Humans release billions of tons of CO2 into the atmosphere each year [Keeling et al., 2005; Solomon et al., 2007], to date, about 30% of this CO2 has been absorbed by the ocean [Canadell et al., 2007; Le Quéré et al., 2009; Sabine et al., 2011]. The resulting decline in seawater pH, Ωar, and [CO32−], a process known as ocean acidification [Raven et al., 2005], poses a significant threat to many marine ecosystems worldwide. Coral reefs are considered particularly vulnerable to ocean acidification because reef-building corals and calcifying algae use CO32− to produce calcium carbonate (CaCO3) skeletons that ultimately build the reef [Kleypas et al., 1999]. Much of our current understanding of the impacts of ocean acidification on coral reef futures is shaped by results of controlled CO2-manipulation experiments, and information from coral reef communities inhabiting naturally low pH environments suggest potential ecosystem-level consequences of prolonged exposure [Manzello et al., 2008; Crook et al., 2011; Fabricius et al., 2011]. While none of these naturally more acidic coral reef environments are perfect analogs for anthropogenic ocean acidification [Field et al., 2011], consistent patterns have emerged from these studies [Manzello et al., 2008; Crook et al., 2011; Fabricius et al., 2011]. Typically, hard coral diversity is low; in some instances, the area of reef floor covered with live corals is reduced; and in eastern Pacific upwelling zones, elevated rates of bioerosion and low levels of abiogenic cementation result in reef structures that are highly porous and structurally fragile [Manzello et al., 2008; Crook et al., 2011; Fabricius et al., 2011]. These observations, combined with the fact that today's most well-developed and diverse tropical reefs occur within a narrow geographic range characterized by open ocean [CO32−] > 200 µmol kg−1 and Ωar > 3.3 [Kleypas et al., 1999; Hoegh-Guldberg et al., 2007], imply that coral communities may have limited capacity to adapt to levels of acidification projected for the 21st century [Hoegh-Guldberg, 2012] and that healthy coral reefs could cease to exist within this time frame [Hoegh-Guldberg et al., 2007; Hoegh-Guldberg, 2011]. Here we report the existence of healthy, diverse coral reef communities living under levels of natural acidification approaching those projected for the tropical western Pacific open ocean by 2100. Understanding the combinations of genetic and/or environmental factors that enable coral communities to function under relatively extreme conditions of pH and Ωar will inform projections of reef futures under climate change and ocean acidification.
Surface water (0–3 m) samples were collected at nine stations across the Palauan reef system (7.27 to 7.58°N; 134.39 to 134.56°E) (Figure 1) during both the wet (19–24 September 2011) and dry (25 March to 07 April 2012) seasons, from sunrise to sunset, and throughout the tidal cycle. As shown by previous studies [Gattuso et al., 1993; Silverman et al., 2007a, 2007b; Shamberger et al., 2011], diurnal extremes in reef carbonate chemistry occur 0–2 h after sunrise and before sunset. Thus, these samples provide insight into both the seasonal and tidal range of carbonate chemistry, as well as the diurnal range at our sampling stations. The carbonate chemistry of Palauan reef seawater is significantly different from open ocean source water (Figures 1 and 2). The full seawater CO2 system calculated from total alkalinity (TA), dissolved inorganic carbon (DIC), salinity, and in situ temperature measurements shows that surface water pH, [CO32−], and Ωar decrease with distance from offshore waters (Figures 1, 2, and supporting information Figure S1). Just inshore of the barrier reefs, average Ωar values are 0.2 to 0.3 lower and pH values are 0.02 to 0.03 lower than they are offshore, declining further as water moves across the back reef, lagoon, and into the meandering bays and inlets that characterize the Rock Islands (sites 7–9) (Figures 1 and 2). These Rock Island coral communities inhabit seawater with average Ωar values of 2.7 or less, and as low as 1.9 (Figure 2). Among the nine stations occupied along our offshore-inshore transect, average Ωar is 3.26 ± 0.16. This is at the previously estimated geographic Ωar limit for coral reef accretion [Kleypas et al., 1999; Hoegh-Guldberg et al., 2007].
The relatively high levels of acidification of Palauan reef seawater are produced through a combination of natural biological processes and circulation patterns within the reef system. The specific processes and their relative contribution, particularly to the lowering of Ωar values, can be determined by comparing offshore source water temperature, salinity, TA, and DIC data to those measured at our reef sites (supporting information). Water temperatures inside the reef are within 1.3°C of offshore values, a difference that is too small to account for the large difference in Ωar (Table S1). Rather, calcification, respiration, and dilution (mixing of offshore source water with low salinity rainwater and island runoff) appear to be the main factors driving the change in seawater chemistry. Dilution of reef water with freshwater can lower seawater Ωar because freshwater in this region has low [CO32−]. Using our offshore salinity, TA, and DIC data; a previously established relationship between TA and salinity for the tropical Pacific open ocean [Lee et al., 2006]; and the in situ reef seawater salinity, we estimate that dilution accounts for 1–17% of the difference in Ωar between offshore and reef waters (Figure S2, supporting information). Calcification further lowers seawater Ωar by consuming CO32− and adding CO2 to the system, while dissolution raises Ωar by producing CO32− and consuming CO2 (Figure S1). Because calcification (respiration) decreases (increases) TA and DIC in a 2:1 ratio, we can use our data to estimate the net contribution of calcification and dissolution to the lowering of Ωar as seawater moves across the barrier reefs and into the bays (Figure S3). Our calculations reveal that 68–99% of the difference in Ωar between offshore source water and reef water is driven by net calcification by reef organisms (Figures 3 and S2). Respiration lowers Ωar by producing CO2 which increases seawater acidity and DIC without altering TA, whereas photosynthesis raises Ωar by consuming CO2. At our barrier reef and exposed sites (sites 1–6), the dilution corrected DIC-TA data fall within the error of the modeled calcification relationship (Figure 3) indicating an insignificant influence of photosynthesis and respiration on mean DIC and Ωar. Photosynthesis and respiration rates may be high on the barrier reef and exposed sites but are approximately balanced and so do not significantly affect Ωar. However, in the three sheltered Rock Island bay sites (sites 7–9), where Ωar levels are extremely low (Figures 1 and 2), the corrected DIC-TA data fall to the right of the calcification line indicating an additional input of DIC (Figure 3). This input of DIC may reflect respiration occurring within the bays (by the benthic community and microbial decomposition of organic matter), or discharge of groundwater with elevated CO2 due to terrestrial respiration. Our calculations reveal that in situ respiration and/or groundwater discharge contributes between 17 and 30% of the difference in Ωar between offshore source water and reef water at the Rock Island sites (Figure S2). Residence time of seawater in the Rock Island bays is likely to be much longer than at the well-flushed exposed sites, enabling calcification and respiration to drive Ωar to very low levels.
Average annual calcification rates of massive Porites corals from 2007 to 2009 (supporting information), calculated from 3-D Computerized Tomography scan images of skeletal cores (method described in Crook et al. ), are comparable on reefs with high (site 4: 0.89 ± 0.02 g cm−3 yr−1) and low (site 9: 0.91 ± 0.02 g cm−3 yr−1) Ωar, suggesting that calcification by at least one dominant reef-building species is maintained under relatively acidic conditions. This result is contrary to predictions based on laboratory manipulation experiments but consistent with findings at CO2 seeps in Papua New Guinea [Fabricius et al., 2011]. Three additional indices were thus examined to assess the health of the coral communities across Palau's natural acidification gradient: percentage of live coral cover, coral diversity (Shannon diversity index), and coral taxonomic richness (number of coral genera). This analysis reveals patterns different from those observed in other naturally more acidic reef systems. In the Rock Island bay sites (Ωar ≤ 2.7), coral cover is maintained at relatively high levels: 32 to 63%, significantly higher than the western Pacific average of 25% (Figure 4 and supporting information Figure S4) [Bruno and Selig, 2007]. Hard coral diversity is also high, averaging 1.7, compared with 1.1 to 1.6 on the barrier reef and more exposed sites within Palau (Figure 4). Although genus richness is a somewhat crude measure of coral community health, it is widely measured and useful for comparing coral reef systems where diversity data have not been reported. In Palau's naturally low Ωar sites, hard coral richness averages 12 genera transect−1 (Figure 4), higher than on the barrier reef and more exposed sites (8 to 10 genera transect−1) and higher than on neighboring Micronesian reefs (4 to 10 genera transect−1). At comparable Ωar, the naturally more acidic Papua New Guinea CO2 seeps support 33% live coral cover and an average of 2.6 hard coral genera transect−1 [Fabricius et al., 2011]. Likewise, although biogeographic factors contribute to the generally low numbers of genera on eastern Pacific and Caribbean reefs, within these systems, coral richness declines with increasing levels of acidity. For example, reefs of the Galapagos and Gulf of Panama, where daytime Ωar averages 2.7 and 2.9, respectively [Manzello, 2010], support six hard coral genera although coral cover can be high in monospecific stands [Cortes, 1997]. Similarly, reefs of the Yucatan Peninsula, where groundwater discharge causes natural acidification, support just two genera of hard coral where Ωar values are less than 2.5, compared to seven genera on nearby unaffected reefs [Crook et al., 2011]. Thus, among the handful of naturally low pH, low Ωar coral reef sites identified to date, Palau is currently unique in maintaining extraordinarily dense and diverse coral communities.
None of the naturally acidified reefs that exist today, including Palau, provide an exact representation of the chemical conditions and adaptive pressures coral communities will face as CO2 levels continue to rise over the course of this century. In the eastern Pacific, for example, low Ωar is coupled with large seasonal swings in temperature, significantly elevated nutrient concentrations, and a community structure heavily influenced by biogeography [Glynn and Colgan, 1992; Manzello et al., 2008; Manzello, 2010]. Where discharge of high CO2 groundwater causes natural acidification, there are concurrent increases in TA, DIC, and nutrient concentrations [Crook et al., 2011]. At volcanic CO2 seeps [Fabricius et al., 2011], the scale of connectivity is generally larger than the acidified area so that larvae of many species are continuously recruited from external, unaffected source populations, limiting selective pressure for adaptation [e.g., Cigliano et al., 2010]. On Palau, natural acidification is caused by a combination of hydrographic processes; calcification by barrier, patch, and bay reefs; CO2 emitted through respiration; and influences from the land, not solely by absorption of excess CO2. Despite the fact that none of these sites provide a perfect analog for global ocean acidification due to anthropogenic CO2, information from each of them provides important clues about the potential responses of coral reef communities to future levels of acidification. Coral communities that occupy Palau's relatively acidic reef areas developed over thousands of years, and unlike the communities in the CO2 vent sites and areas of high CO2 groundwater discharge, experience low but relatively stable pH and Ωar over tidal and seasonal cycles (Table S2). By comparing conditions and community responses among the full spectrum of naturally acidified coral reef sites, we will gain insight into the factors that enable healthy coral communities to persist under relatively acidic conditions.