Introduction
Ocean acidification (OA) caused by human-induced increase of atmospheric
CO2 (Sabine et al., 2004; Feely et al., 2009) is considered one of the
major threats to marine calcifying organisms and ecosystems (Fabry et al.,
2008; Hofmannn et al., 2010; Doney et al., 2012; Gattuso et al., 2015). Among
all marine habitats, tropical coral reefs are recognized as the most
endangered (Hoegh-Guldberg et al., 2007; Kleypas and Yates, 2009; Pörtner
et al., 2014), since in addition to reduced calcification (Langdon et al.,
2000; Marubini et al., 2008; Doney et al., 2009; Gattuso et al., 2014), a
lower pH also weakens the reef framework by favoring bioerosion and enabling
carbonate dissolution (Gattuso et al., 2014; Manzello et al., 2014; Barkley
et al., 2015). According to the IPCC business-as-usual scenario, about
90 % of the ocean's surface waters will become undersaturated with
respect to aragonite in the next decades (Gattuso et al., 2015), emphasizing
the need to study the response of natural ecosystems to OA. Nowadays,
aragonite undersaturated surface waters occur naturally in some parts of the
ocean, as a consequence of underwater volcanic seeps (Hall-Spencer et al.,
2008; Fabricius et al., 2011, 2015; Enochs et al., 2015) or upwelling that
drags corrosive deep water into the surface mixed layer (Feely et al., 2008;
Hauri et al., 2009; Fassbender et al., 2011; Harris et al., 2013).
Aside from some studies at volcanic seeps (Fabricius et al., 2011, 2015;
Kroeker et al., 2011; Enochs et al., 2015) or at reefs in the eastern
tropical Pacific (ETP) (Manzello, 2008, 2010a, b; Manzello et al., 2008,
2014), our understanding of OA impacts on corals derives mainly from
laboratory and seawater enclosure experiments (Pörtner et al., 2014;
Hall-Spencer et al., 2015). These results are used to predict ecosystem
responses to future OA (Kleypas et al., 2006; Kleypas and Langdon, 2006), but
their reliability is challenged by the artificial conditions under which the
experiments are conducted. For example, the duration of studies is often too
short to allow a full adaptation or acclimatization of the organisms/systems
to the changing environmental conditions, and the missing connectivity
between ecosystems in seawater enclosures restricts natural interactions
between organisms (Kleypas et al., 2006; Kleypas and Langdon, 2006; Hofmann
et al., 2010). In situ studies in natural low-pH conditions are able to
overcome some of these problems and the ETP is well known for its
CO2-enriched and acidic subsurface waters (Takahashi et al., 2014).
Upwelling events decrease the carbonate saturation state (Ω) along
the Central American coast (Manzello et al., 2008; Manzello, 2010b; Rixen et
al., 2012) and have the potential to produce poorly cemented coral reefs
with low accretion rates that are subject to rapid bioerosion (Manzello et
al., 2008; Alvarado et al., 2012).
Corals in the northern part of the Costa Rican Pacific coast are developing
under the influence of the seasonal Papagayo upwelling (Jiménez et al.,
2010; Rixen et al., 2012; Stuhldreier et al., 2015a, b). To contribute to the
general understanding of OA impacts on coral reefs, we investigated the
variability of the carbonate system in the upwelling-influenced Bahía
Culebra, Costa Rica. The main objectives of this study were (1) to describe
the behavior of the carbonate system on diurnal and seasonal timescales,
(2) to characterize the controlling processes and (3) to determine
ecological impacts of changing carbonate systems. Furthermore, our results
will allow us to draw some conclusions concerning future thresholds of coral
reef development within this bay.
Methods
Study site
Bahía Culebra, located in the Gulf of Papagayo, North Pacific coast of
Costa Rica (Fig. 1), is strongly influenced by the north easterly Papagayo
winds. The strongest wind jets develop during the boreal winter (Amador et
al., 2016) and are driven by large-scale variations of the trade winds
(Chelton et al., 2000; Alfaro and Cortés, 2012). When Papagayo winds blow
through the mountain gap between southern Nicaragua and northern Costa Rica,
the resulting strong offshore winds on the Pacific side can lead to upwelling
of cold and nutrient-enriched subsurface waters between December and April
(McCreary et al., 1989; Brenes et al., 1990; Ballestero and Coen, 2004;
Kessler, 2006). These cyclonic eddies also influence the magnitude and
location of the Costa Rica Dome (CRD), which is located approx. 300 km off
the Gulf of Papagayo (Fiedler, 2002). However, the CRD changes its distance
to the Costa Rican coast throughout the year, as a result of differences in
wind forcing (Wyrtki, 1964; Fiedler, 2002). During the dry season,
particularly between February and April, offshore moving water masses
strengthen upwelling at the coast and shoal the thermocline in the Gulf of
Papagayo (Wyrtki, 1965, 1966; Fiedler, 2002). In May–June, during the onset
of the rainy season, the CRD moves offshore (Fiedler, 2002; Fiedler and
Talley, 2006) and the North Equatorial Countercurrent (NECC) can carry
tropical water masses into Bahía Culebra until December, when upwelling
sets in again (Wyrtki, 1965, 1966).
Location of Bahía Culebra (square) in the Gulf of Papagayo,
North Pacific coast of Costa Rica (insert). Measurements were made at Marina
Papagayo (star). Main ocean currents influencing the Gulf of Papagayo (dashed
arrows): NECC indicates the North Equatorial Countercurrent; CRCC indicates
the Costa Rica Coastal Current.
Measurements
We measured in situ pH, pCO2 and seawater temperature (SWT) during two
non-upwelling periods (15 days in June 2012 and 7 days in May–June 2013;
Fig. 2). Measurements were undertaken with two Submersible Autonomous Moored
Instruments (SAMI-pH and SAMI-CO2) (www.sunburstsensors.com, last access: 10 April 2017), in
sampling intervals of 15 (June 2012) and 30 min (May–June 2013).
SAMI sensors were deployed at the pier of Marina Papagayo
(85∘39′21.41′′ W, 10∘32′32.89′′ N), on top of a
carbonate sandy bottom in the inner part of Bahía Culebra (Fig. 1). The
water depth varied approximately between 5 and 8 m depending on the tide, but
sensors, hooked to the pier, moved up and down with the tide and were always
at the same depth, 1.5 m below the surface. SAMI instruments measured pH
(total hydrogen ion scale) and pCO2 spectrophotometrically by using a
colorimetry reagent method (DeGrandpre et al., 1995, 1999; Seidel et al.,
2008). Salinity from discrete samples was measured with a WTW probe
(Cond3310) and was used for correction of pH values. Calculation of aragonite
saturation state (Ωa) from parameters measured in situ with
SAMI sensors is accurate (Cullison Gray et al., 2011; Gray et al., 2012), but
discrete water samples were collected as often as possible to validate the
instruments (Fig. 3). The 250 mL borosilicate bottles were filled with seawater
at 30 cm below the surface and preserved with 200 µL of 50 %
saturated HgCl2 solution to inhibit biological activity (Dickson et al.,
2007). Samples were stored at 3–4 ∘C until analysis. Total
alkalinity (TA) and dissolved inorganic carbon (DIC) were measured using a
VINDTA 3C (Versatile INstrument for the Determination of Total
inorganic carbon and titration Alkalinity; Marianda, Kiel, Germany) coupled with a UIC
CO2 coulometer detector (UIC Inc., Joliet, USA). Both instruments were
calibrated with Dickson Certified Reference Material (Batch 127) (Dickson et
al., 2003). DIC concentrations as well as TA and Ωa were
calculated with the CO2SYS program as a function of measured pH and
pCO2, with dissociation constants of Mehrbach et al. (1973) for
carbonic acid as refit by Dickson and Millero (1987) and Dickson (1990) for
boric acid.
Measured parameters (wind speed, SWT, pH and pCO2) during the
non-upwelling seasons of June 2012 (a, b) and May–June 2013 (c, d) at
Bahía Culebra. Shaded area in panels (a, b) indicates the 2012
upwelling-like event.
Validation of in situ measurements of pH (a) and
pCO2 (b)
using discrete water samples. SAMI sensors measured pH and pCO2 directly
in the water column. The pH and pCO2 values used for validation were
calculated with the CO2SYS program as a function of measured TA and DIC;
discrete samples were measured with a VINDTA 3C system.
Wind speeds were obtained from a station of the Instituto Metereológico
Nacional (National Meteorological Institute of Costa Rica), located at the
nearby Liberia airport. The Módulo de Información Oceanográfica
of the University of Costa Rica (www.miocimar.ucr.ac.cr, last access: 27 September 2016) supplied the
tidal data. All coral growth values were taken from the literature; linear
extension rates from Bahía Culebra were measured by Jiménez and
Cortés (2003), whilst coral growth in Panama and Galápagos was
measured by Manzello (2010a). For the correlation between coral growth and
Ωa, we used the mean Ωa values from
Panama and Galápagos previously reported by Manzello (2010b).
Data analysis
We compared our data with values measured during the upwelling season in 2009
(Rixen et al., 2012). In 2009, xCO2 was measured by an underway
pCO2 system (SUNDANS) equipped with an infrared gas analyzer
(LI-7000), and pH was measured using an Orion ROSS electrode (an Orion
Star™). Correlations between tidal cycles and physicochemical parameters
(pH, pCO2, T, wind) during non-upwelling periods were tested via
Pearson correlation in Python. Differences in parameters (temperature, pH,
pCO2, TA, DIC and Ωa) between all periods (2009, 2012,
2013) were tested with a general linear model (GLM) in the statistical
package R. The GLM was evaluated using graphical methods to identify
violations of assumptions of homogeneity of variance and normality of
residuals. All GLM assumptions were met. Additionally, we developed a simple
model to improve our understanding of processes controlling the observed diel
trends, as seen in the time series data of pH and pCO2 (Figs. 2, 4).
The model simulates combined effects of metabolic processes (photosynthesis,
respiration, calcification and dissolution) on the carbonate chemistry. Input
parameters for starting the model were the calculated DIC (in 2012:
2037 µmol kg-1 at 07:00 UTC - 6
and 2019 µmol kg-1 at 15:00; in 2013:
1883 µmol kg-1 at 05:00 and 1805 µmol kg-1 at
15:00) and TA (in 2012: 2284 µmol kg-1 at 07:00; in 2013:
2193 µmol kg-1 at 05:00) values, corresponding to the highest
and lowest measured pCO2 during the day. Calculation of TA and DIC
from the pair pH and pCO2 is prone to errors (Millero, 2007; Cullison
Gray et al., 2011); however, the values used as input parameters in the model
are in range with those reported from other studies in tropical areas
(Manzello, 2010b; Cyronak et al., 2013b). The difference between the two DIC
concentrations (ΔDIC) was assumed to be caused by photosynthesis and
respiration and the resulting formation and decomposition of particulate
organic carbon (POC), as well as calcification and dissolution and the
precipitation and dissolution of particulate inorganic carbon (PIC, Eq. 1).
ROI describes the ratio between the production of organic carbon
(POC) and precipitation of calcium carbonate carbon (PIC) and was used to
link ΔPOC to ΔPIC (ROI = POC / PIC)
(Eq. 2, 3). The ROI was further constrained by the determined change of
TA (ΔTA). Therefore, it was considered that photosynthesis and
respiration of one mole of carbon increases and reduces TA by 0.15 units,
respectively (Broecker and Peng, 1982). Calcification and dissolution of one
mole of carbon decreases and increases TA by two units (Eq. 4). To verify the
results from the model, we used the output ΔDIC and ΔTA to
calculate new pCO2 and pH values, which were further compared to the
measured ones (Fig. 5). The best fit between modeled and measured values was
achieved with a respective ROI of -2.6 for 2012 and 1.0 for
2013, whereas the assumption of calcium carbonate dissolution caused the
negative sign.
ΔDIC=ΔPOC+ΔPICΔPIC=ΔPOCROIΔPOC=ΔDIC/1+1ROIΔTA=ΔPOC⋅0.15-ΔPOCROI⋅2
This was calculated on hourly time steps, separately for 2012 and 2013, using
the mean SWT (2012 = 29.61 ± 0.93 ∘C,
2013 = 30.08 ± 0.27 ∘C) and salinity (2012 = 32.5,
2013 = 32.5).
Diel pattern of parameters measured in Bahía Culebra. Data
points are hourly averages of 15 and 7 consecutive days in 2012 (a, b) and
2013 (c, d), respectively. The shaded area represents daylight hours.
Measured and calculated (*) parameters, during upwelling (2009)
and non-upwelling seasons (2012, 2013) at Bahía Culebra, Costa Rica.
pH
pCO2
CO2
T
DIC*
TA*
Ω∗
(total scale)
(µatm)
(µmol kg-1)
(∘C)
(µmol kg-1)
(µmol kg-1)
2009
Mean ± SD
7.91 ± 0.32
578.49 ± 42.82
16.44 ± 1.35
25.09 ± 0.57
2098.71 ± 103.81
2328.42 ± 118.45
2.71 ± 0.29
2012
Mean ± SD
7.98 ± 0.04
456.38 ± 69.68
11.77 ± 1.99
29.61 ± 0.93
1924.65 ± 195.07
2204.54 ± 212.18
3.32 ± 0.46
2013
Mean ± SD
8.02 ± 0.03
375.67 ± 24.25
9.56 ± 0.64
30.08 ± 0.27
1800.92 ± 142.78
2102.66 ± 174.79
3.50 ± 0.49
Discussion
Natural OA beyond the upwelling season
The observed differences in pH and pCO2 between 2012 and 2013 suggest
that the non-upwelling season exhibits a strong interannual variability
(Table 1). In 2012, pH was lower and pCO2 higher than in 2013 (Fig. 2b,
c). The June 2012 time series data showed that SWT decreased and pCO2
increased from 300 to 650 µatm in less than a week, after several
days of strong afternoon winds (Fig. 2a). Similarly, this increase in
pCO2 was accompanied by a drop in pH from 8.04 to 7.83 (Fig. 2a).
This suggests that an enhanced wind-driven vertical mixing entrained cooler
and CO2-enriched waters from greater water depth into the surface layer.
The associated SWT drop from 31.4 to 27.1 ∘C was similar to that
observed during the onset of the 2009 upwelling event (26.2 to
23.7 ∘C; Rixen et al., 2012). Nevertheless, the higher SWT during
the 2012 non-upwelling season suggests that the entrained water originated
from a shallower water depth, compared with the water upwelled in 2009. The
pCO2 values with up to 650 µatm reached the same level
during both events, which is partially caused by the higher SWT in 2012.
However, DIC concentrations in 2012
(1924.65 ± 195.07 µmol kg-1) were lower than those in
2009 (2098.71 ± 103.81 µmol kg-1) but exceeded those
in 2013 (1800.92 ± 142.78 µmol kg-1; Table 1). During
the 7 days of the cold-water intrusion event in 2012
(10–17 June), the DIC concentrations dropped from
2355.39 µmol kg-1 down to 1715.30 µmol kg-1.
This implies that in addition to high SWT, the entrainment of
CO2-enriched subsurface water increased the pCO2 not only during
the upwelling periods but also during the 2012 non-upwelling season.
Correlations between tide height and four parameters during
the non-upwelling seasons (2012, 2013).
Year
pH
pCO2
T
Wind
2012
-0.004
0.037
-0.005
0.033
2013
0.111
0.026
-0.093
-0.126
All p values > 0.05.
Since in 2012 the pCO2 had already increased by 7 June and the SWT
decreased 2 days later (10 June), the inflow of CO2-enriched waters
seems to have increased the pCO2 already prior to the strengthening of
local winds (Fig. 2b). Later, local wind-induced vertical mixing seems to
have amplified the impact of the inflowing CO2-enriched water mass on
the pCO2 in the surface water by increasing its input into surface
layers. Accordingly, the CO2-enriched waters were apparently supplied
from a different location than they are during the upwelling season. Since the
NECC carries offshore waters towards the Costa Rican shore during the
non-upwelling season (Wyrtki, 1965, 1966; Fiedler, 2002), it is assumed that
the CO2-enriched subsurface water originated somewhere south of our
study area in the open ETP. The absence of such a cold event during the
non-upwelling season in 2013 suggests that the occurrence of this kind of
event might be an irregular feature (Fig. 2c, d), and the driving forces are
still elusive. Nevertheless, these types of events have the potential to
affect the metabolic processes in the bay as will be discussed in the
following section, which analyzes the daily cycles during the non-upwelling
seasons in 2012 and 2013.
Processes behind the variability of the carbonate system
In 2012, the pH and the pCO2 values followed a pronounced diurnal
cycle with highest pH and lowest pCO2 values during the late afternoon
and lowest pH and highest pCO2 values around sunrise in the early
morning (Fig. 4a). Such daily cycles are typical for tropical regions and are
assumed to be caused by photosynthesis during the day and respiration of
organic matter during the night (Shaw et al., 2012; Albright et al., 2013;
Cyronak et al., 2013a). The aragonite saturation state as well as the DIC / TA
ratio followed this pattern, with higher Ωa and lower DIC / TA
ratio values during the day as well as lower Ωa and higher
DIC / TA values at night (Fig. 4b). Although the pCO2 cycles in 2013
followed a similar pattern to 2012, pH cycles were less predictable (Fig. 4).
To characterize the relative importance of the processes responsible for the
observed changes in pH and pCO2 (photosynthesis, respiration,
calcification and dissolution), we used the model described earlier, which is
based on the determined DIC concentrations during times when pH and
pCO2 revealed their daily minima and maxima, respectively. For
example, if photosynthesis of organic matter dominates the transition from
early morning maxima of pCO2 to late afternoon minima of pCO2,
it should be associated with a decline in DIC. Whether photosynthesis was
accompanied with enhanced calcification can be detected by an associated
decrease of TA. Since decreasing DIC raises the pH and a decrease in TA
lowers the pH, such photosynthetic-enhanced calcification hardly affects the
pH and could explain the weak daily cycle observed in 2013. Alternatively, if
photosynthesis is accompanied by carbonate dissolution during the day, this
would amplify the daily cycle of pH and pCO2 as seen during the
cold-water intrusion event in 2012. Likewise, an increased photosynthesis
resulting from higher nutrient concentrations (Pennington et al., 2006) could
also be causing the observed large amplitude during the event in 2012.
However, in our case, the determined TA and DIC concentrations constrain the
impact of the formation of organic matter (POC is equivalent to photosynthesis
minus respiration) and calcification (PIC is equivalent to calcification minus dissolution) on
the carbonate system. This sets the boundaries within which the observed
diurnal cycle of pH and pCO2 has to be explained (Fig. 5c, d). In
order to reconstruct the diurnal cycle of pH and pCO2 within these
boundaries, we assumed a photosynthetic-enhanced calcification during the day,
and vice versa dissolution and respiration at night. Thereby, the best fit
between pH and pCO2 measured in 2013 and the respective calculated
values could be obtained by using a ROI of 1. This approach
failed to explain the diurnal cycle of pH and pCO2 as observed during
the 2012 cold-water intrusion event (10–17 June). The only solution we found
to explain these pronounced diurnal cycles within the given DIC and TA
boundaries was to assume that photosynthesis and dissolution prevailed during
the day and respiration and calcification occurred at night. The
ROI of -2.6 resulted in the best fit between the measured and
calculated pH and pCO2 for the 2012 event, whereas the negative sign
reflects the contrasting effects of calcification and dissolution on the DIC
concentration.
Mean aragonite saturation states (Ωa) – from
present and former studies – versus previously reported mean linear extension
rates of (a) Pocillopora damicornis and (b) Pavona clavus
from upwelling areas in Costa Rica (CR) (Jiménez and Cortés, 2003),
Panama (PAN) and Galápagos (GAL) (Manzello, 2010a). The red dotted line
shows the regression equation as estimated by Rixen et al. (2012). The red mark
represents our estimated Ωa threshold for Bahía Culebra,
when coral growth equals zero.
Dissolution taking place during daytime is peculiar but not completely
unusual, as it has been reported on tropical sandy bottoms under ambient
(Yates and Halley, 2006a, b; Cyronak et al., 2013b)
and high-CO2 conditions
(Comeau et al., 2015). Similarly, dark calcification is not entirely uncommon
and occurs in both sandy bottoms and coral reefs (Yates and Halley, 2006b;
Albright et al., 2013). Accordingly, the entrainment of CO2-enriched
water from the NECC seems to shift the carbonate chemistry of Bahía
Culebra from a system where photosynthesis and calcification are the
controlling processes during daylight hours to a system in which daytime is
dominated by photosynthesis and dissolution. The net effect, as observed, is
an enhanced pCO2 and lower Ωa during periods
characterized by the inflow of CO2-enriched waters (Table 1). This has
strong ecological implications for local coral reef ecosystems.
Ecological implications for coral reefs
Coral reefs in Bahía Culebra were dominated by Pocillopora spp.
and Pavona clavus (Jiménez, 2001; Jiménez et al., 2010),
whereas Porites lobata is the main reef forming coral in the
southern part of the Costa Rican Pacific coast (Cortés and Jiménez,
2003; Glynn et al., 2017). Although the reefs in the north are naturally
exposed to periodic high-CO2 conditions during upwelling events (Rixen
et al., 2012), as well as during cold-water intrusions in the non-upwelling
season, the linear extension rates of Pocillopora spp. and
P. clavus exceeded those of the same species in other regions
(Fig. 6) (Glynn, 1977; Jiménez and Cortés, 2003; Manzello, 2010a;
Rixen et al., 2012). This suggests that local corals are adapted and/or
acclimatized to the upwelling of cold and acidic waters.
Aragonite saturation state (Ωa) is known as one of the main
variables influencing coral growth and therefore reef distribution around the
world (Kleypas et al., 1999). By integrating the data from the present study
and values previously reported by Rixen et al. (2012), we estimated that the
annual mean Ωa in Bahía Culebra is 3.06. Additionally,
earlier studies in the ETP measured Ωa values and coral
extension rates from locations that are under the influence of upwelling
events (Manzello, 2010a), whilst extension rates from Bahía Culebra were
measured by Jiménez and Cortés (2003). The correlation between our
estimated Ωa with the available data from Bahía
Culebra, Panama and Galápagos indicates that coral extension rates in
each of those locations are predictable by their corresponding
Ωa values (Fig. 6).
The dependency of coral growth on Ωa and the mean Ωa (2.71) during the upwelling season (Table 1) suggests that
upwelling of acidic waters should reduce corals' relatively high annual mean
growth rates in Bahía Culebra. The increased Ωa during
the non-upwelling season in turn must enhance linear extension and explains
corals' high annual mean growth rates. The Ωa values from
this study suggest that most favorable conditions for coral growth occur
during the non-upwelling season, the period that coincides with development of
the rainy season. This implies that during the main growing season the
eutrophication and siltation caused by human impacts on river discharges, as
well as the development of harmful algal blooms, could also strongly affect
the corals' annual mean growth rates (Cortés and Reyes-Bonilla, 2017).
Despite the corals' high annual mean linear extension rates, studies carried
out in 1973 showed that the thickness of the reef framework within our study
area was with 0.6 to 3 m (mean 1.8 m) among the lowest in the ETP, where
Holocene framework accumulation in Pocillopora-dominated reefs could
reach up to 9 m (Glynn et al., 1983; Toth et al., 2017). During the last
decade, it further decreased (Alvarado et al., 2012), and during the period of
our observation the reef frameworks of Pocillopora spp. in
Bahía Culebra hardly exceeded a thickness of 0.5 m. This denotes that
although Pocillopora spp. and P. clavus are adapted to the
entrainment of acidic waters, these reefs are growing in an environment at
the limit of reef-building corals' tolerance in terms of temperature, nutrient
loads and pH (Manzello et al., 2017). Gaps in coral reef accretion at the ETP
are known from the geological record (Toth et al., 2012, 2015, 2017). They
have been linked to increased El Niño–Southern Oscillation (ENSO) variability (Toth et al., 2012, 2015) and
stronger upwelling conditions (Glynn et al., 1983), favoring dissolution and
erosion of reef frameworks while at the same time restricting coral growth.
The y intercept of the regression equation derived from the correlation
between linear extension rates and Ωa furthermore implies
that linear extension of P. damicornis and P. clavus should
approach zero under a carbonate saturation state of
Ωa < 2.5 (P. damicornis) and < 2.2
(P. clavus). According to climate predictions, the global
Ωa will reach values < 2.0 by the end of this century
(IPCC, 2014), and major upwelling systems such as those off California and
South America will intensify (Wang et al., 2015). Combined effects of ocean
acidification and impacts of stronger upwelling on Ωa in the
ETP and on Ωa in Bahía Culebra are difficult to
predict. Worldwide, OA is expected to reduce coral reefs' resilience by
decreasing calcification and increasing dissolution and bioerosion (Kleypas
et al., 1999; Yates and Halley, 2006a; Anthony et al., 2011). Coral reefs
from the ETP are affected by chronic and acute disturbances, such as thermal
stress and natural ocean acidification resulting from ENSO and upwelling
events, respectively (Manzello et al., 2008; Manzello, 2010b). Historically,
these reefs have shown a high resilience to both stressors separately, but
their coupled interaction can cause coral reefs to be lost within the next decades.
The ETP has the lowest Ωa of the tropics, near the
threshold values for coral reef distribution; therefore, the reefs from this
region may be the most affected by the increasing levels of anthropogenic
CO2 and also show the first negative impacts of this human-induced OA
(Manzello et al., 2017). This emphasizes the importance of the Paris
Agreement and all the global efforts to reduce the CO2 emission into the
atmosphere (Figueres et al., 2017).