Article

High light alongside elevated PCO2 alleviates thermal depression of photosynthesis in a hard coral (Pocillopora acuta)

Abstract and Figures

The absorbtion of human-emitted CO2 by the oceans (elevated PCO2) is projected to alter the physiological performance of coral reef organisms by perturbing seawater chemistry (i.e. ocean acidification). Simultaneously, greenhouse gas emissions are driving ocean warming and changes in irradiance (through turbidity and cloud cover), which have the potential to influence the effects of ocean acidification on coral reefs. Here, we explored whether physiological impacts of elevated PCO2 on a coral–algal symbiosis (Pocillopora acuta–Symbiodiniaceae) are mediated by light and/or temperature levels. In a 39 day experiment, elevated PCO2 (962 versus 431 µatm PCO2) had an interactive effect with midday light availability (400 versus 800 µmol photons m−2 s−1) and temperature (25 versus 29°C) on areal gross and net photosynthesis, for which a decline at 29°C was ameliorated under simultaneous high-PCO2 and high-light conditions. Light-enhanced dark respiration increased under elevated PCO2 and/or elevated temperature. Symbiont to host cell ratio and chlorophyll a per symbiont increased at elevated temperature, whilst symbiont areal density decreased. The ability of moderately strong light in the presence of elevated PCO2 to alleviate the temperature-induced decrease in photosynthesis suggests that higher substrate availability facilitates a greater ability for photochemical quenching, partially offsetting the impacts of high temperature on the photosynthetic apparatus. Future environmental changes that result in moderate increases in light levels could therefore assist the P. acuta holobiont to cope with the ‘one–two punch’ of rising temperatures in the presence of an acidifying ocean.
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RESEARCH ARTICLE
High light alongside elevated P
CO
2
alleviates thermal depression
of photosynthesis in a hard coral (Pocillopora acuta)
Robert A. B. Mason
1,2,
*, Christopher B. Wall
1,3
, Ross Cunning
1,4
, Sophie Dove
2
and Ruth D. Gates
1
ABSTRACT
The absorbtion of human-emitted CO
2
by the oceans (elevated P
CO
2
)
is projected to alter the physiological performance of coral reef
organisms by perturbing seawater chemistry (i.e. ocean acidification).
Simultaneously, greenhouse gas emissions are driving ocean
warming and changes in irradiance (through turbidity and cloud
cover), which have the potential to influence the effects of ocean
acidification on coral reefs. Here, we explored whether physiological
impacts of elevated P
CO
2
on a coralalgal symbiosis (Pocillopora
acutaSymbiodiniaceae) are mediated by light and/or temperature
levels. In a 39 day experiment, elevated P
CO
2
(962 versus 431 µatm
P
CO
2
) had an interactive effect with midday light availability (400
versus 800 µmol photons m
2
s
1
) and temperature (25 versus 29°C)
on areal gross and net photosynthesis, for which a decline at 29°C
was ameliorated under simultaneous high-P
CO
2
and high-light
conditions. Light-enhanced dark respiration increased under
elevated P
CO
2
and/or elevated temperature. Symbiont to host cell
ratio and chlorophyll aper symbiont increased at elevated
temperature, whilst symbiont areal density decreased. The ability of
moderately strong light in the presence of elevated P
CO
2
to alleviate
the temperature-induced decrease in photosynthesis suggests that
higher substrate availability facilitates a greater ability for
photochemical quenching, partially offsetting the impacts of high
temperature on the photosynthetic apparatus. Future environmental
changes that result in moderate increases in light levels could
therefore assist the P. acuta holobiont to cope with the onetwo
punchof rising temperatures in the presence of an acidifying ocean.
KEY WORDS: Scleractinia, Irradiance, Multiple stressors, Ocean
acidification, Ocean warming, Symbiodiniaceae
INTRODUCTION
Atmospheric carbon dioxide concentrations are increasing as a result
of human activities and the burning of fossil fuels. The oceans have
absorbed two-thirds of anthropogenically emitted CO
2
,andthe
resulting perturbation of seawater pH and carbonate chemistry (i.e.
ocean acidification) is an unprecedented threat to global marine life
(Kleypas et al., 1999). The elevation of the partial pressure of CO
2
in
seawater (P
CO
2
) results in an increase in proton and bicarbonate ion
concentrations (Miller and Wheeler, 2012), while decreasing carbonate
concentration and the aragonite saturation state (Ω
arag
) (Miller and
Wheeler, 2012). In coralalgal symbioses, the physiological impacts of
elevated P
CO
2
have included declines in adult and juvenile calcification
(Albright and Langdon, 2011; Cohen and Holcomb, 2009; Zunino
et al., 2017), symbiont density (Kaniewska et al., 2012) and lipid
biomass (Wall et al., 2017), altered protein metabolism (Edmunds
and Wall, 2014) and photophysiology (Iguchi et al., 2012; Noonan and
Fabricius, 2016), and compromised sexual reproduction and
recruitment (Albright et al., 2010).
Studies of the impacts of elevated P
CO
2
on corals have most
commonly focused on calcification; however, impacts on other
aspects of coralalgal holobiont physiology are often more salient.
For instance, a broad survey of physiological responses in the coral
Pocillopora acuta demonstrated robustness of calcification under
961 μatm P
CO
2
at low- and high-light conditions and found no
changes in the density of the intracellular dinoflagellate symbionts
(Symbiodiniaceae), total chlorophyll (a+c
2
) concentrations or total
biomass (Wall et al., 2017). However, declines (of up to 20%) in
several forms of energy storage (lipids, protein and total energy
content) were observed (Wall et al., 2017). Owing to the central role
that the coralalgal symbiosis plays in energy acquisition and
carbonate deposition in coral reefs, even moderate impacts on its
physiology may result in significant changes to these ecosystems.
Physiological robustness or vulnerability to elevated P
CO
2
by itself is
noteworthy; however, it is important to recognise that elevated P
CO
2
will
co-occur alongside other environmental impacts. The impacts of climate
change in increasing seawater temperature is well recognised (Hoegh-
Guldberg et al., 2014), and the weather conditions that cause heat stress
at coral reefs usually also cause very high levels of insolation (Skirving
and Guinotte, 2000). However, climate change will have other direct
impacts on light levels at reefs. Climate change is predicted to affect
cloud cover (Schneider et al., 2019), atmospheric light attenuation
(Haywood et al., 2011) and seawater turbidity [via sea level rise (Ogston
and Field, 2010) and intensification of both dry spells and precipitation
(Fischer and Knutti, 2015)]. Expected decreases in anthropogenic
aerosol emissions will also affect irradiance as regulations for reducing
air pollution are implemented globally (Rosenfeld et al., 2019; Sato and
Suzuki, 2019). These multiple pathways of climate impact will cause
irradiance to increase at some reefs and decrease at others, influencing
the impact of warming on coral photoinhibition.
Indeed, interactive effects of light with elevated P
CO
2
,temperature
with elevated P
CO
2
, or light with temperature on coralalgal holobiont
physiology have been empirically demonstrated with outcomes that
range from antagonistic to synergistic. For instance, Bahr et al. (2016)
found that elevated P
CO
2
reduced P. damicornis calcification;
however, elevated P
CO
2
also remedied the negative effect of high
temperature on calcification seen at present-day P
CO
2
levels (Bahr
et al., 2016). Light and temperature also interact to shape symbiont
photobiology in hospite (Ban et al., 2014), and light availability
influences the susceptibility of coral calcification to P
CO
2
effects in
Received 10 February 2020; Accepted 12 August 2020
1
Hawaii Institute of Marine Biology, School of Ocean and Earth Science and
Technology, University of HawaiiatMa
̄noa, PO Box 1346, Ka
̄neohe, HI 96744,
USA.
2
ARC Centre of Excellence for Coral Reef Studies, and Centre for Marine
Science, School of Biological Sciences, University of Queensland, St Lucia , QLD
4072, Australia.
3
Pacific Biosciences Research Center, University of Hawaiʻiat
Ma
̄noa, Honolulu, HI 96822, USA.
4
Daniel P. Haerther Center for Conservation and
Research, John G. Shedd Aquarium, Chicago, IL 60605, USA.
*Author for correspondence (robert.mason1@uqconnect.edu.au)
R.A.B.M., 0000-0002-2725-2449; C.B.W., 0000-0002-7164-3201; R.C., 0000-
0001-7241-1181; S.D., 0000-0003-1823-8634
1
© 2020. Published by The Company of Biologists Ltd
|
Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
juvenile (Dufault et al., 2013) and adult corals (Suggett et al., 2013).
Together, these lines of evidence suggest that combinations of light
and temperature will mediate how the coralalgal symbiosis will
respond physiologically to rising seawater P
CO
2
.
Owing to the forecast upsurge in mass coral bleaching events
under climate change, the combined effects of P
CO
2
, light and
temperature on symbiont densities in corals is of particular interest.
Anlauf et al. (2011) documented a synergistic impact of temperature
and P
CO
2
on symbiont densities in new coral recruits, wherein
elevated P
CO
2
ameliorated the decrease in symbionts caused by high
temperature stress. Elevated P
CO
2
synergistically lowered coral
luminance (a proxy of bleaching) in two coral species under
naturally high irradiances (ca. 1000 µmol photons m
2
s
1
)
(Anthony et al., 2008; but see Wall et al., 2014). Meta-analysis
has shown that, in general, symbiont densities in corals decline
under elevated P
CO
2
, but there is not yet broad evidence for an
interaction between high temperature and elevated P
CO
2
in causing
symbiont loss (Mason, 2018b).
Here, we explore the impact of simultaneous alteration of P
CO
2
,
light and temperature on a pocilloporid coral (P. acuta)inafactorial
design to assess the influence of ecologically relevant scenarios for
multiple stressors on performance of the coralalgal holobiont. We
measured a range of physiological parameters on which P
CO
2
, light
and temperature are thought to have a major influence in the current
understanding of coralalgal holobiont physiology (mechanisms
summarised in Table 1): symbiont cell densities, chlorophyll a(chl a)
concentrations, respiration rates, light-enhanced dark respiration,
photosynthesis, photosynthesis to respiration (P/R) ratio and
symbiont to host (S/H) cell ratio. Given the known or theoretical
impacts of each stressor in isolation (Table 1), we hypothesised that
the combined stressors of elevated P
CO
2
, irradiance differences and
elevated temperature will have an interactive effect on each aspect of
physiology of the P. acuta holobiont. For symbiont densities, where
single-stressor effects are the most clear-cut (Table 1), we
hypothesised that this variable will see its most severe decline under
the combination of high light, elevated P
CO
2
and high temperature.
MATERIALS AND METHODS
Coral collection
Whole colonies of Pocillopora acuta (Lamarck 1816) were collected
on 13 and 29 October 2014 (n=5 and 3 colonies, respectively) at 0.2
1.5 m depth, from the windward reef of Moku o LoeinKāneohe
Bay, Oahu, HI, USA. Colonies were identified as P. acut a through
the prominent pigmented rings around polyps and acute branch tips
that distinguish this species from the morphologically similar
P. damicornis (Schmidt-Roach et al., 2014). Collections were
performed in accordance with permitting guidelines of the Hawaii
Department of Land and Natural Resources Division of Aquatic
Resources under Special Activity Permit 20158. At the Hawaii
Institute of Marine Biology, colonies were fragmented into nubbins
(<5 cm), mounted onto bases (as per Wall et al., 2017) and
maintained for 2137 days in outdoor aquaria under 60% shade
cloth (daily peak of 200300 µmol photons m
2
s
1
: Putnam et al.,
2016) in flow-through seawater pumped from Kāneohe Bay and
cooled to 26.05±0.01°C (mean±s.e.m., n=4869). Nubbins were then
distributed among 24 indoor tanks (n=8 nubbins per tank with one
from each colony). This sample size exceeds that used in most coral
tank experiments (3 to 6 per tank), achieving a simulated power of
80% in the detection of a three-factor interaction on symbiont
densities at an effect size of ca. 0.36×10
6
cells cm
2
(see online
code). Nubbins were maintained at 25.78±0.04°C (n=168) under two
light regimes (described below) for a tank acclimation period of
25 days prior to the commencement of the experiment. During this
period (21 November 2014 to 15 December 2014), the differential
between the ambient P
CO
2
and the high P
CO
2
treatment tanks was
partly introduced (Fig. S1). Each tank also contained 14 additional
P. acut a nubbins for other studies that were removed on day 32 of the
experiment. Corals were not given supplemental food, but dietary
items (dissolved organic matter, microbes and plankton <100 µm in
size) were present in the flow-through seawater.
Experimental design
CO
2
treatments (431 and 962 µmol P
CO
2
) reflect present-day P
CO
2
and
end-of-century ocean acidification under Representative Concentration
Pathway 8.5 (Meinshausen et al., 2011). The high light treatment
(15.7 mol photons m
2
day
1
) sits within the range of insolation
(7-day moving average) seen during the 20142015 December
JanuaryFebruary (DJF) period at Moku o Loeat2mdepth.Thelow
light treatment (7.5 mol photons m
2
day
1
) reflects lower light
conditions seen in the more turbid northern Kāneohe Bay during the
20142015 DJF period (Cunning et al., 2016). Temperature treatments
(25°C and 29°C) reflect a non-stressful sea temperature (near the
DJF climatological mean sea surface temperature) and a stressful
temperature (2°C in excess of the maximum monthly mean) for the
Hawaiian Islands (NOAA Coral Reef Watch, 2019).
Our exposure of P. acuta used a staged introduction of multiple
stressors. Four treatments, consisting of two P
CO
2
levels crossed
with two light levels, were administered for 39 days (16 December
2014 to 23 January 2015). During the final 7 days of the experiment,
each treatment was divided into two temperature levels (design
illustrated in Fig. S2). Twelve 44.8 litre tanks received
400 µmol photons m
2
s
1
(LL) at the midday light maximum
and 12 received 800 µmol photons m
2
s
1
(HL) at the midday light
maximum (Aqua Illuminations Sol Light Emitting Diode lamps; C2
Development Inc., Ames, IA, USA). The photoperiod (12 h:12 h
light:dark) consisted of sunrise at 05:00 h, 5 h of linear increase in
light intensity, stable peak light from 10:00 to 12:00 h, 5 h of linear
decrease in light intensity, and sunset at 17:00 h. During the first
4 days of the acclimation period, a longer duration of peak
light during the daytime was used (07:0015:00 h), with possible
paling of tissue observed in the high light treatment. Each tank
received flow-through seawater at a mean±s.e.m. of 431±8 µatm
P
CO
2
(ambient/low, LCO
2
)or962±27µatmP
CO
2
(high, HCO
2
)
(Table 2), at a flow rate of ca. 1.5 l min
1
. The procedures used for
List of symbols and abbreviations
chl achlorophyll a
CTAB cetyl trimethylammonium bromide
DR dark respiration
HCO
2
high P
CO
2
HL high light
HT high temperature
LCO
2
ambient/low P
CO
2
LEDR light-enhanced dark respiration
LL low light
LT low temperature
P/R photosynthesis to respiration ratio
P
CO
2
partial pressure of carbon dioxide
P
gross
gross photosynthesis
pH
T
pH on the total scale
P
net
net photosynthesis
PSII photosystem II
qPCR quantitative polymerase chain reaction
S/H symbiont to host cell ratio
2
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
Table 1. Mechanisms by which elevated light, elevated temperature and elevated P
CO2
could affect [increase (), decrease () or no change ()] the physiology of coralalgal symbioses
Aspect of physiology Stressor
Direction of
change in
physiology Mechanism References
Respiration rate High P
CO
2
Reduced seawater pH may interfere with the disposal of protons from respiration Jokiel (2011), Kaniewska et al. (2012), Mackey et al.
(2015)
Elevated metabolism as a result of increased cost of cellular processes or growth under
elevated P
CO
2
McCulloch et al. (2012)
High light Enhances energy budget, alleviates metabolic depression Davies (1980), Jacobson et al. (2016), Rogers (1979)
,Photobleaching, leading to reduced energy income and metabolic depression Tremblay et al. (2012), Yakovleva and Hidaka (2004)
High temperature Kinetic rate of respiratory reactions will increase Gillooly et al. (2001)
Reduced energy acquisition and expenditure due to bleaching; thermally induced
mitochondrial degradation
Dunn et al. (2012)
Light-enhanced dark
respiration rate
High P
CO
2
Decreased photorespiration; reduced seawater pH impacts proton disposal Rowan et al. (1996), Mackey et al. (2015)
Greater photosynthate availability drives respiration following illumination Crawley et al. (2010)
High light Increased availability of photosynthate post illumination Stokes et al. (1990)
High temperature ,As for respiration
Symbiont density per unit
area
High P
CO
2
,Proliferation of symbiont cells initially occurs owingto enhanced photosynthesis; however,
at extremes of light and/or temperature, CO
2
demand outpaces supply, leading to
symbiont loss
Wooldridge (2009)
High light Mild decrease during photoacclimation to high light Muller et al. (2009)
Substantial decrease under photobleaching Krämer et al. (2013)
High temperature Apoptosis, shedding of zooxanthellate host cells, or reactive oxygen species production Nii and Muscatine (1997), Gates et al. (1992), Tchernov
et al. (2011), Dunn et al. (2002), Weis (2008)
Heterotrophy or lipid stores may postpone or prevent bleaching Anthony et al. (2009)
Chl acontent per cell High P
CO
2
Elevated P
CO
2
increases photoacclimation to low light Crawley et al. (2010)
High light Long-term decrease in chl aper cell as part of photoacclimation to high light Cohen and Dubinsky (2015)
Photoinhibition and consequent pigment loss Hoegh-Guldberg (1999)
High temperature Symbiont loss results in decreased self-shading, increased investment in pigment Caroselli et al. (2015)
Heat-impairment of PSII leads to reactive oxygen damage to pigments Hoegh-Guldberg (1999)
Photosynthesis rate
(area-standardised)
High P
CO
2
Increased bicarbonate and CO
2
(aq) availability Mackey et al. (2015)
Inefficient carbon-concentrating mechanisms in some coral species Noonan and Fabricius (2016)
Symbiont loss causes photophysiological dysfunction in those remaining in tissue Anthony et al. (2008)
High light Increased availability of light drives increased photosynthesis Dubinsky and Falkowski (2011)
Photoinhibition at very high light levels Hoegh-Guldberg (1999)
Increase in quenching via photoprotective mechanisms Gorbunov et al. (2001)
High temperature Inhibits the protein synthesis-based repair of photo-damage to PSII and causes
photoinhibition, damage to thylakoid membranes
Iglesias-Prieto et al. (1992), Iglesias-Prieto (1995),
Takahashi et al. (2004); Warner et al. (1996); Warner
et al. (1999)
Symbiont to host cell ratio High P
CO
2
,As for symbiont density
High light As for symbiont density
High temperature ,Initial increase under moderate warming; decreases at high temperature Cunning and Baker (2013)
That some stressors elicit both a positive and a negative effect on physiology is often because moderate doses of that stressor may be beneficial, and high doses (that exceed physiological tolerances) detrimental.
3
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
modifying P
CO
2
levels and for biweekly measurements of tank
carbonate chemistry are reported in Wall et al. (2017). During the
first stage (32 days), corals in each CO
2
×light treatment
(n=6 tanks treatment
1
) were maintained at seasonally ambient
conditions of 24.59±0.06°C (mean±s.e.m., n=153). For the final
7 days, each CO
2
×light treatment was split, with three tanks kept at
24.59±0.06°C (n=11; LT) and three tanks raised to 29.05±0.22°C
(n=11; HT), using immersion and in-line aquarium heaters.
Alkalinity measurements performed on experimental treatment
water at intervals over one 24 h period indicated diel variations in
P
CO
2
of ca. 150 and 400 µatm in the ambient P
CO
2
and elevated
P
CO
2
treatments, respectively, with minima during midday (Fig.
S3). As experimental tanks were downstream from the header
sumps (where P
CO
2
was controlled) and the residence time
(duration to turnover 99% of water; Escobal, 1996) in each tank
was moderate (137 min), diel P
CO
2
fluctuations in each tank were
likely a result of net respiration at night and net photosynthesis
during the day. This compares with diel fluctuations of 200
300 µatm P
CO
2
on the Kāneohe Bay barrier reef (Shamberger
et al., 2011).
Respirometry
Respirometry measurements were performed on four nubbins per
tank on days 36 and 37 (non-heated treatments) and days 38 and 39
(heated treatments), in two magnetically stirred 260 ml cylindrical
Perspex chambers containing filtered seawater (0.25 µm) from the
P
CO
2
treatment relevant to each nubbin. To maintain the relevant
temperature, chambers were controlled to 24.77±0.03°C (n=45) or
29.68±0.02°C (n=44) via immersion in a water bath. Following a
period of low light acclimation (30 min at <10 µmol photons
m
2
s
1
), each nubbin was incubated for 10 min in darkness
(measuring dark respiration, DR), illuminated for 10 min at the
midday light level of the relevant treatment (measuring daytime net
photosynthesis, P
net
),exposedtodarknessagainfor10 min
(measuring light-enhanced dark respiration, LEDR) and then
repatriated to its original treatment tank. Intra-chamber oxygen
concentrations were determined at 1 s logging intervals with a Fospor
fibre optic probe on a Neofox Oxygen Sensing System (Ocean
Optics, Dunedin, FL, USA). Gross photosynthesis under midday
light (P
gross
) was calculated as P
net
LEDR (assuming no respiration
of energy acquired via heterotrophy, and that LEDR approximates
light respiration) (but see Stokes et al., 1990). Photosynthesis and
respiration measurements were normalised to coral surface area. The
ratio of photosynthesis to respiration (P/R ratio) was calculated by
dividing P
net
by DR.
Symbiont density, chl aand surface area
On the final day of the experiment, nubbins were snap-frozen in
liquid nitrogen and stored at 80°C. Tissue was airbrushed off
thawed nubbins with a pressurised stream of buffer at 4°C
(0.4 mol l
1
NaCl, 0.05 mol l
1
EDTA) and the slurry was
processed for 10 s with a T25 500 W variable speed homogeniser
(IKA Works Inc., Wilmington, NC, USA). The presence of planula
larvae (planulae), visible in the coral tissue as it was being removed,
was noted when observed. Symbiont cells were pelleted (1 ml of
slurry centrifuged at 4500 gfor 5 min), extracted in 100% acetone
(48 h at 20°C), and chl awas determined as per Jeffrey and
Humphrey (1975). Chl awas normalised to coral surface area (chl a
density) and to symbiont cell count (chl aper symbiont). Symbiont
densities were determined by counts in a Neubauer haemocytometer
chamber (n=24) (Reichert Inc., Buffalo, NY, USA) and normalised
to coral surface area. Coral surface areas were estimated by double
wax dipping (Vytopil and Willis, 2001).
S/H cell ratios
DNA was extracted from 300 µl of tissue slurry using a CTAB
chloroform protocol (dx.doi.org/10.17504/protocols.io.dyq7vv).
Symbiont to host (S/H) cell ratios were determined by quantitative
PCR (qPCR) on a StepOnePlus Real-Time PCR machine (Applied
Biosystems, Foster City, CA, USA). We used taxon-specific primers
that separately target the actin gene of dinoflagellate symbionts within
Symbiodiniaceae clade C (genus Cladocopium) and clade D (genus
Durusdinium)andP. acut a ( primers and qPCR protocol as per
Cunning and Baker, 2013). Clades C and D are the only clades
typically detected in the genus Pocillopora (Cunning et al., 2013;
Pochon et al., 2010; Stat et al., 2008, 2015; M. Stat, personal
communication). qPCR reactions were excluded if they had a cycle
threshold (C
T
) within three cycles of the C
T
(if any) observed in the
respective negative control. We corrected the S/H cell ratios with the
symbiont to host DNA extraction efficiency ratio for CTAB
chloroform extraction, 0.828 (Cunning and Baker, 2013). We
assumed the same actin copy number (three) as measured in
P. damicornis by these authors owing to its close taxonomic affinity
to P. acuta. Actin gene copy numbers for clades C and D were
Table 2. Seawater physical and chemical parameters
Treatment
PAR
(µmol photons
m
2
s
1
)
Temperature
a
(°C)
Temperature
b
(°C) pH
T
TA
(µmol kg
1
)
P
CO
2
(µatm)
HCO
3
(µmol kg
1
)
CO
32
(µmol kg
1
)Ω
arag
LCO
2
HLHT 800 24.6±0.2 28.8±0.2 8.01±0.01 2174±4 420±17 1702±16 190±6 3.03±0.10
LCO
2
HLLT 800 24.6±0.2 24.6±0.1 8.02±0.01 2177±4 410±16 1708±13 189±6 3.01±0.09
LCO
2
LLHT 400 24.8±0.2 29.8±0.2 7.99±0.01 2173±4 444±16 1716±13 184±5 2.94±0.08
LCO
2
LLLT 400 24.5±0.2 24.5±0.1 7.99±0.01 2176±4 449±13 1735±10 178±4 2.82±0.06
HCO
2
HLHT 800 24.5±0.2 29.4±0.3 7.71±0.03 2179±6 974±72 1912±19 108±7 1.72±0.11
HCO
2
HLLT 800 24.4±0.2 24.7±0.3 7.72±0.02 2181±6 919±44 1916±12 107±5 1.70±0.08
HCO
2
LLHT 400 24.9±0.2 28.3±0.4 7.70±0.02 2179±5 984±47 1916±13 106±5 1.70±0.08
HCO
2
LLLT 400 24.3±0.2 24.5±0.1 7.71±0.02 2181±5 960±53 1917±16 107±6 1.69±0.10
Values are expressed as means±s.e.m. pH
T
(pH on the total scale), temperature (°C), total alkalinity (TA) and salinity were measured as per Wall et al. (2017).
P
CO
2
,HCO
3
concentration, CO
32
concentration and Ω
arag
(aragonite saturation state) were calculated from pH
T
, TA, salinity and temperature using the R
package seacarb. Treatments are low and high P
CO
2
(LCO
2
,HCO
2
), low and high light (LL, HL), and low and high temperatures (LT, HT). Seawater chemistry
parameters (pH
T
,TA,P
CO
2
,HCO
3
,CO
32
,Ω
arag
) had sample sizes of n=2324 for all treatments, except for the treatments HCO
2
HLLT and HCO
2
HLHT
(n=16). PAR, photosynthetically active radiation at midday.
a
Temperature (°C) at time of water sampling during days 132 at sample size n=2021, except for HCO
2
HLHT and HCO
2
HLLT (n=14).
b
Temperature (°C) at time of water sampling during days 3339 (n=23).
4
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
estimated using a singular value decomposition method (Cunning
et al., 2016).
Statistical analysis
Differences between the two CO
2
treatments for carbonate chemistry
variables (P
CO
2
,pH
T
and total alkalinity) were assessed viat-tests. To
explore tank effects on these variables, one-way ANOVAs were
performed to compare all tanks within each of the two CO
2
treatments. Analyses of physiological responses (symbiont density,
chl aper symbiont, chl adensity, P
net
,P
gross
, DR, LEDR, P/R and S/
H ratios) were performed via mixed-effects models in the package
lme4 (Bates et al., 2015) in R (https://www.r-project.org/).
Temperature, light and P
CO
2
were designated as fixed effects; tank
and colony were designated as random effects, and random effects
were retained or dropped according to the function {step} (lmerTest).
Normality of distribution was checked using quantilequantile plots
and transforms were applied if needed, and homoscedasticity was
checked using plots of residuals versus fitted values. Type III
ANOVAs were performed in the package lmerTest (Kuznetsova
et al., 2017). S/H cell ratio was log-transformed prior to analysis
(Cunning and Baker, 2013). Post hoc tests of significant interactive
effects were performed using least-square means with the Tukey
method for P-value adjustment.
RESULTS
Treatment conditions
Seawater carbonate chemistry was effectively controlled to deliver
consistent conditions at each P
CO
2
level (Table 2). Mechanical issues
in one HCO
2
HLHT tank and one HCO
2
HLLT tank towards the
end of the experiment led to the aprioriremoval of these tanks and
the nubbins within from further analyses, leading to final replication
of two tanks per treatment for these treatments and three for all other
treatments. The two carbonate chemistry treatments differed in
P
CO
2
(P<0.001) and pH
T
conditions (P<0.001). Total alkalinity was
not affected by CO
2
treatment (P=0.147). P
CO
2
and pH
T
did not differ
among replicate tanks in the HCO
2
treatment (P0.668). At ambient
CO
2
,P
CO
2
and pH
T
differed between two tanks (tank 14: 376 μatm
P
CO
2
and pH 8.05; tank 21: 498 μatm P
CO
2
and pH 7.95) (one-way
ANOVA P0.026, post hoc P=0.036). However, these differences
were within an acceptable range for the LCO
2
treatment and no
pairwise difference in P
CO
2
or pH
T
was found between either tank and
any other LCO
2
tanks ( post hoc P0.064), nor between any other
pairs of LCO
2
tanks ( post hoc P0.264).
Physiological responses
Symbiont density was not affected by P
CO
2
(F
1,21
=0.40, P=0.536),
but declined by 23 and 25% at high light (F
1,21
=18.20, P<0.001)
and high temperature (F
1,22
=30.69, P<0.001), respectively
(Tables 5 and 6). Symbiont density experienced no interactive
effect among any factors (F
1,21
3.78, P0.065) (Table 3). Chl aper
symbiont did not change under high P
CO
2
(F
1,14
=0.09, P=0.763),
decreased by 17% at high light (F
1,14
=21.82, P<0.001) (Table 5)
and increased by 24% at high temperature (F
1,14
=28.24, P<0.001)
(Table 6). Chl aper symbiont was not affected by an interaction
among any factors (F
1,14
0.51, P0.485) (Table 3). Chl adensity
declined by 36% at high light (F
1,20
=47.71, P<0.001) (Table 5) but
was not affected by P
CO
2
(F
1,20
=0.68, P=0.418), temperature
(F
1,20
=3.02, P=0.097) nor any interactive effects (F
1,20
3.59,
P0.073) (Table 3).
A significant interactive effect among all three factors was found
for P
net
(F
1,80
=5.26, P=0.024). Post hoc tests indicated that high
temperature caused declines in P
net
at LCO
2
HL (of 40%) and
HCO
2
LL (62%), but not at HCO
2
HL or LCO
2
LL (Fig. 1). Whilst
main effects are difficult to interpret under a significant interaction, a
significant main effect of temperature (F
1,80
=31.53, P<0.001, decline
of 41% at HT) (Table 6) but not light (F
1,80
=0.39, P=0.536) or CO
2
(F
1,80
=1.04, P=0.311) was found, and no two-factor interactions were
detected (F
1,80
1.85, P0.178) (Table 3).
A significant three-factor interaction among light, temperature and
CO
2
affected P
gross
(F
1,80
=4.08, P=0.047). Post hoc tests found that
high temperature depressed P
gross
by 34% at HCO
2
LL, but not at
LCO
2
LL, LCO
2
HL or HCO
2
HL (Fig. 2). For the main effects,
P
gross
increased by 12% at high P
CO
2
(F
1,80
=4.78, P=0.032) (Table 4)
but did not change under high light (F
1,80
=1.44, P=0.233) and
decreased by 20% under high temperature (F
1,80
=12.72, P<0.001)
(Table 6). No two-factor interactions were detected (F
1,80
1.79,
P0.184) (Table 3).
Dark respiration was not affected by P
CO
2
(F
1,76
=1.81, P=0.183) or
light (F
1,76
=1.21, P=0.276), but increased by 24% at high
temperature (F
1,76
=6.86, P=0.011) (Table 6). No significant two-
or three-factor interactions were found (F
1,76
2.03, P0.158)
(Table 3). LEDR increased by 15% at high P
CO
2
(F
1,76
=5.05,
P=0.028) (Table 4), was not affected by light (F
1,76
=1.34, P=0.250),
and increased by 21% at high temperature (F
1,76
=6.63, P=0.012)
(Table 6). No significant interactive effects among any factors
affected LEDR (F
1,76
1.40, P0.241) (Table 3).
The P/R ratio was not affected by P
CO
2
(F
1,76
=0.01, P=0.905) or
light (F
1,76
=0.24, P=0.629), and decreased by 56% at high
temperature (F
1,76
=26.47, P<0.001) (Table 6). No two- or three-
factor interactions affected P/R ratio (F
1,76
3.25, P0.075) (Table 3).
The S/H cell ratio was not affected by P
CO
2
(F
1,149
=1×10
4
,
P=0.991) nor light (F
1,149
=4×10
4
,P=0.984), but increased by
65% at high temperature (F
1,149
=6.31, P=0.013) (Table 6). No two-
or three-factor interactions affected S/H cell ratio (F
1,149
1.71,
P0.192) (Table 3).
Though not statistically significant, S/H cell ratio values at
HCO
2
LLHT (0.16±0.04, mean±s.e.m.) and LCO
2
HLHT
(0.15±0.03) were higher compared with those at LCO
2
LLHT
Table 3. P-values given by ANOVAs performed on linear models for all physiological response variables
Factor
Symbiont
density
(cells cm
2
)
Chl aper
symbiont
(pg cell
1
)
Chl adensity
(µg cm
2
)
S/H cell
ratio
DR
(μmol O
2
cm
2
h
1
)
P
net
(μmol O
2
cm
2
h
1
)
P
gross
(μmol O
2
cm
2
h
1
)
LEDR
(μmol O
2
cm
2
h
1
) P/R ratio
Temperature 2×10
5
1×10
4
0.097 0.013 0.011 3×10
7
6×10
4
0.012 2×10
6
Light 3×10
4
4×10
4
9×10
7
0.984 0.276 0.536 0.233 0.250 0.629
CO
2
0.536 0.763 0.418 0.991 0.183 0.311 0.032 0.028 0.905
T×L 0.065 0.657 0.073 0.969 0.419 0.178 0.184 0.876 0.126
T×CO
2
0.535 0.998 0.704 0.915 0.158 0.515 0.836 0.342 0.267
L×CO
2
0.910 0.522 0.838 0.359 0.162 0.249 0.288 0.241 0.894
T×L×CO
2
0.467 0.485 0.346 0.192 0.763 0.024 0.047 0.989 0.075
Fstatistics and degrees of freedom corresponding to each P-value are given in Table S1. T, temperature; L, light.
5
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
(0.10±0.03) and HCO
2
HLHT (0.11±0.04). All treatments at
25°C had mean S/H cell ratios between 0.06 and 0.09.
DISCUSSION
In order to project how climate change will influence coral reef
ecosystems, it is necessary to determine how multiple environmental
parameters interact to attenuate and exacerbate climate change
stressors. However, experimental explorations of such interactions are
faced with the challenge that elevated P
CO
2
owing to human activities
is a chronic stressor, whereas high temperature is an acute
phenomenon. As impacts of elevated P
CO
2
maytakesometimeto
manifest (Anthony et al., 2008), the application of heat stress as a
chronic stressor could obscure any effect of elevated P
CO
2
(e.g. by
continually exerting a strong downward pressure on symbiont
population size). The present study utilised an experimental design
for the analysis of the combined impacts of elevated P
CO
2
, light and
temperature that provided time for physiological changes to elevated
P
CO
2
and light to occur (over 32 days) before heat stress was applied
(additional 7 days), thus providing the proper context of elevated
P
CO
2
and heat as chronic and acute impacts, respectively.
A significant three-way interaction between elevated P
CO
2
, light
and temperature was detected for net and gross photosynthesis. For
P
net
, declines were detected at 29°C versus 25°C within the P
CO
2
light combinations of LCO
2
HL and HCO
2
LL. Circumstantial
evidence suggests that elevated S/H cell ratios may have been linked
to depressed P
net
. S/H cell ratio was elevated at 29°C versus 25°C
(significant main effect); however, at LCO
2
HL and HCO
2
LL, this
difference in S/H cell ratio was far more pronounced, 74141%
(trend only), compared with 1824% in the other P
CO
2
light
combinations. As the three-factor interaction for S/H cell ratio was
not statistically significant, further work will be required to
investigate this link.
For P
gross
, a decline at 29°C versus 25°C was supported for HCO
2
LL but not LCO
2
HL or other P
CO
2
light combinations. Several
explanations exist for why P
net
and P
gross
differed with respect to the
LCO
2
HL treatment. Firstly, differences in light respiration among
treatments, if any, may introduce real differences between P
net
and
P
gross
. Secondly, LEDR, used here as a proxy for light respiration to
calculate P
gross
, may underestimate light respiration rates (Schrameyer
et al., 2014). Finally, P
gross
, as calculated here, contains measurement
error from both P
net
and LEDR and this added variation may have
served to reduce the statistical power of the post hoc tests.
A consideration of how the experimental treatments may limit the
light and dark reactions of photosynthesis could help to explain
the interactive effects observed for P
net
and P
gross
. Increases in
temperature are known to decrease the capacity for photosynthetic
electron transport, such as by damaging the D1 protein (Warner et al.,
1999). Under high light conditions, this can lead to overreduction of
the remaining intact electron transport chains and to further damage
through the production of oxygen radicals (Hoegh-Guldberg, 1999),
decreasing the areal rate of photosynthesis (as was seen for P
net
at
1.75 25°C
29°C
1.50
1.25
1.00 b,c,d
c,d
a,b,c
400 800
Midday light (µmol photons m–1 s–1)
431 µatm PCO2962 µatm PCO2
400 800
a,b
d
a
b,c,d
a,b,c,d
0.75
Net photosynthesis (µmol O2 cm–2 h–1)
0.50
0.25
0
Fig. 1. Net photosynthesis in Pocillopora acuta is affected by a
synergistic interaction of P
CO
2
, light intensity and temperature. Bars are
means±s.e.m. with sample sizes of n=6 (HCO
2
HLLT), n=7 (HCO
2
HLHT),
n=11 (LCO
2
HLLT) and n=12 (all other treatments). The light levels are the
daily maxima in the light treatments (the light intensity between 10:00 and
12:00 h). Above the bars, treatments that share at least one letter are not
significantly different from one another (P>0.05) in the post hoc test of the
interactive effect of light, temperature and P
CO
2
.
400 800
Midday light (µmol photons m–1 s–1)
431 µatm PCO2962 µatm PCO2
400 800
1.75 25°C
29°C
1.50
1.25
1.00
a,b
a,b a,b a,b
aa
b
a
0.75
Gross photosynthesis (µmol O2 cm–2 h–1)
0.50
0.25
0
Fig. 2. Gross photosynthesis in P.acuta is affected by a synergistic
interaction of P
CO
2
, light intensity and temperature. These data suggest
that the depression of photosynthesis, which may occur under high
temperature (sixth bar from the left), is ameliorated by exposure to higher
irradiance combined with ocean acidification (eighth bar from the left). Bars are
means±s.e.m. with sample sizes of n=6 (HCO
2
HL-LT), n=7 (HCO
2
HL
HT), n=11 (LCO
2
HLLT) and n=12 (all other treatments). The light levels are
the daily maxima in the light treatments (the light intensity between 10:00 and
12:00 h). Above the bars, treatments that share at least one letter are not
significantly different from one another (P>0.05) in the post hoc test of the
interactive effect of light, temperature and P
CO
2
.
Table 4. Statistically significant main effects of P
CO2
Parameter Units
Value at 435 µatm
P
CO
2
(mean±s.e.m.)
Value at 961 µatm
P
CO
2
(mean±s.e.m.)
% change at
high P
CO
2
P
gross
μmol O
2
cm
2
h
1
1.18±0.05 1.32±0.07 12
LEDR μmol O
2
cm
2
h
1
0.49±0.02 0.56±0.03 15
6
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
elevated temperature and ambient P
CO
2
). However, under high
substrate availability (elevated P
CO
2
), an enhanced capacity for
CalvinBenson activity may help to keep electron transport chains
sufficiently open to cope with high light influx, offsetting the
inhibiting effect of high temperature. Enhanced turnover rate of the
CalvinBenson cycle at moderately elevated temperature (Dusenge
et al., 2018), and/or faster repair of damaged D1 proteins owing to an
improved energetic status of the organism, might also contribute
(Hoogenboom et al., 2012). This interpretation offers an explanation
for why photosynthesis (both P
net
and P
gross
)increaseswith
irradiance under elevated temperature combined with elevated
P
CO
2
. It is likely that these effects would only occur within a range
of elevated light that is sufficient to deliver adequate reducing power,
but still low enough to avoid substantive photodamage. As a case in
point, under very high light conditions, ocean acidification and
warming were found to synergistically decrease net photosynthetic
productivity in Porites lobata by Anthony et al. (2008).
In previous studies involving fully crossed levels of P
CO
2
and
temperature, the effect of these variables on photosynthesis was
independent in some coral species but interactive in others. In
Seriatopora hystrix,P
net
and P
gross
decreased under high temperature
and increased under high P
CO
2
, with both stressors having an
additive, but not interactive, effect (Noonan and Fabricius, 2016). In
Acropora millepora, no interactive effect of temperature and
acidification nor of light (at low levels) and acidification on P
net
and P
gross
has been found (Noonan and Fabricius, 2016; Vogel et al.,
2015), but P
gross
may decrease under acidification at high light
(Kaniewska et al., 2012). In Stylophora pistillata,P
net
increased
under high temperature and decreased under high CO
2
, but no
interaction between the two factors was found (Reynaud etal., 2003).
In Acropora intermediata and P. lobata, net productivity decreased
over a gradient of low to high P
CO
2
at ambient temperature, with
warming interactively altering this pattern by effecting an increase in
net productivity at intermediate P
CO
2
in A. intermediata and
exacerbating the size of the net productivity decline in P. lobata
(Anthony et al., 2008). P
gross
increased across a range of coral
species at a natural CO
2
seep by 2337% (Biscéré et al., 2019),
moderately more than the increase in P
gross
under acidification (12%)
observed as a main effect in the present study. Physiological
differences such as in carbon-concentrating mechanisms or
symbiont photophysiology may account for inter-specific
differences in P
net
and P
gross
responses (Brading et al., 2011).
Multiple stressors can have a compound effect on corals through
interactive effects, where present, or through additive impacts where
each stressor exhibits a main effect. The latter was seen with chl aper
symbiont (discussed later) and LEDR. LEDR increased by 15%
under elevated P
CO
2
, and increased by 21% at elevated temperature.
Increased LEDR can relate to several forms of photochemical
quenching. Increased rates of respiration can occur as a result of
increased CalvinBenson cycle activity or production of ATP and
NADPH by thylakoid electron transport under illumination (Parys
and Jastrzębski, 2006). LEDR may also indicate oxygen consumption
through the alternate photochemical quenching mechanisms of
chlororespiration and the Mehler ascorbateperoxidase cycle, or re-
oxidation of spent electron carriers(Roberty et al., 2014; Stokes et al.,
1990). Significantly, in a prior study of Acropora muricata,LEDR
increased under acidification whilst DR remained constant, and
evidence from xanthophyll cycling suggested that increased Mehler
ascorbateperoxidase cycle activity could have been the cause
(Crawley et al., 2010). This may also occur in the P. acuta holobiont;
however, the increase in P
gross
under acidification leaves open the
possibility of increased photosynthetic substrate as a cause of elevated
LEDR. As LEDR increased under elevated temperature, likely owing
to the increased kinetic rate of metabolic reactions (Gillooly et al.,
2001), an additive impact of increased temperature and elevated
P
CO
2
on LEDR in some coralalgal holobionts is to be expected under
future global change.
The additive impact on LEDR of increased temperature and
P
CO
2
may lead to energetic consequences for the P. acut a holobiont.
In the case of the latter stressor, Wall et al. (2017) identified that lipids
and energy content (measured per unit biomass and thus robust to the
effects of skeletal extension) are depleted in P. acut a under
acidification at two light levels. Depletion of energy reserves could
be due to decreased availability of heterotrophically derived energy,
or to an increased rate of energy usage, which, in most cases, will
manifest as an increased rate of respiration. Our finding of increased
LEDR under elevated P
CO
2
suggests a greater rate of metabolism of
photosynthates immediately after their production, and thus could
provide a plausible hypothesis for the decreased energy reserves of
P. acut a observed by Wall et al. (2017).
Maintenance of calcification rate may explain the lack of decline in
DR and the increase in LEDR under elevated P
CO
2
. The lack of decline
in DR [also observed in P. damicornis (Comeau et al., 2017)], and its
increase under elevated P
CO
2
at 29°C (Fig. 2) is notable as the increased
Table 5. Statistically significant main effects of light
Parameter Units
Value at 400 µmol
photons m
2
s
1
(mean±s.e.m.)
Value at 800 µmol
photons m
2
s
1
(mean±s.e.m.)
% change at
high light
Symbiont density 10
5
cells cm
2
7.89±0.25 6.10±0.19 23
Chl adensity µg cm
2
3.64±0.12 2.32±0.07 36
Chl aper symbiont pg cell
1
4.65±0.08 3.86±0.09 17
Table 6. Statistically significant main effects of temperature
Parameter Units
Value at 25°C
(mean±s.e.m.)
Value at 29°C
(mean±s.e.m.)
% change at
high temperature
Symbiont density 10
5
cells cm
2
8.11±0.23 6.06±0.21 25
Chl aper symbiont pg cell
1
3.85±0.07 4.77±0.09 24
P
net
µmol O
2
cm
2
h
1
0.91±0.06 0.54±0.04 41
P
gross
µmol O
2
cm
2
h
1
1.38±0.06 1.10±0.05 20
DR µmol O
2
cm
2
h
1
0.48±0.03 0.59±0.03 24
LEDR µmol O
2
cm
2
h
1
0.47±0.02 0.57±0.03 21
P/R ratio 2.31±0.26 1.01±0.09 56
S/H cell ratio 0.08±0.01 0.14±0.02 65
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RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
seawater proton concentration under elevated P
CO
2
could make
respiration more energetically costly (Mackey et al., 2015).
Pocillopora damicornis and P. acut a maintain their rate of
calcification, normalised to bothbiomassandskeletalarea,and
experience declines in biomass or energy reserves, under elevated
P
CO
2
(Comeau et al., 2013; Comeau et al., 2014a,b; Wall et al., 2017).
This could be a signature of the energetic cost of the maintenance of
calcification under elevated P
CO
2
(Comeau et al., 2013; Galli and
Solidoro, 2018) and/or the increased energetic costs of respiration. In
free-swimming larvae (i.e. a non-calcifying life stage) of Pocillopora
spp., respiration rate displays a trend to decrease under elevated
P
CO
2
(Putnam et al., 2013), supporting the idea that the metabolic
requirements of maintaining calcification under acidification
contributes to stability in DR in adults.
Other vital processes may have also contributed to a changed
energetic balance at high P
CO
2
. Incipient planula larvae were
observed within the adult tissue of many coral specimens at the end
of this study. We were unable to determine from these observations
whether P
CO
2
level influenced the quantity of incipient larvae within
coral tissues, the number of larvae released over the course of the
experiment or their maturation time. However, their presence in this
study suggests that gametogensis warrants investigation as a process
that may potentially effect or be affected by changes in adult coral
condition under elevated P
CO
2
.
Our hypothesis that symbiont density loss would be greatest at the
combination of elevated P
CO
2
, high temperature and high light was
not fully supported by the data. Symbiont density loss was the greatest
under high light combined with high temperature, with statistical
support, and the two stressors together had an additive but not
interactive effect on this variable (also see Ban et al., 2014). Unlike
light and temperature, elevated P
CO
2
had no statistically significant
impact on symbiont cells. However, a decline in symbiont densities
under elevated P
CO
2
has been shown in a meta-analysis across
multiple studies and coral species (Mason, 2018b), indicating that an
effect of P
CO
2
on symbiont densities is often present. In our study, an
effect of P
CO
2
on symbiont densities may have required a greater
period of incubation at high P
CO
2
or may have been moderated byour
particular combination of coral and symbiont species.
Of the three stressors tested (elevated P
CO
2
, light and
temperature), changes in temperature exerted the greatest number
of main effects, significantly affecting almost every response
variable. The ratio of P
net
under midday irradiance to dark
respiration declined to 1.01 at 29°C, which could suggest that
phototrophy may not meet energy expenditure at 29°C if integrated
over a full daynight cycle. The decrease in symbiont densities with
an increase in temperature (from 25°C to 29°C) was accompanied
by an increase in chl acontent per symbiont cell. Increased chl aper
symbiont under stressful temperature has been observed in some
coral species [Seriatopora caliendrum (Baghdasarian et al., 2017),
S. hystrix (Hoegh-Guldberg and Smith, 1989) and the temperate
coral Balanophyllia europaea (Caroselli et al., 2015)], and likely
indicates a photoacclimation response to decreased symbiont
densities. In constrast to temperature, high light caused a decrease
in both symbiont cell density and chl aper symbiont, possibly
indicating some form of light-induced photosynthetic dysfunction,
or rapid linear extension and concomitant thinning of symbiont
densities and chl aper symbiont.
Whilst symbiont density decreased at high temperature, the S/H
cell ratio increased. Decreasing symbiont density and increasing
S/H cell ratio together suggest that host cell density per cm
2
decreased at elevated temperature, but at a rate greater than the loss
of symbiont cells. This pattern is consistent with past observations
of physiological responses of coralalgal holobionts to seasonal
warming, which is thought to cause host cell loss, increasing the S/H
ratio but also triggering a regulatory downwards adjustment in the
symbiont population (Cunning and Baker, 2013). An alternative
explanation, that S/H ratio increases owing to rapid linear extension
and consequent thinning of symbiont cells, is unlikely as 29°C is
above the calcification optima of Kāneohe Bay corals (Jokiel and
Coles, 1977). Increasing S/H cell ratios confirm the nuance revealed
by chl aper symbiont that the symbiont density loss at high
temperature is not yet indicative of a state of coral bleaching, though
loss of host cells is a sign that bleaching may be imminent
(Ainsworth et al., 2008).
It is clear that under future climates, where temperature and
acidification have both already increased, the way that light is
affected by climate change will prove to be important to P. acuta,
impacting the degree to which warming will decrease
photosynthetic rate. Light can decrease under climate change
through sea level rise, which may cause increased tidal resuspension
of sediments (Ogston and Field, 2010), through increased turbidity
owing to stronger precipitation events (Fischer and Knutti, 2015),
and through increased atmospheric water vapour content, which
decreases light transmission (Haywood et al., 2011). In those cases,
P. acuta will clearly not experience the alleviation of temperature-
induced photosynthesis depression. In contrast, cloud cover could
decrease in many areas owing to warming (McCoy et al., 2017;
Schneider et al., 2019), and future reductions in aerosol emissions
will tend to increase light penetration and reduce cloud cover
(Rosenfeld et al., 2019; Sato and Suzuki, 2019). Changes in high
cirrus clouds that trap heat but reduce irradiance could also be
particularly important (Kärcher, 2017; Liou, 1986). We note that
800 µmol photons m
2
s
1
is relatively strong irradiance but still
within the moderate range of light that reefs experience, and future
increases in irradiance will only be beneficial to the extent that they
move P. acuta into this range, but not beyond it (to photoinhibitive
light levels).
Coral species/genotypes and their partner symbionts vary in their
temperature tolerance and photophysiology, such as non-
photochemical quenching and carbon concentrating mechanisms.
As such, it is difficult to infer how general these responses would be
among other coral species/symbiont combinations. However,
increase in photosynthesis under acidification has been observed
in some other species (Biscéré et al., 2019; but not all, see Sweet and
Brown, 2016), and a decrease in photosynthesis at stressful
temperatures is a common phenomenon (e.g. Hoegh-Guldberg,
1999). Therefore, whilst demonstrated in only one species here, a
degree of commonality among corals in displaying the alleviation of
thermally depressed photosynthesis by strong light combined with
high P
CO
2
is an intriguing possibility.
Conclusions
Owing to the roles of light and CO
2
as (respectively) power source and
substrate for photosynthesis, and the role of temperature in optimising
or disrupting this process, the influences of P
CO
2
, light and temperature
on marine photosynthesisers remains a research imperative under
climate change. Of the three factors, temperature exerted the dominant
influence on the physiology of the P. acut aSymbiodiniaceae
symbiosis. Importantly, these effects were observed at a heat stress
level that had not caused bleaching, and hence may reflect
physiological responses to moderate but year-round elevations in
temperature under climate change. Interactions among all three factors
were detected for some key physiological processes. Elevated
P
CO
2
caused an increase in photosynthesis in P. acut a (as found in
8
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
some other coral species), whilst stressful temperature caused a
decrease. However, our results demonstrate that light can alter this
impact: 800 µmol photons m
2
s
1
at high (but not ambient)
P
CO
2
ameliorated the decline in photosynthesis caused by high
temperature, an effect that was clearly not seen at the lower light level.
This is a significant finding, illustrating that the well-known negative
impacts of high temperature on photosynthesis can be alleviated by
moderately strong irradiance if accompanied by elevated seawater
P
CO
2
.
Changes in energetic status at the organism level could have flow
over effects to the broader ecosystem. Coralalgal holobionts supply
vast quantities of energy to other levels of the ecosystem, through the
release of mucus (Crossland et al., 1980) and dissolved organic
carbon (Crossland, 1987), and corallivory (Cole et al., 2011). The
changes in the rate of photosynthesis but also of metabolism of
energy (LEDR) at elevated P
CO
2
observed in this study indicates the
possibility of changes in the release of energy through these other
pathways. Measurement of mucus release, dissolved organic carbon
release and rates of corallivory under ocean acidification will be
useful to ascertain the impacts of these holobiont-level changes on the
coral reef ecosystem.
Acknowledgements
We thank D. Schar, J. Dulin, H. Putnam, R. Ritson-Williams, J. Davidson, B. Lenz,
and W. Skirving for constructivediscussion s and logistical support, and G. Davies for
performing DNA extractions and qPCR runs. Portions of this research formed a part
of the PhD thesis of R.A.B.M. (Mason, 2018a). This is Hawaii Institute of Marine
Biology (HIMB) contribution number 1822 and School of Ocean and Earth Science
and Technology (SOEST) contribution number 11136.
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: R.A.B.M., C.B.W., R.C., S.D., R.D.G.; Methodology: R.A.B.M.,
C.B.W., R.C., R.D.G.; Software: R.C.; Formal analysis: R.A.B.M.; Investigation:
R.A.B.M., C.B.W., R.C.; Resources: R.A.B.M., C.B.W., R.C., R.D.G.; Data curation:
R.A.B.M., C.B.W., R.C.; Writing - original draft: R.A.B.M.; Writing - review & editing:
R.A.B.M., C.B.W., R.C., S.D.; Visualization: R.A.B.M.; Supervision: S.D., R.D.G.;
Project administration: R.A.B.M., R.D.G.; Funding acquisition: R.A.B.M., R.D.G.
Funding
This work was funded by grants to R.A.B.M. from the Linnean Society of New
South Wales, the International Phycological Society, the Australian Wildlife
Society and a Fulbright Scholarship. C.B.W. was supported by an University of
Hawaii Graduate Opportunity Grant, the UH Edmondson Research Fund, and
Environmental Protection Agency (EPA) STAR Fellowship Assistance Agreement
(FP-91779401-1). The views expressed inthis publication have not been reviewed
or endorsed by the EPA and are solely those of the authors. R.C. was supported
by a National Science Foundation Postdoctoral Fellowship in Biology (NSF-DBI-
1400787).
Data availability
Data and R scripts to replicate the analysis are openly accessible online (Mason
et al., 2020) from Zenodo at doi:10.5281/zenodo.3526369.
Supplementary information
Supplementary information available online at
https://jeb.biologists.org/lookup/doi/10.1242/jeb.223198.supplemental
References
Ainsworth, T. D., Hoegh-Guldberg, O., Heron, S. F., Skirving, W. J. and Leggat,
W. (2008). Early cellular changes are indicators of pre-bleaching thermal stress in
the coral host.J. Exp. Mar. Biol. Ecol. 364, 63-71. doi:10.1016/j.jembe.2008.06.032
Albright, R. and Langdon, C. (2011). Ocean acidification impacts multiple early life
history processes of the Caribbean coral Porites astreoides.Glob. Change Biol.
17, 2478-2487. doi:10.1111/j.1365-2486.2011.02404.x
Albright, R., Mason, B., Miller, M. and Langdon, C. (2010). Ocean acidification
compromises recruitment success of the threatened Caribbean coral Acropora
palmata.Proc. Natl. Acad. Sci. USA 107, 20400-20404. doi:10.1073/pnas.
1007273107
Anlauf, H., DCroz, L. and ODea, A. (2011). A corrosive concoction: the combined
effects of ocean warming and acidification on the early growth of a stony coral are
multiplicative. J. Exp. Mar. Biol. Ecol. 397, 13-20. doi:10.1016/j.jembe.2010.11.
009
Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S. and Hoegh-Guldberg, O.
(2008). Ocean acidification causes bleaching and productivity loss in coral reef
builders. Proc. Natl. Acad. Sci. USA 105, 17442-17446. doi:10.1073/pnas.
0804478105
Anthony, K. R. N., Hoogenboom, M. O., Maynard, J. A., Grottoli, A. G. and
Middlebrook, R. (2009). Energetics approach to predicting mortality risk from
environmental stress: a case study of coral bleaching. Funct. Ecol. 23, 539-550.
doi:10.1111/j.1365-2435.2008.01531.x
Baghdasarian, G., Osberg, A., Mihora, D., Putnam, H., Gates, R. D. and
Edmunds, P. J. (2017). Effects of temperature and pCO
2
on population regulation
of Symbiodinium spp. in a tropical reef coral. Biol. Bull. 232, 123-139. doi:10.1086/
692718
Bahr, K. D., Jokiel, P. L. and Rodgers, K. S. (2016). Relative sensitivity of five
Hawaiian coral species to high temperature under high-pCO
2
conditions. Coral
Reefs 35, 729-738. doi:10.1007/s00338-016-1405-4
Ban, S. S., Graham, N. A. J. and Connolly, S. R. (2014). Evidence for multiple
stressor interactions and effects on coral reefs. Glob. Change Biol. 20, 681-697.
doi:10.1111/gcb.12453
Bates, D., Ma
̈chler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-
effects models using lme4. J. Stat. Softw. 67, 1-48. doi:10.18637/jss.v067.i01
Biscéré, T., Zampighi, M., Lorrain, A., Jurriaans, S., Foggo, A., Houlbrèque, F.
and Rodolfo-Metalpa, R. (2019). High pCO
2
promotes coral primary production.
Biol. Lett. 15, 20180777. doi:10.1098/rsbl.2018.0777
Brading, P., Warner, M. E., Davey, P., Smith, D. J., Achterberg, E. P. and
Suggett, D. J. (2011). Differential effects of ocean acidification on growth and
photosynthesis among phylotypes of Symbiodinium (Dinophyceae). Limnol.
Oceanogr. 56, 927-938. doi:10.4319/lo.2011.56.3.0927
Caroselli, E., Falini, G., Goffredo, S., Dubinsky, Z. and Levy, O. (2015). Negative
response of photosynthesis to natural and projected high seawater temperatures
estimated by pulse amplitude modulation fluorometry in a temperate coral. Front.
Physiol. 6, 317. doi:10.3389/fphys.2015.00317
Cohen, I. and Dubinsky, Z. (2015). Long term photoacclimation responses of the
coral Stylophora pistillata to reciprocal deep to shallow transplantation:
photosynthesis and calcification. Front. Mar. Sci. 2, 45. doi:10.3389/fmars.2015.
00045
Cohen, A. L. and Holcomb, M. (2009). Why corals care about ocean acidification:
uncovering the mechanism. Oceanography 22, 118-127. doi:10.5670/oceanog.
2009.102
Cole, A. J., Lawton, R. J., Pratchett, M. S. and Wilson, S. K. (2011). Chronic coral
consumption by butterflyfishes. Coral Reefs 30, 85-93. doi:10.1007/s00338-010-
0674-6
Comeau, S., Edmunds, P. J., Spindel, N. B. and Carpenter, R. C. (2013). The
responses of eight coral reef calcifiers to increasing partial pressure of CO
2
do not
exhibit a tipping point. Limnol. Oceanogr. 58, 388-398. doi:10.4319/lo.2013.58.1.
0388
Comeau, S., Edmunds, P. J., Spindel, N. B. and Carpenter, R. C. (2014a). Fast
coral reef calcifiers are more sensitive to ocean acidification in short-term
laboratory incubations. Limnol. Oceanogr. 59, 1081-1091. doi:10.4319/lo.2014.
59.3.1081
Comeau, S., Carpenter, R. C., Nojiri, Y., Putnam, H. M., Sakai, K. and Edmunds,
P. J. (2014b). Pacific-wide contrast highlights resistance of reef calcifiers to ocean
acidification. Proc. R. Soc. B Biol. Sci. 281, 20141339-20141339. doi:10.1098/
rspb.2014.1339
Comeau, S., Carpenter, R. C. and Edmunds, P. J. (2017). Effects of pCO
2
on
photosynthesis and respiration of tropical scleractinian corals and calcified algae.
ICES J. Mar. Sci. 74, 1092-1102. doi:10.1093/icesjms/fsv267
Crawley, A., Kline, D. I., Dunn, S., Anthony, K. and Dove, S. (2010). The effect of
ocean acidification on symbiont photorespiration and productivity in Acropora
formosa.Glob. Change Biol. 16, 851-863. doi:10.1111/j.1365-2486.2009.01943.x
Crossland, C. J. (1987). In situ release of mucus and DOC-lipid from the corals
Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs
6, 35-42. doi:10.1007/BF00302210
Crossland, C. J., Barnes, D. J. and Borowitzka, M. A. (1980). Diurnal lipid and
mucus production in the staghorn coral Acropora acuminata.Mar. Biol. 60, 81-90.
doi:10.1007/BF00389151
Cunning, R. and Baker, A. C. (2013). Excess algal symbionts increase the
susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 259-262. doi:10.
1038/nclimate1711
Cunning, R., Glynn, P. W. and Baker, A. C. (2013). Flexible associations between
Pocillopora corals and Symbiodinium limit utility of symbiosis ecology in defining
species. Coral Reefs 32, 795-801. doi:10.1007/s00338-013-1036-y
Cunning, R., Ritson-Williams, R. and Gates, R. D. (2016). Patterns of bleaching
and recovery of Montipora capitata in Ka
̄neohe Bay, Hawaii, USA. Mar. Ecol.
Prog. Ser. 551, 131-139. doi:10.3354/meps11733
9
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
Davies, P. S. (1980). Respiration in some Atlantic reef corals in relation to vertical
distribution and growth form. Biol. Bull. 158, 187-194. doi:10.2307/1540930
Dubinsky, Z. and Falkowski, P. (2011). Light as a source of information and energy
in zooxanthellate corals. In Coral Reefs: An Ecosystem in Transition (ed. Z.
Dubinsky and N. Stambler), pp. 107-118. Dordrecht: Springer Netherlands.
Dufault, A. M., Ninokawa, A., Bramanti, L., Cumbo, V. R., Fan, T.-Y. and
Edmunds, P. J. (2013). The role of light in mediating the effects of ocean
acidification on coral calcification. J. Exp. Biol. 216, 1570-1577. doi:10.1242/jeb.
080549
Dunn, S. R., Thomason, J. C., Le Tissier, M. D. A. and Bythell, J. C. (2002).
Detection of cell death activity during experimentally induced bleaching of the
symbiotic sea anemone Aiptasia sp. In Proceedings of the Ninth International
Coral Reef Symposium, Bali. 23-27 Oct. 2000 (ed. M. K. Moosa, S.
Soemodihardjo, A. Soegiarto, K. Romimohtarto, A. Nontji, Soekarno and
Suharsono), pp. 145-153. Ministry of Environment of the Republic of Indonesia;
Indonesian Institute of Sciences; International Society for Reef Studies.
Dunn, S. R., Pernice, M., Green, K., Hoegh-Guldberg, O. and Dove, S. G. (2012).
Thermal stress promotes host mitochondrial degradation in symbiotic cnidarians:
are the batteries of the reef going to run out? PLoS ONE 7, e39024. doi:10.1371/
journal.pone.0039024
Dusenge, M. E., Duarte, A. G. and Way,D. A. (2018). Plant carbon metabolism and
climate change: elevated CO
2
and temperature impacts on photosynthesis,
photorespiration and respiration.New Phytol.. 221, 32-49. doi:10.1 111/nph.15283
Edmunds, P. J. and Wall, C. B. (2014). Evidence that high pCO
2
affects protein
metabolism in tropical reef corals. Biol. Bull. 227, 68-77. doi:10.1086/
BBLv227n1p68
Escobal, P. R. (1996). Aquatic Systems Engineering: Devices and How they
Function, 2nd edn. Oxnard, CA: Dimension Engineering Press.
Fischer, E. M. and Knutti, R. (2015). Anthropogenic contribution to global
occurrence of heavy-precipitation and high-temperature extremes. Nat. Clim.
Change 5, 560-564. doi:10.1038/nclimate2617
Galli, G. and Solidoro, C. (2018). ATP supply may contribute to light-enhanced
calcification in corals more than abiotic mechanisms. Front. Mar. Sci. 5, 68. doi:10.
3389/fmars.2018.00068
Gates, R. D., Baghdasarian, G. and Muscatine, L. (1992). Temperature stress
causes host cell detachment in symbiotic cnidarians: implications for coral
bleaching. Biol. Bull. 182, 324-332. doi:10.2307/1542252
Gillooly, J. F., Brown, J. H., West, G. B., Savage, V. M. and Charnov, E. L. (2001).
Effects of size and temperature on metabolic rate. Science 293, 2248-2251.
doi:10.1126/science.1061967
Gorbunov, M. Y., Kolber, Z. S., Lesser, M. P. and Falkowski, P. G. (2001).
Photosynthesis and photoprotection in symbiotic corals. Limnol. Oceanogr. 46,
75-85. doi:10.4319/lo.2001.46.1.0075
Haywood, J. M., Bellouin, N., Jones, A., Boucher, O., Wild, M. and Shine, K. P.
(2011). The roles of aerosol, water vapor and cloud in future global dimming/
brightening. J. Geophys. Res. Atmos. 116, D20203. doi:10.1029/2011JD016000
Hoegh-Guldberg, O. (1999). Climate change, coral bleaching and the future of the
worlds coral reefs. Mar. Freshw. Res. 50, 839-866.
Hoegh-Guldberg, O. and Smith, G. J. (1989). The effect of sudden changes in
temperature, light and salinity on the population density and export of
zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora
hysterix Dana. J. Exp. Mar. Biol. Ecol. 129, 279-303. doi:10.1016/0022-
0981(89)90109-3
Hoegh-Guldberg, O., Cai, R., Poloczanska, E. S., Brewer, P. G., Sundby, S.,
Hilmi, K., Fabry, V. J. Jung, S. (2014). The Ocean. In Climate Change 2014:
Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of
Working Group II to the Fifth Assessment Report of the Intergovernmental Panel
of Climate Change (ed. V. R. Barros, C. B. Field, D. J. Dokken,M. D. Mastrandrea,
K. J. Mach, T. E. Bilir, M. Chatterjee, K. L. Ebi, Y. O. Estrada and R. C. Genova
et al.), pp. 1655-1731. Cambridge University Press.
Hoogenboom, M. O., Campbell, D. A., Beraud, E., DeZeeuw, K. and Ferrier-
Pagès, C. (2012). Effects of light, food availability and temperature stress on the
function of photosystem II and photosystem I of coral symbionts. PLoS ONE 7,
e30167. doi:10.1371/journal.pone.0030167
Iglesias-Prieto, R. (1995). The effects of elevated temperature on the
photosynthetic responses of symbiotic dinoflagellates. In Photosynthesis: from
Light to Biosphere (ed. P. Mathis), pp. 793-796. Netherlands: Kluwer Academic
Publishers.
Iglesias-Prieto, R., Matta, J. L., Robins, W. A. and Trench, R. K. (1992).
Photosynthetic response to elevated temperature in the symbiotic dinoflagellate
Symbiodinium microadriaticum in culture. Proc. Natl. Acad. Sci. USA 89,
10302-10305. doi:10.1073/pnas.89.21.10302
Iguchi, A., Ozaki, S., Nakamura, T., Inoue, M., Tanaka, Y., Suzuki, A., Kawahata,
H. and Sakai, K. (2012). Effects of acidified seawater on coral calcification and
symbiotic algae on the massive coral Porites australiensis.Mar. Environ. Res. 73,
32-36. doi:10.1016/j.marenvres.2011.10.008
Jacobson, L. M., Edmunds, P. J., Muller, E. B. and Nisbet, R. M. (2016). The
implications of reduced metabolic rate in resource-limited corals.J. Exp. Biol. 219,
870-877. doi:10.1242/jeb.136044
Jeffrey, S. W. and Humphrey, G. F. (1975). New spectrophotometric equations for
determining chlorophylls a,b,c
1
, and c
2
in higher plants, algae, and natural
phytoplankton. Biochem. Physiol. Pflanz. 167, 191-194. doi:10.1016/S0015-
3796(17)30778-3
Jokiel, P. L. (2011). Ocean acidification and control of reef coral calcification by
boundary layer limitation of proton flux. Bull. Mar. Sci. 87, 639-657. doi:10.5343/
bms.2010.1107
Jokiel, P. L. and Coles, S. L. (1977). Effects of temperature on the mortality and
growth of Hawaiian reef corals. Mar. Biol. 43, 201-208. doi:10.1007/BF00402312
Kaniewska, P., Campbell, P. R., Kline, D. I., Rodriguez-Lanetty, M., Miller, D. J.,
Dove, S. and Hoegh-Guldberg, O. (2012). Major cellular and physiological
impacts of ocean acidification on a reef building coral. PLoS ONE 7, e34659.
doi:10.1371/journal.pone.0034659
Ka
̈rcher, B. (2017). Cirrus clouds and their response to anthropogenic activities.
Curr. Clim. Change Rep. 3, 45-57. doi:10.1007/s40641-017-0060-3
Kleypas, J. A., Buddemeier, R. W., Archer, D., Gattuso, J.-P., Langdon, C. and
Opdyke, B. N. (1999). Geochemical consequences of increased atmospheric
carbon dioxide on coral reefs. Science 284, 118-120. doi:10.1126/science.284.
5411.118
Kra
̈mer, W. E., Schrameyer, V., Hill, R., Ralph, P. J. and Bischof, K. (2013). PSII
activity and pigment dynamics of Symbiodinium in two Indo-Pacific corals
exposed to short-term high-light stress. Mar. Biol. 160, 563-577. doi:10.1007/
s00227-012-2113-4
Kuznetsova, A., Brockhoff, P. B. and Christensen, R. H. B. (2017). lmerTest
package: tests in linear mixed effects models. J. Stat. Softw. 82, 1-26. doi:10.
18637/jss.v082.i13
Liou, K.-N. (1986). Influence of cirrus clouds on weather and climate processes: a
global perspective. Mon. Weather Rev. 114, 1167-1199. doi:10.1175/1520-
0493(1986)114<1167:IOCCOW>2.0.CO;2
Mackey, K., Morris, J. J., Morel, F. and Kranz, S. (2015). Response of
photosynthesis to ocean acidification. Oceanography 25, 74-91. doi:10.5670/
oceanog.2015.33
Mason, R. A. B. (2018a). Coral Responses to Temperature, Irradiance and
Acidification Stress: Linking Physiology to Satellite Remote Sensing. Brisbane:
The University of Queensland. doi:10.14264/uql.2018.482
Mason, R. A. B. (2018b). Decline in symbiont densities of tropical and subtropical
scleractinian corals under ocean acidification. Coral Reefs 37, 945-953. doi:10.
1007/s00338-018-1720-z
Mason, R. A. B., Wall, C. B., Cunning, R., Dove, S. G. and Gates, R. D. (2020).
Data and code for: High light alongside elevated pCO
2
alleviates thermal
depression of photosynthesis in a hard coral (Pocillopora acuta). Zenodo. doi:10.
5281/zenodo.3526369
McCoy, D. T., Eastman, R., Hartmann, D. L. and Wood, R. (2017). The change in
low cloud cover in a warmed climate inferred from AIRS, MODIS, and ERA-
Interim. J. Clim. 30, 3609-3620. doi:10.1175/JCLI-D-15-0734.1
McCulloch, M., Falter, J., Trotter, J. and Montagna, P. (2012). Coral resilience to
ocean acidification and global warming through pH up-regulation. Nat. Clim.
Change 2, 623-627. doi:10.1038/nclimate1473
Meinshausen, M., Smith, S. J., Calvin, K., Daniel, J. S., Kainuma, M. L. T.,
Lamarque, J.-F., Matsumoto, K., Montzka, S. A., Raper, S. C. B., Riahi, K. et al.
(2011). The RCP greenhouse gas concentrations and their extensions from 1765
to 2300. Clim. Change 109, 213-241. doi:10.1007/s10584-011-0156-z
Miller, C. B. and Wheeler, P. A. (2012). Biological Oceanography, 2nd edn.
Chichester: Wiley-Blackwell.
Muller, E. B., Kooijman, S. A. L. M., Edmunds, P. J., Doyle, F.J. and Nisbet, R. M.
(2009). Dynamic energy budgets in syntrophic symbiotic relationships between
heterotrophic hosts and photoautotrophic symbionts. J. Theor. Biol. 259, 44-57.
doi:10.1016/j.jtbi.2009.03.004
Nii, C. M. and Muscatine, L. (1997). Oxidative stress in the symbiotic sea anemone
Aiptasia pulchella (Carlgren, 1943): Contribution of the animal to superoxide ion
production at elevated temperature. Biol. Bull. 192, 444-456. doi:10.2307/
1542753
NOAA Coral Reef Watch (2019). NOAA Coral Reef Watch 5km Virtual Station Time
Series Data for the Hawaiian Islands. College Park, MD: NOAA Coral Reef Watch.
https://coralreefwatch.noaa.gov/product/vs/timeseries/polynesia.php (accessed
9 February 2019).
Noonan, S. H. C. and Fabricius, K. E. (2016). Ocean acidification affects
productivity but not the severity of thermal bleaching in some tropical corals. ICES
J. Mar. Sci. 73, 715-726. doi:10.1093/icesjms/fsv127
Ogston, A. S. and Field, M. E. (2010). Predictions of turbidity due to enhanced
sediment resuspension resulting from sea-level rise on a fringing coral reef:
evidence from Molokai, Hawaii. J. Coast. Res. 26, 1027-1037. doi:10.2112/
JCOASTRES-D-09-00064.1
Parys, E. and Jastrze
̨bski, H. (2006). Light-enhanced dark respiration in leaves,
isolated cells and protoplasts of various types of C4 plants. J. Plant Physiol. 163,
638-647. doi:10.1016/j.jplph.2005.05.009
Pochon, X., Stat, M., Takabayashi, M., Chasqui, L., Chauka, L. J., Logan,
D. D. K. and Gates, R. D. (2010). Comparison of endosymbiotic and free-living
Symbiodinium (Dinophyceae) diversity in a Hawaiian reef environment. J. Phycol.
46, 53-65. doi:10.1111/j.1529-8817.2009.00797.x
10
RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb223198. doi:10.1242/jeb.223198
Journal of Experimental Biology
Putnam, H. M., Mayfield, A. B., Fan, T. Y., Chen, C. S. and Gates, R. D. (2013).
The physiological and molecular responses of larvae from the reef-building coral
Pocillopora damicornis exposed to near-future increases in temperature and
pCO
2
.Mar. Biol. 160, 2157-2173. doi:10.1007/s00227-012-2129-9
Putnam, H. M., Davidson, J. M. and Gates, R. D. (2016). Ocean acidification
influences host DNA methylation and phenotypic plasticity in environmentally
susceptible corals. Evol. Appl. 9, 1165-1178. doi:10.1111/eva.12408
Reynaud, S., Leclercq, N., Romaine-Lioud, S., Ferrier-Pages, C., Jaubert, J.
and Gattuso, J.-P. (2003). Interacting effects of CO
2
partial pressure and
temperature on photosynthesis and calcification in a scleractinian coral. Glob.
Change Biol. 9, 1660-1668. doi:10.1046/j.1365-2486.2003.00678.x
Roberty, S., Bailleul, B., Berne, N., Franck, F. and Cardol, P. (2014). PSI Mehler
reaction is the main alternative photosynthetic electron pathway in Symbiodinium
sp., symbiotic dinoflagellates of cnidarians. New Phytol. 204, 81-91. doi:10.1111/
nph.12903
Rogers, C. S. (1979). The effect of shading on coral reef structure and function. J.
Exp. Mar. Biol. Ecol. 41, 269-288. doi:10.1016/0022-0981(79)90136-9
Rosenfeld, D., Zhu, Y., Wang, M., Zheng, Y., Goren, T. and Yu, S. (2019). Aerosol-
driven droplet concentrations dominate coverage and water of oceanic low-level
clouds. Science 363, eaav0566. doi:10.1126/science.aav0566
Rowan, R., Whitney, S. M., Fowler, A. and Yellowlees, D. (1996). Rubisco in
marine symbiotic dinoflagellates: form ii enzymes in eukaryotic oxygenic
phototrophs encoded by a nuclear multigene family. Plant Cell 8, 539-553.
doi:10.1105/tpc.8.3.539
Sato, Y. and Suzuki, K. (2019). How do aerosols affect cloudiness? Science 363,
580-581. doi:10.1126/science.aaw3720
Schmidt-Roach, S., Miller, K. J., Lundgren, P. and Andreakis, N. (2014). With
eyes wide open: a revision of species within and closely related to the Pocillopora
damicornis species complex (Scleractinia; Pocilloporidae) using morphology and
genetics. Zool. J. Linn. Soc. 170, 1-33. doi:10.1111/zoj.12092
Schneider, T., Kaul, C. M. and Pressel, K. G. (2019). Possible climate transitions
from breakup of stratocumulus decks under greenhouse warming. Nat. Geosci.
12, 163-167. doi:10.1038/s41561-019-0310-1
Schrameyer, V., Wangpraseurt, D., Hill, R., Ku
̈hl, M., Larkum, A. W. D. and
Ralph, P. J. (2014). Light respiratory processes and gross photosynthesis in two
scleractinian corals. PLOS ONE 9, e110814. doi:10.1371/journal.pone.0110814
Shamberger, K. E. F., Feely, R. A., Sabine, C. L., Atkinson, M. J., DeCarlo, E. H.,
Mackenzie, F. T., Drupp, P. S. and Butterfield, D. A. (2011). Calcification and
organic production on a Hawaiian coral reef. Mar. Chem. 127, 64-75. doi:10.1016/
j.marchem.2011.08.003
Skirving, W. and Guinotte, J. (2000). The sea surface temperature story on the
Great Barrier Reef during the coral bleaching event of 1998. In Oceanographic
Processes of Coral Reefs (ed. E. Wolanski), pp. 301-313. CRC Press.
Stat, M., Morris, E. and Gates, R. D. (2008). Functional diversity in coral
dinoflagellate symbiosis. Proc. Natl. Acad. Sci. USA 105, 9256-9261. doi:10.
1073/pnas.0801328105
Stat, M., Yost, D. M. and Gates, R. D. (2015). Geographic structure and host
specificity shape the community composition of symbiotic dinoflagellates in corals
from the Northwestern Hawaiian Islands. Coral Reefs 34, 1075-1086. doi:10.
1007/s00338-015-1320-0
Stokes, D., Walker, D. A., Grof, C. P. L. and Seaton, G. G. R. (1990). Light
enhanced dark respiration. In Perspectives in Biochemical and Genetic
Regulation of Photosynthesis (ed. I. Zelitch), pp. 319-338. New York: Alan R Liss.
Suggett, D. J., Dong, L. F., Lawson, T., Lawrenz, E., Torres, L. and Smith, D. J.
(2013). Light availability determines susceptibility of reef building corals to ocean
acidification. Coral Reefs 32, 327-337. doi:10.1007/s00338-012-0996-7
Sweet, M. J. and Brown, B. E. (2016). Coral responses to anthropogenic stress in
the twenty-first century: an ecophysiological perspective. Oceanogr. Mar. Biol.
Annu. Rev. 54, 271-314.
Takahashi, S., Nakamura, T., Sakamizu, M., van Woesik, R. and Yamasaki, H.
(2004). Repair machinery of symbiotic photosynthesis as the primary target of
heat stress for reef-building corals. Plant Cell Physiol. 45, 251-255. doi:10.1093/
pcp/pch028
Tchernov, D., Kvitt, H., Haramaty, L., Bibby, T. S., Gorbunov, M. Y., Rosenfeld,
H. and Falkowski, P. G. (2011). Apoptosis and the selective survival of host
animals following thermal bleaching in zooxanthellate corals. Proc. Natl. Acad.
Sci. USA 108, 9905-9909. doi:10.1073/pnas.1106924108
Tremblay, P., Naumann, M. S., Sikorski, S., Grover, R. and Ferrier-Pagès, C.
(2012). Experimental assessment of organic carbon fluxes in the scleractinian
coral Stylophora pistillata during a thermal and photo stress event. Mar. Ecol.
Prog. Ser. 453, 63-77. doi:10.3354/meps09640
Vogel, N., Meyer, F. W., Wild, C. and Uthicke, S. (2015). Decreased light
availability can amplify negative impacts of ocean acidification on calcifying coral
reef organisms. Mar. Ecol. Prog. Ser. 521, 49-61. doi:10.3354/meps11088
Vytopil, E. and Willis, B. (2001). Epifaunal community structure in Acropora spp.
(Scleractinia) on the Great Barrier Reef: implications of coral morphology and
habitat complexity. Coral Reefs 20, 281-288. doi:10.1007/s003380100172
Wall, C. B., Fan, T.-Y. and Edmunds, P. J. (2014). Ocean acidification has no effect
on thermal bleaching in the coral Seriatopora caliendrum.Coral Reefs 33,
119-130. doi:10.1007/s00338-013-1085-2
Wall, C. B., Mason, R. A. B., Ellis, W. R., Cunning, R. and Gates, R. D. (2017).
Elevated pCO
2
affects tissue biomass composition, but not calcification, in a reef
coral under two light regimes. R. Soc. Open Sci. 4, 170683. doi:10.1098/rsos.
170683
Warner, M. E., Fitt, W. K. and Schmidt, G. W. (1996). The effects of elevated
temperature on the photosynthetic efficiency of zooxanthe llae in hospite from four
different species of reef coral: a novel approach. Plant Cell Environ. 19, 291-299.
doi:10.1111/j.1365-3040.1996.tb00251.x
Warner, M. E., Fitt, W. K. and Schmidt, G. W. (1999). Damage to photosystem II in
symbiotic dinoflagellates: a determinant of coral bleaching. Proc. Natl. Acad. Sci.
USA 96, 8007-8012. doi:10.1073/pnas.96.14.8007
Weis, V. M. (2008). Cellular mechanisms of cnidarian bleaching: stress causes the
collapse of symbiosis. J. Exp. Biol. 211, 3059-3066. doi:10.1242/jeb.009597
Wooldridge, S. A. (2009). A new conceptual model for the warm-water breakdown
of the coralalgae endosymbiosis. Mar. Freshw. Res. 60, 483-496. doi:10.1071/
MF08251
Yakovleva, I. and Hidaka, M. (2004). Different effects of high temperature
acclimation on bleaching-susceptible and tolerant corals. Symbiosis 37, 87-105.
Zunino, S., Canu, D. M., Bandelj, V. and Solidoro, C. (2017). Effects of ocean
acidification on benthic organisms in the Mediterranean Sea under realistic
climatic scenarios: a meta-analysis. Reg. Stud. Mar. Sci. 10, 86-96. doi:10.1016/j.
rsma.2016.12.011
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Ocean acidification (OA) is predicted to reduce reef coral calcification rates and threaten the long-term growth of coral reefs under climate change. Reduced coral growth at elevated pCO2 may be buffered by sufficiently high irradiances, however, the interactive effects of OA and irradiance on other fundamental aspects of coral physiology, such as the composition and energetics of coral biomass, remain largely unexplored. This study tested the effects of two light treatments (7.5 vs. 15.7 mol photons m-2 d-1) at ambient- or elevated-pCO2 (435 vs. 957 μatm) on calcification, photopigment and symbiont densities, biomass reserves (lipids, carbohydrates, proteins), and biomass energy content (kJ) of the reef coral Pocillopora acuta from Kāne‘ohe Bay, Hawai‘i. While pCO2 and light had no effect on either area- or biomass-normalized calcification, tissue lipids gdw-1 and kJ gdw-1 were reduced 15% and 14% at high pCO2, and carbohydrate content increased 15% under high light. The combination of high light and high pCO2 reduced protein biomass (per unit area) by ~ 20%. Thus, under ecologically relevant irradiances, P. acuta in Kāne‘ohe Bay does not exhibit OA-driven reductions in calcification reported for other corals; however, reductions in tissue lipids, energy content, and protein biomass suggest OA induced an energetic deficit and compensatory catabolism of tissue biomass. The null effects of OA on calcification at two irradiances support a growing body of work concluding some reef corals may be able to employ compensatory physiological mechanisms that maintain present-day levels of calcification under OA. However, negative effects of OA on P. acuta biomass composition and energy content may impact the long-term performance and scope for growth of this species in a high pCO2 world.
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While research on ocean acidification (OA) impacts on coral reefs has focused on calcification, relatively little is known about effects on coral photosynthesis and respiration, despite these being among the most plastic metabolic processes corals may use to acclimatize to adverse conditions. Here, we present data collected between 2016 and 2018 at three natural CO2 seeps in Papua New Guinea where we measured the metabolic flexibility (i.e. in hospite photosynthesis and dark respiration) of 12 coral species. Despite some species-specific variability, metabolic rates as measured by net oxygen flux tended to be higher at high pCO2 (ca 1200 µatm), with increases in photosynthesis exceeding those of respiration, suggesting greater productivity of Symbiodiniaceae photosynthesis in hospite, and indicating the potential for metabolic flexibility that may enable these species to thrive in environments with high pCO2. However, laboratory and field observations of coral mortality under high CO2 conditions associated with coral bleaching suggests that this metabolic subsidy does not result in coral higher resistance to extreme thermal stress. Therefore, the combined effects of OA and global warming may lead to a strong dec