Consumers mediate the effects of experimental ocean acidification and warming on primary producers

Abstract

It is well known that ocean acidification can have profound impacts on marine organisms. However, we know little about the direct and indirect effects of ocean acidification and also how these effects interact with other features of environmental change such as warming and declining consumer pressure. In this study, we tested whether the presence of consumers (invertebrate mesograzers) influenced the interactive effects of ocean acidification and warming on benthic microalgae in a seagrass community mesocosm experiment. Net effects of acidification and warming on benthic microalgal biomass and production, as assessed by analysis of variance, were relatively weak regardless of grazer presence. However, partitioning these net effects into direct and indirect effects using structural equation modeling revealed several strong relationships. In the absence of grazers, benthic microalgae were negatively and indirectly affected by sediment-associated microalgal grazers and macroalgal shading, but directly and positively affected by acidification and warming. Combining indirect and direct effects yielded no or weak net effects. In the presence of grazers, almost all direct and indirect climate effects were nonsignificant. Our analyses highlight that (i) indirect effects of climate change may be at least as strong as direct effects, (ii) grazers are crucial in mediating these effects, and (iii) effects of ocean acidification may be apparent only through indirect effects and in combination with other variables (e.g., warming). These findings highlight the importance of experimental designs and statistical analyses that allow us to separate and quantify the direct and indirect effects of multiple climate variables on natural communities.

Keywords: food web; global warming; herbivory; species interaction; top-down.

Fig. 1.

Effects of experimental warming, acidification, and mesograzers on (A) sediment chlorophyll a (proxy for benthic microalgae biomass), (B) primary production by benthic microalgae, (C) total biomass of sediment-associated macrofauna, and (D) total biomass of macroalgae. Data are means +SE; n = 5.

Fig. 2.

Path diagrams showing how experimental warming (Warm), acidification (Acid), and the interaction between warming and acidification (Warm × Acid) affect the macroalgae, sediment-associated fauna, Z. marina, light, and benthic microalgal biomass. Path diagram represents (A) seagrass meadows with mesograzers (G. locusta, L. littorea, and Rissoa sp.) absent and (B) seagrass meadows with mesograzers present. Solid paths (blue positive and red negative effects) are statistically significant (P < 0.05) whereas the dashed lines are not. At each significant path the standardized coefficients are represented and interpreted as follows: If, for example, Warm × Acid goes up by 1 SD, the benthic microalgae biomass goes up by 1.43 SD. Standardized coefficients are therefore used to compare the strength of direct vs. indirect effects. Percentages indicate the variance explained by the model.

Fig. 3.

Path diagrams showing how experimental warming (Warm), acidification (Acid), and the interaction between warming and acidification (Warm x Acid) affect the macroalgae, sediment-associated fauna, Z. marina, light, and benthic microalgal production. Path diagram represents (A) seagrass meadows with mesograzers (G. locusta, L. littorea, and Rissoa sp.) absent and (B) seagrass meadows with mesograzers present. Solid paths (blue positive and red negative effects) are statistically significant (P < 0.05) whereas the dashed lines are not. At each significant path the standardized coefficients are represented and interpreted as follows: If, for example, Warm × Acid goes up by 1 SD, the benthic microalgae primary production goes down by 0.45 SD. Standardized coefficients are therefore used to compare the strength of direct vs. indirect effects. Percentages indicate the variance explained by the model.