United
Arab Emirates) is presented. Using image analysis of
photoquadrats, trajectories were examined to describe:
(i) variability of benthic community composition, (ii) the
stability of reef-builders (corals and CCA) relative to algal
turfs and macroalgae through time and (iii) how these
functional groups changed with thermal stress. Relationships
between 1) temperature, and 2) benthic community cover
and composition from 2010–2020 are presented.
Methods
Monitoring sites
Ten sites were monitored across the United Arab Emirates
in the southern PAG for 10years (2010–2011, 2013–2020).
In these sites (Mukasab, Ras Ghanada, Delma, Al Dhabiya,
Saadiyat, Al Hiel, Bu Tinah, Al Saada, Al Yasat, Hawksbill,
Fig.1), temperature data and phototransects for benthic
community analysis were obtained. Not all sites were
consistently revisited every year (in 2018, only 3 sites were
visited).
Temperature data collection
Hourly seawater-bottom temperature was recorded at each
site using HOBO v2 temperature loggers, attached directly to
the reef. All loggers were set to record at one-hour intervals
until replaced. However, over the ten years, temperature
data were not recorded consistently at each location causing
data gaps at some sites. Ras Ghanada had continuous
data collection from January 2011 to December 2020. Al
Dhabiyah had similar exposure and had continuous data
collection from July 2010 to 2020. The other sites provided
additional data of variable lengths but no continuous record.
Therefore, the mean temperature across data from all
available sites at any period was used to obtain a complete
average hourly temperature time series that was relevant to
the region and to explain trends of benthic cover. While this
regional mean data resulted in a loss of granularity at local
scales, gradual and region-wide temperature trends were still
accurately represented.
Benthic community surveys
Coral reef benthic communities were surveyed at the above-
mentioned ten reefs. At each site, surveys were conducted
along six 30m line transects at 6–8m depth. Along each
transect, benthic communities were surveyed within eleven
0.25 m2 quadrats photographed at 3m placement intervals
(Bauman etal. 2013). Composition and percent cover of
benthic communities were quantified within each quadrat
using 50 randomly distributed points using CoralNet image
analysis software (Williams etal. 2019). Benthic cover
was classified into five major categories: (i) hard corals,
(ii) algal turfs (< 10mm in height), (iii) fleshy macroalgae
(> 10mm in height), (iv) coralline crustose algae (CCA),
(v) cyanobacteria, (vi) bivalves and (vii) other sessile
invertebrates. Reefs were surveyed three times per year
Fig. 1 Monitoring sites in the SE Persian/Arabian Gulf in Abu
Dhabi, United Arab Emirates. Sample sites are indicated in red; other
known reef sites are shown by empty circles (Riegl and Purkis 2012)
Coral Reefs
during winter, summer and fall, during the monitoring
period.
Data analysis
All data were analyzed using R version 4.2.2 (R Core Team
2022), variable in its base version and in the tidyverse
(Wickham and Grolemund 2017; Wickham etal. 2019)
utilizing a variety of libraries like stringr (Wickham 2023),
tidyverse (Wickham etal. 2019), ggpubr (Kassambara 2023)
and vegan (Oksanen etal. 2022).
Average hourly mean temperatures were calculated over
the entire monitoring period, from whichever site data were
available. From this dataset, absolute and annual maximum
and minimum temperatures were calculated. Since coral
bleaching thresholds in PAG are published (Riegl et al.
2011; Burt etal. 2019), bleaching periods could be analyzed.
The number of hours and days above stress and lethal
temperature levels (Riegl etal. 2011; Riegl and Purkis 2012)
were calculated.
Point count-cover data were summarized to show intra-
and inter-annual patterns. Annual data were plotted against
sampling years by generalized linear models and a trendline
(GLMs, Crawley 2014). Temperature data were evaluated
for annual and season-specific variability (averages, maxima
and minima) also for timing and frequency of bleaching
levels. When consistent differences among monitoring years
were detected, they were stratified into a warmer and cooler
period. This monitoring information provided an accurate
but static view of benthic cover changes and one of their
most important potential environmental drivers (heat) in
retrospect.
To visualize how the community had changed with time,
non-metric multidimensional scaling based on a Bray–Curtis
dissimilarity matrix (Borcard etal. 2011) plotted sample
years grouped by benthic categories as well as vice versa
within the same ordination diagram. Arrows between
the MDS axis 1 and axis 2 scores were used to illustrate
trajectory.
Results
Temperature data
Sea-bottom temperatures ranged from 17.7°C (2017) to
36.4°C (2018), giving an absolute range of 18.8°C across
the decade (Fig.2). Temperatures were strongly seasonal,
with an average annual range of 16.2°C. Two temperature
periods, 2010 (spring)—2015 and 2015 (summer)—2020,
could be separated (Fig.3). The period 2010–15 differed
from that of 2015–2020 by lower mean winter minimum
(19.0 °C vs. 19.6 °C), lower mean summer maximum
(35.3°C vs. 35.8°C) and lower annual average (28.2°C vs.
28.3°C). While not significant (t = − 1.5854, p = 0.1526 for
maxima, t = − 0.7785, p = 0.4623 for minima, t = − 0.1144,
p = 0.9142 for average), a half degree °C difference in
mean maximum temperatures can mean life or death for
the thermo-sensitive PAG benthos, especially corals, which
exists near the uppermost physiological limit of adaptability.
Corals are the most temperature sensitive of the measured
benthic community. Their PAG bleaching and mortality
threshold (35.7°C; Riegl etal. 2011) were reached in 2012
and exceeded in 2017 and 2018 (Table1), suggesting mass
coral bleaching and mortality in those years. The years
2015 and 2020 came very close to the mortality threshold.
This identifies 4years of significant coral mortality, and a
generally heat-stressed period beginning in 2015 lasting to
2020.
Variability inthebenthic community
Pair plots of data summarized by sampling years and sites
(Fig.4) suggested that clear trends existed across time and
across the sampling region. Each is further analyzed below.
Statistically significant negative correlations (calculated
as sum of squared differences) in trends among benthic
categories were observed between coral cover and
calcareous algae (R2
= − 0.409, p < 0.001), fleshy macroalgae
(R2 = − 0.281, p < 0.01), turf algae (R2
= − 0.694, p < 0.01)
and bivalves (R2 = − 0.266, p < 0.05). Further positive
Fig. 2 Mean bottom temperatures on 10 reef sites across reef sites in
the southern Persian/Arabian Gulf. Dotted red line is set at 35.7°C,
the coral mortality threshold temperature in the Persian/Arabian
Gulf. Red bars represent the approximate duration of bleaching days
in years where bleaching threshold was exceeded and mass coral
mortality encountered. Bleaching continues after the temperature
threshold is reached; therefore, the red bars extend for a variable
period after peak stress. The period is longer after more severe
heat stress. Red dot (2010, 2011) represents years where bleaching
thresholds were reached (red dotted line) but mortality was low
Coral Reefs
significant correlations existed between the cover of
calcareous algae and bivalves (R2
= 0.392, p < 0.001).
Variability acrossspace (sampling sites)
No clear pattern with regard to an East–West gradient in
mean cover data grouped by sampling site across all years
was evident (Fig.5). Data showed scatter in cover values
among the sites and years (Fig.5), as is also evidenced in
Fig.5 by the large standard deviations around the means.
The absence of pronounced patterns (W–E) suggested that
region-wide trends could be considered by pooling sites
every year.
Variability acrosstime—seasonal patterns
Algae are known to exhibit annual variability in PAG
(John 2012). Any variability in the coralline algae, coral
and bivalve data were ignored since they could only have
been based on sample placement. The slower life cycles of
Fig. 3 Annual summary statistics of sea temperatures across all
sampling sites in the southern PAG. 2010 is not shown since data
series begins in July. Cooler and hotter years (that cause biotic stress)
are readily identified by their mean (green dots) and maximum
temperatures (red dots). It is readily seen that the period from 2015 to
2020 is characterized by generally higher means and maxima
Table 1 Coral bleaching and
mortality thresholds in the Gulf
occur after 22days at 35°C,
1day at 35.7°C (Riegl etal.
2011, 2012)
**Coral mortality threshold exceeded, *coral mortality threshold reached. 2010 monitoring began in July
at the onset of the hottest period (July)
Calendar year Days ≤ 35.0°C Days ≥ 35.7°C Maximum temp Total
annual temp
variability
2010 6.9 0 35.4 14.19
2011 7.5 0 35.6 16.69
2012* 21.1 0.83 36.0 18.38
2013 0 0 34.9 16.30
2014 0 0 34.7 15.96
2015 13.08 0.75 35.9 15.59
2016 2.45 0 35.2 15.04
2017** 25.66 2.2 36.0 17.29
2018** 28.75 3.8 36.4 16.69
2019 10.50 0 35.5 14.96
2020 11.91 0.25 35.8 17.23
Coral Reefs
these organisms do not allow intra-annual cycles. Seasonal
data were pooled over all sites. Fleshy macroalgae showed
a peak in the spring season (April, May) that rapidly abated
in summer (Fig.6). Turf algae and cyanobacteria showed
a peak in late summer/autumn (September/October).
Fleshy algae peaked at 4.8% space cover and cyanobacteria
at 0.75% while the lowest values of turf algae in winter
were 27% with a peak of 60.6% in autumn. Thus, despite
wide variances, mean cover across all months of the algae
categories clearly differed (fleshy macroalgae 0.9 ± 1.6%;
turf algae 40.8 ± 11.9%; cyanobacteria 0.2 ± 0.3% mean
cover per month). Also, sessile benthic invertebrates (other
than corals and bivalves) increased in summer over the
warmer period of the year to a cover of 1.25% (mean cover
per month 0.6 ± 0.4%; Fig.6).
Benthic community variability throughtime
Variation in the composition of benthic communities on
an annual basis throughout the decade showed a pattern
of shifts in the dominant benthic taxa. Coral cover showed
a decline in 2013 in response to the bleaching year 2012,
followed by regeneration until summer 2015. After summer
2015, there was no more regeneration, until coral cover had
declined by 78% at the end of the decade. Turf algae in 2010
covered roughly equal space as corals and showed a similar
weakly declining trend until 2015. In stark contrast to corals,
they began increasing strongly over the warmer period
between 2015 and 2020, occupying much more space by the
end of the monitoring period (Table1, Fig.7C). This mirrors
intra-annual trends where turf algae have a peak during the
warmest period of the year. Macroalgae increased until 2017
and were apparently not disadvantaged by the hot summer of
2015, but then abruptly declined as of 2017 (Fig.7D) to end
up with dramatically lower cover in 2020 than in 2010 (83%
less, Table1), declining to roughly 1% of cover on the reefs
(Fig.7B). In 2017, temperatures exceeded the acceptable
threshold for macroalgae (Fig.3). Also, this mirrors the
intra-annual trends where macroalgae decline after a spring
bloom over the hotter summer period. Cyanobacteria
covered essentially 0% of the reef in 2010. While individual,
small patches of cyanobacteria were indeed encountered
on surveys, these were so small that they were missed by
the photo quadrats. From virtually zero cover (0.001%)
throughout the cooler 2010–2015 period, they expanded by
980% through the warmer period to cover about 1% (0.98%)
of the reef in 2020 (Table2, Fig.7D). While their overall
cover on reefs was not significant, their relative increases
were. Cyanobacteria also favored the summer in their intra-
annual variability, which suggests that an overall warmer
temperature regime did not harm them.
Fig. 4 Pair plot showing correlations among benthic categories.
Data are mean values in each of the 10 sampled location in each of
the 10 sampled year. The first two rows show histograms of values
across years (first row) and across sites (second row). The diagonal
shows a density plot of values in each variable. The lower triangular
section consists of pairwise scatterplots of data (row vs. column),
and the upper triangular section shows correlation coefficients.
Stars denote statistical significance level (* = 0.5, *** = 0.001),
Cy = Cyanobacteria etc.
Coral Reefs
Starting the decade with roughly 4% (3.71%) cover of
reef space, coralline algae experienced a series of increases
and decreases. They reached about 10% (9.44%) reef cover
in both 2013 and 2020. The sudden increase from ~ 4 to
~ 10% in 2013 followed a mass coral bleaching and mortality
event in that year. Some of the gained space seems to have
been subsequently lost to competition with other algae and
invertebrates. From 2015, coralline algae show consistent
increase throughout the warm period, in step with increased
space availability due to coral mortality.
The pattern of variable declines and increases in benthic
taxa influenced community structure (Fig.8). The ordination
plot of overall community structure in each sampling year
(arrangement of years based on dissimilarities in benthic
categories) showed a pattern of degradation, regeneration
and renewed further degradation. The underlying
community shift can be read from the ordination plot of the
dominant species (arrangement of benthic categories based
on dissimilarities between years). The community begins
in a setting with high coral cover. The shift away after 2012
to more coralline and turf algae dominance followed mild
bleaching in 2010 and 2011 and severe bleaching and coral
mortality in 2012 (Figs.2, 3). A regeneration trajectory
toward higher coral cover (see also Fig.7) was observed
until 2015, when another strong bleaching and mortality
event was observed (Figs.2, 3). The community moved
toward higher macroalgal cover and further away from the
original coral-dominated state (Figs.7A, D, 8). Two strong
heat events in 2017 and 2019 removed the community from
the macroalgal stage (collapse of macroalgae cover, Fig.7D)
and were characterized by bleached corals. The ongoing
coral mortality reduced coral cover (Fig.7A) and moved into
a community state characterized by the increase of bivalves
and cyanobacteria (Figs.7E, G, 8).
Discussion
There has been argument over what state will succeed that
dominated by corals on degraded reefs, and whether any
Fig. 5 The overall mean coverage values of benthic categories, pooled over all sampling years, did not show patterns along a West–East gradient
Coral Reefs
stable or unstable alternate states exist. Of particular interest
is what type of algae may dominate after coral loss (Fong
etal. 2006, 2017; Bruno etal. 2009; Johns etal. 2018; Precht
etal. 2020). The reefs of southeastern PAG serve as yet
another example, in a hitherto not so well-documented area,
demonstrating the fate of a continuously degrading coral reef
benthic community.
Over the monitored decade (2010–2020), thermal stress
events in southeastern PAG have increased in frequency
and magnitude with a concurrent shift away from coral
dominance. A warmer period (2015–2020) had 0.5 °C
higher mean, minima and maxima than the preceding years
(2010–2015). Mass coral bleaching was frequently recorded
(2010, 2011, 2012, 2017, 2019 and 2020), making it the
highest documented bleaching recurrence rate on any reef
system and identifying temperature-related bleaching and
mortality as the single most important environmental driver
of community structure on the sampled reefs. Absence of
significant regeneration caused a decline in Abu Dhabi coral
cover from 38.7% in 2010 to 8.5% in 2020. As a result, corals
are no longer the dominant benthic taxa on these reefs.
On PAG reefs, also macroalgae decreased in cover during
the study period (− 83%, Table2), unlike observed in studies
from elsewhere (tropical Eastern Pacific: Fong etal. 2006,
2017; Great Barrier Reef: Johns etal. 2018; Red Sea: Anton
etal. (2020); Caribbean: Hughes 1994; Jones etal. 2020).
Seasonal dynamics within PAG benthos align with observed
annual variability of macroalgal dynamics (John 2012), and
the present study showed a peak of macroalgae cover in
spring and early summer. However, fleshy macroalgae never
dominated the southeastern PAG reefs from 2010–2020 but
only briefly benefitted from coral death and exhibited a short
spike in cover (1.18%), then collapsing in 2017, likely due
to heat sensitivity (George and John 2005). They finally
occupied even less space by 2020 than in 2010 (0.05%
from 0.27%), and no macroalgae-dominated state was ever
observed on these reefs. This supports observations of
Bruno etal. (2009) and Precht etal. (2020) from the GBR
and the Caribbean that in the majority of reefs, shifts into
macroalgae dominance hardly occur.
At the same time, coralline algae (like Litophyton
kothschyanum), turf algae and cyanobacteria benefited from
the loss of corals as the primary space competitor, with each
gaining significant cover (+ 154%, + 66%, + 980%, Table2).
This is reminiscent of the situation in the Caribbean, where
turf algae became the most abundant benthic group in
Curacao (Vermeij etal. 2010; Fricke and Teichberg 2011).
Coralline and turf algae showed resilience to increased
temperatures and increased their coverage on the PAG
reefs, with turf algae dominating space cover (35.1–58.3%)
and coralline algae cover more than doubling in cover
(3.71–9.44%). While initially present as small tufts,
Fig. 6 Intra-annual variability of mean monthly space cover of algae, cyanobacteria and sessile invertebrates averaged across all sites between
2010 and 2020
Coral Reefs
cyanobacteria only increased during the multiyear heat
events from 2017 onwards and, although they did not cover
much space on the reefs (~ 1%), showed the most rapid
increase of any category across the entire dataset. They are
a typical crisis biota and reflect the increasing stress levels
in PAG reef ecosystems. Heat events enhance proliferation
(Ford etal. 2018; Beltram etal. 2019), as is the effect of
cyanotoxins (Ritson-Williams etal. 2016), and increased
cyanobacterial cover may be expected to cause community
shifts by reduction of coral larval survival and declines in
Fig. 7 Percent cover (mean and standard deviation) in benthic
categories pooled annually over all sites during the decade 2010–
2020. Data pooled across all sites in the southern Persian/Arabian
Gulf and dynamics in the cooler and warmer periods identified by
temperature measurements shown by trendlines obtained by glm
(generalized liner modeling). Y-axes differ in scale. Dotted lines
represent the separation of time series (2010–15 and 2015–20)
Table 2 Average cover by
benthic cover categories on
ten Abu Dhabi reefs in the SE
Persian/Arabian Gulf over the
entire investigation period
Columns show cover at the beginning of the studyin 2010 in the cooler period, in 2015 at the threshold to
the warmer period and in 2020 at the end of the warmer period
Category % cover in 2010 % cover in 2015 % cover in 2020 Total % gain/loss
Coral 38.7 37.04 8.5 − 78
Coralline Algae 3.71 4.3 9.44 + 154
Fleshy Algae 0.266 1.18 0.045 − 83
Turf Algae 35.1 33.5 58.3 + 66
Cyanobacteria 0.001 0.001 0.98 + 980
Coral Reefs
fleshy and coralline algae (Ford etal. 2018; Beltram etal.
2019; Vizon etal. 2024).
Thermal stress events are increasing in frequency and
magnitude and have driven; over only a decade, dramatic
changes in the partitioning of space cover in southern PAG
coral reef benthos (coral, algae, cyanobacteria). Coral
cover declined by ~ 75%, while turf algae cover increased
by roughly the equivalent amount. Also, macroalgae,
which initially benefited from coral decline, collapsed in
cover during the hot summer of 2017. These trajectories
suggest significant changes in ecological dynamics, as
visualized by the trajectory in multidimensional scaling
(nMDS). Starting the decade in what could be considered a
relatively “healthy” coral-dominated system (2010–2012),
the trajectory headed toward states dominated by different
algal categories (coralline, macro- and turf algae). A short
return or regeneration trajectory period toward the healthy
coral state was observed in a period spared of bleaching for
several years (2014–2015) but ultimately it turned further to
a system dominated by algae, bivalves and cyanobacteria.
Conclusion
This study suggests notable changes in the reef
environment of the southern Persian Gulf over the
decade 2010–20. In 2012 and 2015 temperatures reached
coral bleaching thresholds (35.7°C). 2017, 2018, 2020
exceeded bleaching thresholds and caused mass coral
mortality. The changes in benthic composition, especially
in coral cover, can be attributed to temperatures extremes
with increasingly high recurrence. Corals in 2010 were
roughly at ~ 40% and in 2020 ~ 8% space cover. Also, the
cover of fleshy macroalgae collapsed after the very hot
2017. Concurrently, algae categories (turf-, macro- and
calcareous-) and cyanobacteria increased in cover and
began to dominate most of the reef substrate.
Author contributions BRJr curated and analyzed data and wrote the
paper; JAB oversaw and funded data collection, manuscript preparation
and corrected manuscript; AB and JHH participated in data collections,
manuscript preparation and corrected manuscript.
Fig. 8 Ordination by non-metric multidimensional scaling (nMDS)
of a Bray–Curtis dissimilarity matrix of the benthic cover data.
Ordination of years based on composition of the benthic categories is
connected by arrows to show the community’s trajectory. Also shown
is the ordination of benthic categories based on years
Coral Reefs
Funding JAB appreciates funding by NYUAD, ACCESS and WRC.
Data availability Data available upon request.
Declarations
Conflict of interest The authors declare that they have no conflict
of interest.
Ethical approval No approval of research ethics committees was
required to accomplish the goals of this study because it is a purely
observational study.
References
Abdo DA, Bellchambers LM, Evans SN (2012) Turning up the heat:
increasing temperature and coral bleaching at the high latitude
coral reefs of the Houtman Abrolhos Islands. PLoS ONE
7(8):e43878
Abrego D, Howells EJ, Smith SD, Madin JS, Sommer B etal (2021)
Factors limiting the range extension of corals into high-latitude
reef regions. Diversity 13(12):632
Anton A, Randle JL, Garcia FC, Rossbach S, Ellis JI, Weinzierl M,
Duarte CM (2020) Differential thermal tolerance between algae
and corals may trigger proliferation of algae in coral reefs. Glob
Change Biol 26(8):4316–4327
Baird A, Sommer B, Madin J (2012) Pole-ward range expansion of
Acropora spp. along the East Coast of Australia. Coral Reefs
31:1063
Bauman AG, Feary DA, Heron SF, Pratchett MS, Burt JA (2013)
Multiple environmental factors influence the spatial distribution
and structure of reef communities in the Northeastern Arabian
Peninsula. Mar Pollut Bull 72(2):302–312
Beger M, Sommer B, Harrison PL, Smith SD, Pandolfi JM (2014)
Conserving potential coral reef refuges at high latitudes. Divers
Distrib 20(3):245–257
Beltram FL, Lamb RW, Smith F, Witman JD (2019) Rapid proliferation
and impacts of cyanobacterial mats on Galapagos rocky reefs
during the 2014–2017 El Nino Southern Oscillation. J Exp Mar
Biol Ecol 514–515:18–26
Bento R, Hoey AS, Bauman AG, Feary DA, Burt JA (2016) The
implications of recurrent disturbances within the world’s hottest
coral reefs. Mar Pollut Bull 105(2):466–472
Bernhard M., Riegl Sam J., Purkis Ashraf S., Al-Cibahy Mohammed
A., Abdel-Moati Ove, Hoegh-Guldberg (2011) Present Limits
to Heat-Adaptability in Corals and Population-Level Responses
to Climate Extremes PLoS ONE 6(9) e24802-10.1371/journal.
pone.0024802
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R.
Springer, New York, p 306
Bruno JF, Selig ER (2007) Regional decline of coral cover in the Indo-
Pacific: timing, extent, and subregional comparisons. PLoS ONE
2(8):e711
Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG (2009)
Assessing evidence of phase shifts from coral to macroalgal
dominance on coral reefs. Ecology 90(6):1478–1484
Burt JA, Bauman AG (2020) Suppressed coral settlement following
mass bleaching in the southern Persian/Arabian Gulf. Aquat
Ecosyst Health Manag 23(2):166–174
Burt J, Bartholomew A, Usseglio P (2008) Recovery of corals a decade
after a bleaching event in Dubai, United Arab Emirates. Mar Biol
154:27–36
Burt J, Al-Harthi S, Al-Cibahy A (2011) Long-term impacts of coral
bleaching events on the world’s warmest reefs. Mar Environ
Res 72(4):225–229
Burt JA, Paparella F, Al-Mansoori N etal (2019) Causes and
consequences of the 2017 coral bleaching event in the southern
Persian/Arabian Gulf. Coral Reefs 38:567–589
Carpenter KE, Abrar M, Aeby G, Aronson RB, Banks S, Bruckner
A, Chiriboga A, Cortés J, Charles Delbeek J, De Vantier L,
Edgar GJ, Edwards AJ, Fenner D, Guzmán HM, Hoeksema
BW, Hodgson G, Johan O, Licuanan WY, Livingstone SR,
Lovell ER, Moore JA, Obura DO, Ochavillo D, Polidoro BA,
Precht WF, Quibilan MC, Reboton C, Richards ZT, Rogers AD,
Sanciangco J, Sheppard A, Sheppard C, Smith J, Stuart S, Turak
E, Veron JEN, Wallace C, Weil E, Wood E (2008) One-third of
reef-building corals face elevated extinction risk from climate
change and local impacts. Science 321(5888):560–563. https://
doi. org/ 10. 1126/ scien ce. 11591 96
Cinner JE, Huchery C, MacNeil MA, Graham NA, McClanahan TR
etal (2016) Bright spots among the world’s coral reefs. Nature
535(7612):416–419
Crawley MJ (2014) Statistics: an introduction using R. John Wiley
& Sons
Denis V, Mezaki T, Tanaka K, Kuo CY, De Palmas S, Keshavmurthy
S, Chen CA (2013) Coverage, diversity, and functionality of
a high-latitude coral community (Tatsukushi, Shikoku Island,
Japan). PLoS ONE 8(1):e54330
Fong P, Smith TP, Wartian MJ (2006) Epiphytic cyanobacteria
maintain shifts to macroalagal dominance on coral reefs
following ENSO disturbances. Ecology 87:1162–1168
Fong P, Smith TB, Muthukrishnan R (2017) Algal dynamics:
alternate stable states of reefs in the eastern tropical Pacific.
In: Glynn PW, Manzello DP, Enochs IC (eds) Coral reefs of
the Eastern Tropical Pacific. Springer Netherlands, Dordrecht,
pp 339–367
Ford AK, Bejarano S, Nugues MM, Visser PM, Albert S, Ferse
SCA (2018) Reefs under Siege—the rise, putative drivers, and
consequences of benthic cyanobacterial mats. Front Mar Sci.
https:// doi. org/ 10. 3389/ fmars. 2018. 00018
Fricke A, Teichberg BK (2011) Succession patterns in algal turf
vegetation on a Caribbean coral reef. Bot Mar 54(2):111–126
Gardner TA, Coté MI, Gill JA, Grant A, Watkinson AR (2003)
Long-term region-wide declines in Caribbean corals. Science
301(5635):958–960. https:// doi. org/ 10. 1126/ scien ce. 10860 50
George JD, John DM (2005) The status of coral reefs and associated
macroalgae in Abu Dhabi (UAE) after recent coral bleaching
events. In: Abuzinada A, Joubert E, Krupp F (eds) The extent
and impact of coral bleaching in the Arabian Region. NCWCD,
Riyadh, pp 184–200
Glynn PW (1996) Coral reef bleaching: facts, hypotheses and
implications. Glob Change Biol 2(6):495–509
Glynn PW, Feingold JS, Baker AB, Banks S etal (2018) Status of
corals and coral reefs of the Galapagos Islands (Ecuador): past,
present, and future. Mar Pollut Bull 133:717–733
Grandcourt E (2012) Reef fish and fisheries in the Gulf. In: Riegl BM,
Purkis SJ (eds) Coral reefs of the Gulf: adaptation to climatic
extremes. Springer Netherlands, Dordrecht, pp 127–161
Hoegh-Guldberg O etal (2007) Coral reefs under rapid climate change
and ocean acidification. Science 318(5857):1737–1742
Hughes TP (1994) Catastrophes, phase shifts, and large-
scale degradation of a Caribbean coral reef. Science
265(5178):1547–1551
Hughes TP (2003) Climate change, human impacts, and the
resilience of coral reefs. Science 301(5635):929–933
Coral Reefs
Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A,
Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G,
McWilliam MJ (2018a) Global warming transforms coral reef
assemblages. Nature 556:492–496. https:// doi. org/ 10. 1038/
s41586- 018- 0041-2
Jackson J, Donovan M, Cramer K, Lam V (2014) Status and trends of
Caribbean coral reefs: 1970–2012. Gland, Switzerland: Global
Coral Reef Monitoring Network; International Union for the
Conservation of Nature (IUCN)
John DM (2012) Marine algae (Seaweeds) associated with coral reefs
in the Gulf. In: Riegl BM, Purkis SJ (eds) Coral reefs of the Gulf:
adaptation to climatic extremes. Springer, New York-Heidelberg,
pp 309–335
Johns KA, Emslie MJ, Hoey AS, Osborne K, Jonker MJ, Cheal AJ
(2018) Macroalgal feedbacks and substrate properties maintain
a coral reef regime shift. Ecosphere 9(7):e02349. https:// doi. org/
10. 1002/ ecs2. 2349
Jones NP, Gilliam DS (2024) Temperature and local anthropogenic
pressures limit stony coral assemblage viability in Southeast
Florida. Mar Pollut Bull 200:116098
Jones NP, Figueiredo J, Gilliam DS (2020) Thermal stress-related
spatiotemporal variations in high-latitude coral reef benthic
communities. Coral Reef 39:1661–1673
Kassambara A (2023) _ggpubr: ‘ggplot2’ Based Publication Ready
Plots_. R package version 0.6.0,<https:// CRAN.R- proje ct. org/
packa ge= ggpubr>
Lirman D, Formel N, Schopmeyer S, Ault JS, Smith SG etal (2014)
Percent recent mortality (PRM) of stony corals as an ecological
indicator of coral reef condition. Ecol Ind 44:120–127
Oksanen J, Simpson G, Blanchet F, Kindt R, Legendre P, etal. (2022)
_vegan: Community Ecology Package_. R package version 2.6–4,
https:// CRAN.R- proje ct. org/ packa ge= vegan
Paparella F, Burt JA (2024) Climate of the United Arab Emirates:
present, past and impacts on life. In: Burt JA (ed) A natural history
of the Emirates. Springer Nature Switzerland, Cham, pp 65–94
Precht W, Bruckner A, Aronson R etal (2002) Endangered Acroporid
corals of the Caribbean. Coral Reefs 21:41–42
Precht WF, Aronson RB, Gardner TA, Gill JA, Hawkins JP,
Hernández–Delgado EA, Côté IM (2020) Population Dynamics
of the Reef Crisis. The timing and causality of ecological shifts
on Caribbean reefs. Elsevier 331–360
R Core Team (2022). R: A language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna,
Austria
Ras M, Steyer J-P, Olivier B (2013) Temperature effect on
microalgae: a crucial factor for outdoor production. Rev Environ
Sci Bio/Technol 12(2):153–164
Riegl BM, Glynn PW (2020) Population dynamics of the reef crisis:
consequences of the growing human population. Adv Mar Biol
87:2–30
Riegl B, Piller WE (2003) Possible refugia for reefs in times of
environmental stress. Int J Earth Sci 92(4):520–531
Riegl BM, Purkis SJ, Al-Cibahy AS, Al-Harthi S, Grandcourt
E, Al-Sulaiti K, Baldwin J, Abdel-Moati AM (2012) Coral
bleaching and mortality thresholds in the SE Gulf: highest in
the world. In: Riegl BM, Purkis SM (eds) Coral reefs of the
Gulf: adaptation to climatic extremes. Springer, New York-
Heidelberg, pp 95–105
Riegl BM, Johnston M, Purkis S, Howells E, Burt J, Steiner SC,
Sheppard CR, Bauman A (2018) Population collapse dynamics
in Acropora downingi, an Arabian/Persian Gulf ecosystem-
engineering coral, linked to rising temperature. Glob Change
Biol 24(6):2447–2462
Riegl BM, Purkis SJ (2012) Coral reefs of the Gulf: adaptation to
climatic extremes in the world’s hottest sea. In: Riegl BM,
Purkis SJ (eds) Coral reefs of the Gulf: adaptation to climatic
extremes. Springer Netherlands, Dordrecht, pp 1–4
Ritson-Williams R, Ross C, Paul VJ, Fabricius K, Negri A, Hoegh-
Guldberg O (2016) Elevated temperature and allelopathy impact
coral recruitment. PLoS ONE 11:e0166581. https:// doi. org/ 10.
1371/ journ al. pone. 01665 81
Schils T, Wilson SC (2006) Temperature threshold as a
biogeographic barrier in Northern Indian Ocean macroalgae 1.
J Phycol 42(4):749–756
Schleyer MH, Floros C, Laing SC, Macdonald AH, Montoya-Maya
PH etal (2018) What can South African reefs tell us about
the future of high-latitude coral systems? Mar Pollut Bull
136:491–507
Sheppard CRC, Loughland R (2002) Coral mortality and recovery in
response to increasing temperature in the Southern Arabian Gulf.
Aquat Ecosyst Health Manag 5(4):395–402
Sheppard CRC, Al-Husiani M, Al-Jamali F, Al-Yamani F, Baldwin
R, Bishop J, Benzoni F, Dutrieux E, Dulvy NK, Durvasula SR,
Jones DA (2010) The Gulf : a young sea in decline. Mar Pollut
Bull 60:13–38
Vermeij MJ, van Moorselaar I, Engelhard S, Hörnlein C, Vonk
SM, Visser PM (2010) The effects of nutrient enrichment and
herbivore abundance on the ability of turf algae to overgrow coral
in the Caribbean. PLoS ONE 5(12):e14312
Vizon C, Urbanowiez A, Raviglione D, Bonnard I, Nugues MM (2024)
Benthic cyanobacterial metabolites interact to reduce coral larval
survival and settlement. Harmful Algae 132:102582
Weil E (2004) Coral reef diseases in the wider Caribbean. In:
Rosenberg E (ed) Coral health and disease. Springer, Berlin
Heidelberg, pp 35–68
Weil E, Rogers CS (2010) Coral reef diseases in the Atlantic-
Caribbean. Coral reefs: an ecosystem in transition. Springer,
Dordrecht, pp 465–491
Wickham H (2023) stringr: Simple, Consistent Wrappers for Common
String Operations_. R package version 1.5.1
Wickham R, Grolemund G (2017) R for data science. O’Reilly,
Sebastopol, pp 492
Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R,
Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen
T, Miller E, Bache S, Müller K, Ooms J, Robinson D, Seidel D,
Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H
(2019) Welcome to the tidyverse. J Open Sour Softw 4(43):1686.
https:// doi. org/ 10. 21105/ joss. 01686
Wilkinson CR, Souter D (2008) Status of Caribbean coral reefs after
bleaching and hurricanes in 2005. Global Coral Reef Monitoring
Network, Reef and Rainforest Research Centre, Townsville, pp
150
Williams ID, Couch CS, Beijbom O, Oliver TA, Vargas-Angel B,
Schumacher BD, Brainard RE (2019) Leveraging automated
image analysis tools to transform our capacity to assess status
and trends of coral reefs. Front Mar Sci. https:// doi. org/ 10. 3389/
fmars. 2019. 00222
Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range
expansion of tropical reef corals in response to rising sea surface
temperatures. Geophys Res Lett 38:4
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