Download Predicting the impact of ocean acidification on coral reefs

ICES Journal of
Marine Science
ICES Journal of Marine Science (2016), 73(3), 550– 557. doi:10.1093/icesjms/fsv091
Contribution to Special Issue: ‘Towards a Broader Perspective on Ocean Acidification Research’
Food for Thought
Predicting the impact of ocean acidification on coral reefs:
evaluating the assumptions involved
Paul L. Jokiel*
Hawaii Institute of Marine Biology, PO Box 1346, Kaneohe, HI 96744, USA
*Corresponding author: e-mail: [email protected]
Jokiel, P. L. Predicting the impact of ocean acidification on coral reefs: evaluating the assumptions involved. – ICES Journal of
Marine Science, 73: 550 – 557.
Received 7 March 2015; revised 21 April 2015; accepted 22 April 2015; advance access publication 21 May 2015.
Predictions of future impact of climate change on coral reefs indicate that bleaching mortality due to higher temperature will be the major factor in
the decline of coral reefs. Ocean acidification (OA) is increasingly considered to be an important contributing factor, but estimates of its importance
vary widely in the literature. Models of future reef decline due to OA generally involve four simplifying assumptions that can lead to contradictions.
The assumptions are: (i) Oceanic conditions of Varag control or are at least highly correlated with net calcification rate (Gnet) on coral reefs. (ii)
Calcification rate is driven by bulk water carbonate ion concentration [CO3 2− ] expressed as Varag. (iii) Changes in coral calcification rate can
be used to estimate future changes in coral reef calcification rate. (iv) The impact of OA is additive and not synergistic with other environmental
factors such as increased temperature. The assumption that aragonite saturation state (Varag) of seawater drives calcification is the most widely
used and needs to be further evaluated. An alternate hypothesis is that calcification is limited by the ability of the system to rid itself of the protons
generated by calcification. Recent studies allow further testing of the assumptions and point the way to resolving shortcomings in our understanding of how OA impacts coral reefs.
Keywords: climate change, corals, coral reefs, mathematical models, ocean acidification, proton flux.
Introduction
During 1999, three important publications established the potential
seriousness of future anthropogenic global climate change and laid
the basis for predictive modelling efforts. Kleypas et al. (1999) proposed that coral reef calcification rate depends on the aragonite
saturation state (Varag) of oceanic surface waters based on the correlation between current coral reef distribution and Varag of the
surrounding ocean waters. Gattuso et al. (1999) reviewed the potential effect of global climatic changes (pCO2 and temperature) on
the rate of calcification in marine organisms and showed that the
rate of calcification in various calcifying photosynthetic organisms
decreases as a function of increasing pCO2 and decreasing Varag.
Their calculated decrease in CaCO3 production due to ocean acidification (OA), estimated using the scenarios considered by the
International Panel on Climate Change (IPCC), was 10% between
1880 and 1990, and 9 –30% from 1990 to 2100. Hoegh-Guldberg
(1999) presented a model of future coral reef demise based largely
on modelled climate change temperature projections and coral
mortality due to the higher temperature regimes, with additional
decline resulting from projected changes in seawater Varag.
The saturation state concept is widely used by physical chemists in
describing seawater carbonate chemistry. The concept is especially attractive in relation to biological calcification on coral reefs because
aragonite is the mineral form of CaCO3 precipitated by reef corals.
Aragonite saturation state (Varag) is defined by the equation:
Varag =
[Ca2+ ][CO3 2− ]
,
Ksp
where Ksp is the solubility product of aragonite. The [Ca2+] in presentday oceanic seawater is essentially constant at 10.3 mmol kg21 SW,
normalized to salinity. Likewise, Ksp is a constant (at a given temperature, pressure, and salinity), so Varag is directly proportional to
[CO3 2− ] in shallow oceanic waters. Therefore Varag is essentially a
function of the change in [CO3 2− ] on coral reefs. A correlation
between Varag and calcification rate does not establish cause and
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Predicting the impact of ocean acidification on coral reefs
effect because Varag also correlates with various other components of
the seawater carbonate system. Nevertheless, nearly all the literature on
effects of past, present, and future impact of OA on coral growth
present Varag or [CO3 2− ] as the independent variable and coral calcification rate as the dependent variable, leading to the widely held paradigm that [CO3 2− ] drives calcification (Erez et al., 2011). Therefore,
the idea that [CO3 2− ] drives coral and coral reef calcification is a
central feature of most mathematical model projections of future
climate change on coral reefs and calcification is frequently presented
as a function of Varag. Mathematical modelling is the process of applying mathematics to a real world problem as a means of gaining understanding of a process such as increasing global OA. The modelling
process can shed light on the questions under investigation and
thereby stimulate further inquiry, but assumptions used in developing
models need to be evaluated whenever conflicting results arise.
Models describing impact of OA on corals
and coral reefs
Two major types of modelling have been conducted on the question
of global impact of OA on corals and coral reefs. The first is essentially a metadata analysis of published data showing response of calcification to changes in Varag. The second category includes various
numerical models based on coral or coral reef response to changes
in Varag as well as increased temperature.
about the future of coral reefs as well as the basic assumptions and
data manipulations involved in the analysis.
Pandolfi et al. (2011) further expanded the analysis of Langdon
and Atkinson (2005) using similar techniques. This synthesis
included results of seven CO2 experiments at ambient temperature,
three CO2 experiments at elevated temperature, seven experiments
using different combinations of acid and base to manipulate Varag,
along with two studies using field data. The response of calcification
to decreasing Varag was consistently negative among individual coral
species, coral mesocosms, and in situ reef communities. Results were
found to be highly variable and often non-linear. Calcification was
strongly sensitive to Varag in some experiments. In other experiments, calcification did not change significantly even where corals
were exposed to CO2 levels between two and three times greater
than preindustrial concentrations. In some cases, calcification did
not decline when held at below the aragonite saturation threshold
(Varag ¼ 1). In a few instances, calcification even increased under
moderately reduced Varag.
This series of three progressively larger metadata analyses based
on the relationship between Varag and calcification rate reinforced
the idea that a linear equation can be used to describe the relationship between Varag and calcification on a global basis. However, the
resulting linear model parameters thus derived are of little predictive
value on any given coral reef and are of dubious value in predicting
global changes in corals and coral reefs in general. Nevertheless, this
analysis does make the point that increasing OA is generally detrimental to coral and coral reef calcification rate.
Metadata models
Gattuso et al. (1999) was the first paper to model impact of OA on
coral reefs. They compiled calcification vs. Varag data on four datasets on temperate and tropical coralline algae, two datasets on scleractinian corals and one on a coral reef community. Six of 7 datasets
clearly showed a linear or curvilinear decrease in the rate of calcification as a function of decreasing Varag over the range 0 –6.2. Using
scenarios developed by the IPCC, the equations were used to describe historical and possible future changes in calcification due to
climate change. Decreases in CaCO3 production were calculated
as 10% between 1880 and 1990, and 9 –30% (mid-estimate: 22%)
from 1990 to 2100. This model used the assumption that calcification is a function of Varag. Also, changes in reef pCO2 were
assumed to be directly related to atmospheric pCO2 as estimated
by IPCC scenarios. The model addressed changes in calcification
for organisms and did not consider net calcification rates for reefs,
which is a more complex question.
Langdon and Atkinson (2005) expanded the work of Gattuso
et al. (1999) to include results of 13 investigations on corals and
coral reef systems. They proposed that calcification rate is controlled
by a rate law with calcification being proportional to (Varag 21)n.
The experimental data from the various sources were too scattered
to fit the model directly so they normalized the data. Rates of calcification were calculated from each experiment were calculated as a
percentage of an extrapolated Varag of 4.6, which is their estimated
saturation state of the tropical ocean in 1880 when atmospheric
pCO2 was 280 ppm based on the report of Kleypas et al. (1999).
The resulting plot still showed considerable scatter. The points fell
between a line predicted by the linear first-order rate (n ¼ 1) the
second curvilinear second-order rate (n ¼ 2). These points are
said to predict a decrease of 60% in coral and coral reef calcification
by the year 2065. Another set of points that show an insensitivity to
Varag fell outside of this region and was said to predict a decline of
only 1 –18% by 2065. These findings leave a great deal of uncertainty
Numerical models
Buddemeier et al. (2008) developed a spreadsheet-based numerical
model that calculates the effects of climate change on coral reefs
at local-to-regional scales using equations developed from data
on coral growth and mortality rates. The model calculates the
impacts to coral cover from changes in average sea surface temperature (SST) and Varag, and from high-temperature mortality (bleaching) events. The model uses a probabilistic assessment of the
frequency of high-temperature events under future climate scenarios to address scientific uncertainties about potential adverse
effects. Further, the model demonstrates the relative importance
of high-temperature events, increased average temperature, and
increased CO2 concentration on the future status of coral reefs.
The Buddemeier et al. (2008) model allows comparisons of past environmental history with predictions. Coral growth in this model
was controlled by Varag and the focus was on coral coverage rather
than net ecosystem calcification.
Silverman et al. (2009) made projections of global changes on
coral reefs using a model parameterized by field studies of calcification’s response to medium-term (2-year) fluctuations in calcification and Varag and concluded that most of the world’s reefs will be
compromised once atmospheric CO2 reaches 560 ppm. This is
based on an empirical rate law developed from field observations
for gross community calcification as a function of (Varag), SST,
and live coral cover. Calcification rates were calculated for .9000
reef locations using model values of Varag and SST at different concentrations of atmospheric CO2. The model predicted that when the
atmospheric partial pressure of CO2 reaches 560 ppm all coral reefs
will cease to grow and start to dissolve.
Evenhuis et al. (2015) developed a unified model that linked
increased temperature and OA to coral reef condition. Changes
were modelled by linking the rates of growth, recovery, and calcification to the rates of bleaching and temperature induced mortality
552
for corals. The model has novel aspects including use of is the
Arrhenius equation, thermal specialization, resource allocation
trade-offs, and adaption to local environments. The model was constructed using a range of experimental and observational data, but
assumes that response of corals to Varag can give a reasonable estimate for future impact of OA.
Major assumptions of the models
The models described above have employed simplifying assumptions. Recent findings have shown that in some cases OA model
results do not agree with field and laboratory observations (e.g.
Jury et al., 2010; Pandolfi et al., 2011; Shamberger et al., 2011,
2014; Comeau et al., 2012; Roleda et al., 2012). Such contradictions
give us new insight into the processes controlling response of coral
reefs to OA and allow us to review some of the basic concepts. This is
precisely the purpose of modelling, so it is appropriate to revisit and
re-evaluate basic assumptions involved. Four major assumptions
are listed and evaluated as follows:
Assumption 1: Oceanic conditions of Varag control or are at least
highly correlated with net calcification rate (Gnet) on coral reefs.
The concept that open-ocean Varag controls Gnet and thus coral
reef development was carried forward by many investigators as
described above. More recently however, Duarte et al. (2013)
pointed out that metabolism in inshore waters such as coral reefs
results in strong diel to seasonal fluctuations in pH with characteristic ranges of 0.3 pH units or more over a diurnal cycle. Ohde and
van Woesik (1999) in their Table 3 showed that pH varied 0.7 pH
trough a diurnal cycle (1 d from 8.6 to 7.9; on another day from
8.4 to 7.8). Such extreme variability and presence of multiple,
complex metabolic controls on coral reefs suggest that changes in
the open-ocean Varag cannot be transposed to coastal ecosystems
directly. Hence, Duarte et al. (2013) contend that OA from anthropogenic CO2 is largely an open-ocean syndrome. This
concept has been further supported by the work of Cyronak et al.
(2014) who showed biogeochemical processes can influence the
pCO2 and pH of coastal ecosystems on diel and seasonal time
scales, potentially modifying the long-term predicted effects of increasing atmospheric CO2. By compiling data from the literature
and removing the effects of short-term variability, they showed
that the average pCO2 of coral reefs throughout the globe has
increased 3.5-fold faster than in the open ocean over the past 20
years. This rapid increase in coastal and reef pCO2 has the potential
to negate the results of models that calculate the predicted effects of
OA on coral reef ecosystems based on oceanic Varag. They constructed a model to demonstrate that potential drivers of elevated
pCO2 include additional anthropogenic disturbances such as
enhanced nutrient and organic matter inputs.
P. L. Jokiel
from reef to reef depending on differences in the primary factors
controlling both calcification and Varag. The calcification rate of
reefs is driven largely by photosynthetic rate of the calcifying component and limited by proton efflux from the corals (Jokiel et al.,
2014). Photosynthetic rate of a reef community changes with available irradiance and other factors such as community composition,
nutrient, water motion, herbivore grazing, etc. If Gnet is measured
using the alkalinity depletion method (Kinsey 1978; Smith and
Kinsey 1978) the result is greatly modified by dissolution rate of carbonates and changes in pH due to photosynthesis and other factors
(Jokiel et al., 2014; Murillo et al., 2014). Thus, we find no consistent
relationship between Gnet and Varag on different reefs. Figure 1 presents the results of four field investigations on coral reefs from different parts of the world. There is a lack of consistency in the
relationship between Varag and Gnet for different reefs. The reef
with lowest Varag shows the highest Gnet. Regression line slopes
between Varag and Gnet are generally positive, but the positive
slope observed that had been observed during summer at
Ningaloo Reef did not occur in winter at the same location. Chan
and Connolly (2013) pointed out that the number of experimental
studies seeking to estimate the sensitivity of Gnet to Varag has
increased dramatically in recent years, but the magnitude of the calcification response estimated in these studies has varied enormously, ranging from an increase in 25% to a decrease in 66%, per unit
decrease in Varag. Rodolfo-Metalpa et al. (2015) provide laboratory
evidence that Gnet of three common cold-water corals is not affected
by pCO2 levels expected for 2100 (pCO2 1058 matm, Varag 1.29). A
field transplant experiment with one of the species to 350 m depth
(pHT 8.02; pCO2 448 matm, Varag 2.58) and to a 3 m depth CO2
seep in oligotrophic waters (pHT 7.35; pCO2 2879 matm, Varag
0.76) showed that the transplants calcified at the same rates. The
data suggest that OA will not disrupt cold-water coral calcification,
although falling Varag may affect other organismal physiological
and/or reef community processes.
Assumption 2: Calcification rate is driven by bulk water carbonate
ion concentration [CO3 2− ] expressed as Varag.
This assumption appears flawed. Carbonate ion concentration
(and thus Varag) of bulk water in laboratory incubations and in
field flow metabolism experiments increases with increasing calcification rate, so carbonate ion concentration (or Varag) cannot be limiting calcification (Jokiel et al. 2014). Aragonite saturation state lags
behind calcification by 2 h over the diurnal cycle (Shamberger et al.,
2011; McMahon et al., 2013; Jokiel et al., 2014) and therefore cannot
be driving calcification. However, there is a correlation between
Varag and Gnet. The slope and intercept of the correlation varies
Figure 1. Plot of net calcification rate Gnet vs. Varag from four studies of
calcification conducted in the field: Shamberger et al. (2011), Kaneohe
Bay, Hawaii (solid squares); Ohde and van Woesik (1999), Rukan-sho,
Japan (solid triangles); Silverman et al. (2007), Eilat Israel (open circles);
Falter et al. (2012), Nigaloo Reef, Western Australia summer (open
diamonds) and winter (solid diamonds).
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Predicting the impact of ocean acidification on coral reefs
Asumption 3: Changes in coral calcification rate can be used to estimate future changes in coral reef calcification rate.
This assumption is questionable because corals can continue to
grow relatively well at levels of OA that result in net dissolution of
a coral reef (Andersson et al., 2009). A related issue is that growth
of corals under various conditions of OA is generally measured directly by change in weight or linear extension (Jokiel et al., 1978),
whereas reef calcification is generally measured by the alkalinity
depletion method (Kinsey, 1978, Smith and Kinsey, 1978). The alkalinity depletion method measures Gnet and can include a substantial
contribution of total alkalinity (AT) from dissolving carbonate
sediment and rocks (Murillo et al., 2014) as well as contributions
from other components such as macroalgae, crustose coralline
algae, sediment diagenesis, etc. Important reef calcifiers such as
crustose coralline algae (CCA) are far more sensitive to OA condition than corals and can be dissolving on a reef at OA levels that
still allow substantial coral growth (Jokiel et al., 2008; Kuffner
et al., 2008). There are many reefs in the world that are dominated
by CCA, with a very small component of live coral.
Secondary calcification, bioerosion, and reef dissolution are integral to the structural complexity and long-term persistence of
coral reefs, yet these processes have received less research attention
than reef accretion by corals. Silbiger and Donahue (2015) found
that secondary reef calcification and dissolution responded differently to possible future conditions of global warming and increasing
OA. Calcification showed a non-linear response to the combined
effect of increased pCO2 and increased temperature while dissolution increased linearly, leading to the conclusion that dissolution
may be more sensitive to climate change than calcification.
Comeau et al. (2014) tested impact of OA on coral reef communities
with associated sediments and sediments alone maintained in
outdoor flumes under ambient pCO2 vs. high pCO2 at various
flow rates. Calcification correlated positively with flow and negatively to increased pCO2 with a substantial dissolution component due
to the presence of sediment.
Assumption 4: The impact of ocean acidification is additive and not
synergistic with other environmental factors.
Existing models assume that future reduction in reef coral cover
due to elevated temperature (lower growth and high mortality) and
OA (lower growth) are simply additive (Hoegh-Guldberg et al.
(2007), but more recent reports have demonstrated antagonisms
and synergisms. Reynaud et al. (2003) grew small colonies of the
reef coral Stylophora pistillata in a matrix of two temperature treatments (25 vs. 288C) and two pCO2 treatments (460 vs. 750 matm)
and report no statistical difference between pCO2 treatments at
258C, but a large decline in calcification of 50% at 288C under
acidified conditions. Anlauf et al. (2011) studied the effects of a
18C increase in temperature and a 0.2 –0.25 unit decrease in pH
on the growth of primary polyps in the coral Porites panamensis.
The growth of polyps was reduced marginally by acidic seawater
but the combined effect of higher temperature and lowered pH
caused a significant growth reduction of 30%. A similar 30%
decline at higher temperature—elevated pCO2 was shown by
Edmunds et al. (2012) for the rapidly growing branched coral
Porites rus, but a slower growing massive Porites sp. did not show
the effect. The temperature – pCO2 interaction has been observed
in other calcifying reef organisms. Martin and Gattuso (2009)
observed an interaction effect between temperature and pCO2 on
the coralline alga Lithophyllum cabiochae. Algae were maintained
in aquaria for 1 year at ambient or elevated temperature (+38C)
and at ambient pCO2 (400 matm) or elevated pCO2 (700 matm).
During summer the net calcification of the algae decreased by
50% when both temperature and pCO2 were elevated whereas
no effect was found under elevated temperature or elevated pCO2
alone.
Questioning the assumptions
The assumption that Varag (or its surrogate [CO3 2− ]) drives Gnet has
been challenged by a series of publications (Jokiel, 2011a, b , 2013,
Jokiel et al., 2014; Cyronak et al., 2016). These papers argue that calcification is not limited by [CO3 2− ] but rather by the ability to dissipate excess protons generated by the calcification process. Various
contradictions and inconsistencies in the calcification literature are
resolved by the proposed proton flux model (Jokiel, 2011a, b).
Recent observations have challenged paradigm that Varag controls
Gnet. For example the presence of rich coral reefs in Kāne‘ohe Bay,
Hawai‘i existing at low Varag (high pCO2 levels) as shown in
Figure 1. The elevated pCO2 is due to metabolism of terrigenous
organic material transported into the bay by streams. Fagan and
Mackenzie (2007) found that pCO2 was averaging 500 matm.
Silverman et al. (2009) estimated that “by the time atmospheric
partial pressure of CO2 will reach 560 ppm all coral reefs will cease
to grow and start to dissolve”, yet these reefs are flourishing.
Several reports have shown that Varag lags behind Gnet by 2 h over
the diurnal cycle (Shamberger et al., 2011; McMahon et al., 2013;
Jokiel et al., 2014) which means that Varag is not driving Gnet.
Testing assumptions using exemplary data
from the Rock Islands, Palau
Shamberger et al. (2014) reported the existence of highly diverse,
coral-dominated reef communities under chronically low pH and
low Varag in the Rock Islands of Palau, affording an opportunity
to test the validity of several of the above assumptions and
provide additional explanations. Their comparison was made
between sites located in the open ocean at (1 –3 km offshore) with
sites located in a shallow flow-restricted lagoon located at a distance
of 7 –9 km from open-ocean waters (Figure 2). The Rock Islands are
located in the south lagoon of Palau between Koror and Peleliu. This
area is an uplifted ancient coral reef that forms a complex carbonate
labyrinth of shallow channels and lagoons containing 250– 300
small islands, which are actually carbonate reef outcrops. Some of
the islands display a mushroom shape with a narrow base created
by rapid dissolution and bioerosion by sponges and bivalves and
intense grazing by chitons, urchins, and fish in the intertidal
(Lowenstam, 1974; Glynn, 1997). The extreme bioerosion and carbonate dissolution in the area coupled with very low rates of seawater exchange (Golbuu et al., 2012) produces atypical conditions
on the reef. Measurements made in the Rock Islands showed extremely low Varag (2.4) and low pH (7.8) in this area of high
coral coverage compared with high Varag (3.8) and high pH
(8.1) in the offshore area.
An analysis of the dynamic benthic processes involved in coral
calcification on the Rock Island reefs can be made with the reported
data for [AT], [DIC], and [H+]. The analysis requires that we accept
the assumptions implicit in the experimental design that horizontal
mixing is uniform throughout the area of study and that [AT],
[DIC], and [H+] are not greatly modified by pelagic processes in relation to benthic processes. The environmental gradient between the
lagoon stations and offshore stations is shown for [AT] (Figure 2a),
554
P. L. Jokiel
[DIC] (Figure. 2b), and [H+] (Figure 2c). The strongest gradient
(p , 0.001, Figure 2c) is for net flux of protons out of the lagoon.
Net flux of AT into the lagoon also shows a strong gradient (p ,
0.001, Figure 2a). Net DIC flux into the lagoon did not show a statistically significant correlation (p ¼ 0.089, Figure 2b). This pattern
is consistent with detailed observations made by Jokiel et al. (2014)
showing the lag in proton flux in a rapidly calcifying system.
Dissipation of the protons generated by the process of calcification
is a major factor limiting coral growth. Flushing of the Rock Island
system with oceanic waters removes H+ and brings in water with
higher [AT]. DIC is abundant in seawater and is not limiting.
Proton flux is the important parameter as shown by changes in
[AT] and [H+] with distance from the open ocean.
An explanation for the presence of this rich coral reef growing
under low Varag can be developed based on the proton flux
hypothesis (Jokiel, 2011a). Dissolution of carbonates increases
AT (Wisshak et al., 2013), especially under low pH conditions at
night. Such additional AT will be retained in the system due to
low water exchange and made available to the calcifying organisms
during the day. High rainfall and tidal variation results in submarine groundwater discharge (SGD), which serves as another source
of AT to the calcifying organisms. Furthermore, rainfall in this area
is high and varies from 200 to 450 mm month21 (Australian
Bureau of Meteorology and CSIRO, 2011). Cyronak et al.
(2013a, b) measured increased AT flux due to SGD with the daily
flux rate of up to 1080 mmol m22 d21. Dissolution of the
complex non-living carbonates supplemented with additional AT
from SGD in the low-flushing Rock Island reef system over the
24 h period would provide considerable AT buffering of the
protons being generated by calcification. Supplementary Figure
S4 of the Shamberger et al. (2014) report shows a rich coral
community at the Rock Islands lacking in macroalgae and turf
algae, probably due to intense herbivore grazing pressure and
low inorganic nutrient supply. Presence of a larger macroalgae
component would have increased pH during daylight hours
without altering AT. The higher pH in such situations shifts the
equilibria toward increased [CO3 2− ] and therefore higher Varag.
In this system, as in other systems, Varag simply describes the
portion of DIC that is being expressed as CO3 2− under prevailing
pH conditions (which can be modified to different degrees
by algal photosynthesis without changing AT) and thus is not
of value as a universal metric driving coral calcification. There is
a local correlation between Varag and Gnet, but Varag is a dependent
variable on several factors including Pnet and local dissolution
rate of carbonates (e.g. Murillo et al., 2014). The relationship
of Gnet to Varag relationship holds within a given system, but
varies between systems due to differences in Pnet, which drives
Gnet. Systems with a higher portion of Pnet being provided by
non-calcifying photosynthetic organisms will have a different relationship to Varag than a system dominated by calcifying photosynthetic organisms.
Further evaluation of existing models
and methodology
Figure 2. Change in water chemistry from open ocean to coral lagoon
using data from Shamberger et al. (2014) for: (a) total alkalinity,
(b) dissolved inorganic carbon, and (c) proton concentration.
Jones et al. (2015) evaluated four published models of reef carbonate
production in terms of their predictive power at local and global
scales. The models are based on functions sensitive to combinations
of light availability Varag and temperature and were implemented
within a specifically developed global framework, the Global Reef
Accretion Model. None of the models reproduced the independent
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Predicting the impact of ocean acidification on coral reefs
rate estimates of whole-reef calcification. The output from the
temperature-only based approach was the only model to significantly correlate with coral calcification rates. They pointed out that validation of reef carbonate budgets is severely hampered by limited
and inconsistent methodology in reef-scale observations. Pandolfi
et al. (2011) detected striking inconsistencies between experimental
and field observations of the Varag vs. calcification relationship and
suggested that the role of dissolution could account for the differences. Tribollet et al. (2009) found that carbonate dissolution
by microbial endoliths measured under elevated pCO2 was 48%
higher than under ambient pCO2. Chan and Connolly (2013)
tested whether the methodological and biological factors that have
been hypothesized to drive variation in magnitude of response
explain a significant proportion of the among-study variation.
They found that the overall mean response of coral calcification is
15% per unit decrease in Varag over the range 2 , Varag , 4.
Among-study variation is large (standard deviation of 8% per
unit decrease in Varag). Neither differences in carbonate chemistry
manipulation method, study duration, irradiance level nor study
species growth rate explained a significant proportion of the amongstudy variation. Duarte et al. (2015) evaluated perceived ocean
calamities and concluded that the issue of global decline of ocean
calcifiers due to increasing OA is one of the areas with weak scientific
support. Improved predictive models are needed, which means that
we must sort out the mechanisms and strengthen the models.
Correlation between Gnet and the factor [CO3 2− ] which determines Varag does not establish cause and effect (Jokiel, 2013).
Experiments that documented correlations between Gnet, Pnet,
and seawater chemistry have been conducted repeatedly since
the development of the alkalinity depletion method to measure
coral calcification. Initial experiments described calcification dynamics in static aquaria incubations (Smith and Kinsey, 1978)
and reef field enclosures (Kinsey, 1978). More recently, these
experiments have been expanded to include continuous flow measurements of proton flux in coral reef mesocosms (Jokiel et al.,
2014). There is a basic physiological explanation for the observed
correlation between Gnet and Varag that must be understood.
Daytime coral metabolism rapidly removes DIC (primarily in
the form of HCO3 − ) from the seawater while photosynthesis provides the energy that drives Gnet (Jokiel et al., 2014). Higher pH
resulting from photosynthesis pushes the seawater carbonate
system equilibria toward higher [CO3 2− ] (and therefore higher
Varag) although DIC is decreasing. This scenario results in a positive correlation between Gnet and Varag. Both Varag and Gnet are dependent variables on Pnet and many other factors. The correlation
between Gnet and Varag is modified by changes in pH. Changes in
pH can be due to many processes (e.g. photosynthesis by macroalgae, addition of land-derived material, metabolism of organic
materials). Changes in AT occur due to bioerosion and dissolution
of carbonate sediment and rocks. Other factors such as irradiance,
temperature and water motion influence Pnet, Gnet and Varag.
Therefore, the slope and intercept of the regression line varies
widely (Figure 1).
In conclusion, there are large inconsistencies in descriptions
coral and coral reef response to OA. Part of this problem can be
traced to assumptions used in these studies. Perhaps the major
shortcoming of models lies in the belief that [CO3 2− ] and thus
Varag controls calcification. The alternate explanation is the rate
at which a calcifying system can rid itself of the excess protons produced as a waste product of calcification (Jokiel et al., 2014).
Results of Murillo et al. (2014) should also be considered. They
found that corals growing in a mixed-community experience an
environment that is more favourable to calcification (higher
daytime pH and dissolved oxygen due to algae photosynthesis,
additional input of AT and inorganic carbon from sediments).
They also showed that the widely used alkalinity depletion
method yields a lower net calcification rate for a mixedcommunity vs. a coral-only community due to AT recycling, although the corals may be calcifying at a higher rate under these
conditions. Increased temperature will play the dominant role in
the decline of reefs during future climate change with OA
playing a lesser role, so the uncertainties on the effects of OA
have less impact on the final estimates of reef decline. On the
brighter side, the consequent expansion of OA research will eventually produce a better understanding of the processes that control
coral calcification.
Acknowledgements
This work partially funded by the Pacific Island Climate Change
Cooperative and by the United States Geological Survey, Coastal
and Marine Geology Program cooperative agreement G13AC00130.
N. Silbiger, M Donahue, and three anonymous reviewers provided
comments that improved the original manuscript.
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