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Mesophotic reef corals remain largely unexplored in terms of the genetic adaptations and physiological mechanisms to acquire, allocate, and use energy for survival and reproduction. In the Hawaiian Archipelago, the Leptoseris species complex form the most spatially extensive mesophotic coral ecosystem known and provide habitat for a unique community. To study how the ecophysiology of Leptoseris species relates to symbiont–host specialization and understand the mechanisms responsible for coral energy acquisition in extreme low light environments, we examined Symbiodinium (endosymbiotic dinoflagellate) photobiological characteristics and the lipids and isotopic signatures from Symbiodinium and coral hosts over a depth‐dependent light gradient (55–7 μmol photons m−2 s−1, 60–132 m). Clear performance differences demonstrate different photoadaptation and photoacclimatization across this genus. Our results also show that flexibility in photoacclimatization depends primarily on Symbiodinium type. Colonies harboring Symbiodinium sp. COI‐2 showed significant increases in photosynthetic pigment content with increasing depth, whereas colonies harboring Symbiodinium spp. COI‐1 and COI‐3 showed variability in pigment composition, yield measurements for photosystem II, as well as size and density of Symbiodinium cells. Despite remarkable differences in photosynthetic adaptive strategies, there were no significant differences among lipids of Leptoseris species with depth. Finally, isotopic signatures of both host and Symbiodinium changed with depth, indicating that coral colonies acquired energy from different sources depending on depth. This study highlights the complexity in physiological adaptations within this symbiosis and the different strategies used by closely related mesophotic species to diversify energy acquisition and to successfully establish and compete in extreme light‐limited environments.
Content may be subject to copyright.
Limnol. Oceanogr. 00, 2019, 116
© 2019 The Authors. Limnology and Oceanography published by Wiley Periodicals, Inc. on
behalf of Association for the Sciences of Limnology and Oceanography.
doi: 10.1002/lno.11164
Ecophysiology of mesophotic reef-building corals in Hawaiiis
inuenced by symbionthost associations, photoacclimatization, trophic
plasticity, and adaptation
Jacqueline L. Padilla-Gamiño ,
1
*Melissa S. Roth,
2
Lisa J. Rodrigues,
3
Christina J. Bradley,
4
Robert R. Bidigare,
5
Ruth D. Gates,
5
Celia M. Smith,
6
Heather L. Spalding
6
1
School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington
2
Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California
3
Department of Geography and the Environment, Villanova University, Villanova, Pennsylvania
4
Department of Biological Sciences, Salisbury University, Salisbury, Maryland
5
Hawaii Institute of Marine Biology, University of Hawaii, K
aneohe, Hawaii
6
Department of Biology, College of Charleston, Charleston, South Carolina
Abstract
Mesophotic reef corals remain largely unexplored in terms of the genetic adaptations and physiological
mechanisms to acquire, allocate, and use energy for survival and reproduction. In the Hawaiian Archipelago,
the Leptoseris species complex form the most spatially extensive mesophotic coral ecosystem known and provide
habitat for a unique community. To study how the ecophysiology of Leptoseris species relates to symbionthost
specialization and understand the mechanisms responsible for coral energy acquisition in extreme low light
environments, we examined Symbiodinium (endosymbiotic dinoagellate) photobiological characteristics and
the lipids and isotopic signatures from Symbiodinium and coral hosts over a depth-dependent light gradient
(557μmol photons m
2
s
1
,60132 m). Clear performance differences demonstrate different photoadaptation
and photoacclimatization across this genus. Our results also show that exibility in photoacclimatization
depends primarily on Symbiodinium type. Colonies harboring Symbiodinium sp. COI-2 showed signicant
increases in photosynthetic pigment content with increasing depth, whereas colonies harboring Symbiodinium
spp. COI-1 and COI-3 showed variability in pigment composition, yield measurements for photosystem II, as
well as size and density of Symbiodinium cells. Despite remarkable differences in photosynthetic adaptive strate-
gies, there were no signicant differences among lipids of Leptoseris species with depth. Finally, isotopic signa-
tures of both host and Symbiodinium changed with depth, indicating that coral colonies acquired energy from
different sources depending on depth. This study highlights the complexity in physiological adaptations within
this symbiosis and the different strategies used by closely related mesophotic species to diversify energy acquisi-
tion and to successfully establish and compete in extreme light-limited environments.
Light availability is a crucial factor affecting the physiology,
productivity, distribution, and abundance of life in the ocean
(Gattuso et al. 2006; Falkowski and Raven 2007). Both quan-
tity and quality (spectral composition) of photosynthetically
active radiation (PAR) can inuence the recruitment, physio-
logical performance, and survival of different life stages of
marine organisms (Mundy and Babcock 1998; Falkowski and
Raven 2007; Roth 2014). As depth increases, light intensity not
only decreases exponentially but also ultraviolet and red wave-
lengths decrease faster causing a spectral enrichment in the
blue and bluegreen wavelengths (Kirk 2011). Scleractinian
corals are ecologically and economically important organisms
that live in a mutualistic symbiosis with intracellular algae
(dinoagellates of the genus Symbiodinium) and depend on PAR
to obtain energy for photosynthesis. Symbiodinium translocate
xed carbon to their coral host to meet their hosts metabolic
demands as well as contribute to coral growth and calcication
(Goreau and Goreau 1959; Muscatine 1990). Most symbiotic
*Correspondence: jpgamino@uw.edu
This is an open access article under the terms of the Creative Commons
Attribution License, which permits use, distribution and reproduction in
any medium, provided the original work is properly cited.
Additional Supporting Information may be found in the online version of
this article.
This manuscript is dedicated to the memory of our dearest Ruth Gates, an
incredible scientist, mentor, and friend. We deeply miss you.
1
corals cannot photosynthesize and survive at depths greater
than 60 m as PAR availability is limited in spectral features and
quantity (Fricke et al. 1987; Lesser et al. 2009; Loya et al. 2016).
However, some species persist and even ourish in dimly lit envi-
ronments such as the mesophotic zone, where downwelling irra-
diance can be as low as 1% of surface irradiance (Kahng and
Kelley 2007; Lesser et al. 2009; Bridge et al. 2011; Pyle et al.
2016). Mesophotic coral ecosystems, as currently dened, are
deep fore-reef communities comprised largely of light-dependent
zooxanthellate corals, azoxanthellate scleractinian corals, macro-
algae as well as sponges from 30 m to over 150 m depths (Lesser
et al. 2009; Hinderstein et al. 2010; Baker and Harris 2016). Upper
mesophotic coral reefs inhabit depths from 30 to 60 m, whereas
lower mesophotic reefs are present from 60 to 150 m depths. To
date, mesophotic reef corals remain largely unexplored in terms
of the physiological adaptations and mechanisms that allow resi-
dent species to live and successfully reproduce in these environ-
ments (Lesser et al. 2010; Shlesinger et al. 2018). However, it is
important to study mesophotic reefs because of the fundamen-
tally new scientic insights these environments can provide and
their potential to serve as refuges and nursery habitats for many
ecologically and commercially important species (Riegl and Piller
2003; Lesser et al. 2009; Bongaerts et al. 2010; Bryan et al. 2013;
Holstein et al. 2016).
Light-dependent corals are important members of the meso-
photic community (Lesser et al. 2009). Leptoseris is a common
obligate zooxanthellate genus found in mesophotic environ-
ments around the world including the Pacic Ocean, Red Sea,
and the Caribbean Sea (Bouchon 1981; Fricke and Knauer 1986;
Maragos and Jokiel 1986; Kahng and Maragos 2006; Ziegler et al.
2015). The deepest reported zooxanthellate species is Leptoseris
hawaiiensis, which has been found as deep as 165 m depth at
Johnston Atoll (Maragos and Jokiel 1986).
One of the most studied corals from the deep mesophotic zone
is Leptoseris fragilis from the Red Sea. This species lives exclusively
between 40 and 145 m depths (1541.2 μmol photons m
2
s
1
;
Fricke and Schuhmacher 1983; Fricke et al. 1987) and its success
in the mesophotic zone has been attributed to its photo-
physiological exibility, efcient use of low photon ux densities,
and ability to switch between photoautotrophy and heterotrophy
to meet its metabolic needs (Schlichter et al. 1985; Fricke et al.
1987; Schlichter 1991; Schlichter et al. 1997). However, the popu-
lation genetics of L. fragilis host and Symbiodinum have not been
studied and any physiological differences with depth are likely to
reect adaptations of different host species and/or Symbiodinium
types. The Caribbean coral Montastrea cavernosa shows morpho-
logical and genetic differentiation across depths (Lesser et al.
2010; Brazeau et al. 2013), and displays physiological acclimatiza-
tion and photoadaptation associated with different Symbiodinium
composition between shallow (046 m) and greater depths
(6191 m). Furthermore, a shift from photoautotrophy to hetero-
trophy occurred between 45 and 61 m, and lower productivity
was found at greater depths (Lesser et al. 2010).
Previous studies have found that both photobiological exi-
bility and Symbiodinium type are essential to persist in light-
limited environments (Frade et al. 2008; Cooper et al. 2011;
Ziegler et al. 2015). In the Caribbean, Madracis spp. showed
photoacclimatization by varying Symbiodinium density and
type, as well as efciency of light harvesting across depths from
5 to 40 m (Frade et al. 2008). In Western Australia, Pachyseris
speciosa and Seriatopora hystrix showed different patterns of
hostSymbiodinium specialization across depths (060 m).
P. speciosa hosted mainly Symbiodinium type C across its depth
range (060 m), whereas S. hystrix hosted Symbiodinium type
D1a at shallow depths (020 m) and Symbiodinium Ctypeat
deeper depths (1045 m; Cooper et al. 2011). Interestingly,
S. hystrix had an increase in metabolic costs when hosting Sym-
biodinium C compared to type D1a while exposed to higher irra-
diances, suggesting that metabolic demands may depend on
Symbiodinium type (Hoadley et al. 2015; Leal et al. 2015; Pernice
et al. 2015). In the Red Sea, Symbiodinium densities and ratios of
photoprotective and photosynthetic pigments decreased with
depth (060 m) in Porites,Leptoseris,Pachyseris, and Podabacia.
Porites harbored Symbiodinium type C15 while Pachyseris and
Podabacia hosted mainly Symbiodnium type C1 and had a more
limited depth range (Ziegler et al. 2015). These studies underlie
the importance of genotyping Symbiodinium when investigating
coral physiology from different light regimes. Both adaptation
(change in the genetic makeup of a population over multiple
generations) and acclimatization (when an organism adjusts to
a change in its environment) strategies can play an important
role in an organisms survival when light becomes limited.
In Hawaiian waters, Leptoseris is the dominant coral genus in
the mid to deep mesophotic zones (60160 m) and colonies of
Leptoseris species form the most spatially extensive mesophotic
coral ecosystem documented to date (Costa et al. 2015; Veazey
et al. 2016; Spalding et al. 2019). These reef-building corals form
extensive reefs with up to 100% live coral cover predominantly
at 90100 m (Kahng and Kelley 2007; Rooney et al. 2010). Spe-
cies of Leptoseris form large (> 1 m in diameter), thin-walled col-
onies with plating and foliaceous morphologies that can grow
approximately 1 cm yr
1
(Kahng 2013; Pyle et al. 2016), compa-
rable to some shallow water corals. In contrast, L. fragilis meso-
photic colonies in the Red Sea grow ~ 0.20.8 mm yr
1
and
have a maximum diameter of 810 cm (Fricke et al. 1987).
Because of the signicant role of Leptoseris corals in creating
mesophotic environments, insight into their physiology is criti-
cal to understand the ecosystem.
Leptoseris reefs in Hawaii are hotspots of biodiversity and
productivity with signicantly higher rates of endemism in
shes compared to shallow reefs (Rooney et al. 2010; Kane
et al. 2014; Pyle et al. 2016). These reefs facilitate recruitment
of other species (Supporting Information Fig. S1), may func-
tion as refuges for shery-targeted species already impacted on
shallow reefs (Lindeld et al. 2016), and are distinctive habi-
tats that harbor many undescribed and unique species (Pyle
et al. 2016; Spalding et al. 2016).
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
2
Recent morphological and molecular studies have addressed
the high cryptic diversity in Leptoseris from Hawaii, revealing
new insights about the diversity and adaptation of Leptoseris
Symbiodinium associations in this light-limited environment
(Luck et al. 2013; Pochon et al. 2015). Using the cox-1-rRNA
intron and skeletal micromorphology, Luck et al. (2013)
reported a depth zonation pattern for different Leptoseris clades.
Using a similar molecular approach (cox-1-rRNA intron),
Pochon et al. (2015) examined hostSymbiodinium relationships
in Leptoseris nding ve cryptic species and variation in associ-
ated Symbiodinium across depths. However, the physiological
exibility of these different assemblages or their success in meet-
ing host metabolic demands at different depths remains unex-
amined. Kahng et al. (2012) attributed the success of Leptoseris
in the mesophotic zone to a low level of reectivity associated
with microscale optical geometry of the coral skeleton. How-
ever, this hypothesis remains largely untested.
In this study, we used an integrative approach to explore the
status and exibility of photobiology and trophic ecology of
mesophotic species in the Leptoseris genus. Specically, we
address the following questions: (i) What mechanisms enable the
reef-building coral Leptoseris spp. to live in the mesophotic zone?
(ii) Is the photobiology of Leptoseris inuenced by hostSym-
biodinium specialization? (iii) What are the strategies for energy
acquisition from 60 to 130 m depths? An understanding of the
physiological state and exibility of these species is essential for
characterizing the status and resilience of mesophotic reefs in
Hawaii.
Methods
Study site
Samples of cryptically diverse Leptoseris spp. were collected
across multiple depths (60130 m) in the Auau Channel off-
shore of Olowalu, west Maui (2046.8510N, 15640.3910W), in
April 2009, January 2010, and February and March 2011 using
the Pisces IV and Pisces V submersibles, respectively (Fig. 1A;
Supporting Information Table S1). The Auau Channel (Fig. 1B)
separatestheislandsofMauiandL
anai and has a bottom topog-
raphy consisting of a gently sloping, continuous limestone
bridge. Underwater irradiance was measured at six sites in areas
with Leptoseris spp. reefs in the Auau Channel and Maui Nui
Fig. 1. (A) Submersible Pisces IV,(B) collection site in the Auau Channel, Hawaii, (C) Schilling Titan 4 manipulator arm collecting Leptoseris spp. sam-
ple, (D,E)Leptoseris reef at 90 and 120 m, and (F) coral cover (black bars) by depth plotted with PAR levels (gray line).
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
3
island complex during August 2008 and July 2010 (Supporting
Information Table S2) to characterize the light environment. Irra-
diance was measured by lowering a calibrated spherical (4π)
quantum sensor (Underwater LI-193SA, LI-COR©) through the
waterviaaproling rig; data were stored with a LI-COR© LI-1400
data logger. Scalar irradiance (E
0
)isthebestall-roundmeasureof
light availability for photosynthesis at a given depth, because
photons are equally useful in photosynthesis regardless of their
source direction (Kirk 2011). Furthermore, we observed Sym-
biodinium within coral cells on both the top and undersides of
coral colonies, suggesting that irradiance from multiple direc-
tions could be used for photosynthesis. The sensor was attached
to a 1-m-long arm mounted on a polyvinyl chloride housing to
reduce instrument shading. The housing was integrated with a
calibrated pressure transducer for depth (m) and a temperature
sensor. PAR (in μmol photons m
2
s
1
from 400 to 700 nm) was
recorded at known depths in the water column to maximum
depths ranging from 64 to 94 m on calm, clear days (< 10% cloud
cover) during midday (12:0013:00 h). Furthermore, irradiance
proles were conducted on the sunny side of the vessel to reduce
shadows. The vertical attenuation coefcient for scalar irradiance
(K
0
) from the downward portion of each prole was calculated
according to the relationship in BeersLaw:E
z
=E
0
×e
K0z
where
zrepresents depth, E
z
represents the intensity of irradiance at
depth z,andE
0
represents the irradiance just beneath the surface
(Kirk 2011). K
0
was then used to extrapolate irradiance at every
1 m depth for each prole, and an average irradiance prole (
SE) was calculated from six proles. Optical depths for 1% and
10% surface irradiances were calculated using K
0
(Kirk 2011). In
deep, clear, homogenous waters with little scattering and a diffuse
light environment, the relationship of the vertical attenuation
coefcients K
0
(scalar irradiance) and K
d
(downwelling irradiance)
is nearly one (Kirk 2011), thus allowing for a direct comparison
between K
0
and K
d
. Daily mid-day irradiance vertical proles
showed little stratication in the water column, with r
2
values
rangingfrom0.97to0.99(Supporting Information Table S3). The
vertical attenuation coefcients, K
0
(m
1
), ranged from 0.037 to
0.047 m
1
,withameanK
0
(SE) of 0.041 m
1
(0.001). The
calculated mean optical depths, which correspond to the mid-
point (10% surface irradiance) and the lower limit (1% surface
irradiance) of the euphotic zone, were 56 and 112 m, respectively.
This corresponded to a decrease in irradiance levels from 103 to
11 μmol photons m
2
s
1
, respectively (Supporting Information
Table S3).
Coral collections and abundance
At each site, coral cover was assessed visually by the scien-
tic collector viewing an area ~ 5 m
2
around the site of coral
collection via a submersible window (Fig. 1). Representative
corals approximately 2030 cm in diameter were haphazardly
selected from the middle of Leptoseris reefs, with each sample
separated by at least 10 m from other samples. A small, trian-
gular piece of coral from the middle to the outer edge of each
coral head was removed using a Schilling Titan 4 manipulator
arm (Fig. 1C) and placed in an individual sample container in
the sampling basket. After collection, samples were placed in a
darkened container with ambient seawater at in situ seawater
temperatures and processed in a darkened, air conditioned labo-
ratory, using red light headlamps with an intensity of ~ 1 μmol
photons m
2
s
1
from a distance of 4050 cm, onboard the R/V
Kaimikai-O-Kanaloa within 39 h of ascent. Two sets of coral
samples were collected. One sample set was analyzed for photo-
synthetic potential, host genetics, Symbiodinium genetics, Sym-
biodinium density, photosynthetic pigments, and total lipids. A
second set of samples from different coral colonies was collected
for isotopic analyses. It is important to note that the second set
of samples did not include genetic analyses for host and Sym-
biodinium identication (Supporting Information Table S1).
Sample size for physiological and photobiological analyses dif-
fered due to sample and instrumentation availability and is
reported for each parameter in the sections below. Supporting
Information Table S1 includes the location and date of all col-
lections with the physiological and photobiological analyses
performed on each sample. After collecting and assessing photo-
synthetic potential (in the rst set of coral samples), fragments
were frozen using dry ice and maintained in a 80Cfreezer
until analyzed.
Laboratory analysis
Pulse amplitude-modulated uorometry
Photosynthetic potential was assessed with modulated
chlorophyll uorescence measurements taken with a pulse
amplitude-modulated (PAM) uorometer and a red (650 nm)
excitation beam (Diving-PAM). A 2-cm-long piece of black
tubing (1 cm diameter) was attached to the PAM ber optic
sensor to standardize the area measured and to ease the place-
ment of the sensor onto the coral surface. Actinic PAR values
from the Diving-PAM with the ber optic sensor tubing were
calibrated with a cosine underwater quantum sensor (LI-COR
LI-192SA) and data logger (LI-COR LI-1400). Measurements of
minimum (F
o
) and maximum (F
m
)uorescence were used to
calculate variable (F
v
=F
m
/F
o
)uorescence and subsequently
the maximum quantum yield of photosystem II (PSII) uores-
cence (F
v
/F
m
) or the number of functional photosynthetic
units (Ralph and Gademann 2005). To account for potential
spatial variation in coral physiology, ~ 10 measurements of
F
v
/F
m
were taken from haphazardly selected, spatially sepa-
rated points on the coral tissue surface and averaged for each
sample (n= 57 coral colonies). Rapid light response curves
(RLC) were then taken to measure photosynthetic potential
under different light levels following Ralph and Gademann
(2005). Each RLC exposed the coral to eight incremental steps
of irradiance, similar to the local environment, from 0 to
75 μmol photons m
2
s
1
. This lower range of irradiances was
used on corals from all depths to avoid photoinhibition in
corals from deeper depths. Irradiances were set to provide suf-
cient measurement steps ~ 45 measuring points below
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
4
saturation, for accurate initial slope (α) calculations. The elec-
tron transport rate (ETR) at each irradiance was calculated
using the formula ETR = F
v
/F
m
×PAR ×0.5, where the quan-
tum yield is the parameter measured at each irradiance of
PAR, and 0.5 is the theoretical distribution of absorbed pho-
tons between PSII and photosystem I (PSI), although this bal-
ance was not evaluated for these samples. Average ETRs by
actinic irradiances for each algal sample were t to a three-
parameter nonlinear model as described by Ralph and
Gademann (2005). RLC data were used to estimate the relative
maximum ETR (rETR
max
), α(initial slope of the RLC), and the
light saturation coefcient (E
k
). We used the relative measure
of rETR because the exact absorbance of the coral is unknown
and likely varies by species and depth-related skeletal pheno-
typic differences. Curves were t using the Regression Wizard
in Sigmaplot (v. 12.0, SPSS), and estimates of rETR
max
,α, and
E
k
were used for analyses. In all samples, the model ts the
data well with an r
2
of 0.97 0.01 (mean SEM).
Algal pigments
Algal pigments were extracted as previously described in
Padilla-Gamiño et al. (2013). Briey, glass ber lters (0.7 μm
pore size, GF/F; Whatman) containing the coral and algal tis-
sue homogenate (n= 75) were extracted in 3 mL of high-
performance liquid chromatographygrade acetone in glass
culture tubes along with 50 μL of an internal standard (can-
thaxanthin) at 4C in the dark for 24 h. The extracts were
processed following Bidigare et al. (2005); pigments were
detected with a ThermoSeparation Products UV2000 detector
(λ
1
= 436, λ
2
= 450). Concentrations of photosynthetic (chlo-
rophyll a[Chl a], Chl c
2
, and peridinin) and photoprotective
(β-carotene, dinoxanthin, diadinoxanthin, and diatoxanthin)
pigments and ratios at the colony and algal cellular level were
computed by normalizing to coral surface area (μg pigment
cm
2
) and Symbiodinium density (pg pigment cell
1
). Our
study did not attempt to differentiate the sources of Chl
aamong Symbiodinium and endolithic algae. Approximately
85% of the coral skeletons had visible endoliths; 71% of the
skeletons had green endoliths; and 23% had both green and
orange endoliths. To minimize endolithic contribution in the
pigment extractions, we only used homogenate derived from
coral tissue (not skeleton). Identities of pigments produced
exclusively by dinoagellate symbionts (i.e., peridinin and Chl
c; Kleppel et al. 1989) show proportions or similar patterns to
our Chl adata suggesting that our pigment quantication
mostly represented extracts from Symbiodinium (Supporting
Information Fig. S2).
Symbiodinium densities
The densities and size of Symbiodinium cells were examined
according to Apprill et al. (2007). In brief, coral tissue (n= 75)
was removed from the frozen fragment using a Waterpik
®
and
ltered seawater (FSW, 0.2 μm). The homogenate tissue was
then blended for 30 s and centrifuged for 5 min. Multiple
washing steps were performed with FSW to ensure the com-
plete separation of Symbiodinium and coral tissue. The Sym-
biodinium suspensions were analyzed using a Beckman-Coulter
XL ow cytometer with a 15-mW argon ion laser set to excite
at 488 nm. The ow cytometer was interfaced with an Orion
syringe pump for quantitative sample analysis using a 3 mL
syringe delivering 100 μL of suspended cells at a ow rate of
50 μL min
1
for measurement of uorescence emission of Chl
a(630 nm dichroic lter, 680 nm bandpass lter), as well as
forward and side scatter signals. Duplicate abundance esti-
mates were averaged for each sample. Symbiodinium abun-
dances were standardized to coral surface area measured with
the aluminum foil method (Marsh 1970). Symbiont subpopu-
lations were identied based on side scatter (cell size) and uo-
rescence characteristics. Listmode les generated by the Flow
cytometer were analyzed using FlowJo software (Treestar) by
species. The number of symbionts from each symbiont sub-
population for each individual was quantied using FlowJo
software and converted to the percent distribution of the three
subpopulations and graphically represented using a ternary
diagram (SigmaPlot 13.0 ©2014, Systat Software; Supporting
Information Fig. S3).
Coral and Symbiodinium genetics
Host and Symbiodinium genotypesofoursamples(except
samples used for isotopic signatures) were reported previously in
Pochon et al. (2015) and examined using coral (COX1-1-rRNA
intron) and Symbiodinium (COI) mitochondrial markers (n=74).
Generally, COI haplotypes corresponded with specicITS2 com-
munity sequence proles. Haplotype COI-1 was uniquely associ-
ated with ITS2 sequence type C1v18, haplotype COI-2 was
associated with ITS2 sequence types C1v1d and C1c/C45, and
haplotype COI-3 was associated with ITS2 sequence types
C1v1b, C1v1c, C1v3, and C1v8 (Pochon et al. 2012). However,
ITS2 sequence types C1 and C1v1e were associated with all COI
haplotypes, and ITS2 sequence type C1v6 was associated with
both COI-1 and COI-2 (Pochon et al. 2015).
Total lipids and biomass
Total lipids and biomass (n= 75) were obtained following
Rodrigues and Grottoli (2007). In brief, ground coral samples
were extracted in a 2 : 1 chloroform : methanol solution, the
organic phase was then washed using 0.88% KCl, and the
lipid extract dried to a constant weight. Tissue biomass was esti-
mated using the difference between dry weight and ash free dry
weight. Lipids and biomass were normalized to surface area.
Stable isotopes
Coral tissue and Symbiodinium were removed from skele-
tons using a WaterPik with FSW (n=2125; Johannes and
Wiebe 1970). Host and Symbiodinium fractions were separated
using a centrifuge that isolated zooxanthellae as a pellet. Pel-
lets were washed and resuspended using FSW, then cen-
trifuged, repeating the procedure twice. To ensure separation,
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
5
pellets and supernatant were examined periodically under a
microscope. Both resuspended pellets and supernatant were
separately collected on a precombusted GF/F lter using vac-
uum ltration. Filtered fractions were analyzed for elemental
and isotopic composition of carbon and nitrogen (δ
13
C = ratio
of
13
C:
12
C relative to Vienna Peedee Belemnite Limestone
Standard and δ
15
N = ratio of
15
N:
14
N relative to air, reported
in permil units) using an elemental analyzer coupled to a
Thermo Delta V isotope ratio mass spectrometer. When ample
material was present, sample analyses were duplicated. A sub-
set of samples was acidied on the lter to test for residual
skeletal material. Acidication showed no indication of skele-
tal contamination with replicate standard deviations averag-
ing 0.2for Symbiodinium (C and N) and 0.3and 0.8
for C and N, respectively.
Statistical analyses
Independent data analyses for each species were grouped
based on a depth-dependent light gradient: 70 m (~ 55 μmol
photons m
2
s
1
,6575 m), 80 m (~ 36 μmol photons m
2
s
1
,
7685 m), 90 m (~ 24 μmol photons m
2
s
1
,8695 m), 100 m
(~ 16 μmol photons m
2
s
1
,96105 m), and 120 m (~ 10
5μmol photons m
2
s
1
,115125 m). Physiological values of
Leptoseris papyracea were not included in any of the statistical ana-
lyses associated with depth because the species was found at only
one depth range (90 m). Comparisons of physiological traits
between species were performed using a one-way analysis of vari-
ance (ANOVA). Prior to analyses, data were normalized as neces-
sary using logarithmic or square root transformations to achieve
homogeneity of variances and normality. Homogeneity of vari-
ance and normality was assessed using ShapiroWilk W and
Levene tests, respectively. When signicant effects were identied,
Tukeys post hoc tests were performed to determine differences
between depths. Statistical differences were signicant at the
α< 0.05 level. Wilcoxon-Signed Rank Tests were performed when
normality was not achieved after transformation. Data are repre-
sented as mean SEM. We did not perform ANOVA analyses for
isotopic signatures because genetic information was not available
for this subset of samples, instead the relationship between isoto-
pic signature and depth in Leptoseris spp. was assessed using linear
regressions. Statistical analyses were performed using JMP version
12.2.0 (SAS Institute).
Results
Leptoseris spp. complex depth distribution
Cryptically diverse species of Leptoseris were present
between 60 and 132 m; however, coral cover and diversity of spe-
cies (host and Symbiodinium)variedacrossdepths(Figs.12). The
lowest coral cover was found between 70 and 80 m (~ 36
55 μmol photons m
2
s
1
;Fig.1)withonlyLeptoseris sp. 1,
Leptoseris tubulifera,andLeptoseris scabra present (Fig. 2). At
shallow depths (7080 m), Symbiodinium spp. COI-2 and COI-
3haplotypes were nearly equally abundant, making up 60%
and 40% of the population, respectively (Fig. 2). The highest
coral cover and highest diversity in Leptoseris spp. occurred
between 90 and 100 m (Figs. 12). At these depths, irradiance
(~ 1624 μmol photons m
2
s
1
)correspondedto12% of the
irradiance just below the surface (1066 μmol photons m
2
s
1
)
Fig. 2. Irradiance in the Auau Channel, Hawaii, and distribution of Leptoseris spp. and Symbiodinium spp. COI haplotypes by collection depths (from
Pochon et al. 2015).
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
6
during summer months in 2008 and 2010 (Fig. 2; Supporting
Information Table S2 and S3). Similarly, the highest diversity in
Symbiodinium occurred between 90 and 100 m with all haplo-
types present (Fig. 2). At the deepest depths (110120 m or
~1016 μmol photons m
2
s
1
; Fig. 1EF), coral cover was
around 2035% and L. hawaiiensis was the dominant species,
although sporadic colonies of Leptoseris sp. 1 were present
(Figs. 12). The deepest locations (110120 m) had the lowest
symbiont diversity; Symbiodinium spp. COI-1 was the dominant
symbiont present in 100% and 93% of the samples at 110 and
120 m, respectively (Fig. 2). The lower depth of L. hawaiiensis and
Leptoseris sp. 1 was observed at 125 m (Fig. 2), indicating that
these species live beyond the expected 1% surface values and at
irradiances as low as 5.2 μmol photons m
2
s
1
.
Photophysiological specialization of Leptoseris spp. across
depth
L. scabra
Our data suggest that L. scabra is a broadly shade-tolerant
species, adjusting subcellular photosynthetic components to
maintain optimal performance with decreasing PAR and
depth. Photosynthetic and accessory pigments in L. scabra
increased with depth (p< 0.05; Fig. 3; Supporting Information
Table S4) allowing colonies to maintain ETR
max
. Chl acm
2
concentrations at 70 m were only 28% of the pigment con-
centrations at 100 m depth (0.43 and 1.53 μgcm
2
, respec-
tively; Supporting Information Table S4). Therefore, surface
area for light harvesting is the most important factor limiting
the depth distribution of this species. Despite being found
across a wide depth range (70100 m), L. scabra did not exhibit
signicant changes in other photophysiological variables across
depths, such as pigments per cell, pigment ratios, Symbiodinium
cell size (Fig. 3; Supporting Information Table S4), dark-adapted
quantum yield, maximum rETR, or E
k
(p> 0.05; Fig. 4). Simi-
larly, lipid content did not change with depth in L. scabra or
any of the other Leptoseris spp. (Supporting Information
Table S4). L. scabra showed very similar physiological character-
istics to L. tubulifera including close association with Sym-
biodinium haplotype CO1-2, high tissue biomass, small-size
Symbiodinium, and higher β-carotene : Chl aratios compared to
the other Leptoseris spp. (Table 1).
Leptoseris sp.1
In contrast to L. scabra,Leptoseris sp. 1 was found across a
wider depth range (70120 m) and exhibited changes in Sym-
biodinium haplotype (CO1 and CO2) with depth (Pochon et al.
2015) that may have inuenced the photobiological response
and coral acclimatization capacity with depth. Symbiodinium
density signicantly increased with depth in Leptoseris sp. 1,
with ~ 58% higher Symbiodinium densities at 100 m than at
70 m (3.3 ×10
5
and 5.69 ×10
5
cells cm
2
; 70 and 100 m,
respectively; Fig. 3; Supporting Information Table S4). Simi-
larly, Chl c: Chl aratios increased with depth (Fig. 3). Dark-
adapted quantum yield remained constant across depths,
while rETR
max
and E
k
increased at 80 m depth (F= 3.993,
p= 0.0415; F= 6.367, p= 0.011, rETR
max
and E
k
respectively;
Fig. 4; Supporting Information Table S4). Physiological charac-
teristics of Leptoseris sp. 1 were more closely related to L. scabra
and L. tubulifera than L. hawaiiensis; however, Leptoseris sp. 1
AB
CD
Fig. 3. (A)Symbiodinium density, (B) Chl a(μgcm
2
), (C) Chl c: Chl a, and (D)β-carotene in four species of Leptoseris spp. in Hawaii. L. sca,scabra
(black); L. sp. 1, Leptoseris sp. 1 (dots); L. tub,L. tubulifera (gray); and L. haw.,L. hawaiiensis (diagonal).
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
7
had larger Symbiodinium cells than either L. scabra or
L. tubulifera (Table 1). Finally, Leptoseris sp. 1 and L. payracea
had the highest Symbiodinium densities of all species (Table 1).
L. tubulifera
Similar to L. scabra,L. tubulifera showed an increase in pig-
ment concentrations with depth (p< 0.05; Fig. 3; Supporting
Information Table S4) to maintain optimal performance with
decreasing PAR and depth; with Chl acm
2
increasing ~ 55%
from 80 to 90 m (0.77 to 1.40 μgcm
2
, respectively; Fig. 3).
Although L. scabra was present from 70 to 100 m, we excluded
samples from 70 and 100 m in the statistical analyses due to low
sample size. Not surprisingly, between 80 and 90 m, there was
no signicant change in photosynthetic pigments normalized by
cell, lipids, dark-adapted quantum yield, maximum rETR
max
,or
E
k
(p> 0.05; Figs. 34; Supporting Information Table S4). How-
ever, β-carotene : Chl adecreased ~ 8% from 80 to 90 m depth
(Fig. 3). Physiological trends in L. tubulifera were very similar to
L. scabra (see above; Table 1) most likely due to their shared asso-
ciation with Symbiodinium haplotype CO1-2.
L. papyracea
L. papyracea was very abundant within a narrow depth range
(8695 m, ~ 24 μmol photons m
2
s
1
). This species was deep-
shade adapted showing the highest Chl c:Chlaand Sym-
biodinium densities (~ 0.18 and 0.59 ×106, respectively) and the
lowest lipid values (211 mg cm
2
)amongallLeptoseris species
(p< 0.05; Table 1). Despite their narrow range, L. papyracea colo-
nies at 87 m were strictly associated with Symbiodinium haplo-
type COI-3,whereasL. papyracea colonies at 95 m only hosted
Symbiodinium haplotype COI-1 (Pochon et al. 2015).
L. hawaiiensis
L. hawaiiensis lives at depths with the lowest irradiance
levels (110120 m, 105μmol photons m
2
s
1
, respectively)
and below the threshold-value of the lower limit of the eupho-
tic zone (i.e., at 112 m there is less than 1% surface irradi-
ance). Yet Symbiodinium (COI-1) in these colonies still exhibit
classic shade adaptation. At 120 m, Symbiodinium cell size
decreased ~ 6% compared to Symbiodinium cells at 110 m
(p= 0.011, F= 6.475; Fig. 3). Chl c: Chl aand DDX +
DTX : Chl aratios also decreased (24% and 2%, respectively,
p= 0.004, F= 8.377; p= 0.044, F= 4.069) at 120 m, whereas
β-carotene : Chl aratios increased 10% (Fig. 3; p= 0.011,
F= 6.469; Supporting Information Table S4). Dark-adapted
quantum yield increased at 120 m (F= 15.604, p= 0.001;
Fig. 4), whereas rETR
max
,E
k
, and αdecreased at this depth
(Fig. 4; p< 0.05; Supporting Information Table S4). Compared
to other species, L. hawaiiensis showed the lowest Symbiodinium
densities and the largest Chl acontent per cell (Fig. 4; Table 1).
The relative total xanthophyll pool, β-carotene : Chl aratios,
and tissue biomass were the lowest in L. hawaiiensis compared
to other Leptoseris spp. (Fig. 3; Table 1); however, lipid content
(mg cm
2
) was the highest (Table 1). Fluorescence parameters
showed a very distinct response in L. hawaiiensis;thisspecies
had the lowest rETR
max
,α,andE
k
and the highest values of
dark-adapted yields compared to other species of Leptoseris
(Fig. 4; Table 1).
Leptoseris spp. complex isotopic signatures
Carbon isotopic composition of Symbiodinium ranged from
21.9to 18.9and from 19.1to 22.7in hosts,
with similar means in both fractions (20.3and 20.9,
AB
CD
Fig. 4. (A) Dark-adapted quantum yield, (B) maximum relative ETR, (C)α, and (D)E
k
in Leptoseris spp. in Hawaii. L. sca,scabra (black); L. sp. 1,
Leptoseris sp. 1 (dots); L. tub,L. tubulifera (gray); and L. haw.,L. hawaiiensis (diagonal).
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
8
respectively). Host δ
13
C values decreased linearly with increas-
ing depth (p< 0.0001, F= 49.5; Fig. 5A). However, Sym-
biodinium δ
13
C values did not show a signicant trend with
depth. Bulk stable isotopic values for nitrogen in Symbiodinium
ranged from 1.1to 3.4, whereas that of the host tissue
ranged from 2.7to 6.3(mean 2.4and 4.1, respec-
tively). Symbiodinium δ
15
N values decreased with increasing
depth (p= 0.008, F= 8.69; Fig. 5B). However, host nitrogen
isotopic composition did not show any overall trend with
increasing depth (p= 0.243). Differences between isotopic
composition of coral host and symbiotic algae exhibited dis-
similar trends with depth. With increasing depth, Sym-
biodinium became signicantly more distinct via changed δ
15
N
compared to host tissue, whereas host tissue became signi-
cantly more depleted in δ
13
C compared to Symbiodinium
(p= 0.0397, F= 4.83 and p= 0.007, F= 9.04, respectively;
Fig. 5C). C : N ratios for Symbiodinium increased with depth
(p= 0.025) and ranged from 5.7 to 9.5 (mean = 6.9), whereas
C : N ratios for the host decreased with depth (p= 0.0116)
and ranged from 5.5 to 16.75 (mean = 7.79).
Discussion
In this study, we explore the depth-dependent variability
in trophic strategies, photophysiological, and genetic traits of
four Leptoseris spp. Our robust, cross-cutting approach revealed
different physiological strategies used by the algae and coral
species to obtain energy and persist in a deep-shade environ-
ments. This work uncovered three fundamental insights into
coralalgal symbiosis, photophysiology, and trophic plasticity
Table 1. Physiological differences among Leptoseris spp. in Hawaii.
Species L. scabra Leptoseris sp. 1 L. tubulifera L. papyracea L. hawaiiensis
Depth range (m) 70100 70100 70100
*
90 110120
Symbiodinium haplotype COI-2 COI-2 and COI-3 COI-2 COI-1 and COI-3 COI-1
Biomass (mg cm
2
) 17.33 12.3
(A)
11.73 7.1
(A)
14.51 7.5
(A)
9.04 2.4
(A,B)
7.17 2.7
(B)
Lipids (mg cm
2
) 413.91 334.4
(B)
581.77 319.3
(C,B)
425.45 257.6
(A, B)
211.22 154.6
(A)
845.42 417.3
(C)
Symbiodinium cells cm
2
0.34 0.1
(B,C)
0.41 0.2
(A,B)
0.36 0.1
(B,C)
0.59 0.2
(A)
0.27 0.1
(C)
Cell size (mm) 8.81 0.3
(A)
9.54 0.6
(B)
8.78 0.2
(A)
9.25 0.5
(B)
9.19 0.6
(A,B)
Chl a(mg cm
2
) 0.82 0.5
ns
1.05 0.5
ns
1.09 0.4
ns
1.14 0.4
ns
1.19 0.2
ns
Dinoxanthin (mg cm
2
) 0.02 0.01
(A)
0.03 0.01
(A,B)
0.02 0.01
(A,B)
0.03 0.01
(A, B)
0.03 0.01
(B)
Chl a(pg cell
1
) 2.29 1.0
(A)
2.72 1.3
(A)
3.22 1.3
(A, B)
1.93 0.4
(A)
4.71 2.0
(B)
Chl c/Chl a0.15 0.03
(A)
0.15 0.03
(A)
0.15 0.02
(A)
0.18 0.02
(B)
0.15 0.03
(A)
DDX + DTX/Chl a0.13 0.004
(C)
0.13 0.005
(A)
0.13 0.005
(A, B)
0.13 0.001
(B,C)
0.12 0.122
(D)
Beta-carotene/Chl a0.023 0.002
(A)
0.022 0.002
(A)
0.024 0.002
(A)
0.020 0.001
(B)
0.018 0.002
(B)
Dark-adapted yield 0.65 0.02
(A)
0.65 0.03
(A)
0.65 0.02
(A, B)
0.64 0.02
(A)
0.67 0.02
(B)
rETR
max
5.70 2.3
(A)
5.74 2.7
(A)
4.62 1.1
(A)
6.97 1.2
(A)
2.96 1.4
(B)
Alpha 0.30 0.05
(A)
0.29 0.06
(A)
0.30 0.04
(A)
0.33 0.04
(A,B)
0.23 0.08
(B)
E
k
18.88 5.7
(A)
19.07 6.3
(A)
15.38 3.0
(A,B)
21.15 3.8
(A)
13.14 4.39
(B)
Numbers in the table represent averages and standard deviations for each species including all depths. Signicant differences between species are repre-
sented by superscripts.
DDX, diadinoxanthin; DTX, diatoxanthin.
A
B
C
Fig. 5. (A)δ
13
C, (B)δ
15
N signatures, and translocation between host and
Symbiodinium of Leptoseris spp. at different depths. (A,B) Coral host fraction
in black and Symbiodinium fraction in gray, and (C) difference between animal
and Symbiodinium,δ
13
C(gray)andδ
15
N (black). Means and standard devia-
tions are plotted; lines represent linear regressions for host and Symbiodinium.
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
9
in mesophotic environments. To begin, plasticity of Leptoseris
algal photophysiology across depths was associated with the
type of Symbiodinium spp. Colonies harboring Symbiodinium
spp. COI-2 (L. tubulifera and L. scabra)showedsignicant
increases in photosynthetic pigment content with increasing
depth but no change in chlorophyll uorescence with depth
(Fig. 6), suggesting a complex that is broadly tolerant to its
depth conditions. In contrast, colonies harboring Sym-
biodinium spp. COI-1orCOI-3 (L. hawaiiensis and Leptoseris
sp. 1) showed variability in pigment ratios, chlorophyll uo-
rescence, and Symbiodinium density and/or size (Fig. 6),
suggesting that exibility in photoacclimatization as well as
photoadaptation among these Leptoserisalgal complexes
depends primarily on Symbiodinium genotypes. Furthermore,
despite remarkable differences in photosynthetic adaptive
strategies with depth, we found no differences in total lipid
content of Leptoseris spp. species over the same depth range
(Supporting Information Table S4). This nding suggests that
photosynthetic acclimatization with depth resulted in similar
acquisition and translocation of lipids to the hosts and/or
hosts may be supplementing their total lipid reserves from
nonphotosynthetic sources at deeper depths. Finally, isotopic
Fig. 6. Schematic representing (A)Leptoseris spp. distribution along a depth gradient and (B) physiological trends with depth. -,no difference in the
physiological variable across depth.
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
10
signatures of both host and Symbiodinium changed with
depth supporting the lipid ndings and indicating that coral
colonies may acquire energy from different sources along
their depth gradient. Overall, our results show marked com-
plexity in physiological adaptations of species in the
Leptoseris spp. complex and highlight the diversity of strate-
gies used to acquire energy and succeed in environments
where irradiance is extremely limited.
Photophysiology
Because mesophotic reef-building corals live close to the
limits of the depth distribution for Scleractinian corals, their
photophysiology is likely to reveal novel acclimatization and
adaptation strategies in photosynthetic symbioses. Our results
show that Leptoseris species have different hostSymbiodinium
specializations and physiological plasticity along a depth gra-
dient. L. scabra and L. tubulifera were almost exclusively associ-
ated with Symbiodinium spp. COI-2 haplotype but showed the
ability to increase Symbiodinium pigment concentrations (per
surface area) with depth. This pattern is similar to M. cavernosa
in the mesophotic Caribbean (Lesser et al. 2010), but the
opposite trend was observed for L. fragilis in the mesophotic
Red Sea (Fricke et al. 1987; Schlichter et al. 1997). L. tubulifera,
however, showed greater phenotypic variation in symbiont
populations (Supporting Information Fig. S3) and lower
β-carotene : Chl awith increasing depths, suggesting that this
species has more diverse Symbiodinium (type, size, quantum
yield, or cell division rates) and that β-carotene has primarily a
photoprotective function at shallower depths.
Leptoseris sp. 1 (70100 m) was the only species that increased
Symbiodinium densitywithdepth.Coloniesofthisspeciesat
100 m had twice the density of Symbiodinium than colonies at
70 m. Increased Symbiodinium density under low light condi-
tions has been observed in the eld experimentally in Stylophora
pistillata (Dubinsky and Jokiel 1994; Titlyanov et al. 2001).
Under light-limited conditions (~ 8% surface irradiance), light
harvesting in S. pistillata was maximized by an increase in Sym-
biodinium density, which was primarily regulated by division
and degradation of Symbiodinium cells (Titlyanov et al. 2001).
Thus, it is likely that increased Symbiodinium density may facili-
tate photosynthetic energy acquisition of Leptoseris sp. 1 at
deeper depths. Nutrients have also been associated with
increased densities of Symbiodinium (Sawall et al. 2014); however,
the nutrient dynamics in the mesophotic region and the role of
nutrient limitation or enrichment in the ecophysiology of
Leptoseris spp. in the mesophotic zone remains unknown. Con-
versely, Symbiodinium densities of L. fragilis in the mesophotic
zone of the Red Sea decreased ~ 50% between 100 and 130 m
(Fricke et al. 1987) and Symbiodinium densities decreased in colo-
nies of the genera Leptoseris,Pachyseris,Seriatopora,Porites,and
Podabacia from 1 to 60 m depths in Australia and the Red Sea
(Cooper et al. 2011; Ziegler et al. 2015).
TheincreaseinSymbiodinium densities with depth in Leptoseris
sp. 1 was not associated with changes in Chl acm
2
or
Symbiodinium size. However, Chl c:Chlashowed an increase
with depth (70 to 80 m), indicating photoacclimatization by
increasing light harvesting antennae to gather light and augment
light energy capture to the photosynthetic reaction center (Roth
et al. 2010). Additionally, at shallow depths (7080 m), Leptoseris
sp. 1 was strictly associated with Symbiodinium haplotype COI-3,
whereas at deeper depths colonies were associated with Sym-
biodinium haplotypes COI-2 and COI-3 (Pochon et al. 2015).
Thus, it is likely that the differences in photosynthetic pigment
content, composition, and Symbiodinium density are not only the
result of photobiological adaptation but also the result of strong
selectivepressuresontheinteractionsbetweenthehostsand
their different Symbiodinium assemblages (Baker 2003) to opti-
mize light harvesting at these remarkable depths.
Strikingly, L. hawaiiensis was the dominant species below
the 1% optical depth where irradiance levels are lower than
1% of the surface irradiance. This species exhibited a highly-
specialized association with Symbiodinium haplotype COI-1,
which had the highest variability in photobiology with depth
compared to other species within the Leptoseris complex. In
this species, dark-adapted yield increased with depth, whereas
values for rETR
max
,α, and E
k
declined with depth. At the
deepest depth range (115125 m), we found lower rates of
photosynthetic electron transport and unexpectedly lower
efciency at subsaturating irradiances (α). Similar results were
found in M. cavernosa (Lesser et al. 2010), where rETR
max
and
gross primary productivity decreased with depth (390 m
depth range). For L. hawaiiensis,Symbiodinum size and Chl
c: Chl adecreased with depth, suggesting genetic or energetic
limitations on cell parameters and/or the amounts of pig-
ments that can be produced. This could enforce less reliance
on light capture for carbon gain by the host.
Photoprotective pigments had different patterns with depth
in L. hawaiiensis. As expected, the relative xanthophyll pool : Chl
apool decreased with depth. However, β-carotene in
L. hawaiiensis increased with depth, indicating that it is more
likely to play a role as a structural component of the light-
harvesting complex rather than as a photoprotective pigment.
Further research including collections in different seasons is nec-
essary to quantify the physiological exibility of Leptoseris spp.
over larger temporal scales and examine whether pigment com-
position and relative abundance change as light becomes more
available with higher sun declination and longer day length. It
is important to note that L. hawaiiensis photosynthesizes in a
habitat with approximately half of the light available (~ 6 μmol
photons m
2
s
1
) at the 1% surface irradiance. This is a remark-
able system that warrants further photosynthetic research and a
re-evaluation of our understanding of the mechanisms that set
lower limits of the euphotic zone and the strategies evolved by
these endemic species to persist in these environments.
This study reveals remarkable species differentiation by
Symbiodinium and Leptoseris under extreme light limitation in
the mesophotic zone including changing pigment quantities and
composition, photochemistry parameters, and/or Symbiodinium
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
11
type, density and size. Chlorophyll uorescence RLC measure-
ments should be interpreted with caution given the caveats
and assumptions involved with data collection and interpreta-
tion (Warner et al. 2010). The RLC data should not be con-
fused with traditional oxygen-based photosynthesis to
irradiance (PE) curves, and cannot be used to infer total pho-
tosynthetic productivity. Absorption was not measured in this
study but was assumed to be about 1, given the lower light
environment and likely maximized light harvesting found at
65 to 125 m depths. Measurements of M. cavernosa absorbance
had similar values ranging from 0.951 0.010 to
0.963 0.012 from 45 to 91 m depths, respectively (Lesser
et al. 2009). Future studies should involve simultaneous mea-
surements of photosynthesis and ETR, detailed absorbance
and reectance measurements, and the role of endolithic
green algae in inuencing the spectral signal of mesophotic
corals. The use of a modied ETR equation that uses the spec-
tral reectance of the coral surface where uorescence mea-
surements are recorded and then converted to the absorbance
band at 675 nm (Enríquez et al. 2005) would also be useful for
comparison for future studies.
Another aspect to consider is that morphological, physiologi-
cal, and behavioral adaptations may also occur in the host to
control and optimize light acquisition (Maxwell and Johnson
2000). In response to light, corals can modify skeletal morphol-
ogy (Muko et al. 2000; Enríquez et al. 2005; Todd 2008), pro-
duce antioxidants and uorescent proteins (Muko et al. 2000;
Enríquez et al. 2005; Todd 2008), and change tissue thickness,
polyp size, density, and behavior (Porter 1976; Fitt et al. 2000;
Levy et al. 2003; Wangpraseurt et al. 2014). In Hawaii, Leptoseris
in the mesophotic zone exhibits atter morphologies with
increasing depth (Kahng et al. 2012; J.L.P.-G. personal observa-
tion), nonphotosynthetic uorescent pigments are found in the
host throughout its depth range (Porter 1976; Fitt et al. 2000;
Levy et al. 2003; Wangpraseurt et al. 2014), and skeletal design
and structures maximize light scatter through the coral tissue
(Kahng et al. 2012; Kahng 2014). The upper side of Leptoseris
skeletons has ordered rows of concave cavities that increase the
probability of light scattering to maximize light capture (Kahng
et al. 2012; Kahng 2014).
Energy reserves and acquisition
Despite dynamic changes in photophysiology, total host
lipids were not signicantly different across depths, suggesting
that lipid acquisition is maintained by nonphotosynthetic
sources at some depths. As shown by Muscatine et al. (1989)
and observed here for Leptoseris spp. (Fig. 5), the more rapid
depletion of
13
C in host tissue of Leptoseris spp. compared to
Symbiodinium indicates that animal tissue at depth incorpo-
rates carbon from other sources, including heterotrophy
and/or dissolved organic carbon, in addition to photosynthe-
sis. Moreover, the relative similarity of carbon isotopic compo-
sition between host and Symbiodinium at the shallowest
depths suggests that heterotrophic inputs do not become
signicant until well into the mesophotic realm (120130 m).
Similar patterns were observed in M. cavernosa in the Carib-
bean where δ
13
C values of host and Symbiodinium only dif-
fered at the deepest collection site (91 m), suggesting less
translocation of photosynthates to the host and larger depen-
dency by the host cells on heterotrophy and/or other sources
of carbon at depth (Lesser et al. 2010).
The Leptoseris spp. complex consists of several cryptic spe-
cies (Pochon et al. 2015); however, species data were not avail-
able for the isotopic samples presented (Fig. 5; Supporting
Information Table S1). Therefore, it is possible that the stable
carbon isotopic patterns that we observed in host and symbi-
ont across depth may be the result of differences in heterotro-
phic plasticity as previously described (Muscatine et al. 1989)
or differences in lipid production and storage among species,
as lipids typically lower the δ
13
C values of host tissue (Deniro
and Epstein 1977; Alamaru et al. 2009). Although we cannot
conrm the species analyzed in the isotopic samples, our
study suggest that greater differences in δ
13
C across depth
between host and symbiont tissues are more likely inuenced
by preferential reliance on heterotrophic sources at depth
than differences in storage or production of lipid content
between species (Supporting Information Table S4; Fig. 6).
This is further supported by C : N depth-patterns in host and
Symbiodinium. Lower C : N ratios in the host at deeper depths
indicate higher nitrogen content from heterotrophic activity
and/or less carbon translocated to the host by Symbiodinium
due to lower light levels at depth and increased nitrogen limi-
tation (Dubinsky and Jokiel 1994).
The δ
15
N values were higher in the host than in Sym-
biodinium at all depths. This trend is consistent with previous
observations in M. cavernosa (Muscatine and Kaplan 1994;
Lesser et al. 2010), S. pistillata and Favia favus (Alamaru et al.
2009). Enriched stable nitrogen isotopic signatures in the host
may be attributable to protein catabolism and excretion of iso-
topically light ammonium (Deniro and Epstein 1977; Alamaru
et al. 2009) and/or metabolic fractionation related to changes
in trophic level (Muscatine and Kaplan 1994). Because corals
use the products of photosynthesis by Symbiodinium, an isoto-
pic enrichment in the host is expected.
In Symbiodinium,δ
15
N values decreased with depth, whereas
host δ
15
N values remained constant across depths (Fig. 5). Mus-
catine and Kaplan (1994) found a similar trend of depth-related
depletion of δ
15
NinSymbiodinium of several species of Jamaican
scleractinian corals that corresponded to decreasing nitrogen-
specic growth rates in deeper waters. Likewise, the Sym-
biodinium of S. pistillata and F. favus decreased with depth,
whereas the host tissue remained the same across depth
(Alamaru et al. 2009). The mesophotic depths in the Auau
Channel correspond to the seasonal thermocline in that region
(Pyle et al. 2016), which may serve as a location for turbulent
mixing and upwelling of deep nutrients. During the warmer
months (SeptemberNovember), however, the thermocline is
strongest (Pyle et al. 2016) and during this period vertical
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
12
mixing of nutrients from below may be limited. This pattern of
15
N depletion in the symbiont tissue with depth, while there is
no change in host tissue, is expected if corals are primarily feed-
ing on isotopically heavier allochthonous sources of particulate
organic matter (POM) at mesophotic depths (> 100 m).
In L. fragilis, POM feeding is possible because their gastro-
vascular system works like a ltration system. Water ow
enters through the mouth of L. fragilis and leaves the body
through microscopic pores in the oral epithelia. Moreover,
nematocysts are abundant and present in this species
(Schlichter 1991), suggesting that feeding by predation of
microzooplankton could be another important strategy for
nutrient acquisition in Leptoseris from Hawaii. Further
research is necessary to fully characterize the gastrovascular
system in this species and examine the isotopic signature of
zooplankton and POM in the mesophotic zone; this will help
to better understand the heterotrophic capacity of this impor-
tant genus across depths.
Conclusions
Species of Leptoseris in the mesophotic zone in Hawaii
have different associations with dinoagellate symbionts that
can contribute to the colonys capacity to acquire energy pho-
toautotrophically. Our results show that the distribution of
these species is a consequence of hostSymbiodinium speciali-
zation, physiological plasticity as well as photoadaptation
across species. However, species living at deeper depths also
showed a capacity to acquire energy heterotrophically, possi-
bly by lter feeding (Schlichter 1991) and/or feeding on detri-
tus and/or dissolved organic matter as reected by no change
in total lipid concentrations across depth and supported by
differences between host and Symbiodinum isotopic values.
These ndings serve as a foundation to study physiological
exibility in the mesophotic zone and help us to better under-
stand the ecology and resilience of these understudied but
highly important native ecosystems.
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Acknowledgments
We thank the Hawaii Undersea Research Laboratory (HURL) Pisces V
submersible and RCV-150 pilots, crew, and support staff, as well as the
crew of the R/V Kaimikai-o-Kanaloa, for access to these amazing depths.
This article includes results of research funded by the National Oceanic
and Atmospheric Administration (NOAA) Center for Sponsored Coastal
Ocean Research (Coastal Ocean Program) under award to the Bishop
Museum, NA07NOS4780187 and NA07NOS478190 to the University of
Hawaii and NA07NOS4780189 to the State of Hawaii; submersible sup-
port provided by NOAA Undersea Research Programs Hawaii HURL; and
funding from the NOAA Coral Reef Conservation Program research grants
program administered by HURL under award NA09OAR4300219, project
number HC08-06. Physiological analyses were funded by grants from the
National Science Foundation (NSF) Experimental Program to Stimulate
Competitive Research (EPSCoR, EPS-0903833) and Bio Oce (OCE-
0752604) both awarded to R.D.G. and by Villanova University to
L.J.R. Work by J.L.P.-G. was supported by NSF (IOS-1655682 awarded to
J.L.P.-G.) and work by M.S.R. was supported by the Division of Chemical
Sciences, Geosciences, and Biosciences, Ofce of Basic Energy Sciences,
Ofce of Science, U.S. Department of Energy, FWP number 449B, and
the Agriculture and Food Research Initiative Competitive Grant 2013-
67012-21272 from the USDA National Institute of Food and Agriculture.
Coral samples were collected under SAP permit 2009-72 from the Depart-
ment of Land and Natural Resources, State of Hawaii. However, the major-
ity of corals was collected in U.S. Federal Waters and did not require a
permit for collection. We thank F. Parrish for use of uorescence NightSea
equipment; B. Popp, A. Grottoli, J. Rooney, and K. Binsted for assistance in
collecting and processing samples during the cruise; T. M. Weatherby, T. S.
Christensen, F. Butler, and K. Selph for assistance in processing samples
after the cruise; and K. Puglise for overall support of the project. This is the
School of Ocean and Earth Science and Technology contribution 10662
and Hawaii Institute of Marine Biology Contribution 1754.
Author contribution statement
J.L.P.-G. and H.L.S. conceived, designed, and coordinated the study;
J.L.P.-G. drafted the manuscript; J.L.P.-G., H.L.S., and M.S.R. collected
eld data; J.L.P.-G., H.L.S., L.J.R., and C.J.B. carried out statistical and physi-
ological analyses; J.L.P.-G., H.L.S., M.S.R., L.J.R., C.J.B., R.R.B., R.D.G., and
C.M.S. wrote the manuscript. All authors gave nal approval for
publication.
Conict of Interest
None declared
Submitted 14 May 2018
Revised 17 December 2018
Accepted 25 February 2019
Associate editor: Núria Marbà
Padilla-Gamiño et al. Ecophysiology of mesophotic Leptoseris
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... The most studied aspect of the photobiology of scleractinian corals is the variability in the species of Symbiodiniaceae harbored by different corals (Lajeunesse et al., 2018), and how these different species may facilitate survival during exposure to climate change (Suggett et al., 2017). Additionally, Symbiodiniaceae genotypes also change in corals with increasing depth into the lower MCE (Bongaerts et al., 2015;Einbinder et al., 2016;Lesser et al., 2010;Padilla-Gamiño et al., 2019). Given the effects of reef topography and morphology on incident irradiances at the level of the colony , how does this translate into differences in primary productivity? ...
... But these results do not explain the observed phenotypic plasticity changes in morphology from hemispherical to plating morphology with increasing depth on many coral reefs (e.g., Lesser et al., 2010), or the phenotypic plasticity observed in agaricids with changing irradiances (Anthony et al., 2005;Hoogenboom et al., 2008). Additionally, a significant number of coral species with platelike morphologies exhibit extreme endemism in the lower mesophotic (e.g., Padilla-Gamiño et al., 2019). Another metric that captures photosynthetic performance under a range of irradiances is the minimum quantum requirements for photosynthesis, or 1/ϕ m . ...
... The differences in productivity between coral morphologies reported here do not consider the effects of depth-dependent changes, and endemism, known to occur in the community composition of the photoautotrophic endosymbiont (Symbiodiniaceae) of corals found along the shallow to mesophotic light gradient (Bongaerts et al., 2015;Lesser et al., 2010;Pochon et al., 2015;Ziegler et al., 2015). Additionally, several of these identified Symbiodiniaceae, primarily in the genus Cladosporium sp., are unique and can photoacclimatize a extremely low irradiances (Einbinder et al., 2016;Padilla-Gamiño et al., 2019). Lastly, the difference in the functional performance of an ideal versus a real sensor is very likely to be a function of the small-scale optics in the skeleton of different coral morphologies (Enríques et al., 2005(Enríques et al., , 2017Kühl et al., 1995;Wangpraseurt et al., 2012). ...
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• While the effects of irradiance on coral productivity are well known, corals along a shallow to mesophotic depth gradient (10–100 m) experience incident irradiances determined by the optical properties of the water column, coral morphology, and reef topography. • Modeling of productivity (i.e., carbon fixation) using empirical data shows that hemispherical colonies photosynthetically fix significantly greater amounts of carbon across all depths, and throughout the day, compared with plating and branching morphologies. In addition, topography (i.e., substrate angle) further influences the rate of productivity of corals but does not change the hierarchy of coral morphologies relative to productivity. • The differences in primary productivity for different coral morphologies are not, however, entirely consistent with the known ecological distributions of these coral morphotypes in the mesophotic zone as plating corals often become the dominant morphotype with increasing depth. • Other colony-specific features such as skeletal scattering of light, Symbiodiniaceae species, package effect, or tissue thickness contribute to the variability in the ecological distributions of morphotypes over the depth gradient and are captured in the metric known as the minimum quantum requirements. • Coral morphology is a strong proximate cause for the observed differences in productivity, with secondary effects of reef topography on incident irradiances, and subsequently the community structure of mesophotic corals.
... The fact that Symbiodiniaceae have been found at much greater depth in association with Antipatharians (396 m) [7], raises the possibility that they might also be present in scleractinian corals deeper than 165 m. Previous studies have genetically confirmed and identified endosymbiotic Symbiodiniaceae in Leptoseris down to 70 m on the Great Barrier Reef [8] and down to 125 m depth in Hawaii [9][10][11]. A specific host-Symbiodiniaceae association was reported between deep L. hawaiiensis and a Cladocopium from the ancestral C1 radiation [9][10][11], which represents a diverse group of Symbiodiniaceae commonly found in association with scleractinians on shallow coral reefs [8,9,12,13]. ...
... Previous studies have genetically confirmed and identified endosymbiotic Symbiodiniaceae in Leptoseris down to 70 m on the Great Barrier Reef [8] and down to 125 m depth in Hawaii [9][10][11]. A specific host-Symbiodiniaceae association was reported between deep L. hawaiiensis and a Cladocopium from the ancestral C1 radiation [9][10][11], which represents a diverse group of Symbiodiniaceae commonly found in association with scleractinians on shallow coral reefs [8,9,12,13]. To better understand how scleractinian corals can survive so far away from their presumed light optimum, it is critical to determine if these deep specimens (1) maintain their association with photosynthetic algae and/or (2) if their survival in the deepest mesophotic coral ecosystems requires a shift in their microbial communities, including Symbiodiniaceae and other microorganisms such as endolithic algae and bacteria. ...
... Previous studies have genetically confirmed and identified endosymbiotic Symbiodiniaceae in Leptoseris down to 70 m on the Great Barrier Reef [8] and down to 125 m depth in Hawaii [9][10][11]. A specific host-Symbiodiniaceae association was reported between deep L. hawaiiensis and a Cladocopium from the ancestral C1 radiation [9][10][11], which represents a diverse group of Symbiodiniaceae commonly found in association with scleractinians on shallow coral reefs [8,9,12,13]. To better understand how scleractinian corals can survive so far away from their presumed light optimum, it is critical to determine if these deep specimens (1) maintain their association with photosynthetic algae and/or (2) if their survival in the deepest mesophotic coral ecosystems requires a shift in their microbial communities, including Symbiodiniaceae and other microorganisms such as endolithic algae and bacteria. ...
Article
The symbiosis between scleractinian corals and photosynthetic algae from the family Symbiodiniaceae underpins the health and productivity of tropical coral reef ecosystems. While this photosymbiotic association has been extensively studied in shallow waters (<30 m depth), we do not know how deeper corals, inhabiting large and vastly underexplored mesophotic coral ecosystems, modulate their symbiotic associations to grow in environments that receive less than 1% of surface irradiance. Here we report on the deepest photosymbiotic scleractinian corals collected to date (172 m depth), and use amplicon sequencing to identify the associated symbiotic communities. The corals, identified as Leptoseris hawaiiensis, were confirmed to host Symbiodiniaceae, predominantly of the genus Cladocopium, a single species of endolithic algae from the genus Ostreobium, and diverse communities of prokaryotes. Our results expand the reported depth range of photosynthetic scleractinian corals (0–172 m depth), and provide new insights on their symbiotic associations at the lower depth extremes of tropical coral reefs.
... In addition to changes in the bulk underwater light environment, there are additional changes in the light environment based on reef topography that interact with coral morphology to affect their productivity as depth changes [13,14]. And on smaller spatial scales, we now know that coral skeletal microarchitecture has a significant effect on the ability of scleractinian corals to acclimatize to low irradiances [15][16][17][18][19]. Studies on the photophysiology of corals from mesophotic habitats show both a decrease in productivity with increasing depth [12,14,20] and increased photoacclimatization when exposed to decreasing and very low (i.e., below the compensation point) irradiances from shallow to mesophotic depths [10,[21][22][23][24][25]. ...
... A similar pattern was observed for the SIA analysis of the ubiquitous, light-limited, Leptoseris spp. complex in the lower mesophotic (i.e., 60-132 m) of the Au'au Channel (Maui, Hawai'i), where irradiances decreased from ~55-7 µmol quanta m −2 s −1 [23]. The data for M. cavernosa also agrees with the isotopic niche width (i.e., SIBER) analysis of δ 13 C and δ 15 N values for this coral and support an increasing dependence on heterotrophy along the shallow to mesophotic depth gradient. ...
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Studies on the trophic ecology of scleractinian corals often include stable isotope analyses of tissue and symbiont carbon and nitrogen. These approaches have provided critical insights into the trophic sources and sinks that are essential to understanding larger-scale carbon and nitrogen budgets on coral reefs. While stable isotopes have identified most shallow water (<30 m) corals as mixotrophic, with variable dependencies on autotrophic versus heterotrophic resources, corals in the mesophotic zone (~30–150 m) transition to heterotrophy with increasing depth because of decreased photosynthetic productivity. Recently, these interpretations of the stable isotope data to distinguish between autotrophy and heterotrophy have been criticized because they are confounded by increased nutrients, reverse translocation of photosynthate, and changes in irradiance that do not influence photosynthate translocation. Here we critically examine the studies that support these criticisms and show that they are contextually not relevant to interpreting the transition to heterotrophy in corals from shallow to mesophotic depths. Additionally, new data and a re-analysis of previously published data show that additional information (e.g., skeletal isotopic analysis) improves the interpretation of bulk stable isotope data in determining when a transition from primary dependence on autotrophy to heterotrophy occurs in scleractinian corals.
... Although many coral-Symbiodiniaceae associations are disrupted when symbionts are maintained in dark or dim light conditions and are photosynthetically inefficient (Tolleter et al., 2013;Baker et al., 2018;Morris et al., 2019;Rädecker et al., 2021), some corals can maintain a large population of symbionts within their tissues (Wagner et al., 2011;Polinski and Voss, 2018;Padilla-Gamiño et al., 2019). This is true for mesophotic tropical corals but also for many temperate coral species. ...
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Coral bleaching, the breakdown of the coral-Symbiodiniaceae association has been identified as a major cause of coral reef decline worldwide. When symbiont functions are compromised, corals receive fewer photosynthetic products from their symbionts and suffer significant starvation along with changes in nutrient cycling. Not all coral species are equally susceptible to bleaching, but despite intensive research, our understanding of the causes for coral bleaching remains incomplete. Here, we investigated nutrient exchange between host and symbionts of two coral-Symbiodiniaceae associations that are differentially susceptible to bleaching when maintained under heterotrophy in the dark. We followed the fate of heterotrophic nutrients using bulk isotope and compound-specific (amino acid) isotope analyses. We showed that symbiont starvation is a major cause of symbiotic breakdown in the dark. While Oculina patagonica transferred almost all heterotrophically-acquired amino acids within two weeks in the dark to its symbionts and did not bleach, Turbinaria reniformis, transferred only 2 amino acids to its symbionts after 4 weeks in the dark, and experienced significant bleaching. These results pave the way for future studies on the role of nutrition in coral stress response and the importance of maintaining a healthy symbiont population to avoid coral bleaching.
... Overall, the rates of oxygen production (photosynthesis rates) and DIC assimilation by Symbiodiniaceae associated with both Leptoseris and mesophotic Sinularia species were ca. 10 times lower than the rates measured for most shallow coral-dinoflagellate associations (Tables 3 and 4). Such difference can be due to the Symbiodiniaceae species associated to mesophotic corals (Pochon et al. 2015;Padilla-Gamiño et al. 2019), to lower symbiont densities (Kaiser et al. 1993), to a light limitation of symbiont activity, or to different physiological state and/or nutritional behavior of the symbiotic associations at mid to lower mesophotic depths. Although C translocation rates from symbionts to host could not be estimated in this study, the higher C content (per mg AFDW) of Symbiodiniaceae compared to the host tissue in both Leptoseris or Sinularia further suggests a higher retention of C in symbionts for their own needs, and a limited nutritional mutualism in mesophotic symbioses. ...
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Mesophotic coral ecosystems (30–150 m depth) present a high oceanic biodiversity, but remain one of the most understudied reef habitats, especially below 60 m depth. Here, we have assessed the rates of photosynthesis and dissolved inorganic carbon (DIC) and nitrogen (DIN) assimilation by Symbiodiniaceae associated with four soft coral species of the genus Sinularia and two stony coral species of the genus Leptoseris collected respectively at 65 and 80–90 m depth in the Gulf of Eilat. Our study demonstrates that both Leptoseris and Sinularia species have limited autotrophic capacities at mid‐lower mesophotic depths. DIC and DIN assimilation rates were overall ~ 10 times lower compared to shallow corals from 10 m depth in the same reef. While Leptoseris symbionts transferred at least 50% of the acquired nitrogen to their host after 8‐h incubation, most of the nitrogen was retained in the symbionts of Sinularia. In addition, the host tissue of Sinularia species presented a very high structural carbon to nitrogen ratio (C : N) compared to Leptoseris or to the shallow coral species, suggesting nitrogen limitation in these mesophotic soft corals. The limited capacity of soft coral symbionts to acquire DIN and transfer it to the coral animal, as well as the high C : N ratios, might explain the scarcity of symbiotic soft corals at mid‐lower mesophotic depths compared to their prevalence in the shallower reef. Overall, this study highlights the significance of DIN for the distribution of the Cnidarian‐ Symbiodiniaceae association at mesophotic depth.
... It is also hypothesized that reefs may find refuge from thermal stress in the surface waters by migrating to deeper habitats where temperatures are lower (Riegl and Piller, 2003;Bongaerts et al., 2010;Bridge et al., 2013;Padilla-Gamiño et al., 2019); this has occurred to some extent in Pulley Ridge, though recent surveys have found that these deep water hermatypic corals are not surviving (Slattery et al., 2018). Deeper water, mesophotic reefs have distinct communities and ecosystems when compared to shallow water reefs (e.g., Bongaerts et al., 2010;Pereira et al., 2018;Rocha et al., 2018); thus these deeper habitats likely would make poor refuges for shallow-water reef species. ...
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Shallow water coral reefs and deep sea coral communities are sensitive to current and future environmental stresses, such as changes in sea surface temperatures (SST), salinity, carbonate chemistry, and acidity. Over the last half-century, some reef communities have been disappearing at an alarming pace. This study focuses on the Gulf of Mexico, where the majority of shallow coral reefs are reported to be in poor or fair condition. We analyze the RCP8.5 ensemble of the Community Earth System Model v1.2 to identify monthly-to-decadal trends in Gulf of Mexico SST. Secondly, we examine projected changes in ocean pH, carbonate saturation state, and salinity in the same coupled model simulations. We find that the joint impacts of predicted higher temperatures and changes in ocean acidification will severely degrade Gulf of Mexico reef systems by the end of the twenty-first century. SSTs are likely to warm by 2.5–3°C; while corals do show signs of an ability to adapt toward higher temperatures, current coral species and reef systems are likely to suffer major bleaching events in coming years. We contextualize future changes with ancient reefs from paleoclimate analogs, periods of Earth's past that were also exceptionally warm, specifically rapid “hyperthermal” events. Ancient analog events are often associated with extinctions, reef collapse, and significant ecological changes, yet reef communities managed to survive these events on evolutionary timescales. Finally, we review research which discusses the adaptive potential of the Gulf of Mexico's coral reefs, meccas of biodiversity and oceanic health. We assert that the only guaranteed solution for long-term conservation and recovery is substantial, rapid reduction of anthropogenic greenhouse gas emissions.
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