Influence of cyclonic and anti-cyclonic eddies on plankton biomass, activity and diversity in the southeastern Mediterranean Sea

Planktonic food-webs were studied contemporaneously in a mesoscale cyclonic (upwelling, ~13 months old) and an anti-cyclonic (down-welling, ~2 months old) eddies, as well as in an uninfluenced-background situation in the oligotrophic southeastern Mediterranean Sea (SEMS) during late summer 2018. We show that integrated nutrients concentrations were higher at the cyclone compared to the anti-cyclone or the background stations by 2–13 fold. Concurrently, Synechococcus and Prochlorococcus were the dominant community component abundance-wise in the oligotrophic anti-cyclone (~300 × 1010 cells m−2). In the cyclone, pico- and nanoeukaryotes such as dinoflagellates, Prymnesiophyceae and Ochrophyta contributed substantially to the total phytoplankton abundnce (~14 × 1010 cells m−2) which was ~65 % lower in the anti-cyclone/background stations (~5 × 1010 cells m−2). Primary production was highest in the cyclonic eddy (191 mg C m−2 d−1) and was 2–5 fold lower outside the eddy area. The calculated doubling time of phytoplankton was ~3 days in the cyclone and ~5–10 days at the anti-cyclone/background stations, further reflecting the nutritional differences between these environments. Heterotrophic prokaryotic cell-specific activity was highest in the cyclone (~10 fg C cell−1 d−1), while the least productive cells were found in the anti-cyclone (4 fg C cell−1 d−1). The calculated doubling time of heterotrophic bacteria were 1.4 days in the cyclone and 2.5–3.5 days at the anti-cyclone/background stations. Total zooplankton biomass in the upper 300 m was tenfold higher in the cyclone compared with the anti-cyclone or background stations (1337 vs. 112–133 mg C m−2, respectively). Copepod diversity was much higher in the cyclone (44 species), compared to the anti-cyclone (6 small-size species). Our results highlight that cyclonic and anti-cyclonic eddies show significantly different community compositions and food-web dynamics in oligotrophic environments, with cyclones representing productive oases in the marine desert of the SEMS.

A biodiversity survey on the planktonic protistan grazers of the Gulf of Naples (Italy)

Plankton communities include both unicellular and multicellular organisms. An important unicellular component is represented by those protists (i.e., unicellular eukaryotes) that are non-strictly autotrophic organisms and consume bacteria and other protists. These organisms are an important link between primary producers and metazoans and are usually known as microzooplankton, protozooplankton, or mixoplankton, as many of them couple phagotrophic and photoautotrophic behaviours. Herein we report on the diversity of these organisms sampled at two sampling sites (coastal and offshore stations), at two depths (0 and 10 m), in the Gulf of Naples during the early autumn of 2020. Despite efforts to list plankton biodiversity of primary producers and metazoan grazers made in this area so far, protistan grazers are still poorly investigated and previous information date back to decades ago. Our survey identified dinoflagellates and oligotrich ciliates as the most abundant groups, while tintinnids were less quantitatively relevant. The taxonomic composition in samples investigated herein remarked that reported by previous studies, with the sole exception of the tintinnid Ascampbeliella armilla, which was never reported before. A coastal-offshore gradient in the taxonomical composition of protistan grazers was also observed, with some species more abundant within coastal waters and other better thriving in offshore ones. Surface and sub-surface communities also differed in terms of species composition, with the deeper communities in the two sites being more similar reciprocally than with communities at the surface. These differences were associated with distinct environmental conditions, such as light availability, as well with the standing feeding environment, arising potential implications in the functioning of the planktonic food web at the local scale.

Metabarcoding analysis of trophic sources and linkages in the plankton community of the Kuroshio and neighboring waters

Trophic sources and pathways supporting early life stages are crucial for survival of forage fishes recruiting around the oligotrophic and unproductive Kuroshio. However, information is limited for the Kuroshio planktonic food web and its trophodynamics because of its high biodiversity. Here, we explore trophic sources and linkages in the Kuroshio plankton community using metabarcoding analysis of gut-content DNA for 22 mesozooplankton groups. The major prey was dinoflagellates and calanoids for omnivorous groups, and calanoids and gelatinous organisms for carnivorous groups. Larvaceans and hydrozoans were the most frequently appeared prey for both omnivores and carnivores, whereas they were minor constituents of the available prey in water samples. Although calanoids overlapped as major prey items for both omnivores and carnivores because they were the most available, contributions from phytoplankton and gelatinous prey differed among taxonomic groups. Further analysis of the metabarcoding data showed that in addition to omnivorous copepods like calanoids, gelatinous groups like larvaceans and hydrozoans were important hubs in the planktonic food web with their multiple trophic linkages to many components. These findings suggest that gelatinous organisms are important as supplementary prey and provide evidence of niche segregation on trophic sources among mesozooplankton groups in the Kuroshio.

The importance and movement of mud bacterial carbon within the symbiosis of the New Zealand sea anemone Anthopleura aureoradiata

<p>A. aureoradiata is New Zealand’s only native cnidarian to form a phototrophic symbiosis with dinoflagellate microalgae. It is of particular interest as it can be found in estuarine mudflat habitats attached to cockles, where it spends a portion of the day submerged under the mud, either partially or completely. This scenario is very different to the situation in the tropics, where comparable symbioses (e.g. those with reef-building corals) live in brightly lit, clear waters. How A. aureoradiata maintains a stable symbiosis is therefore of considerable interest, with one potential mechanism involving the acquisition of carbon from the surrounding mud to counter the reduced availability of light and hence the reduced rate of photosynthesis. In this thesis, I established the extent to which organic carbon in mud (especially bacteria) can be assimilated by A. aureoradiata and to what extent, if any, this carbon contributes to symbiosis nutrition and facilitates symbiosis stability under otherwise sub-optimal conditions. In the first instance, anemones were given access to¹³C glucose-labelled mud for 12 hours, in both the light and dark, and the extent of label incorporation (¹³C enrichment) in both the host and symbiont was measured by mass spectrometry. Subsequently, A. aureoradiata was starved of planktonic food for six weeks in the presence of differing quantities of unlabelled mud (‘no-mud’, ‘low-mud’ and ‘high-mud’), either with or without light, and a range of nutritional and biomass parameters measured. These included symbiont density, host protein content, and the accumulation of host lipid and symbiont starch stores. Both the host anemone and its symbiotic algae showed signs of ¹³C uptake from the mud. Host anemones maintained in the dark assimilated more ¹³C label from the mud than did anemones incubated in the light, while the extent of label assimilation by the symbionts was unaffected by irradiance. Enhanced heterotrophic feeding in the dark is consistent with patterns reported for other symbiotic cnidarians, such as reef corals, where the host must counter the reduced availability of photosynthate from the symbiotic algae. However, the reason for the equal labelling of the symbionts in the light and dark is less clear. Nevertheless, factors such as reverse translocation in the dark (i.e. the transfer of organic carbon from host to symbiont), dark fixation of inorganic carbon, and a higher respiration rate of symbionts in the light than dark, could act either alone or in concert to produce the labelling pattern seen. While the host and symbiont showed evidence of carbon uptake from the surrounding mud, mud quantity had no effect on either the host’s or symbiont’s storage products (% of starch in symbiont biomass, host protein content and lipid content), or on symbiont density. The lack of an effect of mud suggests that mud-derived bacteria comprise little of the host’s natural diet. In contrast, increased light availability (independent of mud availability) did lead to elevated symbiont density and symbiont starch content, consistent with the phototrophic nature of this symbiosis. More surprising was that host protein content was highest in the dark, suggesting perhaps that the symbionts were less of an energetic drain on their host when starved in the dark due to their lower population density. In summary, my thesis provides evidence that A. aureoradiata and its symbiotic algae can use organic carbon obtained from the surrounding mud for their nutrition, but that this carbon source is of only negligible importance. These results are consistent with previous findings for the uptake and role of mud-derived nitrogen in this system. Further work to establish how this symbiosis maintains its remarkable stability under apparently sub-optimal, low-light conditions is therefore needed.</p>

The importance and movement of mud bacterial carbon within the symbiosis of the New Zealand sea anemone Anthopleura aureoradiata

<p>A. aureoradiata is New Zealand’s only native cnidarian to form a phototrophic symbiosis with dinoflagellate microalgae. It is of particular interest as it can be found in estuarine mudflat habitats attached to cockles, where it spends a portion of the day submerged under the mud, either partially or completely. This scenario is very different to the situation in the tropics, where comparable symbioses (e.g. those with reef-building corals) live in brightly lit, clear waters. How A. aureoradiata maintains a stable symbiosis is therefore of considerable interest, with one potential mechanism involving the acquisition of carbon from the surrounding mud to counter the reduced availability of light and hence the reduced rate of photosynthesis. In this thesis, I established the extent to which organic carbon in mud (especially bacteria) can be assimilated by A. aureoradiata and to what extent, if any, this carbon contributes to symbiosis nutrition and facilitates symbiosis stability under otherwise sub-optimal conditions. In the first instance, anemones were given access to¹³C glucose-labelled mud for 12 hours, in both the light and dark, and the extent of label incorporation (¹³C enrichment) in both the host and symbiont was measured by mass spectrometry. Subsequently, A. aureoradiata was starved of planktonic food for six weeks in the presence of differing quantities of unlabelled mud (‘no-mud’, ‘low-mud’ and ‘high-mud’), either with or without light, and a range of nutritional and biomass parameters measured. These included symbiont density, host protein content, and the accumulation of host lipid and symbiont starch stores. Both the host anemone and its symbiotic algae showed signs of ¹³C uptake from the mud. Host anemones maintained in the dark assimilated more ¹³C label from the mud than did anemones incubated in the light, while the extent of label assimilation by the symbionts was unaffected by irradiance. Enhanced heterotrophic feeding in the dark is consistent with patterns reported for other symbiotic cnidarians, such as reef corals, where the host must counter the reduced availability of photosynthate from the symbiotic algae. However, the reason for the equal labelling of the symbionts in the light and dark is less clear. Nevertheless, factors such as reverse translocation in the dark (i.e. the transfer of organic carbon from host to symbiont), dark fixation of inorganic carbon, and a higher respiration rate of symbionts in the light than dark, could act either alone or in concert to produce the labelling pattern seen. While the host and symbiont showed evidence of carbon uptake from the surrounding mud, mud quantity had no effect on either the host’s or symbiont’s storage products (% of starch in symbiont biomass, host protein content and lipid content), or on symbiont density. The lack of an effect of mud suggests that mud-derived bacteria comprise little of the host’s natural diet. In contrast, increased light availability (independent of mud availability) did lead to elevated symbiont density and symbiont starch content, consistent with the phototrophic nature of this symbiosis. More surprising was that host protein content was highest in the dark, suggesting perhaps that the symbionts were less of an energetic drain on their host when starved in the dark due to their lower population density. In summary, my thesis provides evidence that A. aureoradiata and its symbiotic algae can use organic carbon obtained from the surrounding mud for their nutrition, but that this carbon source is of only negligible importance. These results are consistent with previous findings for the uptake and role of mud-derived nitrogen in this system. Further work to establish how this symbiosis maintains its remarkable stability under apparently sub-optimal, low-light conditions is therefore needed.</p>

Warming winters in lakes: Later ice onset promotes consumer overwintering and shapes springtime planktonic food webs

Global climate warming is causing the loss of freshwater ice around the Northern Hemisphere. Although the timing and duration of ice covers are known to regulate ecological processes in seasonally ice-covered ecosystems, the consequences of shortening winters for freshwater biota are poorly understood owing to the scarcity of under-ice research. Here, we present one of the first in-lake experiments to postpone ice-cover onset (by ≤21 d), thereby extending light availability (by ≤40 d) in early winter, and explicitly demonstrate cascading effects on pelagic food web processes and phenologies. Delaying ice-on elicited a sequence of events from winter to spring: 1) relatively greater densities of algal resources and primary consumers in early winter; 2) an enhanced prevalence of winter-active (overwintering) consumers throughout the ice-covered period, associated with augmented storage of high-quality fats likely due to a longer access to algal resources in early winter; and 3) an altered trophic structure after ice-off, with greater initial springtime densities of overwintering consumers driving stronger, earlier top-down regulation, effectively reducing the spring algal bloom. Increasingly later ice onset may thus promote consumer overwintering, which can confer a competitive advantage on taxa capable of surviving winters upon ice-off; a process that may diminish spring food availability for other consumers, potentially disrupting trophic linkages and energy flow pathways over the subsequent open-water season. In considering a future with warmer winters, these results provide empirical evidence that may help anticipate phenological responses to freshwater ice loss and, more broadly, constitute a case of climate-induced cross-seasonal cascade on realized food web processes.

Interactions Between the Kleptoplastidic Dinoflagellate Shimiella gracilenta and Several Common Heterotrophic Protists

The newly described dinoflagellate, Shimiella gracilenta, is known to survive for approximately 1 month on the plastids of ingested prey cells during starvation, indicating kleptoplastidy. To understand the population dynamics of this dinoflagellate in marine planktonic food webs, its growth and mortality rate due to predation should be assessed. Thus, we investigated the feeding occurrence of eight common heterotrophic protists on S. gracilenta. We also determined the growth and ingestion rates of Oxyrrhis marina and the naked ciliate, Rimostrombidium sp. on S. gracilenta as a function of the prey concentration. The common heterotrophic dinoflagellates (HTDs) Gyrodinium dominans, O. marina, and Pfiesteria piscicida and a naked ciliate Rimostrombidium sp. were able to feed on S. gracilenta; whereas the HTDs Aduncodinium glandula, Gyrodinium jinhaense, Oblea rotunda, and Polykrikos kofoidii were not. Shimiella gracilenta supported positive growth of O. marina and Rimostrombidium sp. but did not support that of G. dominans and P. piscicida. With increasing prey concentrations, the growth and ingestion rates of O. marina and Rimostrombidium sp. on S. gracilenta increased and became saturated. The maximum growth rates of O. marina and Rimostrombidium sp. on S. gracilenta were 0.645 and 0.903 day−1, respectively. Furthermore, the maximum ingestion rates of O. marina and Rimostrombidium sp. on S. gracilenta were 0.11 ng C predator day−1 (1.6 cells predator−1 day−1) and 35 ng C predator day−1 (500 cells predator−1 day−1), respectively. The maximum ingestion rate of O. marina on S. gracilenta was lower than that on any other algal prey reported to date, although its maximum growth rate was moderate. In conclusion, S. gracilenta had only a few common heterotrophic protist predators but could support moderate growth rates of the predators. Thus, S. gracilenta may not be a common prey species for diverse heterotrophic protists but may be a suitable prey for a few heterotrophic protists.

Response of Growth and Grazing Rate of Nanoflagellates on Synechococcus spp. to Experimental Nutrient Enrichment

As important bacterivores in planktonic food webs, mixotrophic nanoflagellates cancause mortality in marine Synechococcus spp. Our previous study found that the pigmented nanoflagellate (PNF) has a significant grazing impact on Synechococcus spp. In the current study, we applied the dilution approach to test the growth and grazing rates of nanoflagellates on Synechococcus spp. We then compared the differences between experimental nutrient additions and in situ conditions in the coastal waters of the East China Sea during the summer season from July to September. The growth rates of Synechococcus spp. in the ambient environment were between 0.54 and 0.62 day−1, which were slightly higher than the 0.56 and 0.66 day−1 with nutrient enrichment in summer. In contrast, our nutrient enrichment experiments produced a marked decline approximately from 21% to 58%in the nanoflagellate grazing rate on Synechococcus spp. The reason was that the mixotrophic PNFs directly used the added nutrients and reduced their supply of nutrients from prey during the incubation experiments.