Shifts in coral reef biogeochemistry and resulting acidification linked to offshore productivity

Abstract

Oceanic uptake of anthropogenic carbon dioxide (CO 2 ) has acidified open-ocean surface waters by 0.1 pH units since preindustrial times. Despite unequivocal evidence of ocean acidification (OA) via open-ocean measurements for the past several decades, it has yet to be documented in near-shore and coral reef environments. A lack of long-term measurements from these environments restricts our understanding of the natural variability and controls of seawater CO 2 -carbonate chemistry and biogeochemistry, which is essential to make accurate predictions on the effects of future OA on coral reefs. Here, in a 5-y study of the Bermuda coral reef, we show evidence that variations in reef biogeochemical processes drive interannual changes in seawater pH and Ω aragonite that are partly controlled by offshore processes. Rapid acidification events driven by shifts toward increasing net calcification and net heterotrophy were observed during the summers of 2010 and 2011, with the frequency and extent of such events corresponding to increased offshore productivity. These events also coincided with a negative winter North Atlantic Oscillation (NAO) index, which historically has been associated with extensive offshore mixing and greater primary productivity at the Bermuda Atlantic Time-series Study (BATS) site. Our results reveal that coral reefs undergo natural interannual events of rapid acidification due to shifts in reef biogeochemical processes that may be linked to offshore productivity and ultimately controlled by larger-scale climatic and oceanographic processes.O cean acidification (OA) resulting from rising atmospheric CO 2 (1-3) and the associated declines in surface seawater pH and saturation state with respect to CaCO 3 minerals such as aragonite (Ω aragonite = [Ca 2+ ][CO 3 2-]/K sp *, where K sp * is the ion solubility product) have raised concerns on the potential consequences to marine calcifiers and ecosystems (4, 5). Reductions in Ω aragonite have been found to negatively affect organismal CaCO 3 production (6) while accelerating bioerosion and CaCO 3 dissolution (7,8). Hence, it has been hypothesized that coral reefs could shift from a condition of net calcification to net dissolution, with some model estimates predicting a transition for worldwide reefs at atmospheric CO 2 levels of 560 ppm (5, 7).Despite growing concern about the vulnerability of coral reefs, a lack of long-term measurements has prevented direct observation of anthropogenic OA owing to increasing atmospheric CO 2 in these environments. Additionally, short-term observations have revealed large variability and modification of reef seawater CO 2 -carbonate chemistry on diurnal and seasonal timescales as a result of coral reef biogeochemical processes such as photosynthesis, respiration, calcification, and CaCO 3 dissolution (9, 10). It has been hypothesized that these natural processes, quantified as net ecosystem production (NEP = gross primary production − autotrophic and heterotrophic respiration) and net ecosystem calcification (NEC = gro...

Twenty Years of Marine Carbon Cycle Observations at Devils Hole Bermuda Provide Insights into Seasonal Hypoxia, Coral Reef Calcification, and Ocean Acidification

“…The Harrington Sound data indicates that the mean NEP value for the Bermuda reef is +0.02 ± 0.09 g C m −2 d −1 , and thus, the trophic status may not be in balance. Although the mean NEP is close to zero, positive values suggest that the Bermuda reef is slightly net heterotrophic, with a net delivery of offshore sourced organic matter that is respired onshore throughout the reef system (Yeakel et al, 2015). As with anomalies of seawater CO 2 -carbonate chemistry discussed in Section Long-term Trends (1996Trends ( -2016 of Seawater CO 2 -carbonate Chemistry, anomalies of NEC and NEP show significant changes over the past two decades (Figure 8).…”

“…As described earlier (Section Long-term Trend Analysis), comparison of contemporaneous onshore and offshore DIC and TA differences provides estimates of net community calcification (NEC) and net ecosystem production (NEP). This approach has been used before for the Bermuda reef system (e.g., Bates, 2002;Bates et al, 2010;Andersson et al, 2014;Yeakel et al, 2015;Courtney et al, 2016) and many other reefs (e.g., Chisholm and Gattuso, 1991;Suzuki et al, 1995;Gattuso et al, 1998;Suzuki and Kawahata, 2003;Anthony et al, 2011;Kleypas et al, 2011;Albright et al, 2013;Inoue et al, 2013;Lantz et al, 2014;Koweek et al, 2015). Only a few of these studies extend to 5 years, and thus, the Harrington Sound data provides the first long-term assessment of reef metabolism and reef NEC and NEP.…”

“…In a recent study, Yeakel et al (2015) proposed that the Bermuda reef exhibited increased calcification and increased respiration over the past 5 years due to increased coral nutrition. The Harrington Sound data can be used to test this hypothesis over a longer time period and the following questions: (4) Does the Bermuda reef ecosystem exhibit increased calcification and respiration over the past two decades offsetting ocean acidification?…”

“…They also highlighted the strong seasonal coupling and feedback between rates of coral calcification (i.e., coral skeletal growth and water assessment of net ecosystem calcification, NEC), other ecological components of the reef system (i.e., macroalgae) and reef chemistry. However, in a recent paper, Yeakel et al (2015) showed that coral calcification for the Bermuda reef has increased over the past 5 years, despite long-term declines in [CO 2− 3 ] and aragonite . They proposed that this recent change was due to increased coral nutrition in response to offshore, regional changes in North Atlantic Ocean conditions associated with variability of the North Atlantic Oscillation (NAO).…”

Spatiotemporal Assessment of CO2–Carbonic Acid System Dynamics in a Pristine Coral Reef Ecosystem, French Frigate Shoals, Northwestern Hawaiian Islands

“…At night, respiration produces CO 2 , decreases X ar , and calcification often slows, with some benthic communities experiencing net dissolution Halley 2003, 2006;Andersson and Gledhill 2013;Eyre et al 2014). The impact of these processes on the variability in the parameters of the CO 2 -carbonic acid system depends on a number of environmental factors including geographic location, seasonal and daily trends in temperature and light availability, hydrodynamic forcing and nutrients (Suzuki et al 1995;Andersson et al 2005;Bates et al 2010;Drupp et al 2011Drupp et al , 2013Falter et al 2012;Zhang et al 2012;Yeakel et al 2015). Furthermore, community composition upstream of a particular reef environment can alter seawater chemistry and complicate the interpretation of research results in downstream habitats Kleypas et al 2011).…”