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 Earth’s climate system.publishedVersio

Factors controlling plankton community production, export flux, and particulate matter stoichiometry in the coastal upwelling system off Peru

Eastern boundary upwelling systems (EBUS) are among the most productive marine ecosystems on Earth. The production of organic material is fueled by upwelling of nutrient-rich deep waters and high incident light at the sea surface. However, biotic and abiotic factors can modify surface production and related biogeochemical processes. Determining these factors is important because EBUS are considered hotspots of climate change, and reliable predictions of their future functioning requires understanding of the mechanisms driving the biogeochemical cycles therein. In this field experiment, we used in situ mesocosms as tools to improve our mechanistic understanding of processes controlling organic matter cycling in the coastal Peruvian upwelling system. Eight mesocosms, each with a volume of ∼55 m3, were deployed for 50 d ∼6 km off Callao (12∘ S) during austral summer 2017, coinciding with a coastal El Niño phase. After mesocosm deployment, we collected subsurface waters at two different locations in the regional oxygen minimum zone (OMZ) and injected these into four mesocosms (mixing ratio ≈1.5 : 1 mesocosm: OMZ water). The focus of this paper is on temporal developments of organic matter production, export, and stoichiometry in the individual mesocosms. The mesocosm phytoplankton communities were initially dominated by diatoms but shifted towards a pronounced dominance of the mixotrophic dinoflagellate (Akashiwo sanguinea) when inorganic nitrogen was exhausted in surface layers. The community shift coincided with a short-term increase in production during the A. sanguinea bloom, which left a pronounced imprint on organic matter C : N : P stoichiometry. However, C, N, and P export fluxes did not increase because A. sanguinea persisted in the water column and did not sink out during the experiment. Accordingly, export fluxes during the study were decoupled from surface production and sustained by the remaining plankton community. Overall, biogeochemical pools and fluxes were surprisingly constant for most of the experiment. We explain this constancy by light limitation through self-shading by phytoplankton and by inorganic nitrogen limitation which constrained phytoplankton growth. Thus, gain and loss processes remained balanced and there were few opportunities for blooms, which represents an event where the system becomes unbalanced. Overall, our mesocosm study revealed some key links between ecological and biogeochemical processes for one of the most economically important regions in the oceans

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 (similar to 380 mu atm pCO(2)), whereas the others were enriched with CO2-saturated water to simulate realistic end-of-the-century carbonate chemistry conditions (mu 760 mu atm pCO(2)). 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.Peer reviewe

Overview of activities during the KOSMOS mesocosm study 2017 in the coastal upwelling system off Peru

In austral summer 2017 (coincidently during a coastal El Nino event) we deployed eight KOSMOS mesocosm units (53 m3 each) about 4.5 nm off-shore the Peruvian coastline (-12.0554667°, -077.2347667°). The aim of the study was to gather mechanistic understanding of processes controlling plankton productivity, organic matter export, and particle stoichiometry in the coastal upwelling system off Peru. We collected subsurface waters at two different locations in the regional oxygen minimum zone and injected them into four replicate mesocosms, to compare how upwelling of water masses with different oxygen minimum signature influence plankton succession patterns. This video is meant as an illustration of activities during this interdisciplinary mesocosm study in close cooperation with the Peruvian marine institute IMARPE

Orni-eutrophication by Inca terns (Larosterna inca) during the KOSMOS study 2017 in the coastal upwelling system off Peru

In early 2017 we deployed eight KOSMOS [a] mesocosm units (53 m^3 each) close to ‘Isla San Lorenzo’ about 4.5 nm off-shore the Peruvian coastline (-12.0554667°, -077.2347667°). The aim of the study was to improve our mechanistic understanding of processes controlling plankton productivity, organic matter export, and particle stoichiometry in the coastal upwelling system off Peru. About 40 days into the study, Inca terns (Larosterna inca) – an abundant sea bird species in the region – discovered the mesocosms as suitable resting places. The birds were able to start and land on the very small areas lacking anti-bird spikes that were installed on the mesocosm roofs. Resting on the flotation frames as well as the opening of the mesocosm bags, they defecated into the enclosed water columns, adding new nutrients to the system. This orni-eutrophication from day 40 to 50 triggered intense phytoplankton blooms in the uppermost part of the enclosures where light was plentiful. This video illustrates the fertilizing effect of Inca tern defecation on phytoplankton communities during our mesocosm study in the upwelling system off Peru. [a] Kiel Off-Shore Mesocosms for Ocean Simulation

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

KOSMOS Bergen 2015 mesocosm study: plankton abundances

To evaluate the influence of episodic extreme ocean acidification events in coastal regions, we deployed eight pelagic mesocosms for 53 days (Mai to July) in Raunefjord, Norway, and enclosed 60 m³ of local seawater containing a natural plankton community under post-bloom conditions. Four mesocosms were manipulated to simulate extreme pCO2 levels of 2069 µatm while the other four served as untreated controls. To monitor the effects of extreme pCO2 conditions, a variety of planktonic organisms inside and outside the mesocosms were measured over the course of the experiment in regular intervals. The data stems from 55µm and 500µm Apstein net hauls and subsequent microscopic analyses

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

Food web changes under ocean acidification promote herring larvae survival

Ocean acidification—the decrease in seawater pH due to rising CO2 concentrations—has been shown to lower survival in early life stages of fish and, as a consequence, the recruitment of populations including commercially important species. To date, ocean-acidification studies with fish larvae have focused on the direct physiological impacts of elevated CO2, but largely ignored the potential effects of ocean acidification on food web interactions. In an in situ mesocosm study on Atlantic herring (Clupea harengus) larvae as top predators in a pelagic food web, we account for indirect CO2 effects on larval survival mediated by changes in food availability. The community was exposed to projected end-of-the-century CO2 conditions (~760 µatm pCO2) over a period of 113 days. In contrast with laboratory studies that reported a decrease in fish survival, the survival of the herring larvae in situ was significantly enhanced by 19 ± 2%. Analysis of the plankton community dynamics suggested that the herring larvae benefitted from a CO2-stimulated increase in primary production. Such indirect effects may counteract the possible direct negative effects of ocean acidification on the survival of fish early life stages. These findings emphasize the need to assess the food web effects of ocean acidification on fish larvae before we can predict even the sign of change in fish recruitment in a high-CO2 ocean

Survival of herring larvae, Clupea harengus L., under projected end-of-the-century CO2-levels, as part of a complete pelagic food web in a mesocosm experiment (KOSMOS, Kristineberg, Sweden 2013)

Ocean acidification, the decrease in seawater pH due to rising CO2 concentrations, has been shown to lower survival in early life stages of fish and, as a consequence, the recruitment of populations including commercially important species. To date, ocean-acidification studies with fish larvae have focused on the direct physiological impacts of elevated CO2, but largely ignored the potential effects of ocean acidification on food web interactions. In an in situ mesocosm study on Atlantic herring (Clupea harengus) larvae as top predators in a pelagic food web, we account for indirect CO2 effects on larval survival mediated by changes in food availability. The community was exposed to projected end-of-the-century CO2 conditions (~760 µatm pCO2) over a period of 113 days. In contrast with laboratory studies that reported a decrease in fish survival, the survival of the herring larvae in situ was significantly enhanced by 19 ± 2%. Analysis of the plankton community dynamics suggested that the herring larvae benefitted from a CO2-stimulated increase in primary production. Such indirect effects may counteract the possible direct negative effects of ocean acidification on the survival of fish early life stages. These findings emphasize the need to assess the food web effects of ocean acidification on fish larvae before we can predict even the sign of change in fish recruitment in a high-CO2 ocean