Cascading effects of ocean acidification in a rocky subtidal community

Abstract

Temperate marine rocky habitats may be alternatively characterized by well vegetated macroalgal assemblages or barren grounds, as a consequence of direct and indirect human impacts (e.g. overfishing) and grazing pressure by herbivorous organisms. In future scenarios of ocean acidification, calcifying organisms are expected to be less competitive: among these two key elements of the rocky subtidal food web, coralline algae and sea urchins. In order to highlight how the effects of increased pCO2 on individual calcifying species will be exacerbated by interactions with other trophic levels, we performed an experiment simultaneously testing ocean acidification effects on primary producers (calcifying and non-calcifying algae) and their grazers (sea urchins). Artificial communities, composed by juveniles of the sea urchin Paracentrotus lividus and calcifying (Corallina elongata) and non-calcifying (Cystoseira amentacea var stricta, Dictyota dichotoma) macroalgae, were subjected to pCO2 levels of 390, 550, 750 and 1000 µatm in the laboratory. Our study highlighted a direct pCO2 effect on coralline algae and on sea urchin defense from predation (test robustness). There was no direct effect on the non-calcifying macroalgae. More interestingly, we highlighted diet-mediated effects on test robustness and on the Aristotle's lantern size. In a future scenario of ocean acidification a decrease of sea urchins' density is expected, due to lower defense from predation, as a direct consequence of pH decrease, and to a reduced availability of calcifying macroalgae, important component of urchins' diet. The effects of ocean acidification may therefore be contrasting on well vegetated macroalgal assemblages and barren grounds: in the absence of other human impacts, a decrease of biodiversity can be predicted in vegetated macroalgal assemblages, whereas a lower density of sea urchin could help the recovery of shallow subtidal rocky areas affected by overfishing from barren grounds to assemblages dominated by fleshy macroalgae.

Figure 1. Scheme of the experimental set-up.

The top boxes represent the four reservoirs in which the pCO₂ was regulated. Squares represent the 16 experimental aquaria, divided into sub-sections as described in the Methods, to yield a total of 48 independent experimental units. The numbers of samples of each macroalgal item and of P. lividus are reported in brackets.

Figure 2. Box plot on percent weight loss as a function of pCO₂ (µatm), for each macroalga: (a) Cystoseira amentacea, (b) Dictyota dichotoma and (c) Corallina elongata.

Medians are highlighted in bold; bars represent the 25% and 75% quartiles; whiskers represent the lowest and highest data points.

Figure 3. Box plot on the jaw/test ratio as a function of pCO₂ and algal diet: sea urchins fed with (a) Corallina elongata, (b) Cystoseira amentacea and (c) Dictyota dichotoma.

Medians are highlighted in bold; bars represent the 25% and 75% quartiles; whiskers represent the lowest and highest data points.

Figure 4. Box plot on test robustness, expressed as the weight (g) needed to crush the urchin test normalized by the test diameter, as a function of pCO₂ and algal diet: sea urchins fed with (a) Corallina elongata, (b) Cystoseira amentacea and (c) Dictyota dichotoma.

Medians are highlighted in bold; bars represent the 25% and 75% quartiles; whiskers represent the lowest and highest data points.

Figure 5. SEM images (8500x) of portions of the Aristotle's lantern of urchins fed calcifying (C. elongata; a, b) and non-calcifying (C. amentacea; c, d) macroalgae and maintained at pCO₂ levels of 390 (a, c) and 1000 µatm (b, d) for 1 month.