Future reef decalcification under a business-as-usual CO2 emission scenario

Increasing atmospheric partial pressure of CO₂ (pCO₂) is a major threat to coral reefs, but some argue that the threat is mitigated by factors such as the variability in the response of coral calcification to acidification, differences in bleaching susceptibility, and the potential for rapid adaptation to anthropogenic warming. However the evidence for these mitigating factors tends to involve experimental studies on corals, as opposed to coral reefs, and rarely includes the influence of multiple variables (e.g., temperature and acidification) within regimes that include diurnal and seasonal variability. Here, we demonstrate that the inclusion of all these factors results in the decalcification of patch-reefs under business-as-usual scenarios and reduced, although positive, calcification under reduced-emission scenarios. Primary productivity was found to remain constant across all scenarios, despite significant bleaching and coral mortality under both future scenarios. Daylight calcification decreased and nocturnal decalcification increased sharply from the preindustrial and control conditions to the future scenarios of low (reduced emissions) and high (business-as-usual) increases in pCO₂. These changes coincided with deeply negative carbonate budgets, a shift toward smaller carbonate sediments, and an increase in the abundance of sediment microbes under the business-as-usual emission scenario. Experimental coral reefs demonstrated highest net calcification rates and lowest rates of coral mortality under preindustrial conditions, suggesting that reef processes may not have been able to keep pace with the relatively minor environmental changes that have occurred during the last century. Taken together, our results have serious implications for the future of coral reefs under business-as-usual environmental changes projected for the coming decades and century.Tropical coral reef ecosystems face significant challenges from anthropogenic changes in ocean temperature and chemistry (1). Short periods of anomalously high sea temperatures have triggered mass coral bleaching and mortality events since the early 1980s (2, 3), and projected pH and carbonate ion concentrations reduce the calcification rate of many organisms such as reef-building corals and crustose coralline algae (reviewed in ref. 4). Generally, the projected impacts associated with future increases in sea temperature have been examined independently of those associated with ocean acidification (2, 5–8). When multiple drivers have been considered, extrapolation of the results to the future outlook of coral reefs has been complicated by a lack of replication, the use of artificial light, and/or experimental designs that exclude the potentially important influence of natural variation in ocean temperature and chemistry over diel and seasonal cycles (9–11). Furthermore, most studies have focused on corals or calcareous algae in isolation rather than on broader communities that may better represent the responses of coral reefs (9–11). Excluding the interaction of changing temperature and ocean chemistry, natural variability, and the wider set of organisms and processes places important limitations on our ability to understand the future and ascertain whether, for coral reefs, there is any real difference between action and no action regarding CO₂ emissions. This issue is fundamentally important given the time lag between reducing CO₂ emissions and establishing atmospheric stability, but has not been addressed adequately via studies that seek mechanistic understandings for the individual effects of temperature and acidification on specific organisms, because the sum of the parts may not equal the whole.Some argue that the potential and imminent threat to coral reefs posed by anthropogenic CO₂ emissions is mitigated by potential rapid evolutionary adaptation by key reef organisms such as corals (12). Within this argument, greater inherent environmental variability is seen as a facilitator of adaptation (13), and the transition within some corals to thermally tolerant symbionts is presented as a current coral plasticity that is likely to enhance adaptation toward warmer water (12). The latter suggestion is debatable because the enhancement in host performance is not typically recorded in terms of a property that belongs uniquely to the host (e.g., coral survival, growth, or reproduction) but rather as properties (bleaching tolerance, sustained maximum quantum yields of photosystem II) that may be more attributable to the symbiont than to the host (14). That is, it is not always clear that the statement “having thermally tolerant symbionts leads to thermally tolerant hosts” is anything more than a tautology. Especially given observations in the current literature that corals harboring thermally tolerant symbionts experience reduced growth (15, 16), that heterotrophic feeding can sustain some coral species postbleaching (17), and finally that while food may be relatively unavailable in the oceans that surround reefs, this is not typically the case on a reef (reviewed in ref. 18). Evolution will occur over multiple generations. Presently, however, we lack the experimental evidence to support scientifically the contention that organism evolution over the next decades will protect features such as the maintenance of a positive carbonate balance that are essential to reef viability and the functional utility of reefs to mankind (1). However, the ocean environment has changed significantly over the last 100 y in terms of both ocean temperature and acidification (19, 20), suggesting that reefs in the Southern Great Barrier Reef (GBR), where seasonal environmental variability is great, should provide ample opportunity to evaluate experimentally the degree to which key ecosystem features are retained over decadal time frames.In the present study, we simulated past and future ocean temperature and chemistry on replicated patches of coral reef reconstructed from a broad range of organisms collected from the growth zone of a coral reef (Harry’s Bommie, Heron Island, GBR, 151.9357°E, 23.4675°S) (Fig. S1). The experiment was designed to answer two major questions. The first was whether processes such as the maintenance of maximum net reef calcification rates, measured independently of episodic events such as cyclones, are optimal under the preindustrial (PRE) or present-day (control) scenarios. The second was whether the response of coral reefs differs between action scenarios that result in business-as-usual unabated rates of CO₂ emission (A1FI) as compared to reduced rates of CO₂ emission (B1) through 2050. Here, the Special Report on Emission Scenarios (SRES) A1FI is equivalent to a Representation Concentration Pathway (RCP) 8.5; and, SRES B1 is equivalent to RCP4.5 (21).

Table 1.

November composition of the reassembled patch-reefs

Type	Principal components	% cover
Hard coral	Acropora formosa; Seriatopora hystrix*; Stylophora pistillata; Porites cylindrical; Plating Montipora sp.; Goniastrea aspera; Lobophyllia sp.*; Fungia sp.	35 ± 1
Macroalgae	Crustose calcareous algae; red, green, brown filamentous algae; Halimeda sp.; Lobophora sp.; Chlorodesmis fastigiata; Hypnea sp.	15 ± 3
Other invertebrates	Zoanthids; Xenia sp.; sponges (Cliona orientalis); sea cucumbers (Holothuria atra); snails (herbivorous); xanthid crabs	2 ± 0
Vertebrates	Three lawnmower blennies (Salarias fasciatus)
Sediments	Skeletons of corals, crustose calcareous algae, foraminifers, mollusks, and Halimeda (39)	48 ± 3

Open in a separate windowAll organisms were collected from a depth of ca. 5 m at Harry’s Bommie, Heron Island Reef, GBR, Australia.^*Corals excluded from buoyant weight assessment.To incorporate natural variability at day and seasonal scales, a computer-control system tracked water temperature and ocean partial pressure of CO₂ (pCO₂) look-up tables established from two or three hourly measurements made at our reference site (Harry’s Bommie, www.pmel.noaa.gov/co2/story/Heron+Island) during 2010 and 2011 (Fig. S1). Then treatment conditions (with similar natural levels of diurnal and seasonal variability) were established by applying past and projected future anomalies as offsets to these look-up table values (Fig. 1). The precision and accuracy of the control system is evident from the comparison of the data from 2010 and 2011 (black trace in Fig. 1) with the condition replicated in the control (today) mesocosms (blue symbols). PRE conditions were established by reducing the seawater (SW) pCO₂ by 104 ± 11 µatm and temperature by 1 °C. Future conditions were established using anomalies appropriate to the lower (B1: +174 ± 9 µatm, +2 °C) and upper (A1FI: +572 ± 11 µatm, +4 °C) ends of respective scenarios. Temperature profiles for representative mesocosms are shown in Fig. 1, along with the average pH conditions (± SE) measured at 30-min intervals. Experimental treatments were preceded by 2.5 mo in which the coral reef communities were acclimatized to treatment conditions by slowly increasing the relative proportion of treatment water to inner reef flat water control (field) rates of changes over acclimatization period were 0.04 °C d⁻¹ and 6 μatm·pCO₂·d⁻¹; A1FI rates were 0.09 °C·d⁻¹ and 14 μatm·pCO₂·d⁻¹]. Full treatments were applied over the austral summer from early November 2011 to early February 2012 under light conditions appropriate to the reference site.Open in a separate windowFig. 1.Treatment conditions established over the experimental period: daily temperature profiles and average treatment pH obtained through the course of the experiment. PRE, pre-industrial treatment; C, control treatment set to mimic conditions at the reference site (Harry’s Bommie, GBR, Australia, indicated by the solid black line) measured by the Commonwealth Scientific and Industrial Research Organization between November 2010 and February 2011; B1, SRES B1/RCP4.5, reduced CO₂ emission scenario; A1FI, SRES A1FI/RCP 8.5 business-as-usual emissions scenario. The upper dashed line represents the maximum monthly mean (MMM) + 1 °C, established for Heron Island using 50-km pixel satellite data (http://coralreefwatch.noaa.gov). The lower dashed line represents MMM+1 specific to the reference site established by relating satellite nighttime temperatures to same-day average night temperatures logged at Harry’s Bommie. Triangles represent sampling days for community O₂ flux and calcification measurements. Average pCO₂s across sampling days were PRE = 301 ± 11 µatm, C = 405 ± 25 µatm, B1 = 611 ± 17 µatm, and A1FI = 1,009 ± 8 µatm (Table S1).