Tim Boxhammer

Influence of ocean acidification on a natural winter-to-summer plankton succession: First insights from a long-term mesocosm study draw attention to periods of low nutrient concentrations

Every year, the oceans absorb about 30% of anthropogenic carbon dioxide (CO2) leading to a re-equilibration of the marine carbonate system and decreasing seawater pH. Today, there is increasing awareness that these changes–summarized by the term ocean acidification (OA)–could differentially affect the competitive ability of marine organisms, thereby provoking a restructuring of marine ecosystems and biogeochemical element cycles. In winter 2013, we deployed ten pelagic mesocosms in the Gullmar Fjord at the Swedish west coast in order to study the effect of OA on plankton ecology and biogeochemistry under close to natural conditions. Five of the ten mesocosms were left unperturbed and served as controls (~380 μatm pCO2), whereas the others were enriched with CO2-saturated water to simulate realistic end-of-the-century carbonate chemistry conditions (~760 μatm pCO2). We ran the experiment for 113 days which allowed us to study the influence of high CO2 on an entire winter-to-summer plankton succession and to investigate the potential of some plankton organisms for evolutionary adaptation to OA in their natural environment. This paper is the first in a PLOS collection and provides a detailed overview on the experimental design, important events, and the key complexities of such a “long-term mesocosm” approach. Furthermore, we analyzed whether simulated end-of-the-century carbonate chemistry conditions could lead to a significant restructuring of the plankton community in the course of the succession. At the level of detail analyzed in this overview paper we found that CO2-induced differences in plankton community composition were non-detectable during most of the succession except for a period where a phytoplankton bloom was fueled by remineralized nutrients. These results indicate: (1) Long-term studies with pelagic ecosystems are necessary to uncover OA-sensitive stages of succession. (2) Plankton communities fueled by regenerated nutrients may be more responsive to changing carbonate chemistry than those having access to high inorganic nutrient concentrations and may deserve particular attention in future studies.

Phytoplankton blooms at increasing levels of atmospheric carbon dioxide: experimental evidence for negative effects on prymnesiophytes and positive on small picoeukaryotes

Anthropogenic emissions of carbon dioxide (CO2) and the ongoing accumulation in the surface ocean together with concomitantly decreasing pH and calcium carbonate saturation states have the potential to impact phytoplankton community composition and therefore biogeochemical element cycling on a global scale. Here we report on a recent mesocosm CO2 perturbation study (Raunefjorden, Norway), with a focus on organic matter and phytoplankton dynamics. Cell numbers of three phytoplankton groups were particularly affected by increasing levels of seawater CO2 throughout the entire experiment, with the cyanobacterium Synechococcus and picoeukaryotes (prasinophytes) profiting, and the coccolithophore Emiliania huxleyi (prymnesiophyte) being negatively impacted. Combining these results with other phytoplankton community CO2 experiments into a data-set of global coverage suggests that, whenever CO2 effects are found, prymnesiophyte (especially coccolithophore) abundances are negatively affected, while the opposite holds true for small picoeukaryotes belonging to the class of prasinophytes, or the division of chlorophytes in general. Future reductions in calcium carbonate-producing coccolithophores, providing ballast which accelerates the sinking of particulate organic matter, together with increases in picoeukaryotes, an important component of the microbial loop in the euphotic zone, have the potential to impact marine export production, with feedbacks to Earths climate system.

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

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.

Quantifying the time lag between organic matter production and export in the surface ocean: Implications for estimates of export efficiency

The oceans potential to export carbon to depth partly depends on the fraction of primary production (PP) sinking out of the euphotic zone (i.e., the e-ratio). Measurements of PP and export flux are often performed simultaneously in the field, although there is a temporal delay between those parameters. Thus, resulting e-ratio estimates often incorrectly assume an instantaneous downward export of PP to export flux. Evaluating results from four mesocosm studies, we find that peaks in organic matter sedimentation lag chlorophyll a peaks by 2 to 15 days. We discuss the implications of these time lags (TLs) for current e-ratio estimates and evaluate potential controls of TL. Our analysis reveals a strong correlation between TL and the duration of chlorophyll a buildup, indicating a dependency of TL on plankton food web dynamics. This study is one step further toward time-corrected e-ratio estimates

Ocean Acidification-Induced Restructuring of the Plankton Food Web Can Influence the Degradation of Sinking Particles

Ocean acidification (OA) is expected to alter plankton community structure in the future ocean. This, in turn, could change the composition of sinking organic matter and the efficiency of the biological carbon pump. So far, most OA experiments involving entire plankton communities have been conducted in meso- to eutrophic environments. However, recent studies suggest that OA effects may be more pronounced during prolonged periods of nutrient limitation. In this study, we investigated how OA-induced changes in low-nutrient adapted plankton communities of the subtropical North Atlantic Ocean may affect particulate organic matter (POM) standing stocks, POM fluxes, and POM stoichiometry. More specifically, we compared the elemental composition of POM suspended in the water column to the corresponding sinking material collected in sediment traps. Three weeks into the experiment, we simulated a natural upwelling event by adding nutrient-rich deep-water to all mesocosms, which induced a diatom-dominated phytoplankton bloom. Our results show that POM was more efficiently retained in the water column in the highest CO2 treatment levels (>800 μatm pCO2) subsequent to this bloom. We further observed significantly lower C:N and C:P ratios in post-bloom sedimented POM in the highest CO2 treatments, suggesting that degradation processes were less pronounced. This trend is most likely explained by differences in micro- and mesozooplankton abundance during the bloom and post-bloom phase. Overall, this study shows that OA can indirectly alter POM fluxes and stoichiometry in subtropical environments through changes in plankton community structure.

Video of the sampling strategy to empty sediment traps of the “Kiel Off-Shore Mesocosms for future Ocean Simulations” (KOSMOS)

We deployed KOSMOS units in different climate zones and marine ecosystem types between 2011 and 2015, in order to study the influence of ocean acidification on the succession of plankton communities under in-situ conditions. Settling particulate matter within the mesocosms was quantitatively collected in sediment traps attached to the bottom of the mesocosms. We applied a low vacuum sampling strategy to empty these particle traps through silicon tubes reaching down from the sea surface outside of the mesocosm enclosures. The video shows the setup of the traps and the sample recovery from small boats attached to the KOSMOS units. The video can be downloaded from the OceanRep server (GEOMAR) but is also available on the KOSMOS channel of the streaming platform YouTube.

Enhanced transfer of organic matter to higher trophic levels caused by ocean acidification and its implications for export production: A mass balance approach

Ongoing acidification of the ocean through uptake of anthropogenic CO2 is known to affect marine biota and ecosystems with largely unknown consequences for marine food webs. Changes in food web structure have the potential to alter trophic transfer, partitioning, and biogeochemical cycling of elements in the ocean. Here we investigated the impact of realistic end-of-the-century CO2 concentrations on the development and partitioning of the carbon, nitrogen, phosphorus, and silica pools in a coastal pelagic ecosystem (Gullmar Fjord, Sweden). We covered the entire winter-to-summer plankton succession (100 days) in two sets of five pelagic mesocosms, with one set being CO2 enriched (~760 μatm pCO2) and the other one left at ambient CO2 concentrations. Elemental mass balances were calculated and we highlight important challenges and uncertainties we have faced in the closed mesocosm system. Our key observations under high CO2 were: (1) A significantly amplified transfer of carbon, nitrogen, and phosphorus from primary producers to higher trophic levels, during times of regenerated primary production. (2) A prolonged retention of all three elements in the pelagic food web that significantly reduced nitrogen and phosphorus sedimentation by about 11 and 9%, respectively. (3) A positive trend in carbon fixation (relative to nitrogen) that appeared in the particulate matter pool as well as the downward particle flux. This excess carbon counteracted a potential reduction in carbon sedimentation that could have been expected from patterns of nitrogen and phosphorus fluxes. Our findings highlight the potential for ocean acidification to alter partitioning and cycling of carbon and nutrients in the surface ocean but also show that impacts are temporarily variable and likely depending upon the structure of the plankton food web.

Performance of herring larvae in a simulated future ocean food web, using the "Kiel Off-Shore Mesocosms for future Ocean Simulations"

We studied the combined direct physiological and indirect food web effects of ocean acidification on herring larvae inside pelagic mesocosms. A natural plankton community of the Gullmarsfjord, Sweden was enclosed in the Kiel Off-Shore Mesocosms for future Ocean Simulations (KOSMOS) for 113 days from March to June 2013 at ambient and projected end-of-the-century CO2 levels (~760 µatm pCO2). Herring eggs were introduced into the mesocosms, where they hatched in mid of May. The larvae developed inside the mesocosms for ~6 weeks, feeding on prey organisms that experienced treatment CO2 levels for ~9 weeks. This video is meant as an illustration of the herring larvae«s performance inside our mesocosm units.

Video of a plankton community enclosed in a "Kiel Off-Shore Mesocosm for future Ocean Simulations" (KOSMOS) during the long-term study in Gullmar Fjord (Sweden) 2013

From January to July 2013 we deployed ten 19 m long KOSMOS units in a Swedish fjord (Gullmar Fjord, 58° 16’008 N, 11° 28’680E) close to the city of Lysekil, in order to study the influence of ocean acidification on a natural winter-to-summer succession of a plankton community under in-situ conditions. Towards the end of the study (21st of May), we mounted an underwater camera on a diving torch and slowly lowered this setup to a depth of approximately 18.5 m. A variety of different organisms (copepods, fish larvae, jelly fish) and detrital aggregates can be seen during the descent of the camera into the deep. The conical mesocosm sediment trap and particles collected in the funnel can be seen at the end of the video in 19 m water depth. The video shows that we enclosed and studied a lively plankton community within the KOSMOS system.

Video of a plankton community enclosed in a “Kiel Off-Shore Mesocosm for future Ocean Simulations” (KOSMOS) during the SOPRAN study in Raunefjord (Norway) 2011

In May 2011 we deployed nine 25 m long KOSMOS units for 5 weeks in a Norwegian fjord (Raunefjord, 60.265°N, 5.205°E) close to the city of Bergen, in order to study the influence of ocean acidification on the succession of a plankton community under in-situ conditions. Towards the end of the study (7th of June), we mounted an underwater camera on a diving torch and slowly lowered this setup to a depth of approximately 24.5 m. A variety of different organisms (copepods, fish larvae, jelly fish, appendicularians) and detrital aggregates can be seen during the descent of the camera into the deep. The conical mesocosm sediment trap and particles collected in the funnel can be seen at the end of the video in 25 m water depth. The video shows that we enclosed and studied lively plankton communities within the KOSMOS system. The video can be downloaded on OceanRep but is also available on the KOSMOS channel of the streaming platform YouTube.