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.

Analyzing the Impacts of Elevated-CO2 Levels on the Development of a Subtropical Zooplankton Community During Oligotrophic Conditions and Simulated Upwelling

“…Calanoida were positively affected by medium-and high-pCO 2 , although the trend was only visible during the last two sampling days. These results match with previous outcomes described for copepodites and adult Pseudocalanus acuspes in eutrophic waters and pCO 2 levels of ∼760 µatm (Algueró-Muñiz et al, 2017;Taucher et al, 2017b), suggesting a benefit of realistic end-of-century pCO 2 levels on calanoid copepods through higher food availability. Small planktonic copepods are dominant in the plankton communities in many parts of the world's oceans and therefore important members of pelagic food webs (Turner, 2004).…”

“…As reported by other authors (e.g., Isari et al, 2015), responses to OA are not only dependent on species-specific sensitivities, but, much more importantly, depend on CO 2 effects on the community and the trophic interactions taking place in a species' natural habitat. In fact, most of the reported effects of OA on planktonic communities need to be attributed to these community effects, as many indicate a positive effect of OA (or rather carbon availability) on the plankton (Algueró-Muñiz et al, 2017;Taucher et al, 2017b). The temporal trends in major microZP groups (aloricate ciliates, small dinoflagellates) and Calanoida (Figures 3, 4, respectively) were most likely triggered by the food supply for microZP combined with the preference of most copepods for heterotrophic protists (Suzuki et al, 1999;Turner, 2004).…”

“…Plankton community OA studies to date have been mostly carried out in relatively eutrophic environments (but see Sala et al, 2015;Gazeau et al, 2017), and led to varying conclusions. Some studies showed the lack of major effects of elevated pCO 2 levels in micro- (Aberle et al, 2013;Horn et al, 2016) and mesozooplankton abundances (Niehoff et al, 2013), while others detected both changes in community size distributions and biomass (Lischka et al, 2017;Taucher et al, 2017b) as well as positive bottom-up pCO 2 responses on mesozooplankton abundances (Algueró-Muñiz et al, 2017). Inorganic nutrient availability can control these different responses to OA in planktonic communities, thereby the nutrient-deplete phases could determine the transfer of the pCO 2 effects on primary producers to primary consumers (Alvarez-Fernandez et al, 2018).…”

Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change—A review

“…Their findings revealed distinctive CO 2 functional response curves for these diazotrophs, and provided a compelling explanation for the differences observed in the scenario-based studies.Single drivers have also been used in more logistically challenging scenario-based experiments in which the response(s) of entire ecological communities to manipulation have been investigated(Gattuso et al, 2014;Riebesell, Czerny, et al, 2013;Riebesell, Gattuso, Thingstad, & Middelburg, 2013). Outcomes from such studies reflect the combined influence of direct impacts on individual species, and indirect effects resulting from, for example, shifts in community compositionTaucher et al, 2017), prey palatability(Poore et al, 2013) and changes in competition(Hale, Calosi, Mcneill, Mieszkowska, & Widdicombe, 2011). Methods for separating direct and indirect effects are available(Alsterberg, Eklof, Gamfeldt, Havenhand, & Sundback, 2013; see below), but have been applied infrequently in such studies.…”

The effect of elevated CO2 on the production and respiration of a Sargassum thunbergii community: A mesocosm study

“…In case of the studies on open-water ecosystems (e.g. the phytoplankton community (Taucher et al 2017)), the reported effects of OA under those conditions consequently improve our understanding of ecosystem responses to OA, because OA is predicted to occur similarly within large areas in the open oceans (except in the Arctic Ocean) (IPCC 2014). On the other hand, the carbonate dynamics of coastal waters are different from the open ocean and can modify the acidification process in coastal waters.…”