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.

Fig 1. The effects of future climate on absolute flows and transfer efficiency between successive trophic levels of the mesocosm food web.

Absolute flows, shown as line diagrams, refer to the total amount of energy that flows to higher trophic levels through consumption (log10 g Wet Weight/m²/month) aggregated by trophic level. The first trophic level shows flows originating from both the primary producers and detritus, which are transferred to the second and third trophic level through consumption by herbivores and carnivores, respectively. Transfer efficiency, presented as bar charts, refer to the ratio at which absolute flows are transferred from one trophic level to the next. Mean ± SE are based on n = 3 mesocosms. Significant effects (p < 0.05) within trophic levels are based on two-way ANOVAs (df = 1,8) and are indicated with asterisks. See S1 Table for statistical test outcomes. Means with different lower-case letters indicate significant differences among treatments based on posthoc tests corrected for false discovery rate and done separately for different trophic levels. The distribution of organisms within the mesocosms is reflected as their vertical position inside the graph (ranging from the bottom of the mesocosm to the surface of the water column). Species cliparts were obtained or modified from Openclipart (https://openclipart.org/). C, control; not sig, not significantly different; OA, elevated CO₂; OAT, elevated CO₂ and temperature; T, elevated temperature.

Fig 2. Living biomass of primary producers (trophic level 1), primary consumers (level 2), and secondary consumers (level 3) across functional groups within the mesocosms.

The biomass of functional groups with intermediate trophic levels (e.g., trophic level of filter feeders = 2.4) was assigned to the levels 2 and 3 according to their relative contribution to trophic flow (e.g., 60% to level 2 and 40% to level 3). At the third trophic level, the decrease in biomass under T and OAT is primarily driven by filter feeders, while a negative effect was not apparent in most other functional groups such as the fishes (see S2 Fig). Living biomass includes 16 functional groups excluding detritus. Values are means ± SE across mesocosms (n = 3). Significant interactions or main effects (p < 0.05) within trophic levels are based on two-way ANOVAs (df = 1,8) and are indicated with asterisks. See S2 Table for statistical test outcomes. Means with different lowercase letters indicate significant difference among treatments based on posthoc tests corrected for false discovery rate and done separately for different trophic levels. C, control; OA, elevated CO₂, OAT, elevated CO₂ and temperature; T, elevated temperature.

Fig 3. Relative proportion of cyanobacteria (as a percentage) to turf algae in mat-forming algae measured as benthic cover (A). Flows of production (%) to detritus pool relative to primary productivity (B).

Mean ± SE values per mesocosm are given (n = 3). Significant main effects (p < 0.05) are based on two-way ANOVAs (df = 1,8) and are indicated with asterisks. Means with different lowercase letters indicate significant difference among treatments. See S3 Table for statistical test outcomes. C, control; OA, elevated CO₂, OAT, elevated CO₂ and temperature; T, elevated temperature.