Climate change could drive marine food web collapse through altered trophic flows and cyanobacterial proliferation

Abstract

Global warming and ocean acidification are forecast to exert significant impacts on marine ecosystems worldwide. However, most of these projections are based on ecological proxies or experiments on single species or simplified food webs. How energy fluxes are likely to change in marine food webs in response to future climates remains unclear, hampering forecasts of ecosystem functioning. Using a sophisticated mesocosm experiment, we model energy flows through a species-rich multilevel food web, with live habitats, natural abiotic variability, and the potential for intra- and intergenerational adaptation. We show experimentally that the combined stress of acidification and warming reduced energy flows from the first trophic level (primary producers and detritus) to the second (herbivores), and from the second to the third trophic level (carnivores). Warming in isolation also reduced the energy flow from herbivores to carnivores, the efficiency of energy transfer from primary producers and detritus to herbivores and detritivores, and the living biomass of detritivores, herbivores, and carnivores. Whilst warming and acidification jointly boosted primary producer biomass through an expansion of cyanobacteria, this biomass was converted to detritus rather than to biomass at higher trophic levels—i.e., production was constrained to the base of the food web. In contrast, ocean acidification affected the food web positively by enhancing trophic flow from detritus and primary producers to herbivores, and by increasing the biomass of carnivores. Our results show how future climate change can potentially weaken marine food webs through reduced energy flow to higher trophic levels and a shift towards a more detritus-based system, leading to food web simplification and altered producer–consumer dynamics, both of which have important implications for the structuring of benthic communities. Healthy marine ecosystems are crucial for people’s livelihoods and food production. Global climate stressors, such as warming and ocean acidification, can drastically impact the structure and function of marine food webs, diminishing the production of goods and services. Our ability to predict how future food webs will respond to a changing environment is limited by our understanding of species responses to climate change, which are often tested in isolation or in simplified experimental designs. More realistic predictions of the impacts of climate change on ecosystems requires consideration of entire species communities, including the species interactions that can buffer or exacerbate these impacts. We experimentally tested the effects of warming and acidification, both individually and in combination, on a benthic marine food web in a near-natural ecological setting. Energy flow from the first trophic level (primary producers and detritus) to the second (herbivores), and from the second to the third trophic level (carnivores) was quantified under these different regimes. We show that warming, either alone or in combination with acidification, can constrain productivity to the bottom of the food web by enhancing cyanobacterial biomass and reducing energy flow to higher trophic levels, thus lowering energy transfer efficiency between producers and consumers. In contrast, increased ocean acidification alone showed a positive effect on herbivores and carnivores. Our finding is important because it demonstrates that future warming could drive marine food web collapses to potentially simplified and less productive coastal systems.