BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-14-3549-2017Daily variation in net primary production and net calcification in coral
reef communities exposed to elevated pCO2ComeauSteevesteeve.comeau@uwa.edu.auhttps://orcid.org/0000-0002-6724-5286EdmundsPeter J.LantzCoulson A.CarpenterRobert C.Department of Biology, California State University, 18111 Nordhoff
Street, Northridge, CA 91330-8303, USASchool of Earth Sciences, Oceans Institute and ARC Centre of
Excellence for Coral Reef Studies, The University of Western Australia,
Crawley, Western Australia 6009, AustraliaSouthern Cross University School of Environment, Science, and
Engineering, Military Road Lismore NSW 2480, AustraliaSteeve Comeau (steeve.comeau@uwa.edu.au)27July201714143549356021February20171March201718June201722June2017This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/14/3549/2017/bg-14-3549-2017.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/14/3549/2017/bg-14-3549-2017.pdf
The threat represented by ocean acidification (OA) for coral reefs has
received considerable attention because of the sensitivity of calcifiers to
changing seawater carbonate chemistry. However, most studies have focused on
the organismic response of calcification to OA, and only a few have addressed
community-level effects, or investigated parameters other than calcification,
such as photosynthesis. Light (photosynthetically active radiation, PAR) is a
driver of biological processes on coral reefs, and the possibility that these
processes might be perturbed by OA has important implications for community
function. Here we investigate how CO2 enrichment affects the
relationships between PAR and community net O2 production
(Pnet), and between PAR and community net calcification
(Gnet), using experiments on three coral communities constructed
to match (i) the back reef of Mo'orea, French Polynesia, (ii) the fore reef
of Mo'orea, and (iii) the back reef of O'ahu, Hawaii. The results were used
to test the hypothesis that OA affects the relationship between Pnet and Gnet. For the three communities tested,
pCO2 did not affect the Pnet–PAR relationship, but it
affected the intercept of the hyperbolic tangent curve fitting the
Gnet–PAR relationship for both reef communities in Mo'orea (but
not in O'ahu). For the three communities, the slopes of the linear
relationships between Pnet and Gnet were not affected
by OA, although the intercepts were depressed by the inhibitory effect of
high pCO2 on Gnet. Our result indicates that OA can
modify the balance between net calcification and net photosynthesis of reef
communities by depressing community calcification, but without affecting
community photosynthesis.
Introduction
Ocean acidification (OA), which is caused by the dissolution of atmospheric
CO2 in surface seawater, induces profound changes in seawater carbonate
chemistry, involving an increased concentration of dissolved CO2 and
bicarbonate ions, and a decrease in the concentration of carbonate ions and
pH (Feely et al., 2004). The effects of these changes on tropical coral reefs
are beginning to be understood in detail, with most studies reporting a
decrease in calcification of scleractinian corals and coralline algae at
reduced seawater pH (Gattuso and Hanson, 2011; Kroeker et al., 2013).
To date, studies addressing the effects of OA on coral reefs have been
performed mostly at the scale of individual organisms, and have focused on
calcification as a response variable (Schoepf et al., 2013; Comeau et al.,
2013; Okazaki et al., 2016), while studies focusing on larger spatial scales
(i.e., whole communities) have remained rare, mostly because of technical
constraints (e.g., Dove et al., 2013; Comeau et al., 2015, 2016b). The few
experiments addressing the effects of OA on intact coral reef communities
have confirmed the threat to calcification rates previously reported for
individual organisms, notably by showing a decreased capacity of communities
to maintain positive net calcification under conditions mimicking a future
ocean in which seawater pH will be depressed 0.15–0.30 units relative to
present-day conditions (e.g., Dove et al., 2013; Comeau et al., 2015, 2016b).
These community-level studies have focused mostly on the response of
calcification to low pH (Dove et al., 2013; Comeau et al., 2015, 2016b) and,
in contrast, the effect of increasing pCO2 on community net
O2 production has rarely been investigated. Where this issue has been
addressed, community O2 production has been found to be insensitive
to pCO2 (to ∼ 1000 µatm) (Leclerc et al., 2002;
Langdon and Atkinson, 2005, Dove et al., 2013), while a positive effect of
pCO2 on the net production of photosynthetically fixed organic
carbon has been reported during a flume experiment (Langdon and Atkinson,
2005).
Investigating the combined response to OA of primary production and
calcification of benthic coral reef communities is critical, because
increasing dissolved CO2 and bicarbonate ion concentrations
potentially could “fertilize” photosynthesis of marine organisms (Connell
and Russell, 2010; Hepburn et al., 2011; Connell et al., 2013), thereby
perturbing ecosystem trophodynamics. A stimulatory effect of OA on
photosynthesis could, for calcifying taxa such as corals and coralline algae,
support higher rates of calcification by increasing the ease with which the
metabolic costs of these events could be met through enhanced respiration
fuelled by greater availability of carbon substrates (Comeau and Cornwall,
2016). However, a stimulatory effect of OA on photosynthesis has not been
clearly established for coral reef organisms, and to date, the evidence in
support of this possibility is equivocal (e.g., Anthony et al., 2008; Kroeker
et al., 2013; Comeau et al., 2016a).
One reason why studies of the effect of pCO2 on the relationship
between primary production and calcification are technically challenging is
that the relationships between light (photosynthetically active radiation,
PAR) and both photosynthesis and calcification are nonlinear (e.g.,
Borowitzka, 1981; Chalker et al., 1988; Muscatine, 1990; Chisholm, 2000). In
symbiotic reef corals, the relationships between photosynthesis and PAR, and
between calcification and PAR, generally are best fit by a hyperbolic tangent
function (Chalker, 1981; Marubini et al., 2001), which is characterized by a
rapid rise of photosynthesis (or calcification) with initial increases in PAR
from darkness, followed by a plateau of response at saturating light, and
sometimes a reduction in response at the highest PAR intensity (i.e.,
photoinhibition, e.g., Brown et al., 1999). No studies have investigated the
effect of pCO2 enrichment on the mathematical parameters defining
the hyperbolic tangent relationship between PAR and photosynthesis (or
calcification) for coral reef organisms and communities.
Because calcification of coral reef communities is coupled to photosynthesis
on timescales of hours to days (Gattuso et al., 1999), examination of
high-frequency variation in the net O2 production
(Pnet)–net calcification (Gnet) relationships for
these communities has the potential to reveal the capacity to respond
dynamically to varying conditions (i.e., Jokiel et al., 2014). The
relationship between Pnet and Gnet for coral reefs
is relatively well known at the community level, and generally describes a
positive linear relationship (Gattuso et al., 1999; Falter et al., 2012).
Such a relationship reflects emergent properties arising from the stimulation
of Gnet by Pnet at the organism scale (i.e., for
corals and calcified algae) (Jokiel et al., 2014), most likely because
Pnet can supply the carbon resources necessary as substrates for
aerobic respiration (Stambler, 2011), modify the intracellular and
surrounding seawater chemistry (Marubini et al., 2008; Jokiel et al., 2014),
and provide the building blocks necessary to construct the organic matrix
found within coral skeletons (Muscatine et al., 2005). Unfortunately, it is
difficult to test the hypothesis that the Gnet–Pnet
relationship for reef communities is affected by carbonate chemistry, because
the seawater chemistry varies with Pnet in the natural
environment (Jokiel et al., 2014; Shaw et al., 2015). To test for an effect
of seawater carbonate chemistry on the Gnet–Pnet
relationship of reef communities, it is therefore necessary to conduct
experiments in a controlled environment to assess how seawater carbonate
chemistry alone affects the Gnet–Pnet relationship.
The present study tests the hypothesis that the enrichment in seawater
pCO2 due to OA will affect the relationships between
Pnet and PAR, and between Gnet and PAR for intact
reef communities fabricated in outdoor flumes (sensu Atkinson et al., 1994).
The second hypothesis tested is that the Pnet–Gnet
relationships would be affected by OA, based on the rationale that community
Pnet and Gnet would respond in dissimilar ways to
high pCO2. Because the shape of these relationships likely depends
on the community composition (i.e., the taxa present and their relative
abundances, Gattuso et al., 1999), we used results from three independent
experiments to explore variations in the relationships caused by differences
in environmental conditions and differences in the taxonomic assemblages
composing the communities tested. Data from three experiments conducted in
flumes in two locations in the tropical Pacific were combined; one experiment
focused on a back reef community assembled in Mo'orea, French Polynesia,
during the austral spring of 2013 (Comeau et al., 2015); one experiment
focused on a reef flat (back reef) community assembled in Kāne'ohe Bay,
O'ahu, during the winter of 2014; and one experiment focused on a fore reef
community assembled in Mo'orea, during the austral spring of 2014 (Comeau et
al., 2016b). For the communities analysed in Mo'orea, the present
contribution describes in more detail the results for net calcification, as
well as new results for photosynthesis that originate from experiments that
are described in part in previous papers (Comeau et al., 2015, 2016b); the
study conducted in O'ahu has not been described before. The three communities
were incubated in outdoor flumes of similar designs, and were operated under
ambient and elevated pCO2 (∼ 400 and ∼ 1300 µatm, respectively). When the experiments were conducted, community
Pnet and Gnet were measured simultaneously.
Materials and methodsCollection and sample preparation
This study utilizes results from three experiments conducted between August
2013 and October 2014. The first and third experiments were carried out in
Mo'orea, French Polynesia, at the Richard B. Gump South Pacific Research
Station, and the second experiment was conducted in O'ahu, Hawaii, on Coconut
Island at the Hawaii Institute of Marine Biology (Fig. 1).
Map showing the study locations and photos of the three assembled
communities. Experiments were performed on three coral reef communities
representing the back reef of Mo'orea (Experiment 1), the back reef of O'ahu
(Experiment 2), and the fore reef of Mo'orea (Experiment 3). The respective
pCO2 levels and flow speeds used are indicated.
The first experiment took place in August–October 2013, and focused on a
back reef community from 1 to 2 m depth on the northern shore of Mo'orea
(Comeau et al., 2015). When the study was completed, this community consisted
of 22 % coral cover and 6 % coralline alga cover. Two-thirds of the
area of the working section of the flume was occupied by sediments collected
from the lagoon at 2 m depth.
The second experiment was carried out in O'ahu in January–February 2014 and
focused on a benthic community similar to that found at 1–2 m depth on the
Kāne'ohe Bay barrier reef flat in 2013. This community consisted of
Porites compressa (7 % cover), Montiporacapitata (12 %), massive Porites spp. (3 %), and
Pocillopora damicornis (2 %), and the crustose coralline alga
Porolithon onkodes (4 %) (Jokiel et al., 2015). As described
above for Experiment 1, sediments were inserted into the floor of the flume
to recreate ecologically relevant communities. Since the flumes in O'ahu (as
designed and utilized by M. Atkinson, e.g., Atkinson et al., 1994) were not
designed to include sediments, a custom-made sediment box was inserted into
the floor of the flumes to provide an area occupying two-thirds of the floor
of the working section of the flume with sediment to a depth of ∼ 5–8 cm.
The third experiment was carried out from August to October 2014 in Mo'orea,
and focused on outer reef benthic communities prepared from specimens
collected from ∼ 15 to 17 m depth (Comeau et al., 2016b). This
community consisted of 27 % cover of corals and 5 % cover of
coralline algae; 55 % of the floor of the flume was covered by
∼20×20×5 cm pieces of reef pavement collected from ∼ 15 m.
In Mo'orea, the two experiments were performed in four outdoor flumes
consisting of a working section of 5.0×0.3×0.3 m (as in Comeau
et al., 2015) in which water was re-circulated at a constant speed of
10 ± 0.5 cm s-1(mean ± SE (standard error); Experiment 1) or 8 ± 0.5 cm s-1
(Experiment 3) that represented the mean in situ flow speed over the year
measured in the two habitats (Washburn and MCR LTER, 2015; Comeau et al.,
2016b). Two flumes were
maintained at ambient pCO2 (∼ 400 µatm) and two
at elevated pCO2 (∼ 1200–1300 µatm; see below).
Fresh sand-filtered seawater was dispensed continuously into the flumes at
5 L min-1, and the experiments lasted 8 (Experiment 1) or 7 weeks
(Experiment 3).
In O'ahu, the benthic community was constructed in two outdoor flumes, one
with a working section of 9×0.6×0.3 m and one with a working
section of 4×0.4×0.4 m; one of these flumes was
maintained at ambient pCO2 and one at elevated pCO2. To
address the confounding effect of flumes on this design (i.e., the flumes
were allocated to one of two treatments and the flumes were not of an
identical design), the first experiment ended after 3 weeks, the
pCO2 treatments were switched between flumes, and new communities
(with the same taxon composition including sediment) were placed in the two
flumes for a second trial of the same experiment lasting 3 weeks. Fresh
sand-filtered seawater was dispensed continuously into both flumes (at
5–10 L min-1), and a flow speed of 10 cm s-1, similar to that
employed in the earlier trial with the back reef communities of Mo'orea, was
maintained using electric trolling motors (Minnkota USA Riptide 55, Minnkota,
USA).
The three experiments were performed outdoors under natural sunlight that was
attenuated using shade cloth to maintain PAR values similar to ambient PAR
recorded in situ in each habitat. In Experiments 1 and 2, the maximum PAR was
set at ∼ 1000 µmolquantam-2s-1 to represent
light levels at ∼ 1–2 m depth in the back reef (Carpenter et al.,
2016), and in Experiment 3, maximum PAR was set at ∼ 600 µmolquantam-2s-1 to mimic light levels recorded at 17 m depth on
the fore reef of Mo'orea around noon on a cloudless day (Carpenter et al.,
2016). For Experiment 3 (with an outer reef community from deeper water),
blue acetate filters (Lee Filters 183 Moonlight Blue) were placed over the
flumes to filter ambient sunlight in the 600–800 nm range to approximate
the light spectrum found at 17 m depth (Comeau et al., 2016a). Temperature
in all flumes was maintained at ambient seawater temperature when the
experiments were conducted, which corresponded to ∼ 27 ∘C in
Experiments 1 and 3 (both conducted in austral spring) and ∼ 24 ∘C in Experiment 2 (conducted in winter).
Carbonate chemistry manipulations and measurements
For the three experiments, pCO2 levels were chosen to match ambient
pCO2 (∼ 400 µatm) and the pCO2 expected
in the atmosphere by the middle of the next century (∼ 1300 µatm, Moss et al., 2010). pCO2 in the flumes was controlled using
pH controllers (Aquacontroller, Neptune systems, USA) that controlled the
delivery of either pure CO2 or CO2-free air into the
seawater. To match the natural diel variation in seawater pH in shallow back
reef communities (Hofmann et al., 2011; Comeau et al., 2014), in
Experiments 1 and 2, seawater pH was maintained 0.1 units lower at night
(from 18:00 to 06:00 LT (UTC-10) than during the day. It is expected that
diel fluctuations in pH will be larger in the future due to changes in the
buffering capacity of seawater. However, similar fluctuations were chosen
here to apply similar pH fluctuations between ambient and elevated
pCO2 flumes to avoid confounding effects. Diel variation in pH was
not applied during Experiment 3, because seawater pH varies by < 0.1
between day and night on the fore reef of Mo'orea (S. Comeau, unpublished
data).
For the three experiments, pH on the total scale (pHT) was
measured daily using a portable pH meter (Orion 3-stars, Thermo-Scientific,
USA) fitted with a DG 115-SC pH probe (Mettler Toledo, Switzerland)
calibrated every other day with Tris/HCl buffers (Dickson et al., 2007).
pHT also was measured every 2 weeks spectrophotometrically using
m-cresol dye (Dickson et al., 2007). Mean values of pHT measured
spectrophotometrically and using a pH electrode differed by < 0.02 pH
units. Total alkalinity (AT) was measured using open-cell
potentiometric titrations (Dickson et al., 2007) on
∼ 50 g samples of seawater
collected every 2–3 days. Accuracy of AT measurements was
checked by titrating certified reference materials provided by A.G. Dickson
(batch 122 and 140) that yielded AT values within ∼ 4 µmolkg-1 of the nominal value. Parameters of the
carbonate system in seawater were determined with the seacarb R package
(Gattuso et al., 2015) using measured values of pHT,
AT, temperature, and salinity.
Net calcification and primary production measurements
Net community calcification (Gnet) in the flumes was measured
using the total alkalinity anomaly method (Chisholm and Gattuso 1991; Schoepf
et al., 2017), and net community primary production (Pnet) was
measured using oxygen sensors (TROLL 9500, In-Situ) that measured the
O2 concentration at 60 s intervals with an accuracy of
0.2 mg L-1. Oxygen sensors were calibrated at the beginning of the
experiment using a two-point calibration (0 and 100 % O2 seawater
solutions). Measurements of changes in dissolved inorganic carbon (DIC) were
not meaningful with our experimental design because DIC was held constant by
adding pure CO2 during the incubations to maintain pCO2 at
target values.
For the three experiments, community metabolism was measured every 7 days
using single 24 h incubations during which the addition of seawater to the
flumes was stopped, and the flumes were operated in a closed circuit mode.
During these incubations, seawater samples for the determination of
AT were taken every 3 h during the day, and every 6 h at night,
to estimate Gnet, while O2 was constantly monitored. To
maintain AT, nutrient concentrations, and pO2 at values
close to ambient seawater in the sampled habitats, ∼ 50 % of the
flume volume was replaced every 3 h during the day, and every 6 h at night
(i.e., at 06:00, 09:00, 12:00, 15:00, 18:00, and 00:00 LT). AT and DIC changed by < 5 % (∼ 40–50 µmolkg-1) during the incubations, which likely did
not affect the metabolism of organisms. Since only two O2 sensors were
available, and experiments were conducted in four flumes in Mo'orea,
Pnet was measured for each incubation in one ambient flume and
one elevated pCO2 flume that were randomly picked. In O'ahu, one
O2 sensor was used in each flume during the incubations. Acrylic covers
placed on top of the flumes limited gas exchange with the atmosphere but did
not prevent it. Gas exchange between seawater and the atmosphere was
estimated based on the flume surface areas, the flow speed, and the
differences between the O2 concentration measured in seawater and the
theoretical O2 concentrations when in equilibrium with the atmosphere
following equations of Langdon and Atkinson (2005). Wind effects on gas
exchange across the air–water interface were assumed to be negligible
because acrylic covers protected flumes. Gas exchange was estimated to be
small (i.e. < 5–10 %) because ∼ 50 % of the flume volume
was replaced every 3 h during the day. Gas exchange was similar between
treatments and was therefore not taken into account in the present study.
Light was monitored constantly during the incubations using cosine-corrected
PAR sensors (Odyssey, Dataflow Systems Pty Ltd, Christchurch, New Zealand).
Calculations and statistical analysis
Pnet was estimated hourly by calculating the change in O2
during the incubations, except for the hours during which the seawater was
refreshed (06:00, 09:00, 12:00, 15:00, 18:00, and 00:00 LT). Gnet
was estimated at 3 h intervals during the day and 6 h intervals at night by
collecting AT samples at the beginning (after seawater
refreshing) and at the end of each incubation (before adding fresh seawater).
Because there were no significant differences in calcification between flumes
for each treatment (Comeau et al., 2015, 2016a), Gnet was pooled
among replicate flumes in each treatment. Pnet was measured in
Mo'orea in only one flume per treatment at a time, and it was assumed that
the measurements represented the average response to the conditions
experienced in each treatment. Individual measurements of Gnet
and Pnet in O'ahu were considered replicates.
A corrected Akaike information criterion (AIC) approach was used to determine
whether a linear, logarithmic, or hyperbolic tangent function best described
the functional relationships between Pnet and PAR, and between
Gnet and PAR, for each community (see details in Comeau et al.,
2013). A linear relationship was fit to explore a “proportional effect”
model for increasing PAR. A logarithmic function and a hyperbolic tangent
function that are commonly used to describe the relationship between
Pnet and PAR for reef corals (Chalker, 1981; Marubini et al.,
2001) were also fit to the data in cases where photosynthesis (or
calcification) initially rapidly increased with PAR, and then approached an
asymptote at saturating PAR.
The hyperbolic tangent function between PAR and Pnet in the light
corresponded to
Pnet=C0+Pnetmaxtanh(αI)Pnetmax,
where Pnetmax is the maximum photosynthetic rate, I is PAR, α is the slope of the initial
portion of the Pnet versus I relationship, and C0 is the
intercept.
Similarly, the hyperbolic tangent function for the relationship between PAR
and Gnet in the light was
Gnet=C0+Gnetmaxtanh(αI)Gnetmax,
where Gnetmax is the maximum calcification rate, I is
PAR, α is the slope of the initial portion of the Gnet
versus I relationship, and C0 is the intercept.
The best fits of the functions (least squares) were determined using the
nls function in R, and t-tests were used to compare the curve
parameters between pCO2 treatments.
To test the hypothesis that Pnet and Gnet were
associated, mean Pnet corresponding to the Gnet
determination intervals (3 h periods during the day and 6 h at night) were
calculated, and the relationship between Pnet and
Gnet was investigated using a correlation approach (sensu Gattuso
et al., 1999). When the linear associations between Gnet on
Pnet were significant, analyses of covariance (ANCOVA), with
Pnet as the covariate, were used to test the effects of
pCO2 (a fixed effect) on the Pnet–Gnet
relationship for each experiment. All analyses were performed using R
software (R Foundation for Statistical Computing). In this design, both
Pnet and Gnet are random variables for which a test
of association is best accomplished with correlation. Evaluating the slope
and intercept is problematic as it is not appropriate to use Model I (least
squares) approaches for the purpose of describing the functional relationship
between two random variables. In the present case, we report Model I slopes
because we are interested in the capacity to predict Gnet from
Pnet and because Model I slopes are integral to the ANCOVA
approach.
Results
Carbonate chemistry was tightly controlled during the three experiments, with
mean pCO2 maintained at 453 ± 30, 460 ± 23, and
400 ± 14 µatm in the ambient treatments, and
1317 ± 50, 1233 ± 76, and 1176 ± 37 µatm in the
elevated pCO2 treatments during Experiments 1, 2, and 3,
respectively (all ± SE, n=42–56). In all experiments and both
treatments, aragonite saturation states (Ωarag) were ∼ 3.52, 2.59, and 3.71 in the ambient treatments, and 1.64, 1.36, and 1.75
in the elevated pCO2 treatments during Experiments 1, 2, and 3,
respectively (Table 1). Ωarag was lower during Experiment 2
in O'ahu compared to Experiments 1 and 3 in Mo'orea because of naturally
lower AT (∼ 2160 µmolkg-1) and temperature
(∼ 24 ∘C) in this location (cf. in Mo'orea where
AT is ∼ 2340 µmolkg-1 at 27 ∘C).
Mean carbonate chemistry and temperature treatments in the flumes
during the experiments conducted with back reef communities in Mo'orea and
O'ahu, and the fore reef community in Mo'orea. The mean ± SE partial
pressure of CO2 (pCO2) and the saturation states of
aragonite (Ωarag) were calculated from pHT,
total alkalinity (AT), salinity (S), and temperature (T). SE
for salinity was < 0.1.
Benthic community structure in the flumes was not measured during these
short experiments, and we assume that changes were minor as there was no
major coral mortality and planar growth would have been trivial over several
weeks.
Relationships of Pnet and Gnet with PAR
AIC analyses justified the use of a hyperbolic tangent function (versus
linear or logarithmic functions) to fit the relationship between
Pnet and PAR during the day for the back reef communities of
Mo'orea and O'ahu under the two pCO2 conditions (Fig. 2a, b, and c;
Table S1 in the Supplement). Since the hyperbolic tangent function could not
be rejected for the fore reef community of Mo'orea, this model was also
chosen to facilitate comparisons between experiments. For the back reef
community of Mo'orea, the back reef community of O'ahu, and the fore reef
community of Mo'orea, there was no effect of pCO2 on any of the
parameters of the relationship between Pnet and PAR (Table 2).
Results of the t-tests used to compare between pCO2
treatments the parameters of the hyperbolic tangent functions describing the
relationship between community net photosynthesis (Pnet) in the
light and PAR and net calcification (Gnet) in the light and PAR.
Parameters of the hyperbolic function are the maximum rate
(Pnetmax and Gnetmax), the slope of the initial
portion of the relationship (α), and the intercept (C0).
ParameterExperimentFunctionp-valueparameterNet photosynthesisMo'orea – back reefPnetmax0.558(Pnet)α0.387C00.559O'ahu – back reefPnetmax0.840α0.536C00.621Mo'orea – fore reefPnetmax0.942α0.792C00.579Net calcificationMo'orea – back reefGnetmax0.376(Gnet)α0.836C00.046O'ahu – back reefPnetmax0.867α0.126C00.394Mo'orea – fore reefPnetmax0.736α0.715C00.002
Results of the linear regressions modeling the
Pnet–Gnet relationships under ambient and elevated
pCO2. Results are shown for the experiments with back reef
communities in Mo'orea and O'ahu, and fore reef communities in Mo'orea.
Similar to Pnet, AIC tests also confirmed that the relationships
of Gnet with PAR could be fit with a hyperbolic tangent function
for the three experiments under the two pCO2 conditions tested
(Fig. 3a–c; Table S2). For the Mo'orea back reef community, there was no
difference in maximum calcification (Gnetmax) and the slope of
the initial portion of the relationship (α) between pCO2
treatments (Table 2). However, pCO2 affected the intercepts
(C0, p=0.046), with C0 at ambient pCO2
(1.26 mmol m-2 h-1) greater than C0 at elevated
pCO2 (-0.52 mmol m-2 h-1). The relationship of
Gnet with PAR for the back reef communities in O'ahu was
not statistically affected by pCO2 (Table 2). For the fore reef
community of Mo'orea, Gnetmax and α did not differ
between treatments, but C0 was higher
(2.77 mmol O2 m-2 h-1) at ambient versus elevated
pCO2 (0.58 mmol O2 m-2 h-1) (Table 2).
Relationships of net primary production (Pnet) in the
light with PAR in three coral reef communities representing the back reef of
Mo'orea (a), the back reef of O'ahu (b), and the fore reef
of Mo'orea (c). Communities were incubated under ambient
pCO2 (∼ 400 µatm, black symbols and lines) and
elevated pCO2 (∼ 1200 µatm, red symbols and
lines). The curves represent the best fit of a hyperbolic tangent function
for the relationship between Pnet with PAR.
Relationships of net calcification (Gnet) in the light
with PAR in three coral reef communities representing the back reef of
Mo'orea (a), the back reef of O'ahu (b), and the fore reef
of Mo'orea (c). Communities were incubated under ambient
pCO2 (∼ 400 µatm, black symbols and lines) and
elevated pCO2 (∼ 1200 µatm, red symbols and
lines). The curves represent the best fit of a hyperbolic tangent function
for the relationship between Gnet and PAR.
Variations in Gnet as a function of Pnet at
the three study sites: (a) Mo'orea back reef, (b) O'ahu
back reef, and (c) Mo'orea fore reef. Relationships were determined
under control pCO2 (400 µatm, black points and lines)
and elevated pCO2 (∼ 1200 µatm, red points and
lines). For the three communities and the two pCO2 levels, the
slopes of the linear relationships between Pnet and
Gnet were significant.
Relationships between Pnet and Gnet
For the back reef communities of Mo'orea, the relationship between
Pnet and Gnet was significantly and positively
correlated (p<0.001 under ambient and elevated pCO2) with slopes of
0.17 ± 0.03 mmol CaCO3 mmol O2-1 under ambient
pCO2, and
0.18 ± 0.03 mmol CaCO3 mmol O2-1 (both ± SE,
n=48) under elevated pCO2 (Fig. 4a, Table 3). There was no
difference between treatments in slopes (ANCOVA, p=0.749), but intercepts
were 61 % greater under ambient versus elevated pCO2
(p<0.001).
Gnet and Pnet for the back reef communities of O'ahu
also were positively correlated (p<0.001 under both ambient and elevated
pCO2) and their relationships exhibited slopes of
0.14 ± 0.02 mmol CaCO3 mmol O2-1 under ambient
pCO2, and
0.17 ± 0.02 mmol CaCO3 mmol O2-1 (both ± SE,
n=36) under elevated pCO2 (Fig. 4b, Table 3). There was no
difference between treatments in slopes (ANCOVA, p=0.286), but the
intercepts were 32 % greater under ambient versus elevated pCO2
(p<0.001).
For the fore reef community of Mo'orea, the relationships between
Gnet and Pnet were significant under ambient and
elevated pCO2 (p<0.001) and had respective slopes of
0.27 ± 0.05 mmol CaCO3 mmol O2-1 and
0.30 ± 0.06 mmol CaCO3 mmol O2-1 (both ±SE,
n=28; Table 3). For the back reef communities, there were no differences in
the slopes between Gnet and Pnet between treatments
(ANCOVA, p=0.623), but intercepts were 48 % greater under elevated
versus ambient pCO2 (p=0.002).
Discussion
By testing the response of three coral reef communities to OA under natural
PAR, our study demonstrates that the relationships between Pnet
and PAR and Gnet and PAR for back reef and outer reef communities
are not affected by pCO2. Our results also demonstrate that the
slope of the relationship between Pnet and Gnet was
unaffected by increasing pCO2, but in contrast, the intercepts were
more elevated in the ambient treatments. Such results were caused by a
constant effect of OA on Gnet for the range of Pnetvalues measured in the three communities.
For the three assembled communities, pCO2 did not affect the
functional relationship between PAR and Pnet as modeled using a
hyperbolic tangent function. This result suggests that for the organisms
composing the three communities, the additional quantities of bicarbonate and
dissolved CO2 available under OA conditions did not enhance
photosynthesis across the range of light intensities and community structures
tested. However, as our results come from experiments completed in a single
season, we cannot be sure whether the results are consistent throughout the
year, as seasonal variations in community and organismic Pnet and
Gnet are common on coral reefs (e.g., Falter et al., 2012).
Whether increasing pCO2 has beneficial consequences for rates of
photosynthesis of marine organisms is equivocal (Connell and Russell, 2010;
Britton et al., 2016) and, indeed, the absence of an effect of pCO2
on photosynthesis may have important biological meaning (e.g., Kroeker et
al., 2013). For instance, such an outcome could reflect the presence of
diverse carbon concentrating mechanisms (CCM), which allow organisms to
actively concentrate CO2 at the site of Rubisco activity by actively
transporting HCO3- across internal membranes (Giardano et al.,
2005; Raven et al., 2014). Increases in concentration of dissolved
CO2 in seawater that occur as a result of OA (Feely et al., 2004)
could have beneficial consequences for photosynthetic rates of species that
currently are DIC limited (Diaz-Pulido et al., 2016), because these organisms
often rely on inefficient and energetically costly CCMs to access CO2
(Raven et al., 2014).
The present study, as well as previous studies of both coral reef organisms
(corals and calcified algae) (Schneider and Erez, 2006; Comeau et al., 2016b)
and coral reef communities (Leclercq et al., 2002; Langdon et al 2003; Dove
et al., 2013), showed no change in Pnet, measured by changes in
O2 concentrations, in response to OA arising from pCO2 values
as high as 2000 µatm. Stimulatory effects of pCO2 on
Pnet probably were not detected in our communities (i.e., where
coral cover ranged from 22 to 27 %), because such effects are likely to
be minimal for endosymbiotic Symbiodinium in corals that possess a
CCM (Mackey et al., 2015) and, moreover, are able to exploit some of the host
respiratory CO2 as an alternative DIC source (Stambler, 2011).
Beneficial effects of high pCO2 on community carbon production, but
not oxygen production, for shallow water coral reefs have been reported by
Langdon and Atkinson (2005), who found a 20–50 % increase in carbon
production of coral assemblages composed of Porites compressa and
Montipora capitata in Hawai'i. This result led to the hypothesis
that increasing CO2 causes a decrease in the photosynthetic quotient
of corals, which could be a product of the metabolism of the coral host, if
CO2 favors the production of carbohydrates over proteins and lipids
(Langdon and Atkinson, 2005). While this hypothesis is appealing as a means
to resolve discrepancy between studies, it was not possible to test in the
present study because Pnet was determined through measurements
of O2 (see Sect. 2, “Materials and methods”). In order to reconcile
these apparently contradictory results regarding a potential “CO2
fertilization” effect, it would be necessary for future studies to
simultaneously measure changes in O2, DIC, and AT. In
such an experiment, fluxes in DIC should be corrected for changes in
AT due to calcium carbonate precipitation and dissolution
(because 0.5 moles DIC is equivalent to 1 mole AT (Gattuso et
al., 1999). DIC data corrected by this means could then be compared against
contemporaneous measurements of O2 in an experimental setup to
ascertain whether the expected 1:1 molar flux ratio (of DIC : O2)
changes under elevated seawater pCO2. Changes in the value of this
ratio, relative to ambient conditions, may provide insight into the
possibility that coral reef calcifiers alter the allocation of
photosynthetically fixed carbon among carbohydrate,
lipid, and protein pools as a result of exposure to elevated seawater pCO2.
In our three experiments, maximal community Gnet was coincident
with the highest PAR. At low PAR (∼< 50 µmolquantam-2s-1) only
the fore reef community in Mo'orea exhibited positive Pnet at
both pCO2 levels, demonstrating the capacity of this deeper
community to photosynthesize at lower intensities of PAR. Similar to
Pnet, the relationships of Gnet with PAR at the two
pCO2 levels were best fit by a hyperbolic tangent function. The
lack of changes in the parameters of these relationships as a result of the
treatment conditions demonstrated that pCO2 and light did not have
interactive effects on Gnet (Table 2). Only the elevations of the
hyperbolic functions for the two habitats in Mo'orea were affected by high
pCO2, and in this case their reduction relative to ambient
pCO2 demonstrates that Gnet was consistently lower,
regardless of PAR intensity, at high pCO2. Comparative data on the
effect of the intensity of PAR on the response of community calcification to
pCO2 are not available, but of the few studies of similar effects
that have been conducted at the organism scale, contradictory results have
been found (Marubini et al., 2001; Comeau et al., 2013, 2014b; Dufault et
al., 2013; Suggett et al., 2013; Enochs et al., 2014).
The consistently lower Gnet in the high pCO2 treatments
for the three experiments could have resulted from either a decrease in gross
calcification, an increase in calcium carbonate dissolution, or a combination
of both. The constant offset (i.e., difference in elevation of the response)
between Gnet under ambient and high pCO2 at any given
PAR suggests the effect cannot be accounted for solely by changes in gross
calcification (Ggross). Indeed, if only Ggross were
affected by high pCO2, a proportional effect on Gnet
would be expected, with the reduction of Gnet associated with
high pCO2 varying with Ggross and, therefore, PAR. In
contrast, if dissolution and bioerosion, which are mostly chemically and
mechanically driven (Andersson and Gledhill, 2013), were responsible for the
reduced Gnet at high pCO2, it is likely that PAR would
have only a small influence in Gnet. Thus, it is likely that
increasing dissolution and chemical bioerosion in the high pCO2
treatment caused most of the observed decreases in Gnet. However,
the method used in the present study (the alkalinity anomaly technique) did
not permit quantification of mechanical bioerosion, which could also be
affected by OA (Enochs et al., 2016).
Although the two coral reef communities studied in Mo'orea differed in
substratum composition (i.e., with sand present in the back reef versus
pavement in the outer reef, and differences in coral cover), community
structure, and the quality and quantity of light applied (i.e., blue-biased
at depth, and a 40 % reduction in intensity at 17 m versus 2 m depth),
both communities exhibited a 50–60 % decline in Gnet at
1300 µatmpCO2. In contrast, mean Gnet for
the O'ahu back reef community was less affected by pCO2 than for
the communities of Mo'orea. The reduced sensitivity of Gnet to
∼ 1200 µatmpCO2 for back reef communities in
O'ahu may reflect different sediment composition and legacy effects
associated with environmental conditions in the bay from which the organisms
and sediment were collected. Critically, the organisms for the O'ahu
experiment were collected from Kāne'ohe Bay where seawater pCO2
(up to ∼ 450–500 µatm) is higher than current atmospheric
levels (∼ 400 µatm) because of heterotrophy and
calcification (Fagan and Mackenzie, 2007; Drupp et al., 2011). Kāne'ohe
Bay is also affected by strong diurnal cycles in pCO2 and rapid
changes in pCO2 during storm events (Fagan and Mackenzie, 2007;
Drupp et al., 2011). These conditions potentially could have created the
opportunity for physiological acclimatization or local adaptation that might
reduce their sensitivity to high pCO2 in the experimental trials.
The relationship between community Pnet and Gnet is
commonly used as a measure of the coral reef “state” (Gattuso et al., 1999;
Lantz et al., 2014), with coral reefs dominated by high coral cover and low
cover of macroalgae characterized by elevated slopes of the Pnet-Gnet relationship. In the present study, the slopes of the
relationships between Pnet and Gnet in the ambient
treatment were between 0.14 (O'ahu) (this and all following slope values have
units of mmol CaCO3 mmol O2-1) and 0.27 (Mo'orea fore reef). In
Mo'orea, the slopes were higher for the fore reef (0.27 and 0.30) versus the
back reef (0.17 and 0.18) community, which demonstrated that Gnet
was more sensitive to changes in Pnet in fore reef communities,
probably because of a higher cover of calcifiers. The slopes of the
Pnet–Gnet relationships for the communities tested
are within the range estimated from in situ “reef-scale” measurements,
which indicate a mean value of 0.22 based on 52 reefs (Gattuso et al., 1999).
More recently, Shaw et al. (2012) reported a
Pnet–Gnet slope of 0.24 for the reef flat of Lady
Elliot Island, Australia, and a slope of 0.14 was reported for Ningaloo Reef,
Australia (Falter et al., 2012). The consistency between the slopes reported
herein, and values determined in situ (e.g., Shaw et al., 2012; Gattuso et
al., 1999), suggest that our constructed communities, and the conditions to
which they were exposed, reproduced conditions found in situ on coral reefs.
This outcome lends support to the inferences we are able to make regarding
the response of reef communities to elevated pCO2, for which
currently there are no in situ data.
Our results are consistent with the hypothesis that OA will affect the
relationship between community Pnet and Gnet (sensu
Gattuso et al., 1999) because intercepts of the
Pnet–Gnet relationships varied between treatments
and were more elevated under ambient pCO2. The absence of changes
in slopes as a function of pCO2 probably was due to the lack of a
pCO2 effect on Pnet and the lack of a
PAR–pCO2 interactive effect on Pnet and
Gnet. Furthermore, the community composition remained the same in
the ambient and elevated pCO2 conditions, with no mortality or loss
of benthic cover of living organisms during the course of the experiment,
which could potentially have modified the community
Pnet–Gnet relationship (Lantz et al., 2014; Shaw et
al., 2015) due to taxon-specific Pnet–Gnet
relationships (Page et al., 2016). Thus, this result indicates that elevated
CO2 alone (e.g., without considering global warming) can modify the
balance between calcification and photosynthesis at the scale of a whole
reef, because of a decrease in coral reef community calcification while
photosynthesis remains constant.
All the data presented in the manuscript were deposited in
the PANGAEA database and will be available at:
https://www.pangaea.de/?q=Comeau&f.author%5B%5D=Comeau
%2C+Steeve.
The Supplement related to this article is available online at https://doi.org/10.5194/bg-14-3549-2017-supplement.
The authors declare that they
have no conflict of interest.
Acknowledgements
We thank Ruth D. Gates and Holly M. Putnam for access to the infrastructure of
HIMB and laboratory assistance in Hawaii. This study was funded by the
National Science Foundation (OCE 10-41270 and 14-15268) and the Mo'orea Coral
Reef LTER (OCE 04-17413 and 10-26852). This is contribution number 235 of the
CSUN Marine Biology Program. S. Comeau was supported by ARC (Discovery Early
Career Researcher Award; DE160100668) during the writing of the
manuscript. Edited by: Jack
Middelburg Reviewed by: two anonymous referees
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