In Situ Effects of Low pH and Elevated HCO
Juvenile Massive Porites spp. in Moorea,
CHRISTOPHER B. WALL
*, AND PETER J. EDMUNDS
Department of Biology, California State University Northridge, 18111 Nordhoff Street, Northridge,
California 91330-8303, and
College of Life Sciences, Santa Monica College, 1900 Pico Boulevard,
Santa Monica, California 90405-1628
Abstract. Juvenile colonies of massive Porites spp. were
exposed to manipulated pH and bicarbonate ([HCO
situ to test the hypothesis that ocean acidiﬁcation (OA) does
not affect respiration and calciﬁcation. Incubations lasted
28 h and exposed corals to ambient temperature and light
with ecologically relevant water motion. Three treatments
were applied: (1) ambient conditions of pH 8.04 and 1751
(Treatment 1), (2) pCO
acidiﬁcation of pH 7.73 and 2011
(Treatment 2), and (3) pCO
of pH 7.69 and 2730
(Treatment 3). The
third treatment providing elevated [HCO
] was used to test
for stimulatory effects of dissolved inorganic carbon on
calciﬁcation under low pH and low saturation of aragonite
), but it does not reﬂect conditions expected to occur
-driven OA. Calciﬁcation of juvenile massive
Porites spp. was affected by treatments, with an 81% ele-
vation in Treatment 3 versus Treatment 1, but no difference
between Treatments 1 and 2; respiration and the metabolic
expenditure concurrent with calciﬁcation remained unaf-
fected. These ﬁndings indicate that juvenile massive Porites
spp. are resistant to short exposures to OA in situ, and
separately, that they can increase calciﬁcation at low pH and
] is elevated. Juvenile Porites spp. may
therefore be limited by dissolved inorganic carbon under
Coral reefs are threatened by natural and anthropogenic
factors, including global climate change and ocean acidiﬁ-
cation (OA) (Hoegh-Guldberg et al., 2007; Wilkinson,
2008). OA poses a particularly severe threat, because if
corals do not ﬁrst succumb to rising temperature (Hoegh-
Guldberg et al., 2007), OA challenges their capacity to
produce calcareous skeletons (Hofmann et al., 2010). OA
originates in the dissolution of atmospheric CO
ter, resulting in decreases in seawater pH, the concentration
of carbonate ([CO
]), and the saturation state of aragonite
), and an increase in the concentration of bicarbonate
]) (Kleypas et al., 1999). Together, these effects
impair the ability of corals to deposit CaCO
(Jury et al.,
2010; Hofmann et al., 2010; Edmunds et al., 2012; Comeau
et al., 2013b), and diminish their capacity to function as
ecosystem engineers (Wild et al., 2011).
Laboratory studies have contributed much to the under-
standing of the response of corals to OA (Andersson and
Gledhill, 2013), particularly with regard to the underlying
physiological mechanisms (Erez et al., 2011). However,
laboratory experiments typically are performed under con-
ditions that do not replicate the natural environment per-
fectly, notably by providing light at a constant low intensity
throughout the day, and with a spectral composition differ-
ing from ambient sunlight (Kinzie et al., 1984; Schlacher et
al., 2007). Light stimulates coral calciﬁcation (Gattuso et
al., 1999), fuels Symbiodinium photosynthesis, and facili-
tates autotrophic nutrition by the holobiont (Pearse and
Muscatine, 1971). Also of great importance to corals is the
hydrodynamic regime of reef environments (Monismith,
2007), which is difﬁcult to recreate in tanks and yet is
Received 18 February 2013; accepted 5 September 2013.
* To whom correspondence should be addressed. E-mail: cbw0047@
, saturation state of aragonite; OA, ocean acidiﬁca-
tion; PAR, photosynthetically active radiation; TA, total alkalinity.
Reference: Biol. Bull. 225: 92–101. (October 2013)
© 2013 Marine Biological Laboratory
critical for multiple aspects of coral physiology (Dennison
and Barnes, 1988; Patterson et al., 1991). Given the limi-
tations of laboratory experiments, there is a need to evaluate
the effects of OA on corals in the natural environment
(Langdon and Atkinson, 2005; Holcomb et al., 2010). In
situ experiments have been used to study the physiology of
corals and coral reefs for decades (Porter, 1980; Pearson et
al., 1984; Carpenter, 1985; Patterson et al., 1991; Ralph et
al., 1999; Levy et al., 2006), but to our knowledge, there
have been only two studies in which in situ approaches have
been used to study the effects of OA on corals (Chauvin et
al., 2011; Klein et al., 2012). Natural CO
seeps afford the
potential to study aspects of the effects of OA in the natural
environment (Hall-Spencer et al., 2008; Fabricius et al.,
2011), but the rarity of such locations and their suitability
mostly for mensurative analyses (sensu Hurlbert, 1984)
limits the general application of this approach.
The objective of this study was to utilize chambers placed
in situ to examine the effects of low pH and high [HCO
on juvenile massive Porites spp. Three hypotheses were
tested: (1) low pH and high [HCO
] have no effect on
respiration or calciﬁcation, (2) the energetic expenditure
concurrent with calciﬁcation is unaffected by OA, and (3)
low pH impairs calciﬁcation at high [HCO
seawater). As rationales for these hypotheses, we
reasoned that OA typically reduces coral calciﬁcation
(Comeau et al., 2013b) and can increase the rate of respi-
ration (Crawley et al., 2010; but see Edmunds, 2012), with
the energetic cost of depositing CaCO
referred to as a
cause of stimulatory effects of OA on respiration (Fabry et
al., 2008; Erez et al., 2011). As elevated [HCO
mitigate the negative effects of OA in vitro (Marubini et al.,
2008; Comeau et al., 2012), it was compelling to test for
similar effects in situ.
Materials and Methods
We used three seawater treatments of contrasting pH and
carbonate chemistry to examine the effects of OA and
] on juvenile massive Porites spp. Juvenile
massive Porites spp. in Moorea is a functional group con-
sisting of about 85% P. lutea (Edwards and Haime, 1860)
and about 15% P. lobata (Dana, 1846) (Edmunds, 2009),
which are difﬁcult to distinguish from each other while
alive. Experiments were performed in three trials (begin-
ning on 4, 6, and 8 February 2012), with six corals in each
trial exposed to treatments (n⫽2 corals treatment
28 h in acrylic chambers at 1.5-m depth on a fringing reef
(Fig. 1). Seawater treatments contrasted (1) ambient pH and
] (Treatment 1, the control against which
the other treatments were gauged); (2) low pH and high
] (Treatment 2); and (3) low pH and very high
] (Treatment 3). Treatment 1 represented present
seawater conditions on the shallow reefs of Moorea (⬃pH
8.00 and 1750
); Treatment 2 reﬂected
the seawater conditions projected to occur in 100 y (⬃pH
7.70 and 2000
) under representative
concentration pathway (RCP) 6.0 (⬃95 Pa pCO
Vuuren et al., 2011); and Treatment 3 (⬃pH 7.70 and 2700
) tested the hypothesis that elevated
] stimulates calciﬁcation at reduced ⍀
pH. Although Treatment 3 is not a feasible combination of
future seawater conditions attributable to OA, it allowed
further exploration of the role of HCO
in coral calciﬁca-
tion (sensu Comeau et al., 2012), as well as consideration of
the possibility that elevated [HCO
] alleviates the effects
of low pH (Comeau et al., 2012). We reasoned that the
results of Treatment 3 would therefore be valuable in de-
signing future experiments focused on the mechanism by
which corals can respond to OA.
Nine chambers (2.47 l) were made from custom-cast,
UV-transparent acrylic (Industrial Plastics, California),
which transmits UV A and B radiation (280 – 400 nm) and
phosynthetically active radiation (PAR; 400 –700 nm)
(Gleason et al., 2006). A test of the light transmission
qualities (for UV A and PAR) of the acrylic polymer was
performed using a cosine-corrected sensor attached to a
ﬁber optic cable and a spectrophotometer (USB-2000,
Ocean Optics, Dunedin, Florida) and operated using a PC
running the manufacturer’s software (Spectra Suite 2.0,
Ocean Optics). Light was measured with spectral resolution
between 350 and 1000 nm and corrected against a known
color temperature (°Kelvin). There was minimal attenuation
of UV A and PAR, with greater than 96% transmission
through the acrylic of light between 350 nm and 1000 nm
wavelength (Fig. 2); transmission of light at wavelengths
below 350 nm was not measured.
Three chambers were allocated to each treatment, with
two exposing corals to treatments (n⫽1 coral chamber
and one ﬁlled with seawater alone as a control. All cham-
bers were ﬁlled with fresh seawater at the start of each trial
(n⫽3), and stirred with a motor (Playmobil, Zirndorf,
Germany) that provided a mean ﬂow speed of 15.8 ⫾1.3
(⫾SE, n⫽12) in the chamber. Flow speeds were
determined in a preliminary study in which hydrated Ar-
temia spp. eggs within the chambers were photographed
(after Sebens and Johnson, 1991). At the start of each trial,
chambers were ﬁlled with treatment seawater, and bubbles
were removed before the chambers were sealed and placed
on the reef. Chambers remained on the reef for 28 h, but
were retrieved at 4-h intervals to replenish treatment sea-
water and batteries in the stirring motors. This procedure
generally took less than 10 min, and corals were kept
submerged at all times. Light intensity (PAR) and seawater
temperature adjacent to the chambers were recorded at
10-min intervals using a 4spherical quantum sensor
(MkV-L, JFE Advantech Co., Kobe, Japan) and Hobo Wa-
IN SITU EFFECTS OF OCEAN ACIDIFICATION ON CORALS
ter Temp Pro v2 loggers (⫾0.2 °C, Onset Computer,
Coral collection and carbonate chemistry
Juvenile Porites spp. (ⱕ4.0-cm diameter, n⫽18) were
collected from 2–3-m depth in the back reef of Moorea,
between 28 January 2012 and 1 February 2012. Corals were
transported to the Richard B. Gump South Paciﬁc Research
Station, attached to plastic bases with epoxy (Z-Spar A788),
and placed in a ﬂow-through tank (1000 l) to recover. This
tank was ﬁlled with ﬁltered seawater (50
m) at about 27.5
°C and illuminated with two 75-W LED lamps (Sol White
LED Module, Aquaillumination, Iowa) that supplied light at
mol photons m
(mean ⫾SE, n⫽75), as
measured underwater using a spherical quantum sensor (Li-
Cor LI-193). Colonies remained in the recovery tank until
used in the trials.
To create pH and [HCO
] treatments, the pCO
seawater was manipulated by bubbling ambient air or CO
enriched air into three 150-l reservoirs supplied with ﬁltered
m). Gas mixtures were created using a sole-
noid-controlled system (Model A352, Qubit Systems, On-
Figure 1. Photo of (A) juvenile massive Porites spp., (B) fringing reef off the Richard B. Gump South
Paciﬁc Research Station in Cook’s Bay, Moorea, and (C) the 2.47-l experimental chambers (23 x 23 x 8 cm) each
housing a single coral colony in situ.i⫽Location of chambers on the fringing reef at 1.5-m depth, ii ⫽juvenile
colony attached to mesh with epoxy, and iii ⫽submersible stirring motor. (D) Schematic illustrating the location
of coral and stirring motor within chambers. Photo credits (A) D. Liittschwager, used with permission; (B–D)
94 C. B. WALL AND P. J. EDMUNDS
tario, Canada), as detailed in Edmunds (2012). Seawater for
Treatment 1 was un-manipulated; seawater for Treatment 2
was equilibrated with pCO
at 98.9 Pa; seawater for Treat-
ment 3 was obtained by augmenting Treatment 2 seawater
with baking soda (0.9 mmol l
, Church and
Dwight Co., California) to increase [HCO
] to 2730
of 7.69. Seawater conditions within the three
reservoirs were monitored for salinity, pH on the total scale
), total alkalinity (TA,
), and carbonate
chemistry for one week prior to the start of the experiment,
and daily during the experiment (4 –9 February). Analyses
of seawater were conducted according to standard operating
procedure (SOP) 3b of Dickson et al. (2007), as detailed in
Comeau et al. (2012), with ﬁnal values for carbon chemistry
calculated using the seacarb script in R(R Foundations for
Statistical Computing; Lavigne and Gattuso, 2011). Titra-
tions of certiﬁed reference materials (Batch 105) provided
by A. G. Dickson (Scripps Institution of Oceanography)
revealed determination of TA to be within 0.3– 4.5
of certiﬁed TA values (i.e., ⱕ0.2%).
Calciﬁcation and respiration
After 24-h incubations, the response of the corals was
assessed as rates of calciﬁcation and respiration. Calciﬁca-
tion was measured in situ as the change in TA of seawater
over 4 h (after Smith and Key, 1975) from about 1000 to
1400 h, with the volume of the stirring motor and coral
subtracted from each seawater sample. Calciﬁcation was
adjusted for the change in TA in the control chambers, and
standardized by time and the surface area of the coral tissue
). Surface area of the corals was
determined using aluminum foil (Marsh, 1970) and was
completed after the respiration measurements.
After measurements of calciﬁcation (at ⬃1500 h), corals
were transferred to respirometers (0.24 l) ﬁlled with ﬁltered
m) representing the same conditions as the in
situ treatments, and kept in darkness for about 30 min to
reduce the effects of light on respiration (Edmunds and
Davies, 1988). After dark acclimation, respiration of corals
was measured at 28 °C with a stir bar used to create a ﬂow
speed of 3.0 ⫾0.2 cm s
(mean ⫾SE, n⫽16) determined
as described above. Changes in pO
in seawater were mea-
sured with optrodes (Foxy-R, 1.58-mm diameter, Ocean
Optics) calibrated against water-saturated air (100%) and a
zero solution (saturated sodium sulﬁte in 0.01 mol l
sodium tetraborate), and connected to spectrophotometers
(USB2000 and NeoFox, Ocean Optics) that logged O
uration onto a PC running Ocean Optics software (OOISen-
sors, ver. 1.00.08 and NeoFox Viewer ver. 2.3, Ocean
saturation was converted to
using tabulated values for O
solubility [N. Ramsing and J.
Gundersen at Unisense (Aarhus, Denmark), based on Garcia
and Gordon (1992)], yielding a saturated oxygen content of
at 28 °C, a salinity of 36, and 101.3
kPa atmospheric pressure. Respiration rates were deter-
mined by regressing O
concentration against time, correct-
ing for O
ﬂuxes in control chambers, and standardizing
oxygen consumption to the surface area of the coral tissue
Respiration rates were used to estimate the metabolic
energy expenditure concurrent with calciﬁcation by con-
verting hourly O
consumption to energy units (joules)
using a conversion of 440 J mmol O
(Elliot and Davison,
1975), assuming lipids are the primary respiratory substrate
(Patton et al., 1977). Respiratory energy expenditure (J
) was normalized to the calciﬁcation rate (
) and expressed as J g
uate the energy expenditure concurrent with calciﬁcation.
Calciﬁcation, respiration, energy expenditure concurrent
with calciﬁcation, and incubation conditions (pH
]) were compared among treatments using one-way
ANOVA. As consecutive trials were performed over 3 d
with potential differences in physical conditions among
days, a one-way ANOVA was used to test for differences in
PAR and temperature among trials. Post hoc analyses were
performed using Tukey’s Honestly Signiﬁcant Difference
(HSD) test, and statistical assumptions of normality and
homoscedasticity required for ANOVA were tested by
graphical analysis of residuals. Analyses were completed
Figure 2. The spectral comparison of the relative irradiance of sun-
light measured from 350 to 1000 nm and corrected against a known color
temperature (°Kelvin) for natural sunlight (black) and sunlight transmitted
through UV-transmitting acrylic polymer (gray).
95IN SITU EFFECTS OF OCEAN ACIDIFICATION ON CORALS
with Systat 11 software (Systat, Inc., Illinois) using a Win-
dows operating system. Power analysis was performed on
select results according to Zar (2010).
The chemical conditions of seawater used to ﬁll the
chambers were maintained with a high degree of precision
(Table 1) and differed signiﬁcantly among treatments in
terms of pH
⫽44.84, P⬍0.001) and [HCO
⫽720.79, P⬍0.001). Although the chemical con-
ditions were affected by the incubations, notably for oxygen
concentration (through the effects of respiration and photo-
synthesis) and TA (through the effects of calciﬁcation),
these effects were minimized by changing the seawater
every 4 h. Mean salinity throughout the treatments was
35.9 ⫾0.1 (⫾SE, n⫽16), and the mean temperature was
28.8 ⫾0.2 °C (n⫽514, pooled among days). However,
temperature differed among trials (F
0.001) and was slightly warmer during the last trial (8
February, 29.4 ⫾0.2 °C) than the ﬁrst trial (4 February,
28.2 ⫾0.2 °C) (both mean ⫾SE, n⫽170 –171). The mean
light intensity during the daylight portion of the incubations
was 1072 ⫾51
mol photons m
measurements over 3 trials), but sustained maximum inten-
sities reaching about 2300
mol photons m
grated each day, the light regime provided 52.3 ⫾8.5 mol
(⫾SD, n⫽3 days). Over the 4-h period
when calciﬁcation was measured (i.e., 1000 –1400 h), the
mean irradiance at 1.5-m depth was 1769 ⫾60
(⫾SE, n⫽86) and light did not differ
among trials (F
All corals appeared healthy and showed no visible signs
of stress or loss of pigmentation during the experiments;
however, the loss of two seawater samples in Treatment 2
reduced calciﬁcation measurements to four corals. The in
situ incubations proved successful in exposing corals to
seawater of contrasting carbonate chemistry under physical
conditions similar to those in the natural environment. Rates
of calciﬁcation in the light (mean ⫾SE) for control corals
(e.g., Treatment 1) were 67.92 ⫾14.48
and 52.19 ⫾8.76
and 123.04 ⫾
in Treatment 2 and Treatment 3,
respectively. Hourly calciﬁcation rates differed signiﬁcantly
among treatments (F
⫽6.56, P⫽0.011) (Fig. 3).Post
hoc analyses revealed that hourly calciﬁcation was in-
creased signiﬁcantly in Treatment 3 (HCO
compared to Treatment 1 (ambient conditions) (P⬎0.05),
but no other contrasts were signiﬁcant (P⬎0.50). Calciﬁ-
cation in Treatment 3 (HCO
-enriched) was signiﬁcantly
higher than in other treatments and was elevated 82% and
113% relative to Treatment 1 and Treatment 2, respectively
(Fig. 3). Mean respiration (⫾SE) ranged from 0.39 ⫾0.05
(Treatment 2) to 0.46 ⫾0.06
(Treatment 3), but it did not vary signiﬁcantly
among treatments (F
⫽0.37, P⫽0.697) (Fig. 3),
although the power (1-
) of this test was low (⬍0.30).
Converting respiratory O
consumption to joules revealed
a mean energy expenditure of 0.17 to 0.22 J cm
corals across treatments, which corresponded to mean en-
ergy expenditures per colony of 3.30 to 4.38 J h
calciﬁcation rates of 52.19
g and 123.04
. Together these values revealed that the energy expen-
diture coincident with calciﬁcation ranged from (⫾SE)
1804 ⫾260 to 3461 ⫾459Jg
in Treatment 3 and
Treatment 2, respectively (Fig. 3), although these values did
not differ among treatments (F
Laboratory-based mesocosms have dominated studies of
the effects of ocean acidiﬁcation (OA) on corals, in part due
to the logistical challenges of manipulating seawater chem-
istry, but such approaches have limited utility in evaluating
how corals respond to similar conditions in situ. While
laboratory experiments are designed to create conditions
resembling those found in the natural environment at the
site where study corals are collected, many fall short of
attaining this objective. For instance, the common use of
low-intensity artiﬁcial lighting does not reﬂect conditions
Summary of physical and chemical conditions for three treatments of Porites spp. colonies maintained in 2.47-l acrylic chambers in situ at 28.8 °C
between 4 and 9 February 2012
1 8.04 ⫾0.01 2359 ⫾3 41.1 ⫾0.8 1751 ⫾6 246 ⫾2 2008 ⫾4 3.95 ⫾0.03
2 7.73 ⫾0.04 2358 ⫾2 98.9 ⫾9.5 2011 ⫾25 141 ⫾10 2177 ⫾17 2.27 ⫾0.15
3 7.69 ⫾0.03 3131 ⫾8 146.4 ⫾10.5 2730 ⫾21 171 ⫾8 2938 ⫾16 2.75 ⫾0.12
Values are mean ⫾SE (n⫽6 for carbonate chemistry; TA ⫽total alkalinity; DIC ⫽dissolved inorganic carbon; ⍀
⫽aragonite saturation state;
Treatment 1 ⫽ambient pH, ambient HCO
; Treatment 2 (e.g., end of century pCO
)⫽low pH, high HCO
; Treatment 3 (e.g., pCO
enriched) ⫽low pH, very high HCO
. Carbonate chemistry was calculated using the seacarb package in R.
96 C. B. WALL AND P. J. EDMUNDS
on shallow reefs or simulate the intensity and spectral
composition of sunlight reaching the study depth (Kinzie et
al., 1984). As the quality and quantity of light has important
implications for photoautotrophic nutrition and calciﬁcation
in corals (Kinzie et al., 1984; Barnes and Chalker, 1990;
Grottoli and Wellington, 1999) and affects the response of
coral fragments (Suggett et al., 2013) and coral recruits
(Dufault et al., 2013) to pCO
, it is clear that light is one
physical parameter that would beneﬁt from closer attention.
To address this limitation (and others) of laboratory-based
experiments, here we emphasize the utility of simple in situ
approaches (Chauvin et al., 2011). Our in situ approach has
the potential to support tests for short-term biological ef-
fects of OA under physical conditions closely resembling
those found on coral reefs, and may provide a means to
evaluate effects of various light treatments (both UV and
PAR) on coral calciﬁcation under ambient and elevated
The mean intensity of PAR adjacent to the incubation
chambers at 1.5-m depth (1072 ⫾51
mol photons m
) was 2–10 times higher than irradiances reported in OA
studies in which incubations have been conducted in labo-
ratory mesocosms. For instance, Edmunds (2012) reported
an intensity of 537
mol photons m
, Schneider and
Erez (2006) reported a light intensity of about 350
, Crawley et al. (2010) employed a maxi-
mum irradiance of about 110
mol photons m
Albright et al. (2008) used a mean light intensity of less than
mol photons m
. However, a few OA experiments
have been performed under natural irradiances in outdoor
mesocosms on land (noon irradiances 700
mol photons m
; Anthony et al., 2008) and in ﬂumes
(17 mol– 40 mol photons m
; Langdon and Atkinson,
2005). In our study, not only was the light intensity greater
than in most previous studies using corals from shallow
reefs, but our incubations also included UV radiation, which
is important for the rhythmicity of Symbiodinium photosyn-
thesis in hospite (Sorek and Levy, 2012), coral bleaching
(Lesser, 1997), and photooxidative stress in Symbiodinium
(Shick et al., 1995). Moreover, exposure to ecologically
relevant intensities of UV radiation may favor slight reduc-
tions in calciﬁcation rates (Jokiel and York, 1982; Roth et
al., 1982) that are relevant to corals under natural condi-
tions. While explicitly evaluating the role of UV radiation
on coral calciﬁcation was beyond the scope of this study, we
note that in situ chambers create the potential for such
analyses in the future using UV-transparent and UV-absorb-
ing polymers (Shick et al., 1995; Gleason et al., 2006). This
would not be possible in the laboratory using metal-halide
and LED lamps that do not emit signiﬁcant radiation at less
than 400 nm (Schubert and Kim, 2005), and instead would
require specialized UV lights (Shick et al., 1999). We
suggest that our in situ approach could be used to examine
OA effects on corals using light conditions (PAR and UV)
of similar intensity and ﬂux (i.e., diel oscillations) to those
experienced by corals on the reef. Striving for ecologically
relevant light treatments should be a priority of OA research
in the laboratory.
In addition to the advantages of being able to manipulate
UV light to test for interactive effects with OA on corals, in
situ chambers provide access to high intensities of PAR that
are important to symbiotic corals for photosynthesis (Da-
vies, 1991) and calciﬁcation (Barnes and Chalker, 1990;
Anthony et al., 2002; Allemand et al., 2004). Light intensity
also modulates the response of corals to OA (Marubini et
al., 2001; Suggett et al., 2013), with recent work character-
Figure 3. Calciﬁcation, respiration, and the metabolic expenditure
concurrent with calciﬁcation in juvenile massive Porites spp. exposed for
28 h to three treatments (ambient seawater [SW], ocean acidiﬁcation
conditions for the year 2100, and HCO
-enriched/low pH treatment) in
chambers maintained in situ. (A) Calciﬁcation (left ordinate) and respira-
tion (right ordinate) normalized to surface area (cm
). (B) Metabolic
expenditure concurrent with calciﬁcation. Treatments signiﬁcantly affected
calciﬁcation (P⫽0.011), with letters indicating treatments that differed as
determined from post hoc analysis; there was no effect of treatment on
respiration (P⫽0.697) or metabolic expenditure concurrent with calciﬁ-
cation (P⫽0.135). Values displayed are mean ⫾SE.
97IN SITU EFFECTS OF OCEAN ACIDIFICATION ON CORALS
izing a pCO
-dependent shift in the nonlinear relationship
between light and calciﬁcation in recruits of Pocillopora
damicornis (Dufault et al., 2013). For these recruits, light
intensity affected calciﬁcation rates with an effect at 50
versus 89 Pa pCO
at intermediate light intensities (⬃70
mol photons m
), but reduced effects at lower and
higher light intensities (31
mol vs. 226
mol photons m
) (Dufault et al., 2013). It has been hypothesized that the
effect of light intensity on the response of corals to OA is
driven by a light-dependent utilization of HCO
ulates calciﬁcation and reduces the negative implications of
] at low pH (Gattuso et al., 1999;
Comeau et al., 2012). The high rates of calciﬁcation in
Treatment 3 (HCO
-enriched) of the present study lend
support to this possibility, particularly since ecologically
relevant high light intensities were attained with our in situ
Few studies have reported hourly calciﬁcation rates for
massive Porites spp., and no study has attempted to measure
in situ calciﬁcation under pCO
enrichment and ambient
light intensities. As a result, there are no comparable data
with which our results can be contrasted for the purpose of
testing for generality. However, hourly calciﬁcation rates
recorded in the light during the present study are within the
range reported for Porites (Comeau et al., 2013a), and when
extrapolated to a 24-h day assuming calciﬁcation in the light
is 3-fold greater than in the dark (Gattuso et al., 1999) and
each day consists of 12-h light and 12-h dark, daily calci-
ﬁcation for juvenile Porites spp. is similar to that previously
reported for this taxon in Moorea (Edmunds, 2011, 2012).
Therefore, it is reasonable to interpret our results as eco-
logically relevant, with treatment effects that are insightful
for understanding how corals respond to similar conditions
on the reef.
The calciﬁcation rate of juvenile massive Porites spp. in
the light under ambient conditions (e.g., Treatment 1) did
not differ signiﬁcantly from calciﬁcation under conditions
mimicking those expected by the end of the present century
(e.g., Treatment 2). The Treatment 2 result is inconsistent
with studies showing that OA reduces coral calciﬁcation
(Langdon and Atkinson, 2005; Schneider and Erez, 2006;
Comeau et al., 2013b), but is consistent with reports that
Porites is resistant to OA (Fabricius et al., 2011; Edmunds,
2012; Edmunds et al., 2012; Comeau et al., 2013a). How-
ever, interpreting Treatment 2 results relative to previous
studies is complicated by the measurement here of calciﬁ-
cation at high mid-day irradiances that probably would have
maximized both calciﬁcation and photosynthesis. It remains
possible that the present results might have differed during
longer incubations lasting weeks or months that would also
have captured the effects of reduced dark calciﬁcation and
skeletal dissolution at low saturation of aragonite (⍀
In Treatment 3, HCO
increased calciﬁcation 81% relative to ambient conditions,
despite coinciding with reduced ⍀
and low pH. Stimu-
lation of calciﬁcation in corals through elevated [HCO
has been reported previously (Marubini and Thake, 1999;
Herfort et al., 2008; Comeau et al., 2012); furthermore,
under OA conditions, elevated [HCO
] increases coral
calciﬁcation (Marubini et al., 2008; Jury et al., 2010; de
Putron et al., 2011; Comeau et al., 2012). At constant pH
for example, calciﬁcation in Madracis auretenra declined
with reduced [HCO
] but was stimulated with increased
], yet it was unresponsive to pH
(7.6 – 8.1) and
(1.7– 4.3) (Jury et al., 2010). HCO
above ambient seawater) stimulated calciﬁcation
in Stylophora pistillata at pH
7.6, 8.0, and 8.2, suggesting
that calciﬁcation may be carbon-limited in this species
(Marubini et al., 2008). While the exposure period for the
treatments was short in the current study (28 h), short
incubations (⬍3 h) have been useful in past experiments
examining the effects of nutrients and pCO
corals (Furla et al., 2000; Langdon and Atkinson, 2005;
Chauvin et al., 2011; Cumbo et al., 2013). While the im-
plications of the short incubations in the present study
deserve attention, our ﬁnding nevertheless suggests that
calciﬁcation in juvenile Porites spp. may not be DIC satu-
rated in situ at ambient [HCO
In tropical corals, calciﬁcation requires substantial
amounts of metabolic energy and may account for 13%–
30% of the entire metabolic costs (Allemand et al., 2011).
These costs are met by the supply of ATP from aerobic
respiration (with smaller amounts of ATP presumably from
glycolysis), and therefore aerobic respiration is likely to
reﬂect changes in the cost of calciﬁcation. The extent to
which shifts in costs of calciﬁcation can be detected through
measurements of aerobic respiration depends, however, on
the magnitude of the changes involved and the degree to
which the demands of other energy-requiring processes
covary. In the present study, treatments had no effect on
aerobic respiration, and we were unable to detect a change
in the total metabolic costs concurrent with calciﬁcation,
even though calciﬁcation increased 81% with elevated
]. The biological meaning of the null effect of OA
(Treatment 2) and HCO
enrichment (Treatment 3) on
coral respiration is uncertain, in part due to low statistical
power to detect an effect of the treatment on this dependent
Given the effect of [HCO
] on calciﬁcation in Treat-
ment 3 and a mean metabolic cost of calciﬁcation of 1804 J
, aerobic respiration should have increased from
to equal the metabolic costs
scaled proportionately from the control costs (i.e., Treat-
ment 1) associated with calciﬁcation (e.g., Jg
contrast to this prediction, the mean aerobic respiratory
demand in Treatment 3 was indistinguishable from that of
corals in other treatments, indicating that elevated [HCO
stimulated calciﬁcation without affecting metabolic expen-
98 C. B. WALL AND P. J. EDMUNDS
diture. Resolving the causes of this thermodynamic paradox
(i.e., the increase in a metabolically costly process without
an increased demand for metabolic energy) was beyond the
scope of this study, but we suspect it might reﬂect hyperoxic
stimulation of respiration (Shick, 1990) after maximum
photosynthesis in the control corals, which could conceal
the additional costs associated with enhanced calciﬁcation.
Alternatively, it is possible that respiration rates were mass-
transfer-limited in the small respiration chambers em-
ployed, where we were only able to create a ﬂow speed of
3.0 cm s
, which is lower than the 15.8 cm s
in the in
situ chambers where calciﬁcation was measured. Notwith-
standing these limitations, our results for the respiration of
corals exposed to OA are at least inconsistent with the
notion that the metabolic costs of calciﬁcation are elevated
by high pCO
(Erez et al., 2011).
With the important caveats that our short incubations
were conducted in the natural environment where we cannot
separate the effects of incubation duration from the effects
of ecologically relevant physical conditions relative to pre-
vious studies, our results suggest that the respiration of
massive Porites spp. is resistant to short-term exposure to
OA conditions. Previously, using laboratory-based meso-
cosms, we have shown that respiration of juvenile Porites
spp. is depressed 36% after longer exposures (11 d) to 87 Pa
(but not to 77 Pa pCO
), although, as reported here,
the metabolic costs concurrent with calciﬁcation were un-
affected by pCO
(Edmunds, 2012). Analyses of the effects
on the dark respiration of corals generally have
provided equivocal results, with most studies reporting no
effects at pCO
levels as high as 207 Pa (Reynaud et al.,
2003; Anthony et al., 2008; Godinot et al., 2011; S.
Comeau, California State University Northridge, pers.
comm.), one study reporting a trend for increased light-
enhanced respiration with high pCO
(Crawley et al., 2010),
and a few studies reporting metabolic depression at 77– 87
(Edmunds, 2012; Edmunds et al., 2013). Clearly
there is scope for further research on the impacts of OA on
coral respiration, speciﬁcally to resolve the effects of expo-
sure duration, pCO
regime, and the assemblage of physical
and chemical conditions that collectively determine the
ecological relevancy of manipulative experiments. The
completion of the necessary experiments in situ rather than
in vitro will need to be an important part of this agenda and
will likely be critical to advance a mechanistic appreciation
of the effects of OA on marine organisms (Kelly and Hof-
mann, 2013). In situ chambers, such as the ones we use
here, can play an important part in this effort.
This research was funded by the U.S. National Science
Foundation through grants BIO-OCE 08-44785 (to PJE) and
OCE 10-26852 to the Moorea Coral Reef Long-Term Eco-
logical Research site, gifts from the Gordon and Betty
Moore foundation, and a Graduate Thesis Support grant
from California State University, Northridge (CSUN) (to
CBW). This work was submitted in partial fulﬁllment of the
MS degree for CBW. We thank S. Comeau, N. Spindel, E.
Rivest, B. Lenz, and V.R. Cumbo for ﬁeld assistance; D.
Liittschwager for the use of his photograph; and two anon-
ymous reviewers who improved an earlier draft of this
paper. This is contribution number 199 of the CSUN Marine
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