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REPORT
Euphyllia paradivisa, a successful mesophotic coral in the northern
Gulf of Eilat/Aqaba, Red Sea
Gal Eyal
1,2
•Lee Eyal-Shaham
1,2
•Itay Cohen
2,3
•Raz Tamir
2,4
•Or Ben-Zvi
1
•
Frederic Sinniger
5,6
•Yossi Loya
1
Received: 27 January 2015 / Accepted: 27 October 2015
ÓSpringer-Verlag Berlin Heidelberg 2015
Abstract Mesophotic coral ecosystems (MCEs) host a
thriving community of biota that has remained virtually
unexplored. Here we report for the first time on a large
population of the endangered coral species Euphyllia
paradivisa from the MCEs of the Gulf of Eilat/Aqaba
(GOE/A), Red Sea. The mesophotic zone in some parts of
the study site harbors a specialized coral community pre-
dominantly comprising E. paradivisa (73 % of the total
coral cover), distributed from 36 to 72 m depth. Here we
sought to elucidate the strict distribution but high abun-
dance of E. paradivisa in the MCEs at the GOE/A. We
present 4 yr of observations and experiments that provide
insight into the physiological plasticity of E. paradivisa: its
low mortality rates at high light intensities, high
competitive abilities, successful symbiont adaptation to the
shallow-water environment, and tolerance to bleaching
conditions or survival during prolonged bleaching. Despite
its ability to survive under high irradiance in shallow water,
E. paradivisa is not found in the shallow reef of the GOE/
A. We suggest several factors that may explain the high
abundance and exclusivity of E. paradivisa in the MCE: its
heterotrophic capabilities; its high competition abilities; the
possibility of it finding a deep-reef refuge there from fish
predation; and its concomitant adaptation to this
environment.
Keywords Mesophotic coral ecosystems (MCEs) US
Endangered Species Act Deep-reef refugia hypothesis
(DRRH) Light Photosynthesis Photoacclimation
Introduction
Recently, as a result of 5 yr of work by the National
Oceanic and Atmospheric Administration (NOAA) fol-
lowing the petition by the Center for Biological Diversity
to list 83 reef-building corals as threatened or endangered
under the 1973 US Endangered Species Act (ESA), 20
species were listed as threatened (Fisheries NOAA 2014).
These include the species Euphyllia paradivisa Veron
(1990). Three additional Euphyllia species (E. divisa, E.
glabrescens, and E. paraancora) were reported as sensitive
to temperature changes after undergoing bleaching in the
mass bleaching event in Palau, 1998 (Bruno et al. 2001;
Fisheries NOAA 2014), but were excluded from the list for
various reasons. For example, E. paraancora has been
reported at 70 m depth offshore of Saipan, Mariana Islands
(Blyth-Skyrme et al. 2013).
Communicated by Ecology Editor Dr. Stuart A. Sandin
Electronic supplementary material The online version of this
article (doi:10.1007/s00338-015-1372-1) contains supplementary
material, which is available to authorized users.
&Gal Eyal
galeyal@mail.tau.ac.il
1
Department of Zoology, Tel-Aviv University, Tel Aviv,
Israel
2
The Interuniversity Institute for Marine Sciences of Eilat,
Eilat, Israel
3
The Institute of Earth Sciences, The Hebrew University of
Jerusalem, Jerusalem, Israel
4
Faculty of Life Sciences, Bar-Ilan University, Ramat Gan,
Israel
5
R&D Center for Submarine Resources, Japan Agency for
Marine-Earth Science and Technology, Yokosuka, Japan
6
Tropical Biosphere Research Center, University of the
Ryukyus, Nishihara, Japan
123
Coral Reefs
DOI 10.1007/s00338-015-1372-1
Mesophotic coral ecosystems (MCEs) are coral-domi-
nated communities that occur from 30 m depth to the
bottom of the photic zone (Hinderstein et al. 2010).
Although coral reefs are considered among the most
diverse ecosystems on the planet (Veron 2000), they have
been studied to date in only 50 % of the habitats that host
them. The remaining 50 % are those of the MCEs (Harris
et al. 2013). Because MCEs may represent a remarkably
large area (Riegl and Piller 2003; Locker et al. 2010; Smith
et al. 2010) and extensive coral cover (Bak et al. 2005),
they have been hypothesized to function as deep-reef
refugia from various environmental disturbances, such as
climate change (Glynn 1996; Riegl and Piller 2003), as
well as anthropogenic disturbances (Bongaerts et al. 2010;
Bridge et al. 2013). It is still unclear whether MCEs host
specialized coral communities or are merely marginal
extensions of their shallower counterparts (Kahng et al.
2014; Bongaerts et al. 2015), although there are very few
examples of connectivity between the shallow reef and
MCEs (Slattery et al. 2011; Brazeau et al. 2013; Serrano
et al. 2014).
A species’ vulnerability to extinction is assessed
according to a combination of its spatial and demographic
characteristics, threat susceptibilities, consideration of the
baseline environment, and future projections of threats
(Carpenter et al. 2008; Kahng et al. 2014; Fisheries NOAA
2014). Despite the relatively large area of MCEs in pro-
portion to the total reef area, biogeographical data on the
species that inhabit these ecosystems are profoundly lacking.
It is possible that the occupancy of potential refugia, such as
MCEs, might result in less exposure of species to surface-
derived threats (Carpenter et al. 2008). The exclusivity of E.
paradivisa to the MCE in the GOE/A raises the question of
whether this species possesses the properties of a narrow-
niche specialist (adapted to a narrow depth range) and, if so,
what are the potential limiting environmental conditions that
control its spatial distribution?
Limited distribution patterns define most coral species
(Veron 2000; Ziegler et al. 2014). A species’ distribution
can be either negatively or positively affected by abiotic
environmental variables (e.g., light regime, sedimentation
load, temperature, habitat fragmentation, carbonate satu-
ration) (Kleypas et al. 1999; Bongaerts et al. 2015) and
biotic factors (e.g., predation, competition, disease) (Bon-
gaerts et al. 2010; Bridge et al. 2013). For example, the
exponential decrease in irradiance along a depth gradient
establishes a boundary for those corals that have a lower
ability to optimize the attenuated light (Chalker et al. 1983;
Wyman et al. 1987; Falkowski et al. 1990). Thus, corals
that exhibit higher photosynthetic plasticity are more likely
to adapt better to changing light environments in time of
need (Lesser et al. 2010; Nir et al. 2011). In general, corals
have exhibited high physiological plasticity, a mechanism
whereby organisms adjust their physiology, allowing them
to acclimate to a changing environment (Brown 1997;
Gates and Edmunds 1999; Ziegler et al. 2014). However,
the limits of physiological plasticity are unknown for most
corals. The lower limit of the Symbiodinium-bearing coral
populations of MCEs is hypothesized to be determined
primarily by light, while the upper limit coincides with the
depth at which the reef community begins the transition
from shallow to deep-water fauna (Bongaerts et al. 2015).
These boundaries are location-specific and depend on
various physical and bathymetrical parameters (Kahng
et al. 2014; Bongaerts et al. 2015). Here we provide an
insight into the physiological plasticity that has allowed E.
paradivisa, previously attributed solely to the shallow reef
(Veron 1990), to expand its distribution to the MCEs of the
northern GOE/A and Okinawa (Electronic Supplementary
Material, ESM, Euphyllia description).
Following the assumption that spatial variation in the
abundance of a given species reflects the extent to which
local sites satisfy the species’ niche requirements (Brown
et al. 1995), we conducted several in situ and ex situ
experiments on survival, competition, and long-term
transplantations, in addition to examining the restriction of
E. paradivisa to the MCE in the GOE/A. Our aim was to
determine the ecological characteristics and physiological
plasticity of E. paradivisa that have led it to specialize in
the MCE of the GOE/A, and to further examine the spe-
cies’ distribution.
Materials and methods
Study site and ecological photograph survey
The ecological survey was carried out by means of
photography of random quadrats to quantify coral cover
and diversity along a depth gradient (5–50 m) (Fig. 1),
and the presence/absence of E. paradivisa was recorded
at seven locations from the shallow reef down to a depth
of 150 m. Data were evaluated from 4 d of ROV work on
the Israeli side, and more than 100 technical dives using
open-circuit SCUBA and closed-circuit rebreather on
both sides of the northern GoE/A (Fig. 1b). The in situ
photographs were taken at Dekel Beach. The distance and
orientation from the seafloor were fixed using a framer
(70 950 cm). Sixty photographs were taken along three
transects of 30 m (20 photographs per transect) at each
depth: 5, 15, 25, 35, 42, 47, and 50 m. Thirty pho-
tographs from each depth were randomly chosen for
analysis by CPCe software, using the 200 random point
sample method (Kohler and Gill 2006).
Coral Reefs
123
ab
c
Fig. 1 Study site map. aRed Sea area. bNorthern head of the Gulf of
Eilat/Aqaba; green dots represent sites/depths where Euphyllia
paradivisa was present and red dots indicate sites where E. paradivisa
was not found at depths 5–150 m. cHigh-resolution multibeam
bathymetry of Dekel Beach, where E. paradivisa was most abundant.
The yellow dots represent percent cover of E. paradivisa;numbers
represent the average percent cover of E. paradivisa at each depth
Coral Reefs
123
Downwelling irradiance and light spectral
measurements
Winter and summer spectral downwelling irradiance mea-
surements of k(Ed(k)) wavelength were conducted at
Dekel Beach using a profiling reflectance radiometer
PRR800 (Biospherical Instruments, USA) which measures
19 channels (at 300–900 nm) and the integrated PAR. The
PRR800 was deployed at midday (1100–1300 hrs) using
the free-fall technique (Waters et al. 1990) to avoid shade
or reflectance from the boat and to maintain the light sensor
in a vertical orientation. The instrument was lowered from
a boat, and its distance from the sea bed was kept constant
(*1 m) using the boat’s sonar data and the device’s depth
sensor. The data were analyzed using the PROFILER
software (Biospherical Instruments, USA).
Ex situ experiments
Coral collection, preparation, and survival rates
Six coral species—Alveopora allingi, Alveopora ocellata,
Blastomussa merleti, E. paradivisa, Galaxea fascicularis,
and Stylophora kuehlmanni—were chosen for examination
of survival under shallow-water light conditions. One of
the six, G. fascicularis, is a generalist species found in the
GOE/A along the entire depth gradient from shallow water
to the mesophotic reefs. All the other five species are
specialists, with distribution restricted to mesophotic
depths. Three to five colonies of each species were frag-
mented into 10–24 nubbins of ca. 5 cm, which were then
placed under ambient light conditions (ESM Table S1), full
spectral irradiance, and high intensity (simulating ca. 3 m
depth) in running open-circuit seawater aquaria at the
Interuniversity Institute (IUI) for Marine Sciences in Eilat
for a period of 24 months (ESM Fig. S1). Survival/mor-
tality rates were recorded every 1–3 months.
Controlled light competition experiments
The corals that best survived ambient light treatment—E.
paradivisa (strictly mesophotic) and G. fascicularis (gen-
eralist)—were chosen for competition experiments, which
were carried out under several controlled light conditions
(ESM Table S1). Euphyllia paradivisa was fragmented into
individual polyps and G. fascicularis into equivalent size
clusters (ca. 10 polyps). The corals were given 2 months of
acclimation under a blue light filter, ‘deep blue’ (Lee fil-
ters, UK), which simulates light conditions at ca. 40 m
depth, before being transferred to the experimental condi-
tions. One day before transfer to the experimental light
conditions, one nubbin of each of the two species was
glued to a microscope glass slide, 1 cm apart, to examine
the ability of the two species to coexist adjacently. The
experimental nubbins were exposed to three different
conditions, simulating different depths: an ‘ambient light’
group, which was exposed to full natural sunlight; a ‘blue
light’ group; and a ‘dark’ group, located in a darkroom
facility (ESM Fig. S2). Each of the 30 competing pairs (10
in each light treatment) was placed inside a 2-L glass
container with a separate running seawater supply. In
addition, 10 G. fascicularis fragments were placed without
competition as a control group in ‘ambient light’. Sur-
vival/mortality rates were recorded monthly. The experi-
ments lasted for 1 yr.
Zooxanthellae survival and efficiency
Symbiont photosynthetic efficiency (Fv/Fm) was measured
on E. paradivisa polyps under ambient and dark treatments
using a diving PAM (pulse amplitude modulator) fluo-
rometer (Walz, Germany). Measurements were taken in the
morning (0700–0800 hrs), prior to incubation under the
different light treatments, and thereafter at monthly inter-
vals, until 2 months after no further efficiency was detected
in the dark treatment (ESM Fig. S3, Table S2).
In situ experiments
Transplantation experimental design
The transplantation experiments were conducted at Dekel
Beach, approximately 2 km from the northern tip of the
GOE/A. In December 2013, each of 10 colonies of E.
paradivisa from 50 m depth was fragmented in situ into
four equal specimens. Each fragment contained 5–10
polyps. One quarter of each colony was replaced in its
native location, and two of the three remaining quarters
were transplanted to 10 m and 5 m depth (which are non-
native depths for E. paradivisa at the study site) on a bare
rock reef area among other corals. The fourth quarter was
used for a separate experiment (not related to the present
work). Two in situ photophysiological measurements were
taken from each fragment using a diving PAM: the first at
onset of the experiment (T
0
) and the second after 238 d,
upon its termination (T
1
).
Noninvasive photophysiological tests by PAM fluorometry
One rapid light curve (RLC) was measured per polyp in the
transplanted corals and per polyp at the site of origin using
a diving PAM (Ralph et al. 1999). Sampling took place
before noon. The PAM-RLC generates nine increasing
light steps (0, 266, 352, 505, 655, 977, 1369, 1966, and
3114 lmol photons m
-2
s
-1
) for 10 s each, followed by a
saturation pulse. The following RLC parameters were
Coral Reefs
123
calculated using R (R Development Core Team 2012), after
fitting to a nonlinear hyperbolic tangent function (Chalker
1981): I
k
, minimum saturating irradiance; a, maximum
light utilization coefficient (equivalent to initial slope of
the RLC); and rETR
max
, maximum relative electron
transport rate. rETR
max
was calculated following Ralph and
Gademann (2005) and Beer et al. (2014).
Statistical analyses
Statistical analyses were performed using R (R Develop-
ment Core Team 2012) and SigmaPlot 12 (Systat Soft-
ware). Data were checked for normality (Kolmogorov–
Smirnov test) and homogeneity of variance (Ftest) and
tested with parametric or nonparametric ANOVA, or
repeated measure ANOVA in cases of measuring the same
samples for more than two different time intervals. Cor-
relation was tested according to Pearson’s method. Post
hoc tests were done using Tukey test with Bonferroni
correction for parametric tests or Dunn’s method for non-
parametric tests. Pvalues \0.05 were considered statisti-
cally significant.
Results
Ecological and presence/absence surveys
Total percentage coral cover was maximal at 35 m depth
(Fig. 2), with high diversity (Shannon–Weaver index,
H0=2.39). Percentage cover dropped sharply at deeper
depths, with H0=1.41 at 42 m depth. In contrast,E.
paradivisa, which is absent from the shallow reef,
predominated in the MCE ([35 m), with approximately
30 % of the total available substrate cover at 42 m and
73 % of total scleractinian cover (Figs. 1c, 2). There was a
significant difference between depths in total coral cover
(one-way ANOVA, F=7.242, P\0.001) and in E.
paradivisa cover (one-way ANOVA, F=31.768,
P\0.001) (Table 1). However, no correlation was found
between depth and total cover (r=0.0847, P=0.857) or
E. paradivisa cover (r=0.724, P=0.0657). Analysis of
the presence/absence data indicated a high dispersal of E.
paradivisa in different locations of the northern GOE/A,
but limited to MCE depths only (Fig. 1b).
Downwelling irradiance and light spectral
measurements
There were seasonal differences in irradiance along the
depth gradient, with higher variation in the shallow envi-
ronment. The Euphyllia zone (Fig. 3c, d) showed intensity
of ca. 5.5 % PAR (60.2 lmol m
-2
s
-1
) at 36 m to ca.
0.5 % PAR (7.1 lmol m
-2
s
-1
) at 72 m in the winter and
approximately triple values in the summer (160.4 and
26.7 lmol m
-2
s
-1
at 36 and 72 m, respectively). The
irradiance spectrum showed similar trends of narrowing
wavelength penetration with depth and lower intensities in
the winter (Fig. 3e, f).
Ex situ experiments
The manipulative experiments were aimed at determining
the boundary of coral species in the MCE. Of the six MCE
corals that were tested under the shallow environment light
conditions, only two coral species survived: E. paradivisa,
an MCE specialist species in the GOE/A, demonstrated a
93.3 % survival rate (n=15 fragments of a polyp origi-
nating from five mother colonies), and G. fascicularis,a
generalist species in the GOE/A, exhibited an 80 % sur-
vival rate (n=15 fragments each of *10 polyps from five
mother colonies) after 24 months (Fig. 4). All other coral
species did not survive more than 12 months under such
conditions (Fig. 4). There was no significant difference
between E. paradivisa and G. fascicularis (Tukey test,
Q=1.188, P=0.958) in survival rates. However, there
were significant differences in survival rates between these
two species and the other corals (one-way repeated mea-
sures ANOVA, F=22.527, P\0.001).
Competition experiments
The second part of the study, which examined possible
competition between E. paradivisa and G. fascicularis
under different light treatments (Fig. 5), revealed complete
competitive superiority of E. paradivisa. Mortality of G.
Depth (m)
Cover (%)
0
20
40
60
80 Euphyllia paradivisa
01020304050
Fig. 2 Living coral cover along a depth gradient off Dekel Beach,
Eilat. Gray histograms represent total coral cover, and black
histograms represent Euphyllia paradivisa cover within the same
quadrats. n=30 quadrats per depth. Error bars 95 % CI of the mean
Coral Reefs
123
fascicularis fragments was constant over time (roughly
50 % per 100 d), and no significant differences were found
between the three light treatments (one-way repeated
measures ANOVA, F=0.296, P=0.752). However,
significant differences were found between the G. fascic-
ularis fragments of the control group (i.e., not in compe-
tition), with 93 % survivorship compared to the treatment
groups (Tukey, Q=3.204, P=0.037), which showed less
than 10 % survivorship, with gradual tissue degradation on
the side facing the competitor. Euphyllia paradivisa
experienced no mortality due to competition whatsoever
and exhibited extended healthy tentacles throughout the
experiment.
Zooxanthellae survival and efficiency
The third part of the study examined the efficiency of the
host’s symbiotic algae according to the photosynthetic
maximal quantum yield (Fv/Fm) of the 17–42 individual
polyp PAM measurements under ambient light and dark
conditions. The measurements continued for an additional
2 months following a light capture lower than could be
detected by the PAM instrument in the dark treatment. The
yield (Fig. 6) differed significantly between months (two-
way repeated measures ANOVA, F
Interaction
=315.007,
P\0.001). However, multiple pairwise comparisons
among different times showed no significant differences
Table 1 One-way ANOVA parameters for changes in total percentage cover of all corals and percentage cover of Euphyllia paradivisa along a
depth gradient at Dekel Beach
Source of variation DF SS MS FP
Total percentage cover between depths 6 71,779 11,963 7.242 \0.001
Euphyllia paradivisa percentage cover between depths 6 46,432 7738 31.768 \0.001
300 400 500 600 700 800
0.1
1
10
100 0 m
10 m
20 m
30 m
40 m
50 m
60 m
70 m
80 m
90 m
100 m
110 m
120 m
Winter PAR (µmol photons m-2 sec-1)
Depth (m)
Spectral irradiance
(µW cm-2 nm-1)
Wavelength (nm)
ba
Summer PAR (µmol photons m-2 sec-1)
0 m
10 m
20 m
30 m
40 m
50 m
60 m
70 m
80 m
90 m
100 m
300 400 500 600 700 800
Wavelength (nm)
0 200 400 600 800 1000 1200 1400 1600 1800
0
20
40
60
80
100
120
30
40
50
60
70 Euphyllia zone
806040200
0 200 400 600 800 1000 1200 1400 1600 1800
0
20
40
60
80
100
120
30
40
50
60
70 Euphyllia zone
200150100500
cd
ef
Fig. 3 Changes in downwelling irradiance and spectral composition
measurements along a depth gradient off Dekel Beach in winter
(November) and in summer (August). a,bPAR intensities from
surface to 120 m; gray crosses represent the actual measurements and
the black line the running median. c,dShows the values of
measurements in the Euphyllia zone (36–72 m). e,fDepth-dependent
changes in spectral irradiance every 10 m from surface to 120 m
depth
Coral Reefs
123
under ambient light treatments (ESM Table S2). A non-
significant increase in efficiency was observed at the
beginning of the treatment but by the end point, efficiency
was lower than the initial values (Fig. 6). Under the dark
treatment, the corals demonstrated a logarithmic efficiency
loss (Fig. 6) and the differences between months were
significant (ESM Table S2). There was very low mortality
of the host under both treatments (ambient and dark) during
the experiment, similar to the mortality rate in the other
experiments (Figs. 4,5).
In situ experiments
The translocation experiments were aimed at examining
the ability of E. paradivisa to photoacclimate and survive
stressful irradiance. There was strong predation activity by
fishes on the transplanted corals (ESM Table S3) but not in
their native location.
The photosynthesis parameters evaluated from RLCs at
time zero (T
0
) and after 238 d (T
1
) showed a significant
difference between times and translocated depths (two-way
ANOVA, F
Time
=12.6, F
Depth
=27.9, P\0.001). How-
ever, unlike the transplanted corals, rETR of the native
corals demonstrated a similar trend between time T
0
(winter) and T
1
(summer) at the site of origin (Fig. 7). The
transplanted corals in the shallow reef did not show any
decrease in rETR under the high light intensities of the
measurement (i.e., photoinhibition). RLC parameters, after
fitting to nonlinear hyperbolic tangent (Table 2), showed
significant differences among treatments in the slope (a)
(two-way ANOVA, F
Time
=136.41, F
Depth
=33.32,
P\0.001), minimum saturating irradiance (I
k
) (two-way
ANOVA, F
Time
,=24.32, F
Depth
=10.52, P\0.001), and
maximum rate of photosynthesis (Pmax) (two-way
ANOVA, F
Time
=8.14, F
Depth
=4.04, P\0.05).
Discussion
The scleractinian coral E. paradivisa has been listed as
threatened (Fisheries NOAA 2014), partly due to its narrow
distribution. In this study, we provide evidence of a wider
global distribution of E. paradivisa than previously
thought, as well as a wider depth distribution (ESM Eu-
phyllia distribution). We also examined possible ecological
and physiological parameters that may elucidate the strict
distribution but high abundance of this species in the MCEs
in the GOE/A. Our survey results indicate a similar pattern
to that described from Eilat by Loya (1972) (i.e., the
highest coral cover was found at 30 m depth). We further
found an acute decrease in coral diversity between 35 m
depth (H0=2.39) and 42 m depth (H0=1.41). The
dominance of E. paradivisa (73 % of the total coral cover
at 42 m depth) in reduced light conditions (at 36–72 m
depth), characterized by low coral species diversity, sug-
gests a successful adaptation process resulting in the cur-
rent demographic status of this species.
Along a depth gradient, the intensity and spectral dis-
tribution of light appear to be the most significant envi-
ronmental factors affecting corals (Achituv and Dubinsky
1990). Accordingly, high photosynthetic plasticity is
Months after onset of experiment
10 15 20 25
Survivorship (%)
0
20
40
60
80
100
50
Fig. 4 Survivorship of six mesophotic corals tested in running open-
circuit seawater aquaria for 24 months under ambient light identical
to light at 3 m depth. The corals were Euphyllia paradivisa (black
squares,n=5), Galaxea fascicularis (open triangles,n=3),
Alveopora allingi (open circles,n=3), A. ocellata (open circles,
n=5), Blastomussa merleti (black diamonds,n=5), and Stylophora
kuehlmanni (black ??,n=5). Corals were collected at 60 m depth
(see ESM Fig. S1 for experimental design)
Days after onset of experiment
0 100 200 300
Survivorship (%)
0
20
40
60
80
100
Fig. 5 Survivorship of the mesophotic coral Galaxea facicularis in
the manipulated competition experiments with Euphyllia paradivisa.
Treatments: ambient light (black circles); blue light filter (open
circles); in complete darkness (black triangles); a control group under
ambient light (i.e., without competition, open triangles) and all the E.
paradivisa competitors (black squares). n=10 pairs per treatment
(see ESM Fig. S2 for experimental design)
Coral Reefs
123
imperative for acclimation to changing light conditions.
Consequently, only highly specialized species are antici-
pated to be able to survive under an extremely low-light
environment such as that of MCEs (Kahng et al. 2014).
Shallow transplantation of low-light corals usually results
in bleaching (Baker 2001) and high mortality rates (Lang
1973; Dustan 1982; Vareschi and Fricke 1986; Yap et al.
1998; Iglesias-Prieto et al. 2004), resulting from the light
harvesting properties of the low-light-acclimated corals
(Stambler and Dubinsky 2005). However, when E.
paradivisa was exposed to full-light conditions in the
survivorship experiments (Fig. 4) it demonstrated the
highest survival rates (93.3 %) among the six mesophotic
corals tested. This survival rate was much higher than in
other in situ experiments on shallow coral species (Clark
and Edwards 1995). Such a photoacclimative response is
also known for shallow-water-dominating corals trans-
ferred to deeper water (Ziegler et al. 2014; Cohen and
Dubinsky 2015).
Many studies have monitored mortality rates following
bleaching and found major differences among species,
depths, and geographic locations (e.g., Fisk and Done
1985; Ghiold and Smith 1990; Loya et al. 2001; Stimson
et al. 2002). While tissue biomass parameters decreased in
Montastraea annularis and Agaricia lamarcki during
bleaching (Porter et al. 1989), no correlation of these
parameters to the level of bleaching was found in Mon-
tastrea franksi (Edmunds et al. 2003). This species-specific
capacity to survive bleaching was shown by Grottoli et al.
(2004) to depend on a depletion of lipid concentration,
representing energy reserves (Edmunds and Davies 1986;
Stimson 1987). Prolonged conditions of dramatically
reduced illumination, in which the respiratory demands of
the holobiont exceed the photosynthetic carbon input, can
be seen in nature during coastal development and runoff
from floods and storms. Rogers (1979) simulated such
prolonged turbidity in the water by shading a 20 m
2
reef
for 5 weeks, during which he observed bleaching and
mortality of only some coral species, and concluded that
such conditions will alter community function, particularly
at deeper depths where the light is already limiting.
n= 34 17 34 17 42 23 37 19 37 32 38 28 36 36 21 21
012345
Light Dark
6
Light Dark Light Dark Light Dark Light Dark Light Dark Light Dark
7
Light Dar
k
Fv/Fm’
Months after onset of experiment
0.0
0.2
0.4
0.6
0.8 1 1
1.05
1.03 1.04 1.04 1.02 1.01 1
0.24
0.72
0.41
0.17
0.09
00
Fig. 6 Photosynthetic quantum
yield (Fv/Fm)ofEuphyllia
paradivisa symbionts over
7 months under ambient light
and dark conditions. Open boxes
represent ambient light
treatment, and gray boxes
represent dark treatment; black
center lines show the medians;
the notches are defined as
±1.58*IQR/Hnand represent
the 95 % confidence interval for
each median; box limits indicate
the 25th and 75th percentiles;
whiskers extend to minimum
and maximum values; decimal
numbers above the boxes
represent the percentage from
time zero. n=17–42 individual
polyp measurements, as
indicated under the boxes
0 500 1000 1500 2000
0
20
40
60
80
100
T0 (n=13)
T1-50m (n=10)
T1-10m (n=13)
T1-5m (n=9)
PAR (μmol photons m-2 sec-1)
rETR (µmol e
-
m
-2
s
-1
)
Fig. 7 Relative electron transport rate (rETR) of Euphyllia paradi-
visa symbionts in situ measured by rapid light curve (RLC). Black
circles represent measurements at 50 m before transplantation (T
0
);
open circles represent native population at 50 m after 238 d (T
1
);
black triangles represent transplanted polyps at 10 m (T
1
), and white
triangles represent transplanted polyps at 5 m (T
1
). n=13, 10, 13,
and nine measurements, respectively
Coral Reefs
123
Spencer Davies (1991) estimated that under cloudy con-
ditions, lipid stores of the corals Pocillopora damicornis,
Porites lobata, and Montipora verrucosa could sustain
their normal caloric demand for 28, 71, and 114 d,
respectively. To the best of our knowledge, the year-long
survival of bleached E. paradivisa is the longest ever
reported in the literature. Stylophora pistillata, one of the
most abundant species in the shallow and deeper reef of the
Red Sea, experiences seasonal bleaching at mesophotic
depths (Nir et al. 2014), which might also impede its ability
to dominate in the MCE. After 8 d in the dark S. pistillata
fragments began to show visible bleaching, and by day 44
complete bleaching was observed (Koren et al. 2008). The
retention of zooxanthellae in E. paradivisa for a prolonged
period, with a nonlinear gradual reduction, may suggest
that it is adapted to withstand such conditions, which are
typical of MCEs. Under normal conditions hermatypic
corals release about 0.1–1 % of the algal cells to the water
daily, while about 0.5–10 % are produced (Stimson and
Kinzie 1991; Hoegh-Guldberg 1994; Titlyanov et al. 1996).
Euphyllia paradivisa thrives in the MCE as it has sev-
eral advantages over other mesophotic species, advantages
that could theoretically also apply to shallower depths: (1)
high competitive abilities—E. paradivisa proved to be
competitively superior to G. fascicularis, otherwise known
to be one of the most aggressive generalist species in the
GOE/A (Abelson and Loya 1999) (Fig. 5). This may fur-
ther explain its dominance in the area, especially as MCEs
constitute a relatively stable environment (Lesser et al.
2009; Bongaerts et al. 2010; Slattery et al. 2011); (2) high
effective quantum yield (DF/Fm0) and low minimal satu-
ration irradiance (I
k
) of its symbionts compared to other
MCE species (Lesser et al. 2010); (3) the ability to survive
without photosynthetic symbionts, as shown in the dark
treatment in the competition experiments (Fig. 5), and in
the symbiont depletion efficiency experiments (Fig. 6). In
these experiments, E. paradivisa presented a very low and
nonsignificant difference in mortality in comparison with
the corals in the ambient light treatment. The ability to
survive without symbionts may provide a species with a
competitive advantage in its own niche through hetero-
trophic predation (Hairston et al. 1960), resistance to cli-
mate change, ‘winning’ in bleaching episodes (sensu Loya
et al. 2001), and extension of its habitat to deeper envi-
ronments of the euphotic zone (Fricke and Hottinger 1983).
It has been shown that decreased autotrophy under low
light fosters heterotrophy in several coral species (Ferrier-
Pages et al. 1998; Palardy et al. 2005,2008; Lesser et al.
2010). Heterotrophic plasticity is species-specific, and
colony growth form and polyp size influence prey capture
rates (Anthony 1999; Anthony and Fabricius 2000; Palardy
et al. 2005). Thus, flexibility in carbon acquisition may be a
trait determining a species’ ecological niche and distribu-
tion range (Hoogenboom et al. 2010). The possible high
heterotrophic plasticity of E. paradivisa may enable it to be
particularly resistant to disturbance, due to its variable
ways of acquiring nutrients. For instance, during bleaching
events, increased heterotrophy significantly contributes to
stress resistance and recovery (Grottoli et al. 2006;
Rodrigues and Grottoli 2007). In contrast, several gener-
alist corals (distributed from shallow to mesophotic depths)
with small-sized polyps were shown to display low rates of
heterotrophy, with no differences, or even decreased
heterotrophy, with depth (Alamaru et al. 2009), suggesting
that this advantage is species-specific and may be corre-
lated with the relatively large polyps of E. paradivisa.
Differences in the light spectrum and irradiance along a
depth gradient (Fig. 3) resulted in a change in the photo-
synthetic performance of the transplanted E. paradivisa.
Our findings present evidence of photosynthetic symbiont
adaptation to the shallow reef light conditions through a
reduction in efficiency and an increase in I
k
(Table 2).
These photoacclimation adjustments constitute typical
mechanisms for shifting between extreme high and low
light (e.g., Chalker et al. 1983). One of the mechanisms
allowing such acclimation relies on the ability of the coral
host to change its symbionts and shift to a more suit-
able clade when conditions change (Baker 2001), although
Table 2 Rapid light curve
(RLC) parameters Treatment R
2
Slope rETR
max
SE TP I
k
SE TP
T
0
at 50 m 0.9886 0.231 101 2.56 39.49 1.76E-08 437 32.51 13.43 1.05E-05
T
1
at 50 m 0.9885 0.212 90 2.05 43.82 9.45E-09 423 28.99 14.61 6.46E-06
T
1
at 10 m 0.9921 0.154 94 1.6 58.8 1.63E-09 613 25.34 24.2 3.27E-07
T
1
at 5 m 0.9977 0.114 85 1.96 43.21 1.03E-08 745 38.19 19.51 1.18E-06
T
0
represents the RLC parameters of Euphyllia paradivisa colonies at 50 m depth (before translocation) and
T
1
the RLC parameters of the same colonies at 50 m depth upon termination of the experiment after 238 d.
T
1
at 10 and 5 m represents transplanted colonies to non-native depths. n=9–13 individual polyp mea-
surements. Parameters after fitting to a nonlinear hyperbolic tangent function: R
2
=coefficient of deter-
mination; slope =maximum light utilization coefficient (a); rETR
max
=maximum relative electron
transport rate; I
k
=minimum saturating irradiance; SE =standard error of the mean; T=statistical
tvalue and P=statistical Pvalue
Coral Reefs
123
Goulet (2006) has disputed this claim and described the
event as very rare. Iglesias-Prieto et al. (2004) demon-
strated that corals dominating shallow (Pocillopora ver-
rucosa) or deep (Pavona gigantea) reefs had very limited
capability to acclimate to the reciprocal depth even after
8 months, as they maintained their association with their
original symbiont clades. Conversely, Montastrea caver-
nosa can be found at depths between 3 and 91 m due to its
multiple symbiont clades (Lesser et al. 2010). In addition,
Ziegler et al. (2015) found that in some MCE corals,
acclimatization in nature was a function of the host-specific
symbiont physiology. Proliferation of symbionts in the
deeper corals may be due to lower C/Nratios as a result of
the high carbon influx in shallow water, and therefore
better corresponds to Redfield ratios (Dubinsky and Jokiel
1994). At irradiance greater than I
k
, more energy is trapped
by the reaction centers than is ultimately used. This may
lead to damage to components within the photosynthetic
apparatus (Kyle et al. 1984; Hoegh-Guldberg and Jones
1999). During the day, photodamage and non-photochem-
ical mechanisms further reduce quantum yield (Brown
et al. 1999; Hoegh-Guldberg and Jones 1999) in correlation
with the increasing levels of irradiance. The reduction in
Fv/Fm enables assessment of the number of functional
photosystem II (PSII) units (Schreiber 2004) and to esti-
mate the actual amount of light energy utilized during the
day. In addition, at light intensity higher than saturation (I
k
)
the number of functional PSII units does not continue to
decrease. It is also possible that the efficient light attenu-
ation of E. paradivisa symbionts to low irradiance stems
from the fact that this species in its natural habitat expe-
riences a very low irradiance of ca. 7–160 lmol photons
m
-2
s
-1
and a narrow wavelength spectrum (Fig. 3).
However, it was also calculated that some shallow corals
can absorb up to 92 % of solar irradiance, depending on
chlorophyll concentration, when acclimated to shade
(Stambler and Dubinsky 2005) and up to 95 % in corals at
30 m depth (Dustan 1982).
The saturation intensity (I
k
) measured on the mesophotic
specimens is fairly high compared to the illumination at
this depth and increases by a factor of two after transfer to
shallow water, to values much lower than the ambient
illumination at 10 m depth (Fig. 3; Table 2). When deep S.
pistillata was transferred to shallow depth, the I
k
increased
fivefold after only a few weeks (Cohen and Dubinsky
2015). This implies that the photoacclimation adjustment
of the symbionts of E. paradivisa to high light might take
much longer than in S. pistillata. It has been suggested that
corals that host more than one symbiont type acclimate to
different depths by means of a slow shift to the more
suitable symbiont (Baker 2001; Cohen and Dubinsky
2015). Since zooxanthellae remained within E. paradivisa
for much longer under dark conditions compared to those
of S. pistillata (Koren et al. 2008), it is not surprising that
its photoacclimation responses are slower. I
k
is commonly
used as a measure of the adaptation of a plant to its light
regime, and it depends on the reduction state of the primary
electron acceptor of PSII, Q
A
. Under a linear, steady-state
increase in photosynthesis, the reduction state of Q
A
increases linearly with irradiance. When Q
A
is reduced,
excitation energy at PSII is dissipated; however, in the case
of E. paradivisa, the light intensity at shallow depth was
higher than I
k
. Under such conditions, the tissues are sat-
urated with oxygen and the excess photons may lead to the
formation of reactive oxygen species in the tissues of the
host and the symbionts, which can lead to zooxanthellae
expulsion and trigger cell death (Dunn et al. 2002; Franklin
et al. 2004), which might obscure the survival of the
holobiont. The survival of most E. paradivisa specimens
under the intense light in shallow waters, and the lack of
photoinhibition as revealed by the rETR up to 3114 lmol
photons m
-2
s
-1
, should encourage further research on the
photoprotective mechanisms of this species.
Acknowledgments We would like to thank the Interuniversity
Institute for Marine Sciences for making their facilities available to
us. We are grateful to N. Paz for proofreading, Y. Shaked and O. Ben-
Shaprut for diving assistance, and all of YL’s lab members for their
support. GE was supported by the Israel Taxonomy Initiative (ITI)
and Sciences Based Management (SBM) Doctoral Fellowships. This
research was partially funded by the Israel Science Foundation (ISF)
Grant No. 341/12 and USAID/MERC Grant No. M32-037 to YL.
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