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

Metabolic Responses of Subtropical Microplankton After a Simulated Deep-Water Upwelling Event Suggest a Possible Dominance of Mixotrophy Under Increasing CO2 Levels

In the autumn of 2014, nine large mesocosms were deployed in the oligotrophic subtropical North-Atlantic coastal waters off Gran Canaria (Spain). Their deployment was designed to address the acidification effects of CO2 levels from 400 to 1,400 mu atm, on a plankton community experiencing upwelling of nutrient-rich deep water. Among other parameters, chlorophyll a (chl-a), potential respiration (Phi), and biomass in terms of particulate protein (B) were measured in the microplankton community (0.7-50.0 mu m) during an oligotrophic phase (Phase I), a phytoplankton-bloom phase (Phase II), and a post-bloom phase (Phase III). Here, we explore the use of the Phi/chl-a ratio in monitoring shifts in the microplankton community composition and its metabolism. Phi/chl-a values below 2.5 mu L O-2 h(-1) (mu g chl-a)(-1) indicated a community dominated by photoautotrophs. When Phi/chl-a ranged higher, between 2.5 and 7.0 mu L O-2 h(-1) (pg chl-a)(-1) , it indicated a mixed community of phytoplankton, microzooplankton and heterotrophic prokaryotes. When Phi/chl-a rose above 7.0 mu L O-2 h(-1) (mu g chl-a)(-1), it indicated a community where microzooplankton proliferated (>10.0 mu L O-2 h(-1) (mu g chl-a)(-1)), because heterotrophic dinoflagellates bloomed. The first derivative of B, as a function of time (dB/dt), indicates the rate of protein build-up when positive and the rate of protein loss, when negative. It revealed that the maximum increase in particulate protein (biomass) occurred between 1 and 2 days before the chl-a peak. A day after this peak, the trough revealed the maximum net biomass loss. This analysis did not detect significant changes in particulate protein, neither in Phase I nor in Phase III. Integral analysis of Phi/chl-a and B, over the duration of each phase, for each mesocosm, reflected a positive relationship between 4) and pCO(2) during Phase II [alpha = 230.10-5 mu L O-2 h(-1) L-1 (patm CO2)(-1) (phase-day)(-1), R-2 = 0.30] and between chl-a and pCO(2) during Phase III [alpha = 100.10(-5) Ag chl-a L-1 (mu atmCO(2))(-1) (phase-day)(-1), R-2 = 0.84]. At the end of Phase II, a harmful algal species (HAS), Vicicitus globosus, bloomed in the high pCO(2) mesocosms. In these mesocosms, microzooplankton did not proliferate, and chl-a retention time in the water column increased. In these V globosus-disrupted communities, the (Phi/chl-a ratio [4.1 +/- 1.5 /mu L O-2 h(-1) (mu g chl-a)(-1)] was more similar to the Phi/chl-a ratio in a mixed plankton community than to a photoautotroph-dominated one

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

Ocean acidification (OA) is affecting marine ecosystems through changes in carbonate chemistry that may influence consumers of phytoplankton, often via trophic pathways. Using a mesocosm approach, we investigated OA effects on a subtropical zooplankton community during oligotrophic, bloom, and post-bloom phases under a range of different pCO2 levels (from ∼400 to ∼1480 μatm). Furthermore, we simulated an upwelling event by adding 650 m-depth nutrient-rich water to the mesocosms, which initiated a phytoplankton bloom. No effects of pCO2 on the zooplankton community were visible in the oligotrophic conditions before the bloom. The zooplankton community responded to phytoplankton bloom by increased abundances in all treatments, although the response was delayed under high-pCO2 conditions. Microzooplankton was dominated by small dinoflagellates and aloricate ciliates, which were more abundant under medium- to high-pCO2 conditions. The most abundant mesozooplankters were calanoid copepods, which did not respond to CO2 treatments during the oligotrophic phase of the experiment but were found in higher abundance under medium- and high-pCO2 conditions toward the end of the experiment, most likely as a response to increased phyto- and microzooplankton standing stocks. The second most abundant mesozooplankton taxon were appendicularians, which did not show a response to the different pCO2 treatments. Overall, CO2 effects on zooplankton seemed to be primarily transmitted through significant CO2 effects on phytoplankton and therefore indirect pathways. We conclude that elevated pCO2 can change trophic cascades with significant effects on zooplankton, what might ultimately affect higher trophic levels in the future

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

Withstanding multiple stressors: ephyrae of the moon jellyfish (Aurelia aurita, Scyphozoa) in a high-temperature, high-CO2 and low-oxygen environment

Global change is affecting marine ecosystems through a combination of different stressors such as warming, ocean acidification and oxygen depletion. Very little is known about the interactions among these factors, especially with respect to gelatinous zooplankton. Therefore, in this study we investigated the direct effects of pH, temperature and oxygen availability on the moon jellyfish Aurelia aurita, concentrating on the ephyral life stage. Starved one-day-old ephyrae were exposed to a range of pCO2 (400–4000 ppm) and three different dissolved oxygen levels (from saturated to hypoxic conditions), in two different temperatures (5 and 15 °C) for 7 days. Carbon content and swimming activity were analysed at the end of the incubation period, and mortality noted. General linearized models were fitted through the data, with the best fitting models including two- and three-way interactions between pCO2, temperature and oxygen concentration. The combined effect of the stressors was small but significant, with the clearest negative effect on growth caused by the combination of all three stressors present (high temperature, high CO2, low oxygen). We conclude that A. aurita ephyrae are robust and that they are not likely to suffer from these environmental stressors in a near future

Effects of food and CO2 on growth dynamics of polyps of two scyphozoan species (Cyanea capillata and Chrysaora hysoscella)

Increasing anthropogenic CO2 concentration in the atmosphere is altering sea water carbonate chemistry with unknown biological and ecological consequences. Whereas some reports are beginning to emerge on the effects of ocean acidification (OA) on fish, very little is known about the impact of OA on jellyfish. In particular, the benthic stages of metagenetic species are virtually unstudied in this context despite their obvious importance for bloom dynamics. Hence, we conducted tri-trophic food chain experiments using the algae Rhodomonas salina as the primary producer, the copepod Acartia tonsa as the primary consumer and the benthic life stage of the scyphozoans Cyanea capillata and Chrysaora hysoscella as secondary consumers. Two experiments were conducted examining the effects of different levels of CO2 and food quality (experiment 1) and the effect of food quality and quantity (experiment 2) on the growth and respiration of scyphozoan polyps. Polyp growth and carbon content (µg polyp−1) were not affected by the CO2 treatments, but were significantly negatively affected by P limitation of the food in C. capillata but not in Ch. hysoscella. Growth and carbon content were reduced in low-food treatments, but increased with decreasing P limitation in high- and low-food treatments in C. capillata. Respiration was not significantly influenced by food quality and quantity in C. capillata. We conclude that phosphorus can be a limiting factor affecting the fitness of scyphopolyps and that P-limited food is of poor nutritional quality. Furthermore, OA, at least using realistic end-of-century scenarios, will have no direct effect on the growth of scyphistoma

In situ camera observations reveal major role of zooplankton in modulating marine snow formation during an upwelling-induced plankton bloom

Particle aggregation and the consequent formation of marine snow alter important properties of biogenic particles(size, sinking rate, degradability), thus playing a key role in controlling the vertical flux of organic matterto the deep ocean. However, there are still large uncertainties about rates and mechanisms of particle aggregation,as well as the role of plankton community structure in modifying biomass transfer from small particlesto large fast-sinking aggregates. Here we present data from a high-resolution underwater camera system that we used to observe particle sizedistributions and formation of marine snow (aggregates>0.5 mm) over the course of a 9-week in situ mesocosmexperiment in the Eastern Subtropical North Atlantic. After an oligotrophic phase of almost 4 weeks, addition ofnutrient-rich deep water (650 m) initiated the development of a pronounced diatom bloom and the subsequentformation of large marine snow aggregates in all 8 mesocosms. We observed a substantial time lag between thepeaks of chlorophyll a and marine snow biovolume of 9–12 days, which is much longer than previously reportedand indicates a marked temporal decoupling of phytoplankton growth and marine snow formation during ourstudy. Despite this time lag, our observations revealed substantial transfer of biomass from small particle sizes(single phytoplankton cells and chains) to marine snow aggregates of up to 2.5mm diameter (ESD), with most ofthe biovolume being contained in the 0.5–1mm size range. Notably, the abundance and community compositionof mesozooplankton had a substantial influence on the temporal development of particle size spectra and formationof marine snow aggregates: While higher copepod abundances were related to reduced aggregate formationand biomass transfer towards larger particle sizes, the presence of appendicularia and doliolids enhancedformation of large marine snow. Furthermore, we combined in situ particle size distributions with measurements of particle sinking velocity tocompute instantaneous (potential) vertical mass flux. However, somewhat surprisingly, we did not find a coherentrelationship between our computed flux and measured vertical mass flux (collected by sediment traps in15m depth). Although the onset of measured vertical flux roughly coincided with the emergence of marinesnow, we found substantial variability in mass flux among mesocosms that was not related to marine snownumbers, and was instead presumably driven by zooplankton-mediated alteration of sinking biomass and exportof small particles (fecal pellets). Altogether, our findings highlight the role of zooplankton community composition and feeding interactionson particle size spectra and formation of marine snow aggregates, with important implications for our understandingof particle aggregation and vertical flux of organic matter in the ocean

Winter river discharge may affect summer estuarine jellyfish blooms

Dams alter the natural dynamics of river inflow, disrupting biological processes in downstream ecosystems, as observed in the Guadiana estuary (SW Iberian Peninsula, Europe). Here, significant interannual fluctuations in the densities of jellyfish occur during summer, likely due to changes in winter river discharge. Therefore, this study aimed to quantify the relationship between winter river inflow and the abundance of jellyfish in the Guadiana estuary. In addition, the budding and growth of Aurelia aurita polyps, one of the bloom-forming species present in the estuary, were determined at different combinations of constant temperature and salinity. The response of polyps and ephyrae to short-term, low-salinity pulses was also quantified. Maximum winter river discharge and maximum abundance of estuarine medusa (bloom indicator) showed a significant negative correlation. Under constant conditions, polyps showed increased mortality when water temperature was higher than 23°C and salinity was lower than 23, and died when exposed to a short-term, low-salinity pulse (≤3). After exposure to freshets, polyp budding and feeding rates decreased by 69% and 32%, respectively, when salinity reached values as low as 10. Ephyrae died when salinity was lower than 10, and feeding rates decreased by 88% when salinity was 17, compared with full marine conditions. In conclusion, winter freshwater discharge may regulate the strength of estuarine jellyfish blooms, impairing the survival or condition of polyps and ephyrae during late winter or early spring. River basin managers should consider the prescription of freshets to prevent jellyfish blooms from disrupting ecosystem services (e.g. fisheries, tourism)

CO₂ effects on the plankton community.

<p>CO₂-related differences in biomass of copepods and nauplii (A,B) and <i>Coscinodiscus</i> 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 (<i>Coscinodiscus</i>).</p

Temporal changes in plankton community size structure.

<p>Average biomass of <i>Coscinodiscus</i> sp. and different size classes of copepods in the control mesocosms on t1 and t57 (± standard error, SE).</p