Widespread scope for coral adaptation under combined ocean warming and acidification

Abstract

Reef-building coral populations are at serious risk of collapse due to the combined effects of ocean warming and acidification. Nonetheless, many corals show potential to adapt to the changing ocean conditions. Here we examine the broad sense heritability (H²) of coral calcification rates across an ecologically and phylogenetically diverse sampling of eight of the primary reef-building corals across the Indo-Pacific. We show that all eight species exhibit relatively high heritability of calcification rates under combined warming and acidification (0.23-0.56). Furthermore, tolerance to each factor is positively correlated and the two factors do not interact in most of the species, contrary to the idea of trade-offs between temperature and pH sensitivity, and all eight species can co-evolve tolerance to elevated temperature and reduced pH. Using these values together with historical data, we estimate potential increases in thermal tolerance of 1.0-1.7°C over the next 50 years, depending on species. None of these species are probably capable of keeping up with a high global change scenario and climate change mitigation is essential if reefs are to persist. Such estimates are critical for our understanding of how corals may respond to global change, accurately parametrizing modelled responses, and predicting rapid evolution.

Keywords: adaptation; climate change; coral reef; evolution; heritability; ocean acidification.

Figure 1.

Diagram illustrating the experimental design used in this study. Representative photos of each coral are shown in (a) From top-left to bottom-right these are: Montipora capitata, Montipora flabellata, Montipora patula, Porites compressa, Porites evermanni, Porites lobata, Pocillopora acuta and Pocillopora meandrina. Corals were collected from a total of six locations around O‘ahu, Hawai‘i as indicated by the black dots (b) with each species collected from three to five of the locations, depending on local abundance. The corals were then fragmented into a series of clonal nubbins (ramets) with four genotypes (genets) per species each contributing three ramets per treatment, whereas the remaining 18 genets (Montipora flabellata) or 26 genets (other seven species) each contributed one ramet per genet per treatment, yielding a total of 22 genets for Montipora flabellata and 30 genets for the remaining seven species (c) The ramets were randomly allocated among mesocosms, which were themselves randomly divided among treatments, and with no more than one ramet per coral genet in each mesocosm (d) Mesocosms are colour-coded according to treatment: control (blue), ocean acidification (light blue), ocean warming (red) and combined future ocean (purple). Photos courtesy of Keoki Stender.

Figure 2.

Boxplot of treatment effects on coral calcification rate (G) for each species. All eight species experienced reduced calcification under warming. Three of the species (Montipora flabellata, Porites evermanni and Porites lobata) exhibited reduced calcification under acidification, whereas Pocillopora meandrina showed increased calcification, and the other four species did not respond significantly to reduced pH. For most of the species, temperature and pH effects were additive, whereas for Pocillopora meandrina there was a significant Temp × pH interaction such that the resistance of this species to acidification was diminished under elevated temperature. Horizontal black bar is the median, box edges are 75% confidence intervals, box whiskers are 95% confidence intervals, and points show outliers. Non-bolded letters above each box indicate Tukey HSD post hoc test results for pairwise contrasts among treatments; groups sharing a letter within each panel are not significantly different at α = 0.05. n = 22 genotypes (genets) for Montipora flabellata and n = 30 genets for the remaining seven species. Note differences in scale among rows.

Figure 3.

Broad sense heritability (H ² ) for each coral species under combined warming and acidification. Points show best estimates and error bars are 95% confidence intervals. n = 22 genotypes (genets) for Montipora flabellata and n = 30 genets for the remaining seven species.

Figure 4.

Scatterplot of relative pH and temperature tolerances for each coral species. Relative pH tolerance is defined as the change in calcification rate in the ocean acidification treatment relative to the control treatment whereas relative temperature tolerance is defined as the change in calcification rate in the ocean warming treatment relative to the control treatment for each species (a–h) Grey line in each plot is a linear regression of the relationship between pH and temperature tolerance for each species. The plot in the lower right (i) is a visual guide to aid in interpretation of the panels. Correlation coefficients (r) and p-values for the regressions are shown in each panel; significant p-values at α = 0.05 are shown in bold. Five of the species (Montipora capitata, Montipora patula, Porites lobata, Pocillopora acuta and Pocillopora meandrina) show significant positive associations between pH and temperature tolerance, whereas the other three species (Montipora flabellata, Porites compressa and Porites evermanni) exhibit similar, non-significant trends. This analysis tests for possible calcification trade-offs between pH and temperature tolerance. Only Pocillopora meandrina exhibited a significant Temp × pH interaction in the combined future ocean treatment, which is likely to reduce the capacity of this species to adapt to the combined stressors. All eight species are expected to be capable of adapting to ocean warming, ocean acidification and the combination of both factors, though Pocillopora meandrina is likely to have diminished capacity to respond to the combination as compared with each factor individually. Due to mortality of a few coral ramets not all genets could be included in the analysis. n = 22 genets for Montipora flabellata, n = 26 for Pocillopora acuta and Pocillopora meandrina, and n = 30 for the remaining five species.

Figure 5.

Estimated responses to selection for each species over the next 50 years. For Montipora capitata and Pocillopora acuta, values were empirically derived based on observed change in DHW tolerance between 1970 and 2017. For the remaining species, the values were estimated based on the heritability values derived here and assuming a selection coefficient similar to that for Montipora capitata. Horizontal lines show the mean annual DHW accumulation at warming levels of 1.0, 1.4, and 1.8°C, based on NOAA data for the main Hawaiian islands.