Corals have declined and seaweeds have increased in abundance on reefs world-wide1,2,3,7,9,10. The relative roles of seaweeds damaging corals directly versus simply colonizing coral skeletons following their death from other causes is unclear and variable6, but numerous experimental manipulations indicate that an increase in macroalgae can directly suppress coral growth, survivorship, and recruitment12,42. As corals decline and macroalgae increase, coral-macroalgal contact increases in frequency43, making it critical to understand the mechanisms determining the outcome of coral-macroalgal competition6,25,26,34,36,38.

All three macroalgae we investigated induced considerable coral tissue loss and two were allelopathic to Acropora intermedia under some conditions, but C. cervicornis became allelopathic only under conditions of OA (Fig. 3, Table 2). This increase in allelopathic potency was modest (about a 5% greater suppression of PSII), but occurred after only 24 h of exposure, using only surface extractions, and would be expected to increase in effect over longer durations. A strengthening of macroalgal competition against reef-building corals under enhanced OA was documented previously for a single macroalgal species (Lobophora cf. papenfussii), but the mechanism was unknown and it was unclear if the cause was enhanced algal allelopathy, altered role of DOC, enhanced coral susceptibility, or a combination of processes15. Here we document for the first time that enhanced allelopathy with increasing OA can be a mechanism by which some macroalgae cause higher levels of coral damage under elevated concentrations of CO 2 . Investigations have documented macroalgal allelopathy against corals in about 75% of the 40 + coral-macroalgal combinations assayed to date22,24,38,44,45, and elevated effects of macroalgae on corals have been seen for two of the four contrasts tested under conditions of OA [i.e. C. cervicornis (Fig. 3), and L.cf. papenfussii15). Thus, macroalgal allelopathy against corals is common; if enhanced allelopathic potency under OA occurs in Canistrocarpus (=Dictyota), and likely in Lobophora15, which are widespread and abundant globally3,46,47,48,49,50, corals will experience greater stress from macroalgal competition as OA accelerates.

Surface extracts from the brown macroalga C. cervicornis grown under CO 2 enriched conditions in flow through tanks caused greater damage to in-situ corals than extracts from C. cervicornis grown under ambient CO 2 in equivalent flow through tanks. Because the extract experiment was conducted using in situ corals that had not been exposed to elevated CO 2 , CO 2 effects on the coral can be ruled out. The stronger allelopathy noted in Fig. 3 was due to C. cervicornis becoming more allelopathic rather than the coral becoming more susceptible. The magnitude of the stress caused by the algal extracts in our experimental coral (quantified as a decline in fluorescence levels, EQY, Fig. 3) is smaller than that observed in corals in other coral-algal competition experiments22,25,38. It is likely that different coral species used in these studies have different susceptibilities to algal contact [(e.g. A. prolifera was more resistant to algal allelopathy than A. millepora using same exposure times in pilot studies conducted by the authors GDP, MEH (unpubl. data)], or that the use of different methodologies and exposure times to algal interactions causes variable damage to the corals (e.g. exposure times > 24 hrs would have caused higher coral damage). Importantly, however, coral fluorescence levels were significantly lower when exposed to extracts from C. cervicornis grown under high CO 2 levels, compared to extracts from algae grown under ambient CO 2 , indicating a reduction in the photosynthetic efficiency of the coral symbionts due to lipid-soluble surface extracts alone.

Increased atmospheric CO 2 generally enhances production of secondary metabolites in terrestrial plants29,51. Effects of elevated CO 2 on secondary metabolites in marine plants appear variable. For example, concentrations of polyphenolics decline while concentrations of dimethylsulfoniopropionate (DMSP) appear to increase with elevated CO 2 31,32,52. In these examples, both phenolics and DMSP are more polar (i.e. more water soluble) secondary compounds that can mediate trophic interactions. In our experiment, we extracted lipid-soluble constituents from the surface of macroalgae because surface associated lipids have been identified as the active components in contact competitive interactions with reef corals, and have been shown to cause bleaching, suppression of photosynthesis, and sometimes mortality of corals22,38,44. The allelopathic compounds identified earlier38,44 are hydro-phobic terpenes associated with macroalgal surfaces. Production of some terpenes increases under elevated CO 2 in some terrestrial plants due to higher availability of carbon for plant metabolism53,54. Elevation of CO 2 might have enhanced production of allelopathic lipids in C. cervicornis, but not in the other two macroalgae we investigated (in line with33) (Fig. 3). Because Ch. fastigiata and C. cervicornis both make bioactive terpenes37,38,39, the response appears to vary by species and not simply by the class of compound involved. Enhanced concentrations of allelopathic compounds could have also occurred due to reduced macroalgal growth (as suggested for terrestrial plants53), or changes in other processes not considered in this study. However, reduced macroalgal growth is unlikely as parallel experiments showed the photosynthetic efficiency of our experimental Canistrocarpus did not change with CO 2 (One-Way ANOVA, n = 12, F = 0.69, p = 0.55) (see Supplementary Fig. S1), and our own previous work on a closely related Dictyotaceae macroalga (Lobophora)15 and that of others on Dictyota has demonstrated increased growth under OA conditions17,18. The mechanisms by which elevated CO 2 modifies the potency of Canistrocarpus allelopathy, or the chemical compounds involved in these interactions require additional investigation.

In our outdoor mesocosm experiment, the rates of tissue loss for corals in contact with A. glomerata and Ch. fastigiata also increased under OA conditions, but surface extracts from these species grown under elevated CO 2 did not show enhanced allelopathic activity on corals in situ. Thus, other competitive mechanisms or some processes affecting coral physiology may be driving interactions among these species. Corals exposed to OA but free of macroalgae experienced some tissue loss, suggesting that elevated CO 2 alone is a physiological stressor19, and this stress may have made the corals in our experimental tanks more susceptible to algal effects (including allelopathic effects) and space competition than the in situ corals we used for testing allelopathic potency (Fig. 3)55,56. In addition to producing allelopathic lipids, macroalgae may also stress corals indirectly by releasing dissolved organic carbon (DOC), which may alter microbial community composition and the balance between beneficial versus pathogenic microbes on coral surfaces and lead to coral death25,34,47. Little is known about the effects of elevated CO 2 on DOC production by macroalgae, but it is possible that macroalgae under conditions of OA may uptake excess CO 2 and increase release of DOC, as suggested for planktonic microalgae57. Increased release of DOC could have contributed to coral tissue loss in our experimental tank experiment (Figs 1 and 2), but could not explain the allelopathy seen in our field assays using gel-strips (Fig. 3) because these contained the non-polar, not the polar, extracts from macroalgal surfaces. A combination of enhanced coral sensitivity to macroalgal allelochemicals, shifts in microbial communities, and DOC release may have acted in concert to compromise coral health in the presence of A. glomerata and Ch. fastigiata (and possibly C. cervicornis) under elevated CO 2 . Our results show that although all experimental macroalgae caused damage to the corals when exposed to elevated CO 2 levels, there is variability in the mechanisms by which algae stress and kill corals, suggesting that the relative importance of each mechanism varies under OA. Allelopathy in C. cervicornis, and possibly an altered role of DOC in A. glomerata and Ch. fastigiata, in addition to direct impacts on coral holobiont physiology and coral microbiomes may play important roles in driving coral-macroalgal interactions as concentrations of CO 2 increase in future oceans.

Our study has implications for understanding the impacts of OA on the dynamics of coral-macroalgal interactions, which may cascade to affect coral-algal phase shifts. First, we demonstrate that common macroalgae are allelopathic to corals and that this allelopathy is strengthened for one of the three macroalgae we investigated under elevated CO 2 . This suggests that the competitive advantage of some macroalgae over corals may increase and further accelerate phase shifts as OA continues. This may be exacerbated by enhanced macroalgal growth and cover under projected near-future CO 2 15,16,17,18,20,58. Secondly, our data demonstrate variance in competitive mechanisms and intensity between coral and macroalgae under elevated CO 2 levels. For example, the brown alga C. cervicornis and the green alga Ch. fastigiata both damage corals faster (Fig. 2) than the red alga A. glomerata. C. cervicornis and Ch. fastigiata both produce potent allelochemicals22,38,43. A. glomerata is not known to produce strong, bioactive compounds that damage corals (although it may be allelopathic against bacteria59), and it affects corals more slowly. This variability implies that coral reefs dominated by Dictyotaceae algae like C. cervicornis and Lobophora papenfussii15, may be more susceptible to damage than reefs dominated by A. glomerata as CO 2 concentrations increase. The macroalga Ch. fastigiata is common but rarely abundant on reefs43 and may be a lesser concern under future OA scenarios.