Influence of ocean acidification on plankton community structure during a winter-to-summer succession: An imaging approach indicates that copepods can benefit from elevated CO2 via indirect food web effects

Abstract

Plankton communities play a key role in the marine food web and are expected to be highly sensitive to ongoing environmental change. Oceanic uptake of anthropogenic carbon dioxide (CO2) causes pronounced shifts in marine carbonate chemistry and a decrease in seawater pH. These changes-summarized by the term ocean acidification (OA)-can significantly affect the physiology of planktonic organisms. However, studies on the response of entire plankton communities to OA, which also include indirect effects via food-web interactions, are still relatively rare. Thus, it is presently unclear how OA could affect the functioning of entire ecosystems and biogeochemical element cycles. In this study, we report from a long-term in situ mesocosm experiment, where we investigated the response of natural plankton communities in temperate waters (Gullmarfjord, Sweden) to elevated CO2 concentrations and OA as expected for the end of the century (~760 μatm pCO2). Based on a plankton-imaging approach, we examined size structure, community composition and food web characteristics of the whole plankton assemblage, ranging from picoplankton to mesozooplankton, during an entire winter-to-summer succession. The plankton imaging system revealed pronounced temporal changes in the size structure of the copepod community over the course of the plankton bloom. The observed shift towards smaller individuals resulted in an overall decrease of copepod biomass by 25%, despite increasing numerical abundances. Furthermore, we observed distinct effects of elevated CO2 on biomass and size structure of the entire plankton community. Notably, the biomass of copepods, dominated by Pseudocalanus acuspes, displayed a tendency towards elevated biomass by up to 30-40% under simulated ocean acidification. This effect was significant for certain copepod size classes and was most likely driven by CO2-stimulated responses of primary producers and a complex interplay of trophic interactions that allowed this CO2 effect to propagate up the food web. Such OA-induced shifts in plankton community structure could have far-reaching consequences for food-web interactions, biomass transfer to higher trophic levels and biogeochemical cycling of marine ecosystems.

Fig 1. Images of organism classes (obtained with the ZooScan method) that made up a significant portion of overall biomass.

A: Large copepods (Pseudocalanus acuspes), B: small copepods (likely copepodites), C: copepod nauplii, D: Coscinodiscus sp. cells, E: Hydromedusae. Scale bar is identical for all panels.

Fig 2. Temporal development of size distribution in the control mesocosms (average) over the course of the experiment.

(A): normalized particle size spectrum, (B) weighted biomass spectrum. Note that particle diameter (ESD), as well as abundance and biomass are displayed on a log10-scale. (C) and (D): same as in (A) and (B), respectively, but focusing on t1 and t57. Shaded area denotes range of replicate mesocosms. Note that biomass in (D) is shown on a semi-log scale (i.e. linear y-axis) and not on a log-log-scale as in (B).

Fig 3. Average contribution of copepods and Coscinodiscus sp. to the biomass size distribution in the control mesocosms.

(A) initial conditions (t1). (B) during period of maximum biomass (t57). Shaded area denotes range of replicate mesocosms.

Fig 4. Size structure of the copepod community (including nauplii) in the mesocosms (average of 5 mesocosms in the control treatment).

(A) normalized abundance spectrum and (B) weighted biomass spectrum. Shaded area denotes range of replicate mesocosms.

Fig 5. CO₂ effects on particle size spectra.

Comparison of normalized abundance spectrum (A) and weighted biomass spectrum (B) in the control (blue) and high CO₂ mesocosms (red) on day t57. Shaded area denotes range of replicate mesocosms and asterisks indicate a statistically significant effect of CO₂ on the respective size class (p<0.05).

Fig 6. CO₂ effects on the plankton community.

CO₂-related differences in biomass of copepods and nauplii (A,B) and Coscinodiscus sp. (C,D) in the control (blue) and high CO₂ mesocosms (red) on day t57. Shown are the size distribution of biomass in weighted biomass-size spectra (A,C) and box plots for overall biomass (B,D). Shaded area denotes range of replicate mesocosms and asterisks in panel A and C indicate a statistically significant effect of CO₂ on the respective size class (p < 0.05). Tests for statistical significance of total biomass in the respective groups (B,D) yielded p-values of p = 0.06 (copepods) and p = 0.10 (Coscinodiscus).

Fig 7. Evaluation of image-based method.

Comparison of biomass development estimated from flow cytometry and Zooscan (A) with measurements of particulate organic carbon (POC) (B) in the control (blue) and high CO₂ mesocosms (red). Shaded areas denote range of replicates. (C) Scatter plot comparing biomass estimated in this study with measured POC for all mesocosms and sampling days (n = 140, R² = 0.83)